research paper on abiotic stress

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• Published: 24 September 2021

Abiotic stress responses in plants

• Huiming Zhang   ORCID: orcid.org/0000-0003-0695-3593 1 ,
• Jianhua Zhu 2 ,
• Zhizhong Gong 3 , 4 &
• Jian-Kang Zhu   ORCID: orcid.org/0000-0001-5134-731X 1  

Nature Reviews Genetics volume  23 ,  pages 104–119 ( 2022 ) Cite this article

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• Agricultural genetics
• Molecular biology
• Plant genetics
• Plant sciences

Plants cannot move, so they must endure abiotic stresses such as drought, salinity and extreme temperatures. These stressors greatly limit the distribution of plants, alter their growth and development, and reduce crop productivity. Recent progress in our understanding of the molecular mechanisms underlying the responses of plants to abiotic stresses emphasizes their multilevel nature; multiple processes are involved, including sensing, signalling, transcription, transcript processing, translation and post-translational protein modifications. This improved knowledge can be used to boost crop productivity and agricultural sustainability through genetic, chemical and microbial approaches.

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Acknowledgements

The authors apologize to those colleagues whose work is not cited owing to space constraints. H.Z. and J-K.Z. have been supported by the Chinese Academy of Sciences. Z.G. acknowledges grants from the National Science Foundation of China (31730007, 32030008, 31921001).

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Increased extracellular osmolarity that leads to cell dehydration.

Acidic polysaccharides that are critical for plant cell wall properties such as cohesion and electrostatic potential.

Hydroxyproline-rich glycoproteins that are essential components of the cell wall.

A qualitative change in the state of a system under a continuous change in an external parameter, such as the reversible condensation of certain proteins within cells in response to changing temperature.

Signalling from organelles to the nucleus.

A systemic response to abiotic stimuli, which involves long-distance communication among cells belonging to different tissues or organs.

Isogenic alleles with different epigenetic modifications that are passed from generation to generation.

Chromosome regions that statistically contribute to the variability of a quantitative phenotype.

Approaches searching the entire genome using single-nucleotide polymorphisms for chromosome regions that show consistent correlation with a particular phenotype, within a large population of individuals with contrasting and varying degree of the phenotype.

An approach for breeding in which the selection of desired individuals is based on the score of molecular markers.

The soil layer that surrounds, and is influenced by, plant roots.

All microorganisms that inhabit a defined region.

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EDITORIAL article

Editorial: abiotic stress in plants: sustainability and productivity.

• 1 Faculty of Agricultural Sciences, Federal University of Grande Dourados, Dourados, Mato Grosso do Sul, Brazil
• 2 Department of Agriculture, Mediterranea University of Reggio, Calabria, Italy
• 3 Centre of Natural and Exact Sciences, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

Editorial on the Research Topic Abiotic stress in plants: sustainability and productivity

The Research Topic Abiotic Stress in Plants: Sustainability and Productivity was dedicated to study the effects of stressful conditions of abiotic origin, such as water and thermal stress, heavy metals and soil salinity, on crops and tree species, with focus on molecular and physio metabolic responses or adjustments. Innovative management and cultural treatments as a promising practice to induce tolerance and favor plant survival, as well as efficient recovery and productivity, were also considered in the thirteen articles published on this topic.

In their review, Yang et al. discuss recent advances in heat perception mechanisms in plants, with focus on second messengers. Furthermore, this review reported the regulatory mechanisms that involve specific transcription factors. Calcium ion, hydrogen peroxide, and nitric oxide have emerged as key players in heat perception. After discussing the roles of transcription, thermotolerance, and temperature targeting factors, such as plasma membrane-associated thermosensors, the authors paid attention to unsolved questions in the field of heat perception that require further investigation in the future.

The review by Qin et al . reports the potential of porous fiber materials (PFM) made from mineral rocks in conserving soil and water in areas where flooding and drought may occur. The effectiveness of PFM depends on their porosity and permeability, which, if high they can increase the capacity to retain, replace and infiltrate water into the soil during rainfalls, thereby reducing the risk of flooding, runoff and nutrients loss.

In two of the papers presented here, the issue of abiotic stress effects modulated by the plant’s developmental stage is examined. Zhang et al. observe that, at any stage, mild water deficit reduces the crop coefficient and evapotranspiration intensity in watermelon, and the water demand differs among the stages, increasing rapidly from the seedling stage to vines.

Similarly, Chen et al. describe that management of deficit irrigation is a strategy to conserve water in agriculture. In their study with sunflower, they also report that mild water deficit, both at the seedling stage and maturity, promoted increase in water use efficiency by leaves. The authors conclude that mild water deficit may be an effective irrigation strategy for sunflower production in the cold and arid environment of Northwest China.

In addition to the above focus on developmental stages, the research reported here shows that cultivars and genotypes of the same species respond differently to abiotic stresses as well as the resources used to mitigate adverse environmental conditions. In this context, Safarpour et al. report that, although considered as resistant plant species, barley plants exposed to water stress showed decreases in growth and grain production, as well as an enhanced antioxidants' response. The barley cultivar showing the highest proline content and catalase activity was the one with the highest biomass production and grain yield, which led to the conclusion that foliar urea applications can be effective to increase water stress tolerance, by improving the plant physiological performance.

Zhou et al. evaluated the effect of irrigation management strategies associated with nitrogen fertilization on eggplant, and verified that mild water deficit combined with medium nitrogen application rate (W1N2) is the right choice for growing conditions in arid environment, providing better water and nitrogen use efficiency and productivity.

The germplasm variability in stress responses was also studied by Li et al. , who identified drought-resistant genotypes with potential value for breeding programs within a collection of 42 lettuce genotypes. Drought-resistance was found to be associated with little increases in stomata density, the production of superoxide and the content of malondialdehyde (MDA), but also with large increase in the activities of antioxidant enzymes, on the other hand.

In the same vein, Kumar et al. with the aim of identifying wheat genotypes tolerant to heat stress, verified that those tolerant ones maintained balanced phenological-physiobiochemical characteristics and high activities of their antioxidant enzymes. They also suggested that high photosynthesis and delayed senescence must be the best selection parameters for the heat tolerance in wheat.

The tolerance to a single stress or the combination of heat and drought stresses must be variable according to the cotton genotype, presenting different responses for enzymatic activity and non-enzymatic compounds ( Zafar et al. ). According to these authors, under combined stress, four genotypes exhibited superior performance in terms of agronomic traits and fiber quality, while others maintained gas exchange and relative water content, decreased their levels of H 2 O 2 and MDA and increased levels of chlorophylls, carotenoids and activity of antioxidant enzymes.

Many papers reported here suggest that alternative cultural treatments can mitigate the stressful effects of the environment. In a study on the effect of partial replacement of chemical fertilizer (CF) by Trichoderma biofertilizer (TF) on wolfberry cultivation in saline lands, Yan et al. observed that replacement with 75% CF improves the N use efficiency and promotes higher photosynthetic rate, resulting in greater biomass and fruit production.

Seeking for the mitigation of water stress effects on ‘jatobazeiro’ seedlings ( Hymenaea courbaril L.), Reis et al. confirmed the positive effect of intermediate shading of 30 and 50%, which accelerated the recovery of the photosynthetic rate after the resumption of irrigation. As a consequence, the cultivation under water deficit without shading (0%) should not be adopted for seedlings production in this species.

Considering that heavy metals pollution reduces the yield and quality of vegetables, Sun et al. demonstrated that the foliar spraying with zinc oxide nanoparticles (ZnO NPs) on tomato seedlings improved Cd tolerance, increased photosynthesis efficiency and antioxidant capacity, and reduced Cd accumulation in roots and leaves. Metabolomic analysis showed that exposure to ZnO NPs mitigates Cd toxicity, with higher effect on leaves than roots, with reduction of oxidative damage.

Once more in tomato seedlings, Turan et al. evaluated the potential of growth-promoting rhizobacteria (PGPR) to alleviate the stressful effect of drought, and verified that applying 4 L ha -1 of a biostimulant containing PGPR not only mitigated detrimental effects of water stress on hormonal balance and growth characteristics, but also restored plant growth and improved soil organic matter and the soil contents of total N, P, Ca, and Cu.

Author contributions

SS: Writing – review & editing, Writing – original draft. CS: Writing – review & editing, Writing – original draft. MB: Writing – review & editing, Writing – original draft. LT: Writing – original draft.

Acknowledgments

The Guest Editors would like to thank all the authors who contributed to this Research Topic. We would like to thank all the funding bodies and companies that contributed in some way to the articles published in this Research Topic.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

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Keywords: antioxidant enzymes, photosynthetic metabolism, regulatory mechanisms, salinity, thermal stress, transcription factors, water stress

Citation: Scalon SdPQ, Santos CC, Badiani M and Tabaldi LA (2024) Editorial: Abiotic stress in plants: sustainability and productivity. Front. Plant Sci. 15:1386174. doi: 10.3389/fpls.2024.1386174

Received: 14 February 2024; Accepted: 12 March 2024; Published: 20 March 2024.

Edited and Reviewed by:

Copyright © 2024 Scalon, Santos, Badiani and Tabaldi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY) . The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

*Correspondence: Silvana de Paula Quintão Scalon, c2lsdmFuYXNjYWxvbkB1ZmdkLmVkdS5icg==

Disclaimer: All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.

• Open access
• Published: 17 November 2011

Effects of abiotic stress on plants: a systems biology perspective

• Grant R Cramer 1 ,
• Kaoru Urano 2 ,
• Serge Delrot 3 ,
• Mario Pezzotti 4 &
• Kazuo Shinozaki 2  

BMC Plant Biology volume  11 , Article number:  163 ( 2011 ) Cite this article

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The natural environment for plants is composed of a complex set of abiotic stresses and biotic stresses. Plant responses to these stresses are equally complex. Systems biology approaches facilitate a multi-targeted approach by allowing one to identify regulatory hubs in complex networks. Systems biology takes the molecular parts (transcripts, proteins and metabolites) of an organism and attempts to fit them into functional networks or models designed to describe and predict the dynamic activities of that organism in different environments. In this review, research progress in plant responses to abiotic stresses is summarized from the physiological level to the molecular level. New insights obtained from the integration of omics datasets are highlighted. Gaps in our knowledge are identified, providing additional focus areas for crop improvement research in the future.

Recent advances in biotechnology have dramatically changed our capabilities for gene discovery and functional genomics. For the first time, we can now obtain a holistic "snapshot" of a cell with transcript, protein and metabolite profiling. Such a "systems biology" approach allows for a deeper understanding of physiologically complex processes and cellular function [ 1 ]. New models can be formed from the plethora of data collected and lead to new hypotheses generated from those models.

Understanding the function of genes is a major challenge of the post-genomic era. While many of the functions of individual parts are unknown, their function can sometimes be inferred through association with other known parts, providing a better understanding of the biological system as a whole. High throughput omics technologies are facilitating the identification of new genes and gene function. In addition, network reconstructions at the genome-scale are key to quantifying and characterizing the genotype to phenotype relationships [ 2 ].

In this review, we summarize recent progress on systematic analyses of plant responses to abiotic stress to include transcriptomics, metabolomics, proteomics, and other integrated approaches. Due to space limitations, we try to emphasize important perspectives, especially from what systems biology and omics approaches have provided in recent research on environmental stresses.

Plant responses to the environment are complex

Plants are complex organisms. It is difficult to find an estimate of the total number of cells in a plant. Estimates of the number of cells in the adaxial epidermal layer and palisade mesophyll of a simple Arabidopsis leaf are approximately 27,000 and 57,000 cells, respectively [ 3 ]. Another estimate of the adaxial side of the epidermal layer of the 7 th leaf of Arabidopsis was close to 100,000 cells [ 4 ] per cm 2 of leaf area. An Arabidopsis plant can grow as large as 14 g fresh weight with a leaf area of 258 cm 2 (11 g fresh weight) [ 5 ]. Thus, we estimate that a single Arabidopsis plant could have approximately 100 million cells (range of 30 to 150 million cells assuming 2.4 to 11 million cells per g fresh weight). A one million Kg redwood tree could possibly have 70 trillion cells assuming a cell size 100 times larger than an Arabidopsis cell. Combine that with developmental changes, cell differentiation and interactions with the environment and it is easy to see that there are an infinite number of permutations to this complexity.

