Identification of Genes Involved in the Response of Arabidopsis to Simultaneous Biotic and Abiotic Stresses
TL;DR: The transcriptome response of Arabidopsis to concurrent water deficit and infection with the plant-parasitic nematode Heterodera schachtii and candidate genes with potential roles in controlling the response to multiple stresses were selected and functionally characterized.
Abstract: In field conditions, plants may experience numerous environmental stresses at any one time. Research suggests that the plant response to multiple stresses is different from that for individual stresses, producing nonadditive effects. In particular, the molecular signaling pathways controlling biotic and abiotic stress responses may interact and antagonize one another. The transcriptome response of Arabidopsis (Arabidopsis thaliana) to concurrent water deficit (abiotic stress) and infection with the plant-parasitic nematode Heterodera schachtii (biotic stress) was analyzed by microarray. A unique program of gene expression was activated in response to a combination of water deficit and nematode stress, with 50 specifically multiple-stress-regulated genes. Candidate genes with potential roles in controlling the response to multiple stresses were selected and functionally characterized. RAPID ALKALINIZATION FACTOR-LIKE8 (AtRALFL8) was induced in roots by joint stresses but conferred susceptibility to drought stress and nematode infection when overexpressed. Constitutively expressing plants had stunted root systems and extended root hairs. Plants may produce signal peptides such as AtRALFL8 to induce cell wall remodeling in response to multiple stresses. The methionine homeostasis gene METHIONINE GAMMA LYASE (AtMGL) was up-regulated by dual stress in leaves, conferring resistance to nematodes when overexpressed. It may regulate methionine metabolism under conditions of multiple stresses. AZELAIC ACID INDUCED1 (AZI1), involved in defense priming in systemic plant immunity, was down-regulated in leaves by joint stress and conferred drought susceptibility when overexpressed, potentially as part of abscisic acid-induced repression of pathogen response genes. The results highlight the complex nature of multiple stress responses and confirm the importance of studying plant stress factors in combination.
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TL;DR: This review will provide an update on recent studies focusing on the response of plants to a combination of different stresses, and address how different stress responses are integrated and how they impact plant growth and physiological traits.
Abstract: Contents
'Summary' 32
I. 'Introduction' 32
II. 'Effects of stress combination on growth, yield and physiological traits in plants and crops' 34
III. 'The complexity of stress response signaling during stress combination' 38
IV. 'Conclusions' 39
'Acknowledgements' 41
References 41
Summary
Environmental stress conditions such as drought, heat, salinity, cold, or pathogen infection can have a devastating impact on plant growth and yield under field conditions. Nevertheless, the effects of these stresses on plants are typically being studied under controlled growth conditions in the laboratory. The field environment is very different from the controlled conditions used in laboratory studies, and often involves the simultaneous exposure of plants to more than one abiotic and/or biotic stress condition, such as a combination of drought and heat, drought and cold, salinity and heat, or any of the major abiotic stresses combined with pathogen infection. Recent studies have revealed that the response of plants to combinations of two or more stress conditions is unique and cannot be directly extrapolated from the response of plants to each of the different stresses applied individually. Moreover, the simultaneous occurrence of different stresses results in a high degree of complexity in plant responses, as the responses to the combined stresses are largely controlled by different, and sometimes opposing, signaling pathways that may interact and inhibit each other. In this review, we will provide an update on recent studies focusing on the response of plants to a combination of different stresses. In particular, we will address how different stress responses are integrated and how they impact plant growth and physiological traits.
1,282 citations
TL;DR: The need for developing crops with enhanced tolerance to drought and heat stress combination in order to mitigate the negative impacts of predicted global climatic changes on agricultural production worldwide is emphasized.
Abstract: Under field conditions crops are routinely subjected to a number of different abiotic stress factors simultaneously. Recent studies revealed that the response of plants to a combination of different abiotic stresses is unique and cannot be directly extrapolated from simply studying each of the different stresses applied individually. These studies have also identified specific regulatory transcripts, combinations of metabolites and proteins, and physiological responses that are unique to specific stress combinations, highlighting the importance of studying abiotic stress combination in plants. Here we describe the interactions between drought and other abiotic stresses with emphasis on drought and heat stress. We compile new data about the different molecular, physiological and metabolic adaptations of different plants and crops to this stress combination and we highlight the importance of reactive oxygen species (ROS) metabolism and stomatal responses for plant acclimation to drought and heat stress combination. We further emphasize the need for developing crops with enhanced tolerance to drought and heat stress combination in order to mitigate the negative impacts of predicted global climatic changes on agricultural production worldwide.
