Plant hormone-mediated regulation of stress responses

Organisms are under strong selection to respond adaptively to environmental stress, even when different stresses occur simultaneously or in rapid succession, as they often do in natural environments. However, at a molecular level, stress responses are often studied in isolation and under controlled growth conditions. This leaves us with an ever-finer picture of single stress responses but little understanding of how additional stressors modify those responses. Without companion studies of more complex systems of interacting stresses, we do not know how phenotypes are shaped under natural conditions. Based on whole organism studies in largely agricultural settings, we do know that stresses interact profoundly to shape phenotypes. We also have examples of cross-talk among signalling pathways associated with specific abiotic and biotic stress responses which hint at the existence of mechanisms that may integrate global plant stress responses. To move plant stress biology forward in transformative ways, we need greater collaboration among plant biologists studying different stresses in order to address the complexity of plant stress responses under natural conditions. In 2015, the University of Missouri Interdisciplinary Plant Group (IPG) organized its annual symposium around the topic of Plants Between a Rock and a Hard Place: The Interface between Plant Abiotic and Biotic Stress Responses. A primary goal of the meeting was to promote and enhance multi-stress collaboration within the plant stress biology community by bringing together world-renowned experts in different aspects of plant stress biology who have already begun to study the interactions between different stresses. In this special issue of the Journal of Experimental Botany, we present some of the topics and research that were covered at the symposium. Foyer et al. (2016) set the stage with a detailed look at how an abiotic stress can shape a plant’s response to attack by phloem-feeding aphids. They present a strong case to challenge the oft-held notion that abiotic stress events result in an increased susceptibility to biotic stress factors. The complex signalling pathways that direct plant responses to abiotic and biotic stressors overlap in many ways that lead to cross-tolerance phenomena. The plant’s response to aphid infestation involves interactions between hormone, redox, nitric oxide, kinase, and calcium signalling pathways that mirror aspects of the plant’s response to abiotic factors. The preponderance of evidence suggests that abiotic stressors do not predispose a plant to aphid attack and, in fact, may provide some measure of protection and that this may hold true for other abiotic–biotic stressor interactions. Viruses depend on vectors such as plant-associated insects to move from plant to plant. To spread throughout an infected plant successfully and to facilitate vector transmission to another, viruses must manipulate the cellular processes of the host with a very limited set of proteins encoded in their small genomes. Studying these proteins from viruses and other plant-associated pathogens can provide novel insights into the processes involved in abiotic and biotic stress responses. Schoelz et al. (2016) provide an intriguing overview of the multifunctional P6 protein of Cauliflower Mosaic Virus, a novel function of which is to direct large protein assemblies devoted to virus replication into plasmodesmata for cell-to-cell movement. In contrast to viruses, most microbial pathogens of plants do not enter the host cytoplasm. A first line of defence, therefore, occurs at the plant plasma membrane where receptors detect conserved non-self molecules collectively called microbe- or pathogen-associated molecular patterns (M/PAMPs) to initiate a broad defence response termed PAMP-triggered immunity (PTI) (Macho and Zipfel, 2014). While PAMPs and the corresponding plant receptors have been identified for a variety of microbial pathogens, a notable exception has been PAMPs derived from plant-parasitic nematodes. The review by Holbein et al. (2016) provides a fascinating update on progress in identifying elements of plant PTI responses to nematodes, thus broadening the arsenal for breeding resistance into crop plants. Biotic and abiotic stressors often elicit systemic responses which depend on signalling from local sites of exposure to other areas of the plant. At the cellular or tissue level, the possible interplay between the various signalling pathways can be complex, especially when two or more stressors are combined as is often the case in the field. Huber and Bauerle (2016) describe the hydraulic, chemical, and electrical components that are part of the long-distance communication array of all plants. They provide a comprehensive assessment of what is known about how they operate and interact to co-ordinate a systemic response in the plant. The authors highlight the large gaps in knowledge that need to be addressed and make clear that combinations of stressors often elicit novel responses that differ from responses to single stressors. Plant responses to abiotic and biotic stressors can lead to changes that appear to be ‘memorized’ and influence the stress tolerance of the next generation. The review by Bilichak and Kovalchuk (2016) explores possible epigenetic mechanisms associated with this phenomenon, highlighting the evidence that certain stress-induced epigenetic factors escape full-scale reprogramming of the epigenome during gametogenesis. The authors speculate that a better understanding of these epigenetic factors would enable the engineering of epigenetic modifications to cross-stress tolerance for crop improvement strategies in plant breeding. The symposium was also an opportunity to showcase new and focused unpublished data. The research paper by MacQueen and Bergelson (2016) focuses on plant innate immunity to microbial pathogens. They show that abiotic factors such as temperature and humidity, which are known to influence pathogen aggressiveness, impact expression levels of plant resistance genes. These resistance genes provide a second line of defence against microbial pathogens, but their continued high expression reduces plant fitness. Therefore, modulation of resistance gene expression levels by abiotic factors probably reflects an adaptive advantage by balancing plant defence readiness and fitness in the absence of pathogens. Finally, the research paper by Zhang et al. (2016) identifies an intriguing connection between the auxin and jasmonic acid (JA) signalling pathways via hormone metabolism. Even though auxin and JA regulate quite distinct developmental and stress response pathways, it was found that some of the indole-3-acetic acid (IAA) hydrolases (IAH) also metabolize JA-isoleucine, a bioactive derivative of JA. Manipulation of IAH expression levels led to surprising perturbations of these hormone signalling modules, highlighting the degree to which these two signalling pathways are interconnected via metabolic cross-talk. Worldwide, humans rely on plants for food, fibre, and fuel, and face the daunting task of growing food for nine billion people by 2050 while reducing the carbon, fertilizer, and water footprint of agriculture. In addition, the consensus prediction is that global climate change will destabilize plant growth conditions in terms of higher CO2 levels and increased risks of severe fluctuations in temperature and precipitation (Schroeder et al., 2013). These adverse abiotic conditions will most likely favour the spread of plant pathogens and pests into new geographic areas. Such a scenario increases the need to develop abiotic stress and pathogen- and pest-resistant crop plants at a speed that cannot be met by breeding alone (Dangl et al., 2013). The combination of abiotic and biotic stresses not only threatens agriculture but also plants in natural environments that fulfil important ecosystem services. Addressing these major challenges will require an interdisciplinary and concerted approach. We hope that our readers will find, as we did, that the reviews and research articles in this special issue provide a useful and stimulating contribution towards addressing these challenges. We are grateful to the sponsors of our symposium, in particular the National Science Foundation, the USDA National Institute of Food and Agriculture, and the Journal of Experimental Botany for their support.