There is additional complexity within the cell with multiple organelles, interactions between nuclear, plastidial and mitochondrial genomes, and between cellular territories that behave like symplastically isolated domains that are able to exchange transcription factors controlling gene expression and developmental stages across the plasmodesmata. A typical plant cell has more than 30,000 genes and an unknown number of proteins, which can have more than 200 known post-translational modifications (PTMs). The molecular responses of cells (and plants) to their environment are extremely complex.

Environmental limits to crop production

In 1982, Boyer indicated that environmental factors may limit crop production by as much as 70% [ 6 ]. A 2007 FAO report stated that only 3.5% of the global land area is not affected by some environmental constraint (see Table three point seven in http://www.fao.org/docrep/010/a1075e/a1075e00.htm ). While it is difficult to get accurate estimates of the effects of abiotic stress on crop production (see different estimates in Table 1 ), it is evident that abiotic stress continues to have a significant impact on plants based upon the percentage of land area affected and the number of scientific publications directed at various abiotic stresses (Table 1 ). If anything the environmental impacts are even more significant today; yields of the "big 5" food crops are expected to decline in many areas in the future due to the continued reduction of arable land, reduction of water resources and increased global warming trends and climate change [ 7 ].

This growing concern is reflected in the increasing number of publications focused on abiotic stresses. For example, since the pivotal review of systems biology by Kitano in 2002 [ 1 ], the number of papers published on abiotic stress in plants using a systems biology approach has increased exponentially (Figure 1 ).

The number of publications per year related to systems biology and abiotic stress . Key words used in the search of PubMed included: plant, systems biology, and abiotic stress (including stress sub-terms; e.g. drought or water deficit or dehydration). *The number for the year 2011 was estimated by doubling the 6-month value.

Multiple factors limit plant growth

Fundamentally, plants require energy (light), water, carbon and mineral nutrients for growth. Abiotic stress is defined as environmental conditions that reduce growth and yield below optimum levels. Plant responses to abiotic stresses are dynamic and complex [ 8 , 9 ]; they are both elastic (reversible) and plastic (irreversible).

The plant responses to stress are dependent on the tissue or organ affected by the stress. For example, transcriptional responses to stress are tissue or cell specific in roots and are quite different depending on the stress involved [ 10 ]. In addition, the level and duration of stress (acute vs chronic) can have a significant effect on the complexity of the response [ 11 , 12 ].

Water deficit inhibits plant growth by reducing water uptake into the expanding cells, and alters enzymatically the rheological properties of the cell wall; for example, by the activity of ROS (reactive oxygen species) on cell wall enzymes [ 8 ]. In addition, water deficit alters the cell wall nonenzymatically; for example, by the interaction of pectate and calcium [ 13 ]. Furthermore, water conductance to the expanding cells is affected by aquaporin activity and xylem embolism [ 14 – 17 ]. The initial growth inhibition by water deficit occurs prior to any inhibition of photosynthesis or respiration [ 18 , 19 ].

The growth limitation is in part due to the fundamental nature of newly divided cells encasing the xylem in the growing zone [ 20 , 21 ]. These cells act as a resistance to water flow to the expanding cells in the epidermis making it necessary for the plant to develop a larger water potential gradient. Growth is limited by the plant's ability to osmotically adjust or conduct water. The epidermal cells can increase the water potential gradient by osmotic adjustment, which may be largely supplied by solutes from the phloem. Such solutes are supplied by photosynthesis that is also supplying energy for growth and other metabolic functions in the plant. With long-term stress, photosynthesis declines due to stomatal limitations for CO 2 uptake and increased photoinhibition from difficulties in dissipating excess light energy [ 12 ].

One of the earliest metabolic responses to abiotic stresses and the inhibition of growth is the inhibition of protein synthesis [ 22 – 25 ] and an increase in protein folding and processing [ 26 ]. Energy metabolism is affected as the stress becomes more severe (e.g. sugars, lipids and photosynthesis) [ 12 , 27 , 28 ]. Thus, there are gradual and complex changes in metabolism in response to stress.

Central regulators limit key plant processes

The plant molecular responses to abiotic stresses involve interactions and crosstalk with many molecular pathways [ 29 ]. Systems biology and omics approaches have been used to elucidate some of the key regulatory pathways in plant responses to abiotic stress.

One of the earliest signals in many abiotic stresses involve ROS and reactive nitrogen species (RNS), which modify enzyme activity and gene regulation [ 30 – 32 ]. ROS signaling in response to abiotic stresses and its interactions with hormones has been thoroughly reviewed [ 32 ]. ROS and RNS form a coordinated network that regulates many plant responses to the environment; there are a large number of studies on the oxidative effects of ROS on plant responses to abiotic stress, but only a few studies documenting the nitrosative effects of RNS [ 30 ].

Hormones are also important regulators of plant responses to abiotic stress (Figure 2 ). The two most important are abscisic acid (ABA) and ethylene [ 33 ]. ABA is a central regulator of many plant responses to environmental stresses, particularly osmotic stresses [ 9 , 34 – 36 ]. Its signaling can be very fast without involving transcriptional activity; a good example is the control of stomatal aperture by ABA through the biochemical regulation of ion and water transport processes [ 35 ]. There are slower responses to ABA involving transcriptional responses that regulate growth, germination and protective mechanisms.

A simplified working model of a signaling network of plant responses to abiotic stress . Ovals represent proteins, metabolites or processes. Metabolites have magenta color. Phosphorylated proteins have red circles with a P inside. Sumoylated protein has an orange circle with an S inside. The solid purple circle indicates that DREB2 needs modification to be activated. Solid lines represent direct connections; dotted lines represent indirect connections (acting through some intermediate molecule). The gray line indicates that this reaction has not been shown in plants. Not all linkages and details of stress and hormone effects are shown in this diagram in order to simplify the model. Abbreviations: ABA (abscisic acid), ANAC (Arabidopsis NAC domain-containing protein), CAMTA (calmodulin-binding transcription activator), CBL (calcineurin B-like interacting protein kinase), CCA (circadian clock associated), CPK (calcium-dependent protein kinase), DREB/CBF (dehydration response element binding protein/C-repeat binding factor), ETR1 (ethylene response 1), GCN2 (general control non-repressible 2), HSF (heat shock factor), ICE (inducer of CBF expression), MAPK (mitogen-activated protein kinase), LHY (late elongated hypocotyl), PA (phosphatidic acid), PP2C (protein phosphatase 2C), PRR (pseudo response regulator), PYR/PYL/RCAR (ABA receptors), RNS (reactive nitrogen species), ROS (reactive oxygen species), SIZ (SAP and Miz domain protein), SnRK (sucrose nonfermenting-1 related kinase), TFs (transcription factors), TOR (target of rapamycin), ZAT (zinc finger protein).

Recently, the essential components of ABA signaling have been identified, and their mode of action was clarified [ 37 ]. The current model of ABA signaling includes three core components, receptors (PYR/PYL/RCAR), protein phosphatases (PP2C) and protein kinases (SnRK2/OST1) [ 38 , 39 ]. The PYR/PYL/RCAR proteins were identified as soluble ABA receptors by two independent groups [ 38 , 39 ]. The 2C-type protein phosphatases (PP2C) including ABI1 and ABI2, were first identified from the ABA-insensitive Arabidopsis mutants abi1-1 and abi2-1 , and they act as global negative regulators of ABA signaling [ 40 ]. SNF1-related protein kinase 2 (SnRK2) is a family of protein kinases isolated as ABA-activated protein kinases [ 41 , 42 ]. In Arabidopsis, three members of this family, SRK2D/SnRK2.2, SRK2E/OST1/SnRK2.6, and SRK2I/SnRK2.3, regulate ABA signaling positively and globally, as shown in the triple knockout mutant srk2d srk2e srk2i ( srk2dei )/ snrk2.2 snrk2.3 snrk2.6 , which lacks ABA responses [ 43 ]. The PYR/PYL/RCAR - PP2C - SnRK2 complex plays a key role in ABA perception and signaling.

Studies of the transcriptional regulation of dehydration and salinity stresses have revealed both ABA-dependent and ABA-independent pathways [ 44 ]. Cellular dehydration under water limited conditions induces an increase in endogenous ABA levels that trigger downstream target genes encoding signaling factors, transcription factors, metabolic enzymes, and others [ 44 ]. In the vegetative stage, expression of ABA-responsive genes is mainly regulated by bZIP transcription factors (TFs) known as AREB/ABFs, which act in an ABA-responsive-element (ABRE) dependent manner [ 45 – 47 ]. Activation of ABA signaling cascades result in enhanced plant tolerance to dehydration stress. In contrast, a dehydration-responsive cis-acting element, DRE/CRT sequence and its DNA binding ERF/AP2-type TFs, DREB1/CBF and DREB2A, are related to the ABA-independent dehydration and temperature responsive pathways [ 44 ]. DREB1/CBFs function in cold-responsive gene expression [ 48 , 49 ], whereas DREB2s are involved in dehydration-responsive and heat-responsive gene expression [ 50 ].

Ethylene is also involved in many stress responses [ 51 – 53 ], including drought, ozone, flooding (hypoxia and anoxia), heat, chilling, wounding and UV-B light [ 31 , 33 , 53 ]. Ethylene signaling is well defined [ 51 , 52 ], and will not be discussed in detail here. There are known interactions between ethylene and ABA during drought [ 31 ], fruit ripening [ 54 , 55 ], and bud dormancy [ 56 ]. All of these interactions make the plant response to stress very complex [ 12 , 31 , 52 ].

In yeast, the well-documented central regulators of protein synthesis and energy are SnRK1 (Snf1/AMPK), TOR1 and GCN2 [ 57 – 60 ]. These proteins are largely controlled by the phosphorylation of enzymes; all three are protein kinases acting as key hubs in the coordination of metabolism during stressful conditions [ 61 ]. In plants, TOR activity is inhibited by osmotic stress and ABA [ 62 ] and GCN2 activity is stimulated by UV-light, amino acid starvation, ethylene, and cold stress [ 63 ]. SnRK1 responds to energy depletion, such as low light, nutrient deprivation or hypoxic conditions [ 64 , 65 ], and interacts with both glucose and ABA signaling pathways [ 66 ]. One of the results of this coordinated response is the inhibition of protein synthesis.

Many abiotic stresses directly or indirectly affect the synthesis, concentration, metabolism, transport and storage of sugars. Soluble sugars act as potential signals interacting with light, nitrogen and abiotic stress [ 67 – 69 ] to regulate plant growth and development; at least 10% of Arabidopsis genes are sugar-responsive [ 68 ]. Mutant analysis has revealed that sugar signaling interacts with ethylene [ 70 ], ABA [ 71 , 72 ], cytokinins [ 73 ], and light [ 74 , 75 ]. In grapevine, sugar and ABA signaling pathways interact to control sugar transport. An ASR (ABA, stress-, and ripening-induced) protein isolated from grape berries is upregulated synergistically by ABA and sugars, and upregulates the expression of a hexose transporter [ 76 ]. VVSK1, a GSK3 type protein kinase, is also induced by sugars and ABA, and upregulates the expression of several hexose transporters [ 77 ].

Stresses such as sugar starvation and lack of light stimulate SnRK1 activity ([ 64 ]. Suc-P synthase (SPS), 3-hydroxy-3-methylglutaryl-CoA reductase, nitrate reductase, and trehalose-6-P synthase are negatively regulated by SnRK1 phosphorylation [ 78 ], indicating that SnRK1 modulates metabolism by phosphorylating key metabolic enzymes. Post-translational redox modulation of ADPG-pyrophosphorylase, a key control of starch synthesis, by SnRK1 provides an interesting example of interactions between phosphorylation, redox control and sugar metabolism [ 79 ]. In Arabidopsis, SnRK1 kinase activity is itself increased by GRIK1 and GRIK2, which phosphorylate a threonine residue of the SnRK1 catalytic subunit [ 78 ]. SnRK2 interacts with ABA for the control of stomatal aperture and participates in the regulation of plant primary metabolism. Constitutive expression of SnRK2.6 drastically boosts sucrose and total soluble sugar levels in leaves, presumably by controlling SPS expression [ 80 ].