641 citations
TL;DR: This review attempts to assemble published information on the impact of combined drought and pathogen stresses on crop productivity, and highlights some agriculturally important morpho-physiological traits that can be utilized to identify genotypes with combined stress tolerance.
Abstract: Global warming leads to the concurrence of a number of abiotic and biotic stresses, thus affecting agricultural productivity. Occurrence of abiotic stresses can alter plant-pest interactions by enhancing host plant susceptibility to pathogenic organisms, insects, and by reducing competitive ability with weeds. On the contrary, some pests may alter plant response to abiotic stress factors. Therefore, systematic studies are pivotal to understand the effect of concurrent abiotic and biotic stress conditions on crop productivity. However, to date, a collective database on the occurrence of various stress combinations in agriculturally-prominent areas is not available. This review attempts to assemble published information on this topic, with a particular focus on the impact of combined drought and pathogen stresses on crop productivity. In doing so, this review highlights some agriculturally important morpho-physiological traits that can be utilized to identify genotypes with combined stress tolerance. In addition, this review outlines potential role of recent genomic tools in deciphering combined stress tolerance in plants. This review will, therefore, be helpful for agronomists and field pathologists in assessing the impact of the interactions between drought and plant-pathogens on crop performance. Further, the review will be helpful for physiologists and molecular biologists to design agronomically relevant strategies for the development of broad spectrum stress tolerant crops.
575 citations
Cites background from "Identification of Genes Involved in..."
...Some of the important candidate genes identified so far are methionine homeostasis gene; methionine gamma lyase (AtMGL), rapid alkalinization factor-like 8 (AtRALFL8) involved in cell wall remodeling and azelaic acid induced 1 (AZI1) functioning in systemic plant immunity (Atkinson et al., 2013)....
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...The effect of combined stress factors on crops is not always additive, because the outcome is typically dictated by the nature of interactions between the stress factors (Atkinson et al., 2013; Prasch and Sonnewald, 2013; Pandey et al., 2015a,b; Choudhary et al., 2016; Ramu et al., 2016)....
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...…an increased number of abiotic and biotic stress combinations, which severely affect their growth and yield (Mittler, 2006; Prasad et al., 2011; Atkinson et al., 2013; Narsai et al., 2013; Prasch and Sonnewald, 2013; Suzuki et al., 2014; Mahalingam, 2015; Pandey et al., 2015a; Ramegowda and…...
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15 Oct 2014
TL;DR: An insight is given into cross-tolerance between abiotic and biotic stress, focusing on the molecular level and regulatory pathways, which can lead to a cross-Tolerance and enhancement of a plant’s resistance against pathogens.
Abstract: Plants are constantly confronted to both abiotic and biotic stresses that seriously reduce their productivity. Plant responses to these stresses are complex and involve numerous physiological, molecular, and cellular adaptations. Recent evidence shows that a combination of abiotic and biotic stress can have a positive effect on plant performance by reducing the susceptibility to biotic stress. Such an interaction between both types of stress points to a crosstalk between their respective signaling pathways. This crosstalk may be synergistic and/or antagonistic and include among others the involvement of phytohormones, transcription factors, kinase cascades, and reactive oxygen species (ROS). In certain cases, such crosstalk can lead to a cross-tolerance and enhancement of a plant's resistance against pathogens. This review aims at giving an insight into cross-tolerance between abiotic and biotic stress, focusing on the molecular level and regulatory pathways.
526 citations
Cites background from "Identification of Genes Involved in..."
...Little is known about the “Omics” characterization of abiotic and biotic stress combinations, but recently, several reports have addressed this question [16,51,70,128,129]....
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TL;DR: The role of multi-omics approaches in generating multi-pronged information to provide a better understanding of plant–microbe interactions that modulate cellular mechanisms in plants under extreme external conditions and help to optimize abiotic stresses is described.