The central role of transcription factors in bridging biotic and abiotic stress responses for plants’ resilience

The recent global climate change has directly impacted major biotic and abiotic stress factors affecting crop productivity worldwide. Therefore, the need of the hour is to develop sustainable multiple stress tolerant crops through modern biotechnological approaches to cope with climate change. Hybrid proline rich proteins (HyPRPs) are the cell-wall structural proteins, which contain an N-terminal repetitive proline-rich domain and a C-terminal conserved eight-cysteine motif domain. HyPRPs are known to regulate multiple abiotic and biotic stress responses in plants. Recently, a few HyPRPs have been characterized as negative regulators of abiotic and biotic stress responses in different plants. Disruption of such negative regulators for desirable positive phenotypic traits has been made possible through the advent of advanced genome engineering tools. In the past few years, CRISPR/Cas9 has emerged as a novel breakthrough technology for crop improvement by target specific editing of known negative regulatory host genes. Here, we have described the mechanism of action and the role of known HyPRPs in regulating different biotic and abiotic stress responses in major crop plants. We have also discussed the importance of the CRISPR/Cas9 based genome editing system in targeting known negative regulatory HyPRPs for multi-stress crop tolerance using the tomato crop model. Application of genome editing to manipulate the HyPRPs of major crop plants holds promise in developing newer stress management methods in this rapidly changing climate and would lead in the future to sustain crop productivity.