Systems biology approach to abiotic stress

In the post-genomic era, comprehensive analyses using three systematic approaches or omics have increased our understanding of the complex molecular regulatory networks associated with stress adaptation and tolerance. The first one is 'transcriptomics' for the analysis of coding and noncoding RNAs, and their expression profiles. The second one is 'metabolomics' that is a powerful tool to analyze a large number of metabolites. The third one is 'proteomics' in which protein and protein modification profiles offer an unprecedented understanding of regulatory networks. Protein complexes involved in signaling have been analyzed by a proteomics approach [ 81 , 82 ]. Integration of the different omics analyses facilitates abiotic stress signaling studies allowing for more robust identifications of molecular targets for future biotechnological applications in crops and trees.

Co-expression analyses identify regulatory hubs

An important application of transcriptomics data is co-expression analysis of target genes using on-line analytical tools, such as ATTED-II (reviewed by [ 83 ]). This approach is very promising for understanding gene-gene correlations and finding master genes in target conditions.

In a series of pioneering papers, Hirai et al. [ 84 , 85 ] identified MYB transcription factors regulating glucosinolate biosynthesis in Arabidopsis in response to S and N deficiency using an integrated transcriptomics and metabolomics approach. Genes and metabolites in glucosinolate metabolism were found to be coordinately regulated [ 84 ]. Co-expression analysis was used to identify two MYB transcription factors that positively regulate glucosinolate metabolism [ 85 ]. Then a knock out mutant and ectopic expression of one of the transcription factors was used to validate its positive role in glucosinolate metabolism. Previously unidentified genes were assigned to this biosynthetic pathway and a regulatory network model was constructed [ 85 ].

Mao et al. [ 86 ] performed a gene co-expression network analysis of 1094 microarrays of Arabidopsis using a non-targeted approach. They identified 382 modules in this network. The top three modules with the most nodes were: photosynthesis, response to oxidative stress and protein synthesis. Many of the modules also involved responses to environmental stresses. They constructed a cold-induced gene network from a subset of microarrays. The response to auxin stimulus was the most over-represented of the 18 significant modules.

Carrera et al. [ 87 ] used the InferGene application to construct a regulatory model of the Arabidopsis genome. They used datasets from 1,486 microarray experiments. Ten genes were predicted to be the most central regulatory hubs influencing the largest number of genes. Included in this set were transcription factor genes involved in auxin (KAN3), gibberellin (MYB29), abscisic acid (MYB121), ethylene (ERF1), and stress responses (ANAC036). They computed the top 12 gene subnetworks; four of these were related to biotic and abiotic stresses. Eighty-five percent of the predicted interactions of the 25% most connected transcription factors were validated in AtRegNet, the Arabidopsis thaliana Regulator Network http://arabidopsis.med.ohio-state.edu/moreNetwork.html .

Lorenz et al [ 88 ] investigated the drought response of loblolly pine roots and identified a number of hubs in the transcriptional network. Highly ranked hubs included thioredoxin, an inositol transporter, cardiolipin synthase/phosphatidyl transferase, 9-cis-expoxycarotenoid dioxygenase, zeatin O-glucosyltransferase and a SnRK2 kinase. These genes are involved in phospholipid metabolism, ABA biosynthesis and signaling, and cytokinin metabolism; they appear to be important in stress mediation.

Weston et al [ 89 ] used weighted co-expression analysis to define six modules for Arabidopsis responses to abiotic stress. Two hubs in the common response module were an ankyrin-repeat protein and genes involved in Ca signaling. They created a compendium of genomic signatures and linked them to their co-expression analysis. Using the same approach, they extended their analyses to the responses of three different plant species to heat and light [ 90 ]. Species-specific responses were found involving heat tolerance, heat-shock proteins, ROS, oligosaccharide metabolism and photosynthesis.

Time-series analyses reveal multiple phases in stress responses

Time-series analyses allow one to distinguish between primary and secondary responses to stress. In a comprehensive time-series transcriptomics analysis of 7 abiotic stresses on different Arabidopsis organs [ 28 ], a core set of genes (50% were transcription factors) of non-specific responses for all stresses were elucidated. Included in this set were the AZF2, ZAT10 and ZAT12 transcription factors. This initial response is thought to be involved in the readjustment of energy homeostasis in response to the stress. With time (after 1 h) more stress-specific profiles developed.

Sun et al [ 91 ] applied a complexity metric to a set of time series data of Arabidopsis with 9 different abiotic stresses. They found that genes with a higher complexity metric had longer 5' intergenic regions and a greater density of cis-regulatory motifs than the genes with a low complexity metric. Many of the cis-regulatory motifs identified were associated with previously characterized stress responses.

Vanderauwera et al. [ 92 ] investigated the effects of hydrogen peroxide (H 2 O 2 ) signaling during high light stress using microarray analyses. They found that H 2 O 2 was not only heavily involved in signaling in high light stress, but also salinity, water deficit, heat and cold stress. H 2 O 2 was a key regulator of small and 70 kD heat shock proteins and many genes of the anthocyanin metabolic pathway. Anthocyanins appear to play an important role as antioxidants in plants. A specific UDP-glycosyltransferase (UGT74E2) was highly regulated by H 2 O 2 . In a subsequent study [ 93 ], UGT74E2 responded quickly to H 2 O 2 and glycosylated indole-3-butyric acid (IBA) modifying auxin homeostasis, plant morphology and improving stress tolerance to salinity and water deficit. Furthermore, auxin was found to interact with ABA, increasing the ABA sensitivity of the plant. Silencing a poly(ADP-ribose) polymerase improved high light stress tolerance in Arabidopsis [ 94 , 95 ]. Part of the improved abiotic stress tolerance was ascribed to improved energy-use efficiency and reduced oxidative stress [ 94 , 95 ].

Kusano et al. [ 96 ] conducted a time-series experiment on the effects of UV-B light on Arabidopsis using both metabolomics and transcriptomics analyses. They found that plants responded in two phases with an upregulation of primary metabolites in the first phase and the induction of protective secondary metabolites, especially phenolics, in the second phase. The induction of phenolics corresponded to transcripts involved in the phenylpropanoid pathway, but the transcripts for primary metabolism were less consistent indicating that this pathway may be regulated by other mechanisms (e.g. kinases).

The transcriptomic response to drought can vary with the time of day [ 97 ]. These responses seem to interact with hormonal and other stress pathways that naturally vary during the course of the day. A smaller set of core genes were identified that responded at all times of the day. This set was compared to two previous studies and was whittled down to just 19 genes, including a NF-YB transcription factor, several PP2Cs, a CIPK7, and a sulfate transporter.

Drought stress studies and microarray analyses of three different genotypes of poplar clones grown in two different locations revealed epigenetic regulation to the environment [ 98 ]. The tree clones that had a longer history in the environment showed greater changes in DNA methylation, thereby influencing their response to drought.

Shoot tip growth of grapevines was found to be much more sensitive to osmotic stress than gene expression in a time-series experiment of the effects of gradual osmotic stress on grapevine [ 27 ]. Proteomics data indicated that changes in protein expression preceded and were not well correlated with gene expression (G.R. Cramer, unpublished results). The integration of transcriptomics data and metabolomics data indicated distinct differences of the responses of salinity and an isosmotic water deficit [ 27 ]. Drought-stressed plants induced greater responses in processes needed for osmotic adjustment and protection against ROS and photoinhibition. Salinity induced greater responses in processes involved in energy metabolism, ion transport, protein synthesis and protein fate. A comparison to similar short-term stresses [ 11 ] indicated that a gradual, chronic stress response was more complex than an acute stress response.

The effect of water-deficit on Cabernet Sauvignon berries (a red wine grape) in the field was studied using transcriptomics, proteomics and metabolomics [ 99 – 102 ]. Integrated analyses confirmed that the phenylpropanoid pathway (including anthocyanin and stilbene biosynthesis) was upregulated by water deficit in a tissue-specific manner in the skins of the berries. Other metabolic pathways in the berries were affected by water deficit including ABA, amino acid, carotenoid, lipid, sugar and acid metabolism. Most of these changes were associated with improved quality characteristics of the fruit.

Likewise, Zamboni et al. [ 103 ] investigated berry development and withering in grapevine at the transcriptomics, proteomics and metabolomics levels. A multistep hypothesis-free approach from four developmental stages and three withering intervals, with integration achieved using a hierarchical clustering strategy (multivariate O2PLS technique), identified stage-specific functional networks of linked transcripts, proteins and metabolites, providing important insights into the key molecular processes that determine wine quality. A hypothesis-driven approach identified transcript, protein and metabolite variables involved in the molecular events underpinning withering, which predominantly reflected a general stress response. Berry ripening and withering are characterized by the accumulation of secondary metabolites such as acylated anthocyanins, but withering also involves the activation of osmotic and oxidative stress response genes and the production of stilbenes and taxifolin.

Usadel et al. [ 104 ] investigated the effects of cold temperatures over time using transcriptomics, metabolomics and enzyme activities. They found some enzyme activities and metabolites changed rapidly, whereas others changed more slowly. The early changes (6 h) in enzyme activities were poorly correlated with transcript abundance, but after 78 h these correlations were greatly improved. Much of the long-term changes in metabolism could be ascribed to the CBF regulon.

Caldana et al. [ 105 ] conducted a complex time-series experiment (22 time points) with differing temperatures and light intensities using both metabolomics and transcriptomics analyses. This high-resolution time series experiment revealed that metabolic activities respond more quickly than transcriptional activities, indicating a disconnect between metabolism and transcription in the early phases of stress response and indicating that enzymatic activities may play a significant role. There were common metabolic responses to the changing environment within 1 h of the change including a decrease in energy metabolism and translation and an increase in the transcription of genes involved in signaling cascades. At later time points, condition-dependent metabolism was revealed. For example, protein degradation and energy metabolism derived from amino acids occurred in warm temperatures and darkness. Amino acid catabolism appears to fuel the TCA cycle in the absence of photosynthesis.

Yun et al. [ 106 ] characterized the response of rice to a mild chilling stress (10°C). They found that transcriptional regulation consisted of three dynamic and complex phases over 96 h. The early transcriptional phase appeared to be triggered by oxidative signals (H 2 O 2 ) and lead to the subsequent induction of cellular defense and rescue mechanisms. Combining temporal co-expression data from microarrays with promoter motif enrichment analyses and oxidative responses, transcriptional regulatory network models for the different response phases were constructed. A bZIP-TGA transcription factor module (as1/ocs/TGA), one of seven transcription factor modules, was the most connected regulatory module in phase one. Each of the transcription factor modules consisted of clusters of transcription factors exhibiting combinatorial control of the chilling regulon. The speed of the response of this network was associated with chilling tolerance. Chilling-resistant genotypes had a much more rapid and pronounced response of this transcriptional regulatory network than chilling-sensitive genotypes. In addition, the transcription factors identified in this study were located within known growth and stress QTLs in the rice genome.

Integration of omics analysis identifies molecular networks functioning in abiotic stress responses

Integrated omics analyses have markedly increased our understanding of plant responses to various stresses. These analyses are important for comprehensive analyses of abiotic stress responses, especially the final steps of stress signal transduction pathways.

