Plant Breeding for Biotic Stress Resistance

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  1. Biotic stress - Wikipedia
  2. Translational Genomics in Crop Breeding for Biotic Stress Resistance: An Introduction
  3. Bibliographic Information

In a similar study, the increased susceptibility to a virus after simultaneous application of drought and heat stress was accompanied by down regulation of pathogenesis-related PR genes and R-genes, which were otherwise induced under single viral stress Prasch and Sonnewald, This indicates a direct negative effect of abiotic stress on major defense executors, that adds up to the antagonistic regulation observed in other signaling pathways.

These studies clearly emphasize that even though regulatory pathways overlap between stresses, combinatorial stress needs to be treated and studied as a unique condition. Further functional characterization of individual gene members playing key roles in these pathways is required to extract meaningful conclusions. We will summarize molecular components that according to evidence mentioned above participate in stress crosstalk.

As information under combined stress is limited, and a detailed coverage of all potential interactions is not possible, our intention is to provide leads for future research that will aid to further dissect plant adaptive responses and tolerance under combined abiotic and biotic stress. A scheme for the effects of abiotic and biotic stress at the plant level. A combination of abiotic stress with pathogen infection potentially derails hormone and systemic ROS homeostasis.

Pathogen infection has been shown to impair stomata closure under non-stress conditions, with the dynamics of this interaction under abiotic stress being unknown. Senescence is a common component of both abiotic and biotic stress that can potentially be amplified under combinatorial stress.

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Systemic ROS signals generated after pathogen encounter may alter water relation and salt uptake through their effects in root hydraulic conductance and ion transport. Abiotic stress through ABA signaling negatively affects signals that trigger systemic acquired resistance, enhancing pathogen spread from the initial site of infection. The cuticle and cell wall constitute the first layers of defense against microbial attackers. They not only serve as physical barriers against pathogen penetration, but also as sensitive sensors for the timely activation of the intracellular and systemic defense responses.

Arabidopsis thaliana mutants in long-chain acyl-CoA synthetase 2 LACS2 , a gene that is involved in cuticle biosynthesis, exhibit increased permeability of the cuticular layer which leads to increased resistance to Botrytis cinerea Bessire et al. Interestingly, ABA deficiency causes similar cuticular defects and heightened resistance to B. In the study by Xiao et al. The latter observation points to a positive contribution of a thicker cuticle to resistance against P.

The well-documented increase in cuticular thickness under conditions of water deficiency Kosma et al. The cuticle does appear to be a sensor of the osmotic status and to be essential for the up-regulation of ABA biosynthesis genes under osmotic stress Wang et al. Cell walls similarly appear to be an integrated signaling component for the defense against pathogens.

Changes in pectin properties and composition in the Arabidopsis powdery mildew-resistant pmr mutants pmr5 and pmr6 resulted in a SA, JA, and ET independent increase in resistance to powdery mildew species Vogel et al. Intriguingly, these responses were attenuated when plants were grown under high osmotic pressure which reduced the turgor pressure Hamann et al.

Osmotic stress, which is a common component of many abiotic stresses, may therefore interfere with the ability of plants to sense damage to the cell wall, due to already reduced turgor, resulting in inadequate activation of defense mechanisms. The above-mentioned alterations in plant pathogen interactions in cell wall component biosynthesis mutants may be the consequence of the erroneous activation of integral receptor proteins such as RLKs and RLPs receptor-like kinases and receptor-like proteins, respectively which survey the cell wall integrity and bind to MAMPs and DAMPs microbial- and damage-associated molecular patterns, respectively.

Upon activation these transmembrane proteins e. Changes of cell wall structure and adherence to the plasma membrane upon exposure to abiotic stresses may affect their functional integrity. Down-regulation of NDR1 resulted in alterations in the cell wall-plasma membrane interaction and compromised resistance to virulent P. Abiotic stress may also affect the abundance of cell wall receptors by influencing their transcript levels.