This is the second special issue on Plant Hormone Signaling. Abscisic acid (ABA), ethylene and salicylic acid (SA) have long been recognized as the key plant hormones mediating abiotic and biotic stresses, respectively. The underlying mechanisms of action by which these and other hormones modulate the response of plants to stresses have received considerable attention in the recent past. Research findings in the last two decades have been revealing their fascinating modes of action. Furthermore, the intricate crosstalks among various hormones by which they can modulate growth and development in response to diverse environmental stresses have emerged as a common theme in this field. With the identification of specific receptors for individual hormones, convincing mechanisms explaining the modes of action of these hormones have been proposed. The involvement of ethylene and the AP2/ERF family of proteins, PR proteins and the like in biotic stress response has now been well established. Besides ABA and ethylene, it is now known that salicylic acid, jasmonates, brassinosteroids, and even gibberellins and auxins crosstalk extensively to regulate practically all aspects of plant stress responses. Eminent practitioners in the field have provided enthusiastic support for this issue as with the first special issue, which dealt with general aspects of hormone signaling. The sixteen contributions compiled in this issue are articles dealing specifically with abiotic and biotic stresses. The contributions range from how hormones initiate signal cascades to control grain yield, root development, and DNA repair as well as protein modifications such as SUMOylation. Also included are papers on the crosstalks among ABA, ethylene, gibberellins, brassinosteroids, SA, jasmonates etc. to regulate herbivory and other biotic stresses. It is hoped that the timely reviews of the signaling-related topics in the two special issues will be a useful contribution to plant biologists in general. Exciting new findings continue to be made, and work on plant hormone signaling intermediates holds tremendous promises for introducing new traits and protecting high levels of crop productivity in the face of global climate change. We can be confident in declaring that the proposed modes of action of plant hormones will continue to get refined and such studies will help in boosting crop productivity in the coming decades. Hopefully, this effort to put together a collection of useful reference material will be appreciated by our readers.

Sucrose signaling pathways leading to fructan and anthocyanin accumulation: A dual function in abiotic and biotic stress responses?

Plant intracellular immune receptor NLR (nucleotide-binding leucine-rich repeat) proteins sense the presence of pathogens and trigger strong and robust immune responses. NLR genes are known to be tightly controlled at the protein level, but little is known about their dynamics at the transcript level. In this study, we presented a meta-analysis of transcript dynamics of all 207 NLR genes in the Col-0 accession of Arabidopsis thaliana under various biotic and abiotic stresses based on 88 publicly available RNA sequencing datasets from 27 independent studies. We find that about two thirds of the NLR genes are generally induced by pathogens, immune elicitors, or salicylic acid (SA), suggesting that transcriptional induction of NLR genes might be an important mechanism in plant immunity regulation. By contrast, NLR genes induced by biotic stresses are often repressed by abscisic acid, high temperature and drought, suggesting that transcriptional regulation of NLR genes might be important for interaction between abiotic and biotic stress responses. In addition, pathogen-induced expression of some NLR genes are dependent on SA induction. Interestingly, a small group of NLR genes are repressed under certain biotic stress treatments, suggesting an unconventional function of this group of NLRs. This meta-analysis thus reveals the transcript dynamics of NLR genes under biotic and abiotic stress conditions and suggests a contribution of NLR transcript regulation to plant immunity as well as interactions between abiotic and biotic stress responses.