Integrated analyses of the transcriptome and the metabolome successfully demonstrate connections between genes and metabolites, elucidating a wide range of signal output from ABA under dehydration [ 107 ] and the DREB1/CBF transcription factors in response to low temperature [ 108 , 109 ]. Metabolite profiling reveals that ABA accumulates during dehydration, regulating the accumulation of various amino acids and sugars such as glucose and fructose. In particular, the dehydration-inducible accumulation of BCAAs (branch-chain amino acids), saccharopine, proline, and agmatine are correlated with the dehydration-inducible expression of their key biosynthetic genes ( BCAT2 , LKR/SDH , P5CS1 , and ADC2 , respectively), which are regulated by endogenous ABA [ 107 ]. In addition, metabolome analysis of transgenic Arabidopsis overexpressing DREB1A/CBF3 reveals that there is a striking similarity between the low-temperature regulated metabolome (monosaccharides, disaccharides, oligosaccharides and sugar alcohols) and that regulated by the DREB1A/CBF3 transcription factor [ 108 , 109 ]. In particular, the low-temperature-inducible accumulation of galactinol and raffinose is correlated with the expression of the Gols3 gene, which is a direct target of DREB1A/CBF3 [ 108 , 109 ]. Maruyama et al. [ 109 ] also analyzed DREB2A overexpression, which did not increase the level of any low-temperature regulated metabolites in transgenic plants. Overexpression of DREB2A-CA in transgenic plants increased their tolerance to dehydration stress, but only slightly increased their tolerance to freezing stress [ 50 ]. These results indicate that the increased tolerance to freezing stress in transgenic plants overexpressing DREB1A may depend on the accumulation of low-temperature regulated metabolites, especially sucrose, raffinose, galactinol, and myo -inositol. Similarly, transcriptomics and metabolomics analyses of PSEUDO RESPONSE REGULATOR (PRR) arrhythmic triple mutant revealed that the DREB1A/CBF gene and raffinose amounts appear to be regulated by the circadian clock, varying between day and night as if in anticipation of the colder night temperatures [ 110 ].

Comparing metabolomics between dehydration, salinity, light, heat or low temperature stress have identified metabolites that are generally important in abiotic stress responses or are specific to each stress [ 27 , 95 , 105 , 111 , 112 ]. In a metabolite profiling study of Arabidopsis responses to combined dehydration and heat stresses [ 95 ], heat stress reduced the toxicity of proline, indicating that during the more severe combined stress treatment, sucrose replaces proline in plants as the major osmoprotectant. Comparative metabolite analysis between Arabidopsis responding to heat shock and cold shock revealed that the majority of metabolites in response to heat shock overlapped with those produced in response to cold shock [ 109 , 113 ]. These results indicate that a metabolic network of compatible solutes includes proline, monosaccharides (glucose and fructose), galactinol, and raffinose, which have an important role in tolerance to temperature stress. Wienkoop et al. [ 112 ] identified a RNA-binding protein (ATGRP7) that increased in response to low temperature stress and decreased in response to high temperature stress. Its abundance was significantly correlated with glutamine and proline concentrations. While raffinose and galactinol concentrations were significant markers for temperature responses, their response was independent of the responses of ATGRP7, proline and glutamine.

Transcriptomics, metabolomics and enzyme activities were integrated in a comprehensive study of K deficiency [ 114 ]. Carbon and nitrogen metabolism were significantly affected by K deficiency. This integrated approach pinpointed that pyruvate kinase activity (not transcription) was inhibited directly by K deficiency and was primarily responsible for the metabolic disorders observed.

Systematic application of omics technologies has contributed to the development of stress-tolerant crops in the field

Many genes affect stress tolerance, but few of the identified genes have proven useful in the field. Due to the complexity of stress interactions and stress responses, relevant phenotyping needs to be performed (including field experiments) in abiotic stress studies if we are to make significant progress [ 113 ]. The following studies are discussed to highlight good examples of systems biology and omics approaches that have been used to identify key genes regulating stress tolerance and then followed with validation of those responses and phenotypes in multiple experiments including field conditions.

A SNAC1 gene was identified from microarray experiments of stress treatments on rice [ 115 ]. SNAC1 is a NAC transcription factor that induces the expression of a number of stress-tolerance genes and improves the drought and salt tolerance of rice in the field. The transgenic plants exhibited increased sensitivity to ABA and reduced water loss. In another drought stress study, a LEA (late embryogenesis abundant) gene was identified from microarray experiments of rice and was transformed and tested in the field under drought conditions through the T3 generation [ 116 ]. Spikelet fertility appears to be the main factor contributing to improved yields under drought conditions.

An exhaustive screen of greater than 1500 transcription factors in Arabidopsis identified approximately 40 transcription factors that when overexpressed, improved stress tolerance [ 117 ]. One of these transcription factors NF-YB1 was further characterized and shown to display significant drought tolerance in Arabidopsis. Microarray data of this overexpressing line showed few differences in gene expression and the genes identified were not known previously to be involved in drought tolerance. This functional genomics approach provided a new strategy for improving drought tolerance in plants. A homolog of NF-YB1 was cloned in maize (ZmNF-YB2), overexpressed and tested for drought tolerance in the greenhouse and field plots. The transgenic maize lines were more drought tolerant having increased chlorophyll content, photosynthesis, stomatal conductance and grain yields. One line consistently had more than 50% yield improvement in drought conditions over two different years.

Oh et al. [ 118 ] used microarrays to identify 42 AP2 transcription factors whose expressions were affected by stress. Two of these transcription factors, AP37 and AP59 were functionally characterized. The two transcription factors are closely related but have distinct differences in affecting rice phenotype. AP37 responded to drought, salinity, cold and ABA; over-expression improved stress tolerance to all three environmental conditions. AP59 responded to drought and salinity, but not cold or ABA, and improved stress tolerance to drought and salinity only. Both overexpressing lines showed improved photosynthetic efficiency under stress conditions. Overexpression of the transcription factors induced common and distinct sets of genes. T5 homozygous overexpressing lines of AP59, but not AP37, had yield penalties under normal paddy conditions in the field, whereas AP37 overexpressing lines, but not AP59, had enhanced yields under drought conditions in the field. The reduced yields of the overexpressing lines of AP59 were attributed to effects on spikelet development. This study emphasizes the point that it is important to characterize gene effects on yield under field conditions.

Mapping stress responses has provided new insights and identified gaps in our knowledge of abiotic stress responses

From a meta-analysis of drought-stress related papers from the last 15 years, a complex model for plant responses to drought stress was produced [ 12 ]. This model details the interactions of sugars, ROS/RNS, hormones (ABA, ethylene, auxins, cytokinins, salicylic acid, gibberellin and brassinosteroids) and nitrogen metabolism. It highlights the highly complex nature of stress responses.

From this review, we have constructed a simplified working model summarizing some of the known plant signaling responses to abiotic stress (Figure 2 ). Much of the signaling involves phosphorylation cascades that react quickly in the plant cell, emphasizing the need for proteomics data as well as transcriptomics data in future models. The PYR/PYL/RCAR-PP2C-SnRK2 pathway illustrates that protein phosphorylation and dephosphorylation are the most important factors in ABA signaling. Similar phosphorylation and dephosphorylation processes are involved in ethylene and other abiotic stress signaling pathways (Figure 2 ). Not all connections could be drawn in this two-dimensional figure without obscuring many other connections. For example, the interactions of ROS with abiotic stresses and hormones [ 32 ] are too complex to display here. In addition, the actual signaling response will be dependent upon the signaling pathway present in that organ, tissue or cell at the time of the response. One needs to use more sophisticated bioinformatics programs like Cytoscape [ 119 ] and its plug-ins to visualize the interactions comprehensively in two dimensional or three-dimensional space [ 120 ] or with time series views [ 121 ], which would allow these data to be viewed in four dimensions.

Although there are still some technological issues that must be solved to produce a complete picture of protein phosphorylation, several technologies have been developed for the large-scale analysis of phosphoproteins, known as 'phosphoproteomics' [ 122 ]. Mass spectrometry analyses have identified thousands of phosphoproteins in Arabidopsis, rice, and Medicago truncatula [ 123 – 125 ]. In addition, two studies have reported ABA-responsive changes in the phosphoproteome [ 126 , 127 ]. Phosphoproteomics analyses of mutants for abiotic stress signaling (e.g. PP2C or SnRK) will identify the relevant network of protein phosphorylation events in abiotic stress signaling.

Transcriptome analysis technologies have advanced to the point where high-through-put DNA sequencers and high-density microarrays such as tiling arrays are readily available. These technologies provide new opportunities to analyze noncoding RNAs and can clarify aspects of epigenetic regulation of gene expression [ 128 , 129 ]. Similar approaches [ 130 , 131 ] have revealed the global transcriptomes of plants exposed to abiotic stresses such as dehydration, cold, heat, high-salinity, osmotic stress, and ABA. These analyses indicate that these stresses increase or decrease transcript abundance from not only previously identified stress-responsive genes, but also from thousands of unannotated non-protein-coding regions. Matsui et al. [ 130 ] estimated that approximately 80% of previously unannotated upregulated transcripts arise from antisense strands of sense transcripts. There was a significant linear correlation between the expression ratios (stress-treated/untreated) of the sense transcripts and the ratios of the antisense transcripts. Interestingly, the data suggested that such stress-responsive antisense transcripts are derived from antisense strands of the stress-responsive genes, RD29A and CYP707A1 . Clearly, transcriptional regulation is far more complicated than we previously imagined. Whether or not such antisense transcripts have biological functions is an important issue that remains to be resolved.

Much more research is required in order to fully map plant responses to abiotic stress. The nature of the pathway responses will vary and is highly dependent on the species, organ, tissue, cell type, developmental stage of the plant, the stress or stresses affecting the plant, the level and duration of the stress. Despite the vast amount of research collected on abiotic stress in the last decade, there are still significant gaps in our knowledge. We still do not understand completely how plants perceive stress. We don't know all of the receptors and their sites of action (organs, tissues and cellular components). While we know a lot about downstream signaling (i.e. transcriptional pathways), we know very little about the primary signaling (i.e. proteomics). Most of the literature on abiotic stress responses in plants is based upon transcriptomics data rather than proteomics data. This is not surprising as transcriptomics technology is more advanced, easier to perform and less expensive. However, transcriptomics analyses are insufficient as there is an overall poor correlation of transcriptomics profiles with proteomics profiles [ 101 , 132 , 133 ] or enzyme activities [ 104 , 114 ]. There are only a few studies describing phosphorylation cascades and other post-translation modification activities in response to stress [ 134 ]. Recent efforts to map the hormone [ 126 , 127 ] and light-regulated [ 135 ] phosphorylomes are good first steps. Finally, we need better tools to facilitate systems biology analyses especially in the area of bioinformatics. Transcriptomics data can be collected in a matter of days or weeks, but the data analyses often take more than a year.

Conclusions

We have made great progress in understanding the responses of plants to abiotic stress. There are inherent physical, morphological and molecular limitations to the plant's ability to respond to stress. Systems biology approaches have given us a more holistic view of the molecular responses. Transcriptomics studies are well advanced, but proteomics analyses are lagging behind, especially the study of post-translational modifications. Plant responses to abiotic stress are dynamic and complex. The integration of multiple omics studies has revealed new areas of interactions and regulation. Time series experiments have revealed the kinetics of stress responses, identifying multiple response phases involving core sets of genes and condition-dependent changes. One consistent trend in response to abiotic stress is the early down regulation of energy metabolism and protein synthesis. This may indicate a conservation of energy by the plant and may reflect a shift from plant growth to protective mechanisms. In many examples presented in this review, ABA signaling mediates the plant responses to abiotic stress. Co-expression analyses are useful in that they have revealed key regulatory hubs that can be manipulated to produce different phenotypes. To get a comprehensive understanding of plant responses to abiotic stress, more extensive mapping of these responses at the organ, tissue and cellular level are needed. Such network analyses need to be extended to the proteomics and enzyme activities levels. Models need to be constructed and linked to phenotypic traits. The linkage of key regulatory hubs to phenotypic traits will allow for more rapid progress in the genetic manipulation and production of crop plants. Current progress is exemplified by the identification and validation of several key genes that improved stress tolerance of crops in the field. It is expected that progress in the plant sciences and systems biology will continue to accelerate in the near future.

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Cramer, G.R., Urano, K., Delrot, S. et al. Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biol 11 , 163 (2011). https://doi.org/10.1186/1471-2229-11-163

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Abiotic Stress in Crop Species: Improving Tolerance by Applying Plant Metabolites

Francisca godoy, karina olivos-hernández, claudia stange, michael handford.