THE1 is a member of the CrRLK1L RLK family that is involved in cell wall damage sensing and subsequent control of the downstream accumulation of ROS, and its expression is down-regulated under abiotic stress but up-regulated after pathogen challenge Lindner et al. Pathogen recognition activates a battery of defense responses that target the apoplastic space. These include local cell wall enforcement, secretion of antifungal compounds at the site of intended penetration and up-regulation of enzymes with fungal cell wall degrading activities Van Loon et al.

These events are characterized and regulated by signature changes in pH, ROS homeostasis, and the redox state. Simultaneous exposure to abiotic stress can potentially impinge on the generation and decoding of these signatures, affecting subsequent responses. For example, apoplastic pH is transiently decreased following fungal infection Felle et al. Moreover the downregulation of cell wall peroxidases under abiotic stress Shaik and Ramakrishna, can potentially dampen the production of ROS signatures that trigger defense responses Daudi et al. Physical barriers enforcement after pathogen encounter through crosslinking of lignin monomers by ROS, which are produced by apoplastic peroxidases, NADPH oxidases and germin-like proteins, prevent pathogen penetration.

Lignin content was found to be reduced under mild drought conditions to facilitate the maintenance of growth under conditions of decreased turgor pressure Vincent et al. These findings may provide insight on the mechanisms leading to differential responses under combined stress across different abiotic stress intensities. Another form of inducible defense response at the site of penetration is the formation of papillae that contain callose, antimicrobial secondary metabolites such as phenolic compounds, and ROS.

Antimicrobial compounds are accumulating through vesicles originating from cellular compartments, such as the Golgi apparatus, which become polarized toward the site of infection Underwood and Somerville, The significance of vesicle-mediated secretion in plant immunity has been demonstrated by the discovery of mutants defective in exocytosis of vesicles with mutations in SNARE complex proteins Hv ROR2 and At PEN1 , which display diminished penetration resistance to powdery mildew pathogens Collins et al.

In accordance with these observations the callose-mediated increased resistance of the ocp3 Arabidopsis mutant to necrotrophic pathogens requires ABA Garcia-Andrade et al. Therefore ocp3, a homeodomain TF, appears to be a convergence point for ABA and callose regulation that can be manipulated to enhance resistance under combinatorial stress. Callose accumulation appears to be a point of convergence of abiotic and biotic signaling as variability in environmental conditions, which affect the redox state of the plant, such as light intensity, have a significant impact on the magnitude of callose deposition after pathogen elicitation Luna et al.

As callose deposition is a major component of the pre-invasion defense of plants Ellinger et al. Changes in calcium fluxes and production of ROS are among the earliest plant responses to abiotic stress and pathogen challenge. It is plausible that there are either unique signatures for combinations of stresses, or that there is interference between the abovementioned signals that potentially dampens or strengthens the downstream responses.

The investigation of mutants defective in the induction of a hypersensitive response after pathogen infection has led to the identification of genes encoding for cyclic nucleotide gated channels CNGCs which are non-selective cation transporters Clough et al. CDPKs have a unique feature to both bind calcium and functionally decode the message by target protein phosphorylation.

They appear to represent a central node in the regulation of abiotic and biotic stress responses Schulz et al. These MAPKs appear to have an overlapping function in signal transduction upon abiotic stress and pathogen challenge. In rice, OsMAPK5 appears to be a convergence point of abiotic and biotic stress responses, as its silencing results in sensitized defense responses and resistance to fungal and bacterial pathogens at the expense of salt and drought tolerance Xiong and Yang, These examples emphasize the complexity of MAPK-mediated defense signaling with diverse and sometimes overlapping functions of different members of the signaling pathway.

Probably, the one-dimensional overlap can be resolved by multidimensional regulation, such as different spatiotemporal transcription and protein subcellular localization, activation thresholds, feedback loops with phosphatases and scaffolding Tena et al. Many of the above-mentioned components appear to be an integral part of broad stress tolerance priming by exogenous application of chemicals Beckers et al. Plant hormones are central to the integration of environmental stimuli in the coordination of growth under optimal and stress conditions, including the regulation of defense responses after pathogen attack.