Abstract: Abiotic stresses are the foremost limiting factors for agricultural productivity. Crop plants need to cope up adverse external pressure created by environmental and edaphic conditions with their intrinsic biological mechanisms, failing which their growth, development, and productivity suffer. Microorganisms, the most natural inhabitants of diverse environments exhibit enormous metabolic capabilities to mitigate abiotic stresses. Since microbial interactions with plants are an integral part of the living ecosystem, they are believed to be the natural partners that modulate local and systemic mechanisms in plants to offer defence under adverse external conditions. Plant-microbe interactions comprise complex mechanisms within the plant cellular system. Biochemical, molecular and physiological studies are paving the way in understanding the complex but integrated cellular processes. Under the continuous pressure of increasing climatic alterations, it now becomes more imperative to define and interpret plant-microbe relationships in terms of protection against abiotic stresses. At the same time, it also becomes essential to generate deeper insights into the stress-mitigating mechanisms in crop plants for their translation in higher productivity. Multi-omics approaches comprising genomics, transcriptomics, proteomics, metabolomics and phenomics integrate studies on the interaction of plants with microbes and their external environment and generate multi-layered information that can answer what is happening in real-time within the cells. Integration, analysis and decipherization of the big-data can lead to a massive outcome that has significant chance for implementation in the fields. This review summarizes abiotic stresses responses in plants in-terms of biochemical and molecular mechanisms followed by the microbe-mediated stress mitigation phenomenon. We describe the role of multi-omics approaches in generating multi-pronged information to provide a better understanding of plant-microbe interactions that modulate cellular mechanisms in plants under extreme external conditions and help to optimize abiotic stresses. Vigilant amalgamation of these high-throughput approaches supports a higher level of knowledge generation about root-level mechanisms involved in the alleviation of abiotic stresses in organisms.
515 citations
Cites background from "Identification of Genes Involved in..."
...…Tiwari et al., 2011), elaboration of various antioxidants and osmolytes and activation of transcription factors (TFs), are initiated along with the expression of stress-specific genes to mount appropriate defense system (Koussevitzky et al., 2008; Atkinson et al., 2013; Prasch and Sonnewald, 2013)....
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References
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TL;DR: There is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities, and the exploratory data analyses of the probe level data motivate a new summary measure that is a robust multi-array average (RMA) of background-adjusted, normalized, and log-transformed PM values.
Abstract: SUMMARY In this paper we report exploratory analyses of high-density oligonucleotide array data from the Affymetrix GeneChip R � system with the objective of improving upon currently used measures of gene expression. Our analyses make use of three data sets: a small experimental study consisting of five MGU74A mouse GeneChip R � arrays, part of the data from an extensive spike-in study conducted by Gene Logic and Wyeth’s Genetics Institute involving 95 HG-U95A human GeneChip R � arrays; and part of a dilution study conducted by Gene Logic involving 75 HG-U95A GeneChip R � arrays. We display some familiar features of the perfect match and mismatch probe ( PM and MM )v alues of these data, and examine the variance–mean relationship with probe-level data from probes believed to be defective, and so delivering noise only. We explain why we need to normalize the arrays to one another using probe level intensities. We then examine the behavior of the PM and MM using spike-in data and assess three commonly used summary measures: Affymetrix’s (i) average difference (AvDiff) and (ii) MAS 5.0 signal, and (iii) the Li and Wong multiplicative model-based expression index (MBEI). The exploratory data analyses of the probe level data motivate a new summary measure that is a robust multiarray average (RMA) of background-adjusted, normalized, and log-transformed PM values. We evaluate the four expression summary measures using the dilution study data, assessing their behavior in terms of bias, variance and (for MBEI and RMA) model fit. Finally, we evaluate the algorithms in terms of their ability to detect known levels of differential expression using the spike-in data. We conclude that there is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities. ∗ To whom correspondence should be addressed
10,711 citations
"Identification of Genes Involved in..." refers methods in this paper
...Baseline preprocessing, normalization, and summarization were carried out using the Robust Multiarray Average summarization algorithm, as described by Irizarry et al. (2003)....
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TL;DR: The elucidation ofMYB protein function and regulation that is possible in Arabidopsis will provide the foundation for predicting the contributions of MYB proteins to the biology of plants in general.
3,542 citations
"Identification of Genes Involved in..." refers background in this paper
...…pathway such as anthocyanins and lignin, as well as cell wall biosynthesis (Jin et al., 2000; Patzlaff et al., 2003; Wuyts et al., 2006; Dubos et al., 2010), and may make excellent candidates for the improvement of broad-spectrum stress tolerance (Jin et al., 2000; Vannini et al.,…...
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...…genes contributes to increasing evidence that these factors are central in controlling cross talk and specificity between different stress signaling pathways (Rizhsky et al., 2004; Mattana et al., 2005; Vannini et al., 2007; Abuqamar et al., 2009; Dubos et al., 2010; Atkinson and Urwin, 2012)....