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Received 2020 Oct 30; Accepted 2020 Dec 4; Collection date 2021 Feb.

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Reductions in crop yields brought about by abiotic stress are expected to increase as climate change, and other factors, generate harsher environmental conditions in regions traditionally used for cultivation. Although breeding and genetically modified and edited organisms have generated many varieties with greater abiotic stress tolerance, their practical use depends on lengthy processes, such as biological cycles and legal aspects. On the other hand, a non-genetic approach to improve crop yield in stress conditions involves the exogenous application of natural compounds, including plant metabolites. In this review, we examine the recent literature related to the application of different natural primary (proline, l -tryptophan, glutathione, and citric acid) and secondary (polyols, ascorbic acid, lipoic acid, glycine betaine, α-tocopherol, and melatonin) plant metabolites in improving tolerance to abiotic stress. We focus on drought, saline, heavy metal, and temperature as environmental parameters that are forecast to become more extreme or frequent as the climate continues to alter. The benefits of such applications are often evaluated by measuring their effects on metabolic, biochemical, and morphological parameters in a variety of crop plants, which usually result in improved yields when applied in greenhouse conditions or in the field. As this strategy has proven to be an effective way to raise plant tolerance to abiotic stress, we also discuss the prospect of its widespread implementation in the short term.

Keywords: drought stress, heavy metal stress, primary metabolite, salt stress, secondary metabolites

1. Introduction

Abiotic stress is one of the most important problems currently faced by agriculture. It causes serious losses in crop production worldwide and reduces planted acreage. Amidst a growing population and climate change, this scenario becomes increasingly complex. Because the world population is forecast to increase from 7 to 9–10 billion people by 2050, an increase of between 60 and 110% in global food production will be required ([ 1 ] and references therein). Arable lands are also affected by migration to cities; as urban areas expand, they encroach more into surrounding, often fertile land, which is another factor that pushes agriculture into areas that are less-suited to crop cultivation [ 2 ]. Due to deforestation and the excessive use of fossil fuels, atmospheric CO 2 levels have increased from 280 to 400 ppm and are expected to rise to 800 ppm by 2100 [ 3 , 4 ]. Furthermore, climate change causes extreme weather, such as brusque temperature fluctuations, extreme precipitation, and drought, among other effects. This is subjecting crop species to increased abiotic stress and impacts production. For example, 45% of arable lands are subjected to drought [ 5 ], and the world area under aridity stress increased from 17 to 27% between 1950 and 2000 [ 6 ]. Furthermore, salinity accounts for considerable decreases in crop productivity [ 7 ], because most crop species are sensitive to salt stress (1.0–1.8 dS m −1 ), and it negatively impacts yield by 10 to 50%, depending on the salt concentration present [ 8 ]. Anthropogenic activities, such as mineral extraction and the over-application of fertilisers and pesticides, are also related to increases in heavy metal pollution, including excess hexachromium (Cr), cadmium (Cd), arsenic (As), lead (Pb), copper (Cu), and mercury (Hg). These pollutants affect plant developmental processes, such as seed germination, and the rates of photosynthesis, respiration, and transpiration, thus reducing growth, yield and quality [ 9 , 10 ] ( Figure 1 ). These situations thus demand changes in agricultural practices to respond to the negative impacts of climate change and anthropogenic activities.

Abiotic stress reduces crop yield. Environmental stress factors, such as heat, cold, drought, salinity, and the presence of heavy metals such cadmium, copper, and chromium, elicit stress responses in plants, including an accumulation of reactive oxygen species (ROS) and reduced photosynthetic activity, which ultimately lower plant growth and thus crop yields.

Plants are commonly subjected to different kinds of abiotic stress, such as UV, high temperatures, drought, floods, and heavy metals. As sessile organisms, they have evolved structural and metabolic adaptations to survive these conditions, such as increased root area and leaf curling when exposed to drought; greater production of antioxidant compounds such as carotenoids, proline, and ascorbic acid; and higher activity of enzymes related to the scavenging of reactive oxygen species (ROS). Abiotic stress causes an imbalance of pro-oxidant and antioxidant compounds, also known as oxidative stress, via processes that have been covered by excellent reviews [ 11 ], including in crop species [ 12 ]. Briefly, abiotic stress factors frequently favours stomatal closure, increasing the activity of the photorespiratory pathway, and triggering the production of hydrogen peroxide (H 2 O 2 ). Additionally, the diminished uptake and assimilation of CO 2 results in an imbalance of electron flow through the photosynthetic electron transport chain, again sparking the production of superoxide radicals and singlet oxygen ( 1 O 2 ). Together with hydroxyl radicals (OH • ), the excess H 2 O 2 , superoxide radicals and 1 O 2 are highly reactive to proteins, lipids, and nucleic acids, damaging them and causing cell death. A common marker for lipid peroxidation, considered one of the most damaging processes, is malondialdehyde (MDA), which is an oxidised product of membrane lipids. To overcome oxidative stress, plants possess enzymatic and non-enzymatic detoxification systems. In the enzymatic system, the enzymes superoxide dismutase (SOD), catalase (CAT), monodehydroascorbate reductase (MDHAR), dehydroascorbate reductase (DHAR), glutathione reductase (GR), glutathione transferase (GST), ascorbate peroxidase (APX), glutathione peroxidase (GPX), and guaiacol peroxidases (POXs) among others, are involved in ROS scavenging. These enzymes present higher activity when plants are subjected to stress. The non-enzymatic mechanism involves the production of compounds such as proline, glutathione (GSH), ascorbic acid, carotenoids, flavonoids, and tocopherols, that alleviate oxidative damage by neutralising ROS [ 13 , 14 ]. In the case of GSH, not only its concentration but the ratio with its oxidised form, glutathione disulphide (GSSG), is important. Crop varieties presenting higher endogenous amounts of some of these compounds display improved tolerance. However, under high intensity or continued stress, these strategies are not enough to alleviate the damage, and plant growth and yield are severely affected.

Currently there are several strategies to increase abiotic stress tolerance in crop species: (1) Genetically engineered organisms (GMOs), including transgenic, cisgenic, and intragenic crops; (2) traditional breeding programs; (3) new breeding technologies (NBTs), including the use of the Clustered Regularly Interspaced Short Palindromic Repeats (CRISPR/Cas) edition strategy; and (4) the application of plant biostimulants. Biostimulants are defined as plant fertilisers that improve nutrient use efficiency, tolerance to abiotic stress, quality traits or availability of confined nutrients in the soil or rhizosphere [ 15 ].

Although many GMOs have been bioengineered to tolerate abiotic stress, their practical use depends on the politics and legal aspects of each country, and it is a lengthy process before they are accepted for cultivation and commercialisation. Although more than 500 transgenic crops have been approved for cultivation, only 12 are related to tolerance to abiotic stress due to the high complexity of this trait [ 16 ]. Furthermore, there is a generally negative public perception regarding transgenic crops and a lengthy regulatory process to obtain permission for cultivation. It has been estimated that, on average, it costs USD 35 million to process the regulatory safety assessments and authorisations, and that it takes approximately 13 years from the development of a transgenic crop to its commercial launch [ 16 , 17 ]. Regarding genetically edited crops, the CRISPR mushroom was the first edited commercialised food [ 18 ], but their governance is still being developed in many countries [ 19 ]. Crop varieties obtained by conventional breeding programs are not limited by environmental and biosafety regulations, but present the problem that it takes ten to twenty years to develop a new variety, depending on the species [ 20 ].

On the other hand, a non-genetic approach to improve crop yield in stress conditions involves the exogenous application of biostimulants, including naturally occurring plants and fungal and microbial metabolites. For example, the application of amino acids, sugars, secondary metabolites, or artificial compounds has proven to be an effective way to increase plant tolerance to stress, and is relatively easy to implement in the short term. It has been reported that the application of endogenous metabolites enhances the plant stress response, and these compounds have the advantage in that they participate in combating different kinds of stress. Phytohormones, as key regulators of plant development, have also been applied to crops in order to improve tolerance to different kinds of abiotic stress. Exogenous application of auxin, cytokinins, abscisic acid, salicylic acid, and gibberellin have all proven useful in alleviating the effects of abiotic stress, as have transgenic means to enhance endogenous hormone production ([ 21 , 22 , 23 , 24 , 25 ] and references therein). As the role of phytohormones in abiotic stress has been widely described by other colleagues in the aforementioned publications, this review will focus on primary and secondary metabolites.

It is known that in plants, fungi, and microorganisms, more than 200,000 substances are produced, and they can be grouped into primary and secondary metabolites [ 26 ]. Primary metabolites are synthesised by all organisms and are essential for central, vital processes such as growth and development, and include proteins, lipids, and carbohydrates. In plants, secondary metabolites are synthesised in different cellular compartments, and include phenolics, terpenoids, and alkaloids as main groups, whose many functions include protection against abiotic and biotic stress. Different metabolic routes are involved in the synthesis of these molecules, such as the shikimate pathway, the acetate–malonate pathway, and side reactions emanating from glycolysis and the tricarboxylic acid (TCA) cycle [ 26 , 27 , 28 ]. Compared with primary metabolites, secondary metabolites are produced in low levels (<1% dry weight) and are specific to certain organs or developmental stages.

In this review, we present the latest literature on how the exogenous application of key natural primary and secondary metabolites has been used to improve abiotic stress tolerance (salinity, drought, and heavy metal) in both greenhouse and field conditions, with a focus on their effects on growth, physiological parameters, and yield in crop species. Exogenous metabolite application is an easy-and-feasible-to-implement strategy for producers, although the time interval in which they exert their beneficial effects depends on dose, the time of application and crop species. Finally, we comment on the challenges to overcome so that growers and producers can profit from the knowledge generated in this fast-developing area.

2. Primary Metabolites

2.1. proline.

Proline is one of the most studied osmoprotectants in plants. In 1954, Kemble and McPherson described proline accumulation in wilting rye grass ( Lolium perenne ), and since then, it has been the focus of many studies. Proline can function as a molecular chaperone, protecting protein integrity. Moreover, it acts as a singlet oxygen quencher, contributing to the maintenance of redox balance [ 29 , 30 ]. However, the beneficial effects observed in abiotic stress tolerance depend on species, concentration, phenological time of application, and application system.

Extensive literature exists on the beneficial effects of proline when applied to crop species under abiotic stress. For example, Teh et al. (2016) [ 31 ] applied proline (5 and 10 mM) to 30-day-old rice ( Oryza sativa ) plants cultivated in vitro under saline stress; the higher concentration significantly increased plant height and shoot and root number when compared to control stressed plants. Additionally, in rice, Tabssum et al. (2019) [ 32 ] observed improved water relations in salt+proline-treated plants grown in greenhouse conditions, as well as an increase in SOD and CAT activities, indicating an enhanced effect of proline on ROS scavenging when compared to salt-stress conditions. However, 50 mM-proline treatments had adverse effects on bean ( Vicia faba ), where plant growth and photosynthetic pigment accumulation were similar to that of the sea water treatments [ 33 ], indicating toxic effects. Thus, dose optimisation is a crucial step towards its use for yield improvement in agriculture.

It has been reported that proline treatment in the context of abiotic stress induces changes at the structural and ultrastructural levels. An increase in root surface is one of the strategies adopted by plants to overcome nutrient or water shortage. Proline application during salt stress induced changes in root surface in rice [ 31 ], increasing the number of roots per plant. Regarding the aerial part, proline application in salt-stressed plants produced structural changes in stems and leaves. Rady et al. reported an increase in cortical layers, xylem vessel diameter, and cortex thickness in two varieties of lupine ( Lupinus termis ) grown in salinity conditions, when 3, 6 or 9 mM proline was foliar-applied at 20, 35, and 50 days after sowing, and the best results were obtained with a proline concentration of 6 mM [ 34 ]. At the ultrastructural level, treatments with proline in rice leaves under control conditions produced swelling of thylakoids and an increase in total starch area. Salt stress also had this effect, especially 100 mM NaCl. However, when proline was applied in rice plants under saline stress, chloroplasts maintained their structural integrity, and no thylakoid swelling was observed. This is consistent with reports describing a protecting role of proline on thylakoid membranes by scavenging ROS [ 35 ].