Plant hormones do not act independently, and extensive synergistic or antagonistic interaction between hormonal pathways is observed in development and stress responses after exogenous application, or through mutant analysis Wolters and Jurgens, Transcriptomic studies have aided in unveiling these interactions Nemhauser et al. Abscisic acid is the major hormone that positively contributes to adaptation to osmotic stress, a major component of several abiotic stresses.

Its involvement in the regulation of defense responses has been a topic of recent comprehensive reviews Asselbergh et al. Comprehensive analyses of ABA-deficient mutants revealed further pleiotropic alterations that may be part of ABA-defense crosstalk such as reduced cuticle thickness and sensitized H 2 O 2 production in response to B. Nevertheless, ABA signaling can positively contribute to pre-invasive defense responses and to early defense signaling against certain necrotrophic pathogens Adie et al.

ABA positively contributes to resistance against pathogens that infect through stomata, such as P. Identification of downstream regulatory nodes that channel interactions between hormonal pathways is of great importance in fine-tuning resistance to both abiotic and biotic stress. Besides TFs, which will be discussed in a following section, other regulators of the transcriptional machinery have been uncovered to function in stress crosstalk.

MED25, a subunit of the mediator complex which is a component of the transcriptional machinery, is involved in the antagonistic crosstalk between ABA and JA Chen et al. Transcriptome analysis of the ahg mutant revealed complex interactions between ABA and SA signaling involving altered mitochondrial and RNA metabolism Nishimura et al.

Recent research has highlighted the direct involvement of the growth hormones gibberellin, cytokinin, auxin, and brassinosteroid in responses to adverse growth conditions and pathogen attack Robert-Seilaniantz et al. DELLA proteins appear to be central nodes in abiotic and biotic stress cross-talk. This may provide an explanation for the often-observed positive correlation between resistance to abiotic stress and resistance to necrotrophs Navarro et al.

Cytokinins were shown to positively regulate defense responses to biotrophic pathogens Argueso et al. This suggests that the increased cytokinin catabolism observed under abiotic stress-induced senescence may potentially contribute to further down-regulation of SA responses and increased susceptibility to biotrophic pathogens.

The roles of auxin and brassinosteroids in stress responses and their potential participation in stress crosstalk remains elusive. Auxin signaling shows antagonistic crosstalk with SA Wang et al. Brassinosteroid BR signaling positively affects abiotic stress tolerance, as is evident by both BR exogenous application Divi et al. In tobacco and rice exogenous application of BRs appeared to clearly enhance resistance to a wide range of pathogens Nakashita et al.

Similar results were obtained in cucumber, which showed heightened resistance to Fusarium oxysporum as a result of activated production of H 2 O 2 by NADPH oxidase and expression of defense related genes Li et al. On the contrary BRs appear to be negatively regulating resistance to the root-infecting oomycete Pythium graminicola by antagonizing SA and GA related defense responses De Vleesschauwer et al. Contradictory effects of BR signaling on immune responses have been recently reported in Arabidopsis Albrecht et al. It is clear that hormonal crosstalk is extensive and occurs in multiple combinations.

Further understanding of plant responses under combined stress exposure is required to dissect the multilevel responses under these conditions. As an example of the underlying complexity, both drought stress and exogenous ABA application result in an increased endogenous ABA content in tomato, but they differentially affect resistance to powdery mildew and Botrytis , with drought enhancing and ABA application compromising resistance Achuo et al.

Notably the ABA-deficient tomato mutant sitiens exhibited increased resistance similar to the effect of drought Achuo et al. Besides the effects of direct hormonal interactions on abiotic and biotic stress tolerance mechanisms additional indirect interactions should be considered, such as the alteration of developmental programs and the regulation of senescence which may be critical for evolutionary species fitness and yield performance in crop plants Wu et al.