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TL;DR: Attention is drawn to the perception and signalling processes (chemical and hydraulic) of water deficits, which are essential for a holistic understanding of plant resistance to stress, which is needed to improve crop management and breeding techniques.
Abstract: In the last decade, our understanding of the processes underlying plant response to drought, at the molecular and whole-plant levels, has rapidly progressed. Here, we review that progress. We draw attention to the perception and signalling processes (chemical and hydraulic) of water deficits. Knowledge of these processes is essential for a holistic understanding of plant resistance to stress, which is needed to improve crop management and breeding techniques. Hundreds of genes that are induced under drought have been identified. A range of tools, from gene expression patterns to the use of transgenic plants, is being used to study the specific function of these genes and their role in plant acclimation or adaptation to water deficit. However, because plant responses to stress are complex, the functions of many of the genes are still unknown. Many of the traits that explain plant adaptation to drought - such as phenology, root size and depth, hydraulic conductivity and the storage of reserves - are those associated with plant development and structure, and are constitutive rather than stress induced. But a large part of plant resistance to drought is the ability to get rid of excess radiation, a concomitant stress under natural conditions. The nature of the mechanisms responsible for leaf photoprotection, especially those related to thermal dissipation, and oxidative stress are being actively researched. The new tools that operate at molecular, plant and ecosystem levels are revolutionising our understanding of plant response to drought, and our ability to monitor it. Techniques such as genome-wide tools, proteomics, stable isotopes and thermal or fluorescence imaging may allow the genotype-phenotype gap to be bridged, which is essential for faster progress in stress biology research.
3,287 citations
Additional excerpts
...Vol. 162, 2013 turgor loss (Chaves et al., 2003)....
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TL;DR: Tolerance to a combination of different stress conditions, particularly those that mimic the field environment, should be the focus of future research programs aimed at developing transgenic crops and plants with enhanced tolerance to naturally occurring environmental conditions.
2,432 citations
"Identification of Genes Involved in..." refers background in this paper
...Vol. 162, 2013 2033 individual stress, leading to severe agricultural losses (Craufurd and Peacock, 1993; Savin and Nicolas, 1996; Mittler, 2006)....
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...…of water deficit and nematode stress treatments displayed a distinct program of gene expression, supporting the theory that plant responses to stress are highly specialized and unique to the exact set of environmental conditions encountered (Mittler, 2006; Yasuda et al., 2008; Ton et al., 2009)....
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TL;DR: A full-length cDNA microarray containing approximately 7000 independent, full- length cDNA groups is prepared to analyse the expression profiles of genes under drought, cold (low temperature) and high-salinity stress conditions over time, suggesting that various transcriptional regulatory mechanisms function in the drought,cold or high- salinity stress signal transduction pathways.
Abstract: Full-length cDNAs are essential for functional analysis of plant genes in the post-sequencing era of the Arabidopsis genome. Recently, cDNA microarray analysis has been developed for quantitative analysis of global and simultaneous analysis of expression profiles. We have prepared a full-length cDNA microarray containing approximately 7000 independent, full-length cDNA groups to analyse the expression profiles of genes under drought, cold (low temperature) and high-salinity stress conditions over time. The transcripts of 53, 277 and 194 genes increased after cold, drought and high-salinity treatments, respectively, more than fivefold compared with the control genes. We also identified many highly drought-, cold- or high-salinity- stress-inducible genes. However, we observed strong relationships in the expression of these stress-responsive genes based on Venn diagram analysis, and found 22 stress-inducible genes that responded to all three stresses. Several gene groups showing different expression profiles were identified by analysis of their expression patterns during stress-responsive gene induction. The cold-inducible genes were classified into at least two gene groups from their expression profiles. DREB1A was included in a group whose expression peaked at 2 h after cold treatment. Among the drought, cold or high-salinity stress-inducible genes identified, we found 40 transcription factor genes (corresponding to approximately 11% of all stress-inducible genes identified), suggesting that various transcriptional regulatory mechanisms function in the drought, cold or high-salinity stress signal transduction pathways.
1,989 citations
"Identification of Genes Involved in..." refers background in this paper
...Previous studies have aimed to identify genes important in multiple stress tolerance by comparing lists of genes induced by each stress individually (Seki et al., 2002; Swindell, 2006; Kilian et al., 2007; Kant et al., 2008)....
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