The effectiveness of proline in the alleviation of metal toxicity has also been studied. Treatment by excess caused a decrease in growth parameters, an increase in MDA and H 2 O 2 levels, and SOD and POX activities in eggplant ( Solanum melongena ). However, As+proline treatment caused an increment in dry weight (DW) and root length, reduced As content in eggplant seedlings, decreased H 2 O 2 and MDA levels, and increased activity of ROS scavenging-related enzymes. It also generated higher activity levels of the two proline biosynthesis enzymes, Δ1-pyrroline-5-carboxylate synthetase (P5CS) and proline dehydrogenase [ 36 ]. Likewise, in rice treated with Cr, proline application significantly decreased MDA levels [ 37 ]. In a pot experiment where wheat ( Triticum aestivum ) was subjected to Cu stress, proline application increased yield (100-grain weight), although it depended on the cultivar used [ 38 ].

Further studies evaluating crop yield improvement under field conditions and long-term stress are needed in order to validate the use of proline by producers.

2.2. L-Tryptophan (TRP)

Auxin is the most studied hormone in plants. Because abiotic stress impairs plant development and growth, one of the approaches to overcome this has been the application of L-tryptophan (β-3-indolylalanine), an essential amino acid that serves as precursor for auxin biosynthesis [ 39 ].

The effect of TRP in ameliorating salt-induced damage in crops has also been studied. Red peppers ( Capsicum annuum ) grown in pots in a wire house were subjected to different salinity levels and TRP treatments. Plant growth parameters, such as plant height, root length, shoot, and root DW, increased in all conditions when TRP was applied, as did chlorophyll and carotenoid levels. Moreover, fruit weight was higher when compared to untreated controls. At high salinity, control plants did not produce fruit; however, under TRP treatment, plants were able to develop fruits, albeit small ones [ 40 ]. Other studies carried out in sugar beet ( Beta vulgaris ) showed that several root parameters at harvest were improved in plants subjected to different salinity levels whose seeds had been pre-soaked with TRP when compared to salt-stressed plants which had not been treated with this amino acid [ 41 ]. Furthermore, salinity decreased root quality by increasing K + , Na + , and α-amino-N, which are considered impurity parameters. TRP seed treatment improved said parameters, thus enhancing root quality [ 41 ].

Regarding drought stress, TRP has proven to improve yield. Jamil, 2018 [ 42 ], performed a pot experiment, where wheat ( Triticum aestivum ) was subjected to different irrigation treatments. TRP was foliar sprayed every week, starting 15 days after germination and ending two weeks after the filling stage. TRP treatment increased growth parameters, such as plant height, root length, and root DW, in all irrigation conditions when compared to control plants, as well as the amount of photosynthetic pigments. TRP also increased yield, either under control or drought conditions [ 42 ].

Moreover, TRP improves yield in crops subjected to heavy metal stress. In rice subjected to Cd stress, a decrease in plant growth (plant height and number of tillers) and yield parameters (number of panicles, 1000 grain weight, and paddy yield) was observed when compared to control plants. However, Cd+TRP treatment increased those parameters when compared to plants subjected to Cd stress alone [ 43 ], indicating that TRP is effective at alleviating Cd-induced damage.

Hanci et al. evaluated the effect of TRP on seed germination under temperature stress [ 44 ]. They treated onion ( Allium cepa ) and leek ( Allium porrum ) seeds with different concentrations of TRP, and subjected them to 7, 21, and 35 °C in a germination chamber for 21 days. In onion, germination percentage at the lowest temperature was slightly increased by TRP treatment (125 ppm), although higher doses of this metabolite decreased the germination rate. In leek, beneficial effects of TRP were observed only in cold stress conditions (7 °C). The authors conclude that although TRP application may improve germination, further studies are needed to identify the appropriate dose for each species [ 44 ].

In summary, TRP has been seen to induce plant growth and yield parameters in crops subjected to different kinds of stress, such as salt, drought, and excess Cd, although the cost of applying in the field must be considered and evaluated.

2.3. Glutathione (GSH)

GSH (γ-l-glutamyl-l-cysteinylglycine) is a ubiquitous low molecular weight tripeptide, composed of the essential amino acids glutamine, cysteine, and glycine [ 45 ], although some plants exhibit a variation called homoglutathione, with the same biological properties. It is present in most plant tissues, and among its major functions are ROS detoxification, formation of phytochelatins that bind heavy metals, detoxification of methylglyoxal, and its role as a cysteine reservoir [ 46 , 47 ].

GSH application in mungbean ( Vigna radiata ) seedlings grown under salt stress in growth chambers improved the relative water content (RWC) and chlorophyll ( a and b ) levels at 24 and 48 h after GSH treatment. Classic stress marker levels such as H 2 O 2 , MDA, and superoxide generation rate were also significantly decreased in the salt+GSH treatment when compared to the salt stress treatment alone. The GSH/GSSG ratio was also significantly increased when comparing GSH treatment to salt stress alone, indicating a better redox state. Enzyme activities from the ROS scavenging system (SOD, APX, GST, MDHAR, DHAR, GR, and GPX) were also increased in plants subjected to salt+GSH when compared to control plants under salt stress alone [ 48 ]. Zhou et al. also evaluated the enzyme activity and transcript abundance of ROS scavengers under GSH and salt treatments in tomatoes ( Solanum lycopersicum ) grown under greenhouse conditions [ 49 ]. They found that salt stress decreased the activity levels of SOD, POD, CAT, MDHAR, DHAR, and APX, as well as GSH, when compared to control conditions, but GSH treatment improved enzyme activity when compared to salt stress. The foliar application of GSH to tomato seedlings grown under salt stress reduced H 2 O 2 , MDA, and superoxide generation rate levels, as well as a decrease in Na + and Cl - uptake and accumulation when compared to salt-stressed plants [ 49 ]. Even though the study evaluated the effect of GSH at 5, 10, and 15 days after treatments, the results were consistent with those reported for other species [ 48 , 49 ].

Moreover, eleven soybean ( Glycine max ) varieties grown under nets showed significant increments in plant growth and production parameters when GSH was applied to leaves of salt-stressed plants in comparison to stress-only conditions [ 50 ]. For example, the number of seeds per plant increased by 22–62% (depending on the genotype examined) when compared to stressed treatment. Furthermore, other parameters interesting for their impact on crop yield were significantly improved, such as pods per plant (by 12–60%) and yield per plant (by 16–67%), when compared to plants subjected to salt stress alone [ 50 ]. Finally, genotypes categorised as susceptible to salt stress presented better responses when also treated with GSH [ 50 ], emphasising the importance of conducting studies of the effects of exogenous metabolite application for each genotype. Such studies will be very important for encouraging the cultivation of salt-susceptible varieties with desirable or unique commercial traits, even in saline soil conditions.

Given the importance of GSH as a precursor for phytochelatin synthesis, its effect on alleviating heavy metal toxicity in crops has been evaluated. Khan et al. reported that Pb toxicity decreased photosynthetic attributes such as photosynthetic rate, stomatal conductance, intercellular CO 2 concentration, transpiration rate, and photosynthetic pigments, and also increased MDA, H 2 O 2 , and Pb levels in upland cotton ( Gossypium hirsutum ) grown in hydroponic conditions [ 51 ]. GSH applied to the nutrient medium improved the aforementioned parameters when compared to Pb-treated plants, reaching in many cases the levels present in control conditions. It also amended Pb-induced damage observed at the ultrastructural level, maintaining the integrity of chloroplasts and other organelles [ 51 ]. Additionally, in a study conducted by Kim et al. [ 52 ], GSH improved seed germination and seedling growth in tobacco ( Nicotiana tabacum ), red pepper and even a model Brassicaceae species ( Arabidopsis thaliana ) under Hg stress. They also demonstrated that GSH presented stronger binding affinity to Hg when compared to other heavy metals such as Cd, Cu, or zinc [ 52 ], indicating that GSH may be better suited to alleviate Hg-induced damage.

GSH application also had positive effects on plants subjected to high temperatures. Mungbean seedlings grown in growth chambers were exposed to 42 °C or normal conditions (25 °C) and pretreated with GSH 24 h before the high temperature treatment. Leaf RWC, chlorophyll, and proline content increased in plants treated with GSH when compared to the plants subjected to high temperature. The stress markers MDA and H 2 O 2 content, as well as superoxide generation rate, were diminished in GSH-treated plants when compared to the stress treatment. Additionally, the ascorbic acid content and GSH/GSSG ratio were increased in GSH-treated plants in comparison to the levels found in heat-stressed plants [ 53 ].

2.4. Citric Acid (CA)

Citric acid (CA), the initial intermediate of the TCA cycle, is synthesised by citrate synthase from the condensation of oxaloacetate and acetyl CoA [ 54 ]. This molecule is a mild antioxidant that can also quelate metals such as Cu, Pb, and aluminium [ 55 ]. Problems induced by salinity can be alleviated by CA application. For instance, the addition of CA to the irrigation solution of tomatoes in calcareous soils (high concentration of CaCO 3 ) improved the uptake and assimilation of Zn, Na, Ca, and N in leaves, and Mn, Na, Mg, and P in fruits [ 56 ]. Likewise, maize ( Zea mays ) plants grown in soil with high salinity and 100–200 ppm CA showed restored height, chlorophyll a and b contents, enhanced growth, and an improvement in yield when compared to salt-treated controls [ 57 ].

Regarding heavy metal stress, exogenous applications of CA to mustard ( Brassica juncea ) leaves reduced the harmful effects of Cd by improving the enzymatic antioxidant response, via increased CAT, POX, and SOD activities. Additionally, the chlorophyll content and stomatal conductance and aperture all rose, leading to a 14% increase in CO 2 availability, improved photosynthetic rate (by 42%) and growth (by 12%) of the Cd+CA plants compared to mustard stressed with Cd [ 58 ].

On other hand, the application of CA can revert the reduction in germination, mineral absorption, hormone homeostasis, and lower growth and yield produced by Pb stress. In the case of castor bean ( Ricinus communis ) grown in soil with 600 mg kg −1 Pb and with applications of 5 mM CA, an improvement was observed in the length of the roots and shoots and the number and area of leaves per plant compared to the plants grown in soil with Pb alone, resulting in phenotypes similar to those of control plants (without application of Pb or CA). The photosynthetic parameters, transpiration rate, water use efficiency, and stomatal conductance were improved, as were chlorophyll a and b and carotenoid levels. The activities of antioxidant enzymes, such as POX, CAT, APX, and SOD, were also enhanced in both roots and leaves of Pb+CA plants [ 59 ].

Another case is the stress inflicted by Cu, a metal cofactor for many enzymes involved in electron transfer and an essential micronutrient. Nevertheless, at higher concentrations, it has a toxic effect on seed germination, photosynthetic activity, and cell division; induces changes in the ionic form of nutrients; and generates oxidative stress. It has been shown that canola ( Brassica napus ) can tolerate soils contaminated with an excess of Cu, but plant growth, shoot and root length, and photosynthetic pigments all suffer decreases, whilst the activity of antioxidant enzymes increases, affecting yield. However, the application of CA can counteract this effect [ 60 ]. Specifically, the application of 2.5 mM CA in soil together with 100 µM Cu recovered growth and increases of 20–31% were observed in shoot and root length and the number and area of leaves when compared with Cu (100 µM) alone. Similarly, the photosynthetic pigment content and the activities of antioxidant enzymes (SOD, CAT, POX) were raised in Cu+CA-treated canola compared to the Cu-treated controls. A similar finding was discovered in pea ( Pisum sativum ), in that the application of 100 µM CA in the Cu-containing germination medium restored biomass production in roots and shoots, reduced cell death, and corrected cellular redox state versus seeds treated with Cu alone [ 61 ]. In white jute ( Corchorus capsularis ), a plant that is used in phytoremediation due to its tolerance to heavy metals, the application of 2 mM CA in the solution media improved parameters like plant growth, biomass, chlorophyll, and carotenoid contents, whilst lowering the activities of SOD and POX [ 62 ].