The cellular redox state is the sum of reducing and oxidizing redox-active molecules Potters et al. It acts as a central integrator of ROS, energy and metabolic regulation under stress as well as optimal conditions. Its major constituents are ascorbate, glutathione GSH , NADP H , small proteins acting as antioxidants like thioredoxin and glutaredoxins as well as many diverse metabolites such phenolics, amino acids, carotenoids, and tocopherols. The cellular redox state is dependent on both their accumulation and their reduction-oxidation state Potters et al. Genetic manipulation of redox homeostasis results in altered hormone homeostasis and responses to pathogens and abiotic stresses Mhamdi et al.

As abiotic and biotic stress commonly impinge on the redox status albeit not in a similar manner; Foyer and Noctor, , redox homeostasis is potentially a central orchestrator of the phenotypic response to stress combinations.

Biotic stress - Wikipedia

Redox perturbations after imposition of a stress factor may affect responses to subsequent challenges by additional stressors, thereby shaping the response to combined stresses. Plant hormone signaling can directly perturb the redox status by modifying the expression and activities of antioxidant enzymes. SA inhibits the function of catalase and cytosolic ascorbate peroxidase Corina Vlot et al. Programed cell death PCD is a plant response to developmental and environmental stimuli e.

APX isoforms are also commonly up-regulated under abiotic stress Miller et al. Considering the important role of APX in the drought—heat stress interaction Koussevitzky et al. Redox status changes can directly impact protein function through post-translational modifications. One pronounced example of post-translational modifications controlling protein activity and localization is the interplay of S -nitrosylation and thioredoxin-mediated reduction in the control of the oligomeric and monomeric state of NPR1 Tada et al.

Identification of the dynamics of post-translational modifications on these and newly identified proteins under various stress combinations will shed light on their significance for plant adaptation responses to these conditions. NO was recently found to exhibit biphasic control over cell death triggered by pathogens and pro-oxidants in Arabidopsis. In initial stages S -nitrosothiol SNO accumulation results in enhanced and accelerated cell death Yun et al. This differential regulation might have implications in conditions of combined abiotic and biotic stress as both result in increased NO levels.

At a certain plateau concentration of NO, signaling components may be desensitized or inversely regulated, as exemplified by AtRBOHD, with detrimental effects on stress acclimation. Redox changes and post-translational modification appear to be integral in priming for stress tolerance after exogenous application of chemicals Tanou et al. This provides a potential explanation of the mechanism of action of diverse chemicals in plant defense sensitization. H 2 O 2 and NO priming for salt tolerance in citrus moderately increased the abundance of oxidized and S -nitrosylated proteins, which then remained relatively similar after the application of stress.

Non-treated plants were more stress sensitive and exhibited increased protein carbonylation and oxidation Tanou et al. As both compounds provide increased tolerance to both abiotic and biotic stress, further characterization including the timing and magnitude of these post-translational modifications under different stress treatments and under stress combination may help to better understand the redox changes leading to stress cross-tolerance. Metabolites are the end products of gene expression and protein activities and therefore are the penultimate regulatory component for the phenotypic expression under stress conditions.

As metabolites can have multiple functions such as being energy carriers, structural molecules and redox regulators or exerting direct antimicrobial activity against pathogens, uncovering their regulation and homeostasis under combined stress is of great significance. Adaptation to both abiotic and biotic stress impinges significantly on primary metabolism homeostasis. Synthesis of antimicrobial metabolites and defense proteins is energy demanding Bolton, , while abiotic stress potentially leads to energy deprivation as photosynthesis is reduced under abiotic stress De Block et al.

As a result, it is fair to assume that under stress combinations these strong antagonistic effects will result in disturbed energy balance. However, recent results challenge the carbohydrate deprivation notion under mild dehydration stress Hummel et al. More evidence that sugar homeostasis and signaling drives defense responses are demonstrated by the down regulation of cell wall invertases.