Cr, another heavy metal, can become toxic to plants in high concentrations. In plants, the stress induced by Cr diminishes seed germination, growth, uptake of mineral nutrients available in the soil, and photosynthesis. Such effects can be reverted by the exogenous application of CA. In rice plants, supplementing the irrigation solution with 100 µM CA restored parameters like root and shoot length and DW. Rice plants also had higher internal Cr concentrations (by 50%), demonstrating the capacity of CA to chelate metals, mirrored by enhanced activities of the detoxification enzymes (CAT, POD, SOD, and GR) and metabolites (GSH and proline), enabling the Cr+CA plants to cope better with scavenging ROS [ 63 ]. Similar findings have also been discovered in Cr+CA-treated spinach ( Spinacia oleracea [ 64 ]).

The multiple effects of adding the aforementioned primary metabolites are summarised in Figure 2 , and the principles of their modes of action also hold true for studies that have evaluated the consequences of applying secondary metabolites to different crop plants in greenhouse and field conditions.

Application of primary and secondary plant metabolites ameliorates the negative effects of abiotic stress. By applying primary metabolites such as proline, tryptophan (TRP), glutathione (GSH), and citric acid (CA), or secondary metabolites like polyols, lipoic acid (LA), ascorbic acid (AA), glycine betaine (GB), α-tocopherol (α-Toc), and melatonin as foliar sprays or in irrigation water, the tolerance of crops is enhanced when faced with environmental challenges.

3. Secondary Metabolites

3.1. polyols.

Polyols or sugar alcohols are organic compounds derived from sugars, in which the carbonyl group (CO) has been reduced to an alcohol (OH). They include linear and cyclic forms, termed alditols and inositols, respectively. Examples of polyols are mannitol (reduced form of mannose), sorbitol (from glucose), and inositol, synthesised from glucose 6-phosphate followed by dephosphorylation [ 65 , 66 , 67 ].

3.1.1. Mannitol

Protective effects on maize with foliar applications of mannitol (15 and 30 mM) have been observed under saline stress (100 mM NaCl). The combined treatment increased total plant DW, RWC, and chlorophyll content ( a and b ), demonstrating that mannitol was mitigating, directly and/or indirectly, the harmful effects of saline stress and enhanced biomass production due to its role in cellular osmotic adjustment [ 68 ]. Such beneficial properties have also been discerned in the field: the reduced productivity seen in saline-stressed cabbage ( Brassica oleracea ) was alleviated by the foliar application of 2–4 g L −1 mannitol [ 69 ].

As mentioned above, Cr stress affects several important parameters of crops. The application of mannitol to pot-grown maize can alleviate these effects. The height, leaf area, root length, number of leaves per plant, and DW of all plant parts were improved by the foliar application of 50 and 100 mg L −1 mannitol to cultivars under Cr stress (5 and 10 mg kg −1 soil) when compared to plants without mannitol, and phenotypes were similar to control plants (without Cr or mannitol). Oxidative stress levels in roots and leaves were also lowered, especially in a more-tolerant cultivar, as well as the activity of antioxidant enzymes (SOD, POD, CAT, and APX) and the content of chlorophylls and carotenoids, suggesting a protective role of mannitol in maize under heavy metal stress [ 70 ]. Even though the application of 100 mM mannitol alone might have negative effects on wheat growth under normal conditions, because of induction of stomatal closure, when this polyol was combined with Cr (0.25 and 0.5 mM), pot-grown plants had enhanced shoot and root DWs, as well as husk and kernel weights, facilitated by increases in antioxidant systems in both leaves and roots [ 71 ].

Boron (B) toxicity is another kind of stress that has been observed mainly in arid and semi-arid environments, such as those found in South Australia, Turkey, California, and Chile. At high concentrations, B causes necrotic lesions in leaf tips and patches on leaves, reducing photosynthesis, growth and yield [ 72 ]. Two wheat cultivars, with different sensitivities to B, were analysed under increasing B concentrations (0, 30, 45, and 60 mg kg −1 ) and mannitol treatments (0, 1, 5, and 10 g kg −1 ) in pots. It was observed that the content of B in leaves was higher in the sensitive cultivar, and that application of mannitol reduced considerably the B content in both cultivars. In this crop, it was determined that 1 g kg −1 mannitol was more effective than the other concentrations in reducing the symptoms of B toxicity [ 73 ].

3.1.2. Sorbitol

The eggplant is a crop classified as moderately sensitive to salinity. To mitigate the damage caused by salt, the effects of foliar applications of sorbitol (5 and 10 mg L −1 ) to plants in greenhouse conditions subjected to different NaCl treatments (1.5, 3, and 6 dS m −1 ) was studied. It was observed that 5 mg L −1 sorbitol was the most efficient, increasing parameters like plant height, the number, weight, and diameter of fruits, as well as chlorophyll a and b and carotenoid levels in all salt treatments, compared to the controls (without sorbitol) [ 74 ]. Studies in rice [ 75 ] and wheat [ 76 ] have uncovered similar effects, although finding the correct concentration is key for success. For example, in rice, 10 mM sorbitol lowered H 2 O 2 and MDA levels in 170 mM NaCl-treated plants, increasing growth and DW [ 75 ], whereas in wheat, either 50 or 100 mM sorbitol had particularly beneficial effects on root and shoot lengths and DW, proline content, and photosynthetic pigment levels [ 76 ].

3.1.3. Inositol

The application of this cyclic polyol has been used to improve abiotic stress tolerance in a few cases. For instance, pre-treating crab apples ( Malus hupehensis ) with 50 µM myo-inositol in the hydroponic media reduced salt stress (200 mM) symptoms, as determined by improvements in plant height and DW, as well as root length, volume and surface area, compared to plants subjected to salt stress, whilst lowering relative electron leakage, H 2 O 2 production, and Na+ accumulation [ 77 ].

In the case of drought stress, exogenous myo-inositol can reduce its harmful effects by protecting the water status of leaves. It was observed that foliar application of 5, 15, and 25 µM myo-inositol to pepper plants under drought stress (7 days without watering) in pots raised the RWC and reduced H 2 O 2 , proline and MDA levels [ 78 ].

3.2. Lipoic Acid (LA)

Lipoic acid (LA, 6,8-thioctic acid or 1,2-dithiolane-3-pentanoic acid) is a powerful sulphur-containing antioxidant, whilst also acting as a cofactor in several multienzyme complexes involved in primary metabolism [ 79 ].

The antioxidant properties of LA have been used to benefit crop production. For example, in canola under salinity stress (<150 mM NaCl), the foliar application of 100 µM LA reduced lipid peroxidation levels, and raised cysteine content and POD and CAT activities, improving overall yield and providing tolerance to salt stress [ 80 ]. Additionally, in pot-grown wheat irrigated with different dilutions of seawater (<14.6 dS m −1 ), the foliar application of 0.1 mM LA buffered the deleterious effects by increasing levels of proline, the RWC, and activities of antioxidant enzymes (such as CAT, SOD, POX, and APX), which benefited agronomic parameters (leaf area, plant height, and grain yield) and improved tolerance to salt stress [ 81 ].

In the case of drought stress, exogenous application of LA also can be beneficial to plants, as shown in hydroponically propagated maize. Supplementation of the nutrient solution with PEG6000 simulates water deficit. However, the addition of 12 µM LA in the growth media can reduce lipid peroxidation and increase RWC, endogenous LA, chlorophyll a and b levels, and the expression of key genes ( rubisco large and small subunits ( LSU and SSU ), whilst also improving stomatal conductance and photosynthetic and transpiration rates compared to plants treated with PEG6000 alone [ 82 ].

Similar effects occur in Pb-treated (1.5 mM) wheat seeds, imbibed with 2 µM LA; these had longer roots and coleoptiles, even though both organs contained more Pb than seeds not treated with LA. The altered ratio of GSH/GSSG demonstrated that the LA-treated plants had a greater capability to withstand the potentially toxic effects of internal Pb [ 83 ].

These examples of the use of LA clearly highlight how the combination of species and abiotic stress influences the dose of the metabolite required to alleviate negative effects (100 µM canola/saline; 12 µM maize/drought; 2 µM wheat/Pb).

3.3. Ascorbic Acid (AA)

Ascorbic acid (AA), or vitamin C, is another secondary metabolite which can be synthesised de novo from several pathways, such as D-glucose, L-galactose, uronic acid, L-gulose, and myo-inositol pathways, or by recycling its oxidised form. It is a cofactor for many enzymes, and can neutralise ROS, repair oxidised organic molecules, and regulate physiological processes (such as cell division, growth, development, and stress tolerance) in plants [ 84 , 85 , 86 ].

The application of this metabolite can improve the tolerance of many species to a variety of abiotic stresses. In the cereal crop, quinoa ( Chenopodium quinoa ), different intensities of drought stress reduce quinoa shoot and root length, DW, levels of chlorophylls a and b , and total carotenoids, whilst raising H 2 O 2 and soluble sugar levels. However, when 150 mg L −1 AA was applied to leaves during the vegetative stage in greenhouse conditions, tolerance to drought stress was dramatically enhanced, as demonstrated by improvements in metabolic, biochemical, morphological and production parameters [ 87 ]. Similarly, for two pot-grown varieties of peach tree ( Prunus persica ), growth, nutrient uptake, yield, and fruit quality were all favoured by spraying leaves with 250 ppm AA subjected to water stress [ 88 ], as a consequence of higher net CO 2 assimilation rate, stomatal conductance, proline levels, and antioxidant enzyme activities. Such positive effects have also been seen in the field: the application of AA to wheat leaves (200 mg L −1 ) over two seasons in an experimental farm increased the relative water and chlorophyll content, with higher antioxidant enzyme activities (CAT and POX), resulting in improvements in the number of grains per spike, the number of spikes, and, consequently, yield [ 89 ].

In wheat under stress by Pb (2 mM), the application of 0.6 mM AA in the watering solution restored parameters such as root and shoot length; fresh weight (FW); the content of N, P, K, Ca, Mg, and cysteine; and total chlorophyll content, allowing the plant to develop with no serious consequences on yield, thus resembling treatment controls (without Pb or AA) and performing better than Pb-treatment alone. The antioxidant effect of AA also protected the chloroplasts from oxidative damage, as well as altering the concentration of plant hormones such as auxin, gibberellins, and abscisic acid [ 90 ].

Heat is another stress that affects the defence system of plants. For example, cotton is cultivated in various climates, but is sensitive to extreme temperatures, although even minor variations in the temperature can reduce the photosynthetic rate and generate ROS. However, the foliar spray application of 70 ppm AA to cotton cv. AA-802 can enhance the activity of SOD and CAT, raise chlorophyll content and antioxidants, and alleviate oxidative stress to such an extent that fibre lengths and, thus, the yields of the plants are affected to a much lesser extent or may even improve compared to the controls [ 91 ]. Such results are similar to those discovered in a previous study [ 92 ] in which the application of different concentrations of AA to cotton plants during the squaring and flowering stages under heat stress enhanced their RWC, total chlorophyll, the activity of antioxidant enzymes (POX, CAT, and SOD), and the yield compared to controls sprayed with water.

At the other extreme, low temperatures (chilling stress) can also affect crops, causing phenotypic changes such as chlorosis, wilting, metabolic changes, and the leakage of cellular solutes. An example of this can be seen in tomato plants stressed by chilling (4 °C), where leaf area, length, and width are reduced [ 93 ]. However, chilled seedlings incubated in AA solution (0.5 mM for 48 h) behaved similarly to the non-chilled controls, showing reduced oxidative damage and increased proline, chlorophyll, mineral nutrition, and expression of molecular chaperones (HSP70, HSP90, and HSP80) and CAT genes [ 93 ]. Likewise, AA application can also aid fruits, even after harvesting. In banana ( Musa spp), chilling affects many phenotypical characteristics important for consumers, such as the colour of fruit peel and pulp, that hinder the sale of the product. Yet a simple procedure of immersing the fruits in a solution of AA at different concentrations (the best was 9 mM) followed by cold storage (27 days at 6 °C) reduced the overall chilling injury index score, reflected in improvements in total chlorophyll, total phenolic and flavonoid content, and the activity of antioxidant enzymes (APX, POD, SOD, and CAT) [ 94 ]. AA applications can even improve extreme chilling (freezing) tolerance, as seen in assays with spinach [ 95 ].