This results in dampening of defense responses and increased susceptibility to pathogens as a result of decreased availability of carbohydrates to fuel the defense responses at the site of infection Essmann et al. Cell wall invertases appear to be down regulated under abiotic stress Wingler and Roitsch, and as the regulation of their activity is a convergence point of hormonal and sugar signals for stress tolerance and senescence progression Wingler and Roitsch, , fine tuning of their expression might be a focal point in enhancing combined stress tolerance.

The metabolic status of the host is also crucial for pathogen growth as it appears that pathogens manipulate different aspects of plant metabolism to achieve optimal conditions for their growth Chen et al. The significance of amino acid homeostasis for the induction and regulation of defense responses was recently highlighted Zeier, Amino acids may function as precursors in hormone biosynthesis and affect the redox state through their chemical properties or as precursors of redox regulators such as GSH. Amino acid abundance can impact hormone signaling through conjugation-mediated regulation of hormone activity Woldemariam et al.

Amino acid concentration appears to be significantly perturbed by abiotic stress as is revealed by metabolomics studies Obata and Fernie, On the other hand a direct link between amino acid abundance and activation of SA-induced defense responses was recently demonstrated with heat-shock factor HsfB1, the translation of which is initiated under conditions of phenylalanine starvation Pajerowska-Mukhtar et al. Phenylalanine appears to be accumulated under abiotic stress conditions Urano et al. Metabolic alterations under abiotic stress include the accumulation of compounds such as the raffinose family oligosaccharides raffinose and galactinol and the amino acid proline.

These exhibit osmoprotective and antioxidant functions and have been positively correlated with abiotic stress tolerance Korn et al.

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Galactinol overproduction was recently associated with increased resistance to necrotrophic pathogens Mi et al. Moreover, proline metabolic regulation at the site of pathogen infection is important for both HR deployment and containment, probably through modulation of ROS levels as shown by expression and functional studies of proline dehydrogenase Senthil-Kumar and Mysore, Myo-inositol metabolic regulation appears to be a convergence point for abiotic and biotic stress responses.

Myo-inositol is accumulating under most abiotic stress conditions and is positively contributing to tolerance as a compatible solute Tan et al. A negative relationship between myo-inositol accumulation and pathogen resistance and PCD initiation was found in Arabidopsis , with a positive correlation between myo-inositol depletion and increased SA production and cell death Chaouch and Noctor, Analysis of mutants that exhibit qualitative and quantitative alterations in the accumulation of fatty acid metabolites demonstrated that fatty acids are not only structural components of the cellular membranes, but they also exert a multitude of signaling functions.

Fatty acid release from the membranes after pathogen encounter triggers the defense response Savchenko et al. Linolenic acid is a precursor for the production of the major cellular signaling components JA and oxylipins Reinbothe et al. A reduction of the levels of oleic acid triggers constitutive defense responses that are independent of SA signaling Kachroo et al. Fatty acid homeostasis is disturbed under abiotic stress, as membrane composition changes are vital for the maintenance of membrane rigidity and functionality. Dehydration stress is shown to result in a reduction in and increase in lipid levels Upchurch, , and increased levels by FAD3 or FAD8 overexpression enhanced drought tolerance in tobacco Zhang et al.

Manipulation of fatty acid composition can provide further insight into their function under stress combination. Regulatory modules like MAPKs-based pathways and core hormone signaling modules control the expression of a vast number of genes and therefore their manipulation in most cases have severe pleiotropic effects. Identification of downstream regulators involved in abiotic and biotic stress crosstalk such as TFs is important for more targeted manipulation and adaptation of plants to multiple stresses.

The appropriate fine-tuning of their expression is an important aspect toward translation of scientific knowledge in crop plant improvement Kasuga et al. Many members of these families are involved in regulation of leaf senescence, an integral component of both abiotic and biotic stress Breeze et al. Moreover, in most cases the TFs identified are stress hormone-regulated, and therefore potentially act as molecular switches for the fine-tuning of hormonal responses. Characterization of the mechanism of action of the candidate TFs involved in stress crosstalk is of great importance.

For example, a TF with positive contribution to both abiotic and biotic stress tolerance can be directly useful for breeding combined stress tolerance. Functional characterization of several TFs has revealed various members that confer both abiotic and biotic stress tolerance. Overexpression of the rice OsNAC6 conferred tolerance to salt and dehydration stress as well as resistance to blast disease Nakashima et al.

Overexpression of AtHSFA1b provided stress hormone independent, but H 2 O 2 signaling dependent increased tolerance to drought and resistance to bacterial and oomycete pathogens Bechtold et al. Whole genome expression meta analyses can provide evidence of potential antagonistic regulation in different stress responses for a given TF, by analyzing expression patterns under different stress conditions Shaik and Ramakrishna, Detailed characterization of spatiotemporal expression and cis -element binding patterns is, however, required for the understanding of the underlying mode of regulation.

This was recently elegantly demonstrated in the characterization of OsWRKY13 which exhibits tissue specific expression and condition specific binding to cis -elements of downstream genes and thereby inversely regulated resistance to drought and bacterial infection of rice Xiao et al. Functional conservation of TF functions across species can be exploited to take advantage of the wealth of experimental data generated in the model plant Arabidopsis thaliana. Further similar efforts should be undertaken to accelerate the translation of experimental observations obtained in model plants species to crops.

The results obtained by the functional characterization of TFs are encouraging as many of them appear to regulate cross-resistance in a unidirectional manner, in contrast to the observations at the level of hormonal regulation that point to antagonistic relationships. Therefore, their manipulation offers many opportunities to bypass the antagonistic effects on abiotic and biotic stress tolerance observed in the more upstream regulatory nodes.

Epigenetic modifications such as DNA cytosine methylation and histone residues methylation and acetylation contribute to the transcriptional control of amongst others adaptive responses to environmental stimuli Mirouze and Paszkowski, A significant portion of these modifications appears to be persistent across generations and significantly contributes to phenotypic variation Johannes et al.

While cytosine methylation generally has repressive effects on gene transcription, leading to gene silencing, histone modifications can lead to transcriptional activation through local chromatin de-condensation which facilitates the accessibility of TFs Liu et al. Recently, epigenetic modifications and specifically chromatin-regulated gene activation have been proposed to govern priming responses Conrath, Genome wide approaches studying DNA methylation under abiotic and biotic stress have demonstrated widespread methylation alterations Bilichak et al.

It would be of particular interest to further examine the occurrence of differential alterations and their impact under combinatorial stress. Functional studies of chromatin remodeling enzymes have revealed a functional involvement of these enzymes in the regulation of both abiotic and biotic stress responses. The histone lysine methyltransferase ATX1 is likely to be involved in dehydration stress signaling, as atx1 mutants were sensitive to drought and ATX1 methyltransferase activity positively regulated the expression of the ABA biosynthesis enzyme NCED3 Ding et al.

Chromatin structure can also be altered by the active deposition of variants of the canonical histones.

Translational Genomics in Crop Breeding for Biotic Stress Resistance: An Introduction

Deposition of one of the these variants, H2A. Z, is linked to transcriptional activation in response to environmental stimuli Coleman-Derr and Zilberman, , and disruption of this mechanism leads to misregulated responses to both pathogens and elevated temperature March-Diaz et al. It would be highly interesting to investigate how a previously imposed stress predisposes plants at the methylation and chromatin level for the encounter of a subsequent stress, de sensitizing subsequent responses. The plant immune system consists of successive layers counteracting suppression of defense responses by pathogens through secretion of effector proteins Hemetsberger et al.

Recognition of the effectors by corresponding R-genes belonging to NB-LRR protein family or the effect of effectors on intracellular host proteins guarded proteins results in effector-triggered immunity ETI. This is usually but not always manifested by localized cell death, termed the hypersensitivity response Coll et al.