3.4. Glycine Betaine (GB)

GB (N,N′,N′′-trimethylglycine) is an amphoteric quaternary ammonium compatible osmolyte that confers tolerance under environmental stress [ 96 , 97 ]. Its main beneficial effects are through osmotic adjustment and stabilisation of the photosystem II complex, amongst others [ 96 , 98 ]. Not all plants are able to accumulate GB under abiotic stress, although crops and cultivars that produce higher amounts of GB are usually more tolerant to abiotic stress [ 97 ].

Foliar application of GB to safflower ( Carthamus tinctorius ) plants subjected to salinity stress and grown under greenhouse conditions induced higher chlorophyll b and carotenoid levels, as well as a higher Fv/Fm rate. Moreover, a decrease in Na + levels in leaf tissue was observed, indicating that GB application has positive effects in the response of safflower to abiotic stress [ 99 ]. Exogenous application of GB in lettuce ( Lactuca sativa ) grown under salt stress and greenhouse conditions also resulted in higher tolerance to salinity, reflected in increased DW, organic acid, and amino acid levels when compared to control plants [ 100 ].

Application of GB to enhance abiotic stress tolerance on plants grown under field conditions has also been promising. In pea, GB application ameliorated the effects of drought stress by increasing yield and soluble protein concentration. This study evaluated short- and long-term drought stress, at different developmental stages, generating comparable scenarios to those found in field conditions [ 101 ]. In wheat, a field study using 19 genotypes grown under prolonged drought stress showed that foliar applications of this metabolite improved flag leaf net photosynthetic rate and stomatal conductance when compared to stress conditions alone. Although significant differences in chlorophylls and carotenoid accumulation were not observed, increases in AA were detected when compared to plants subjected to drought. However, responses to GB were genotype specific [ 102 ]. However, the effects of GB may be species specific—for example, no improvements were observed in growth or yield when applied to tomatoes [ 103 ], which may also be related to the dose used, the time of application, and the time of tissue collection.

Like the effect of AA on banana shelf quality [ 94 ], studies have shown that GB application also has a positive impact in the post-harvest life of commercial fruits. Immersion of hawthorn berries ( Crataegus monogyna ) in different GB concentrations and stored at 1 °C for 20 days suffered 25% less chilling injury compared to untreated controls. Application also caused significant increases in endogenous GB, AA, and proline levels, and raised activity levels of ROS scavenging enzymes (Razavi et al., 2018). Similar results were obtained in papaya ( Carica papaya ) immersed in GB after harvesting but prior to cold storage (6° for 40 days) [ 104 ].

Thus, GB not only alleviates damage produced by abiotic factors, but also enhances post-harvest life. Progress is being made in additional field studies that are identifying the species and genotypes that respond best to GB.

3.5. Alpha-Tocopherol (α-Toc)

Tocopherols are lipophilic compounds belonging to the vitamin E family. The four isomers α, β, γ, and δ play important roles in plant growth, stress responses, senescence, and signal transduction, among other processes [ 105 ]. Of these compounds, α-tocopherol (α-Toc) is the most abundant and is present in chloroplasts. One of its main functions is to prevent oxidative damage to thylakoid membranes by quenching and scavenging singlet oxygen (one α-Toc quenches approximately 120 singlet oxygen molecules) [ 106 ] and scavenging lipid peroxyl radicals, maintaining photosynthetic membrane integrity.

In recent years, the role of α-Toc in stress tolerance in crops has been examined. Most studies have investigated the beneficial effects of foliar α-Toc application during saline or drought stress. In a field experiment, Semida et al. reported a significant increase in growth parameters such as shoot length, number of leaves, leaf area, shoot DW, and FW in onion (considered a salt-sensitive crop) grown under saline condition [ 107 ] when α-Toc was used. The time of application also influences the effects of α-Toc on plant development. Lalarukh et al. [ 108 ] treated seeds of two sunflower ( Helianthus annuus ) varieties with different α-Toc concentrations and grew them in pots under NaCl treatment. Given that sunflower is moderately tolerant to salt stress, it is a good candidate for growing in saline soils. α-Toc seed priming increased shoot and root FW and shoot and root length, although the precise effect depended on both the cultivar and the metabolite concentration. It also improved yield: the authors reported up to 33 and 16% increases in total achene weight and hundred achene weights, respectively [ 109 ]. Similar results were obtained in wheat and mungbean, both grown under natural field conditions, when this metabolite was applied to plants under a water-stress regime [ 110 , 111 ]. Regarding yield improvement, α-Toc increased the number of seeds, pods, weight of ripened pods, and weight of 100 mungbean seeds [ 111 ]. In wheat, yield per plant increased by 18% when α-Toc was applied under water-stress conditions, mirrored by improvements in nutritional quality due to rises in α-, β-, γ-tocopherols, phenolics, and flavonoids [ 110 ]. Foliar application of this secondary metabolite also raised chlorophyll a and b levels and antioxidant enzyme activities in mungbean, wheat, and onions under saline stress conditions [ 107 , 110 , 111 ].

α-Toc has thus proven to enhance growth parameters and yield in crop species grown under field conditions and drought, indicating a potential use in commercial formulations. However, its beneficial effects in crops under other kinds of abiotic stress have yet to be addressed.

3.6. Melatonin

Melatonin (N-acetyl-5-methoxytryptamine) is a tryptophan derivative that was discovered in plants in 1995 [ 112 , 113 ]. Although its role in physiological processes in mammals has been extensively described [ 114 ], its function and action mechanism in crops is still being elucidated. Melatonin participates in different developmental processes, such as seed germination, growth regulation, fruit ripening, and rhizogenesis, among others [ 115 ]. Because melatonin also presents natural antioxidant capacity and delays leaf senescence, it has been proposed as a potential biostimulant for crops. An excellent review on melatonin and its function in the regulation of the plant antioxidant machinery in stressed conditions was recently published [ 116 ], thus, this section will focus on physiological parameters.

Melatonin treatment of salt-stressed tomato plants in growth chamber conditions improved growth parameters, generated higher chlorophyll a and b accumulation, and increased the activities of carbonic anhydrase and rubisco [ 117 ]. This is consistent with previous reports in other species, where melatonin treatment downregulated the expression of chlorophyllase and pheophorbide a oxygenase, two enzymes involved in chlorophyll degradation [ 118 ], thus improving photosynthetic efficiency of plants under cold stress [ 119 ].

Moreover, melatonin application increased proline levels and the activity of the enzyme required for its biosynthesis, P5CS [ 117 ]. Crosstalk of melatonin with other phytohormones, including auxin, cytokinin, gibberellins, abscisic acid, ethylene, jasmonic acid, and salicylic acid, has been determined [ 120 ]. It is a ROS scavenger and also increases the activities of antioxidant enzymes and metabolite contents [ 119 , 121 , 122 ]. Taking advantage of this crosstalk might optimise its use as a biostimulant for crops cultivated under abiotic stress. Melon seedlings ( Cucumis melo ) subjected to cold stress in growth chamber conditions presented higher chlorophyll a and b contents, net photosynthetic rate, stomatal conductance, and transpiration rate when treated with melatonin, with an optimum dose of 200 µM [ 123 ].

Other benefits attractive to the agronomical industry may be associated with abiotic stress tolerance. For instance, table grape bunches ( Vitis vinifera ) treated with melatonin presented a significantly lower berry abscission rate and a reduced rotten index, as well as more extended post-harvest life [ 124 ].

Whether melatonin should be considered a new phytohormone or a metabolite is currently under discussion [ 115 ]. Nevertheless, field trials evaluating the effects of melatonin on crops subjected to abiotic stress should be carried out in order to assess its potential impact on the yield of other species.

4. Conclusions and Future Prospects

Application of primary and secondary metabolites naturally found in plants has proven to be effective at ameliorating abiotic stress damage in crops. A variety of effects are observed in applying chemically diverse natural compounds. Some effects are common to most crop species studied, whereas others are species and even genotype specific (such as GB application in wheat [ 102 ] and Thin, 2015). Moreover, certain metabolites might perform better at alleviating specific types of stress: GSH seems to induce more tolerance to heavy metal stress, especially Hg [ 52 ]. Some of the differences observed within application of the same metabolite can be attributed to experimental design, the duration of stress, and the stage of plant development at the time of treatment. However, as Paracelsus noted, “the dose makes the poison”, and plant metabolites are not the exception (Paracelsus, “The Third Defense”). Careful consideration must be given to the dosage used, as excess of a certain metabolite might have detrimental effects on plant growth and yield.

An interesting development is the application of combinations of plant metabolites. For example, the use of ascorbic acid (AA) in addition to citric acid (CA) (2:1) had a particularly beneficial effect on stressed plants. In salt-stressed cowpea ( Vigna sinensis ; 75 mM) foliar application of AA + CA increased parameters FW and DW by 120 and 131%, respectively, as well as the number of pods and yield per plant, compared with the control (salt-stress alone). Improvements in photosynthetic pigment levels and the content of nitrogen/phosphorus/potassium were also observed, leading to greater tolerance to salt stress [ 125 ]. A similar effect occurred in apple ( Malus x domestica cv. Red Spur); AA + CA treatment increased total anthocyanin content, the total antioxidant capacity, and the activity of antioxidant enzymes (CAT), and decreased activity of polyphenol oxidase (responsible for flesh oxidation), resulting in improved nutritional quality and fruit colour [ 126 ]. These studies show that the combination of two natural metabolites (in these cases, AA + CA) is beneficial for plant development and enhancing the commercial characteristics of crops.

Although the use of natural primary and secondary metabolites has proven useful to improve abiotic stress tolerance in crops, there is a limitation to their chemical diversity. To further broaden the spectrum of compounds that can be used for this purpose, chemical genomics can be used. As the discovery of new compounds to improve abiotic stress tolerance in crops is needed, this technique has been applied to the challenge of identifying novel molecules that promote plant growth under stress conditions. Chemical genomics allows the screening of thousands of compounds from chemical libraries, based on leaf and root growth parameters in a cost- and time-efficient manner [ 127 ] [ 128 ]. This approach has proven to be effective for evaluating and selecting new compounds that could modulate plant growth under stress conditions in crops [ 127 ], and the further exploration of chemical genomics will no doubt be invaluable for progress in this field.

For several of the metabolites presented, the scalability and cost of application in crops cultivated in the field must still be evaluated. Nevertheless, in general, they are readily available for widespread implementation, and a concentrated formula could be applied in the field with the application equipment that producers already use. Although field experiments are being carried out to test the effectiveness of plant metabolites on yield, there is still the need to evaluate their potential interactions with other chemicals (both natural and artificially added) in irrigation waters. Furthermore, the availability and production costs should be built into the equation to determine their viability as commercial products. Finally, there are salt-susceptible crop varieties that present unique or customer-valued attributes, and for these reasons, they cannot be replaced, or it is difficult to do so. In such cases, the application of different metabolites (alone or in combination with others) will allow its cultivation in saline soil conditions, maintaining its yield.

Acknowledgments

We thank all members of the Centro de Biología Molecular Vegetal for helpful and constructive discussions.

Author Contributions

Conceptualisation, F.G. and M.H.; writing—original draft preparation, F.G. and K.O.-H.; writing—review and editing, F.G., K.O.-H., C.S. and M.H.; funding acquisition, M.H. and C.S. All authors have read and agreed to the published version of the manuscript.

This research was funded by CONICYT PIA ACT192073 (MH, CS) and Fondecyt 1181198 (MH).

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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