The complexity in the regulation of ETI is outlined by network analyses of individual and combined hormone mutants, which revealed compensatory interactions in contrast to synergistic interaction observed in PTI PAMP-triggered immunity; Tsuda et al.

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  • This robustness may be ideal in building tolerance to combinatorial stress through pyramiding R-genes with genes conferring abiotic stress tolerance. However, it is becoming clear that there are multiple aspects of regulation at the NB-LRR protein level that are indispensable for the deployment of R-gene resistance Heidrich et al. Interestingly, mutants with reduced sensitivity to heat-induced defense inhibition were found to be based on changes in among others ABA biosynthesis enzymes, indicating that abiotic stress factors may affect R-gene compartmentation through ABA biosynthesis and signaling, although no further evidence is available.

    The heat shock protein HSP90 is a component of this chaperone machinery. HSP90 is also required for the maintenance of folding of other proteins under stress conditions Wang et al. Initial pathogen perception and interception through PTI or ETI triggers systemic signals that prime plant defense responses to effectively counter subsequent infection attempts and limit spreading of the disease.

    This is referred to as SAR. Many compounds and genes have been identified that function in mobile signal generation and transport. Additional metabolites such as pipecolic acid, dehydroabietinal, azelaic acid, and glyceraldehyde 3-phosphate probably function in the amplification of the signal, with no clear conclusions yet on their precise placement in the SAR circuit pathway Dempsey and Klessig, SAR has been shown to be affected by environmental conditions such as exposure to light Griebel and Zeier, and abiotic stresses such as salinity, through ABA suppression of SA biosynthesis Yasuda et al.

    The further investigation of the patterns of accumulation and transport of these metabolites under conditions of combined abiotic and biotic stress may reveal potential connections between their regulation and plant phenotypic responses to combined stress. As a result improving crops to these complex stress conditions first requires an extensive phenotypic characterization at different levels of cellular regulation, i. As evidence from research on individual abiotic and biotic stress responses points to a strong dependency on developmental Skirycz et al.

    Breeding for resistance to combinatorial stress is challenging. However, various novel approaches can aid in dissecting interactions between various types of stressors and identifying genetic components that can be breeding targets. They provide information about the biological function of the whole gene set of an organism, and overlapping expression patterns might imply participation in common pathways Quackenbush, , enabling more efficient reverse genetic approaches. Manipulations that induce resistance to abiotic and biotic stress such as application of priming chemicals, followed by comprehensive phenotypic characterization can be used for candidate gene identification and molecular processes underlying stress cross-tolerance.

    Moreover as the effects of chemical priming are shown to, in part, be exerted through induction of phosphorylation and other post-translational modifications Beckers et al. Breeding for resistance to exposure to combined abiotic and biotic stress by incorporation of genetic components regulating the response to both stresses faces various challenges. For example, TFs can have thousands of binding sites across the genome Lu et al. Both expression regulation and binding specificity can be altered through promoter and binding domain engineering Desai et al.

    As selective and stimulus specific TF binding drives stress responses regulation Xiao et al. A potential drawback of TF utilization is that resistance typically achieved by this approach is partial, and potentially prone to numerous antagonistic effects between stresses that cannot be predicted and can hinder efficient deployment for crop improvement to combined stresses. Pyramiding genes that provide increased tolerance to either stress and do not negatively interact with each other offers an alternative route. Strong resistance mediated by R-genes, that appear to be robust to perturbations, can be pyramided with well-characterized genes conferring abiotic stress tolerance Hu and Xiong, ; Kissoudis et al.

    R-gene robustness can be assessed by testing resistance responses under different abiotic stressors prior to pyramiding. The drawback of this approach is the quick breakdown of resistance due to evolving pathogens, and the fact that necrotrophic fungi resistance cannot be acquired with these genes. R-gene stacking aided by novel biotechnological approaches can reduce the risk of breakdown of R-gene-mediated resistance.

    Pre-invasion defense mechanisms can be exploited, especially the one that is conferred by preformed or inducible physical barriers such as callose and antimicrobial compound deposition at the site of attempted penetration. As discussed earlier, callose deposition appears to be positively regulated by ABA signaling, therefore positive or no interaction should be expected under abiotic stress. Genes such as the OCP3 TF can be utilized, and for instance pyramiding abiotic stress tolerance with resistance conferred by mlo loss of function which sensitizes callose deposition at the site of infection for resistance against powdery mildew Buschges et al.

    However, pleiotropic effects reported in mlo mutants such as compromised resistance against necrotrophic pathogens Kumar et al. The mechanisms through which abiotic stress tolerance is conferred can have a differential effect on disease resistance. As mentioned earlier, drought tolerance through ABA upregulation at the whole-plant level is expected to have antagonistic effects with SA signaling and therefore compromises resistance to biotrophs. Localized ABA sensitization in stomata Bauer et al. Manipulation of developmental traits such as root system architecture can be beneficial for drought tolerance Uga et al.

    Deployment of genes that have a protective function on proteins and cellular components under abiotic stress, such as dehydrins, LEA proteins or RNA chaperones Kang et al. Approaches that result in greater antioxidant capacity such as the accumulation of flavonoids appear to confer resistance to abiotic and oxidative stress Nakabayashi et al. Therefore engineering for increased flavonoid accumulation can be promising in conferring resistance to multiple stressors, however, it is unknown how it can affect the deployment of hypersensitivity response due to disturbed ROS homeostasis and thus resistance against biotrophic pathogens.

    Approaches for building combined abiotic and biotic stress tolerance in plants. Two strategies are proposed through either the manipulation of genetic components which potentially regulate resistance to both stresses in a preferentially unidirectional manner, or the pyramiding of genes that independently confer abiotic or biotic stress resistance and do not negatively interact. The selection of individual components might differ depending on the pathogen and the abiotic stress scenario. 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.

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    Bibliographic Information

    Journal List Front Plant Sci v. Front Plant Sci. Published online May Author information Article notes Copyright and License information Disclaimer. Received Mar 18; Accepted Apr The use, distribution or reproduction in other forums is permitted, provided the original author s or licensor 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. This article has been cited by other articles in PMC.

    Abstract Plants growing in their natural habitats are often challenged simultaneously by multiple stress factors, both abiotic and biotic. Keywords: salinity, drought, disease resistance, R-genes, crosstalk, hormones, transcription factors, post-translational modifications. Open in a separate window. Cell wall-apoplastic space Cell walls similarly appear to be an integrated signaling component for the defense against pathogens. Vesicular trafficking and callose deposition Another form of inducible defense response at the site of penetration is the formation of papillae that contain callose, antimicrobial secondary metabolites such as phenolic compounds, and ROS.

    Hormone signaling Plant hormones are central to the integration of environmental stimuli in the coordination of growth under optimal and stress conditions, including the regulation of defense responses after pathogen attack. Cellular redox state The cellular redox state is the sum of reducing and oxidizing redox-active molecules Potters et al. Metabolite homeostasis and signaling Metabolites are the end products of gene expression and protein activities and therefore are the penultimate regulatory component for the phenotypic expression under stress conditions.

    Transcription factors Regulatory modules like MAPKs-based pathways and core hormone signaling modules control the expression of a vast number of genes and therefore their manipulation in most cases have severe pleiotropic effects. Epigenetic modifications Epigenetic modifications such as DNA cytosine methylation and histone residues methylation and acetylation contribute to the transcriptional control of amongst others adaptive responses to environmental stimuli Mirouze and Paszkowski, R-gene resistance and systemic acquired resistance The plant immune system consists of successive layers counteracting suppression of defense responses by pathogens through secretion of effector proteins Hemetsberger et al.

    Conflict of Interest Statement 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. Crosstalk between biotic and abiotic stress responses in tomato is mediated by the AIM1 transcription factor.

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