Plants, rooted in one place, are constantly subjected to diverse biotic and abiotic stresses that limit their growth and development, resulting in significant crop losses. In response to stresses, plants deploy several integrated signaling networks to rapidly reprogram gene expression thereby altering cellular processes to adapt and survive under unfavorable conditions. Among the key signaling mechanisms that plants use, calcium- and calcium/calmodulin-mediated signal transduction pathways have emerged as one of the ubiquitous players. The calcium-signaling networks include many calcium and calcium/calmodulin-binding transcription factors. In this review, we focus on the functions of a family of highly conserved calcium/calmodulin-binding Transcription Factors (TFs) called calmodulin-binding transcription activators (CAMTAs) in plants. This family of transcription factors was first identified in plants as calmodulin-binding proteins and discovered later in animals. Genetic studies in the model plant Arabidopsis and crop plants such as rice uncovered crucial roles for CAMTAs in modulating plant responses to both biotic and abiotic stresses. Depending on the type of stress, CAMTAs function as either positive or negative regulators for plant growth and stress responses. Arabidopsis CAMTA3 is the most studied member of CAMTA proteins. It modulates the expression of many key genes involved in different hormone signaling pathways and plays a central role in biotic (bacterial, fungal, and viral pathogens) as well as abiotic (cold, drought, salt, and wounding/mechanical) stress responses. Studies with many point, truncated, loss-of-function, and suppressor mutants of CAMTA3 revealed a complex regulation of its function. Here we summarize the advances in the study of the CAMTA family with a focus on CAMTA3. Further, we identify critical gaps in furthering our understanding of the molecular mechanisms by which these TFs function and discuss potential opportunities to engineer them for biotechnological applications to develop stress-resilient crops.

NAC transcription factors belong to a unique class of transcription factors in plants. The common characteristics of the NAC proteins are the presence of a conserved NAC domain, comprising of about 150 amino acids in N-terminals and a highly variable transcriptional regulation region in C-terminals. Extensive studies have revealed that NAC transcription factors not only play important roles in plant growth and development, but also have functions in regulation of responses to biotic and abiotic stresses. In this minireview, we summarized the functions and mechanisms of the NAC transcriptional factors in plant abiotic and biotic stress responses. We also discussed future directions towards understanding the biological functions of the members of the NAC transcriptional factors in plants.

Biotic and abiotic stresses are significant factors limiting the production of food and other supporting materials required to sustain increasing world population. Plant health is directly related to human health and is increasingly becoming significant and demands more attention towards limiting the damages caused by biotic and abiotic stresses. Significant progress has been made towards our understanding of the processes, which mediate both biotic and abiotic stress signaling in plants. Significant role is played by various plant hormones, e.g., salicylic acid (SA) and jasmonic acid (JA) in biotic stress and abscisic acid (ABA) in abiotic stress (Annu Rev Cell Dev Biol 28:489–521, 2012). Other hormones with minor role include the cytokinins (CK), auxins (indole 3 acetic acid. IAA), and the brassinosteroids (BR) (Annu Rev Cell Dev Biol 28:489–521, 2012). Cross talk between these plant hormones is significant and may result in either synergistic or antagonistic effect on stress responses (Annu Rev Cell Dev Biol 28:489–521, 2012). In recent years, extensive research carried out in various laboratories has implicated cross talk between the ABA and the SA in abiotic stress response. This is significant in light of SA being key player in biotic stress responses in plants. This review will discuss the role of SA in biotic and abiotic stress signaling and its cross talk with other hormones in mediating abiotic stress signaling in plants.

BackgroundThe ubiquitin 26S proteasome system (UPS) selectively degrades cellular proteins, which results in physiological changes to eukaryotic cells. F-box proteins are substrate adaptors within the UPS and are responsible for the diversity of potential protein targets. Plant genomes are enriched in F-box genes, but the vast majority of these have unknown roles. This work investigated the Arabidopsis F-box gene F-BOX STRESS INDUCED 1 (FBS1) for its effects on gene expression in order elucidate its previously unknown biological function.ResultsUsing publically available Affymetrix ATH1 microarray data, we show that FBS1 is significantly co-expressed in abiotic stresses with other well-characterized stress response genes, including important stress-related transcriptional regulators. This gene suite is most highly expressed in roots under cold and salt stresses. Transcriptome analysis of fbs1–1 knock-out plants grown at a chilling temperature shows that hundreds of genes require FBS1 for appropriate expression, and that these genes are enriched in those having roles in both abiotic and biotic stress responses. Based on both this genome-wide expression data set and quantitative real-time PCR (qPCR) analysis, it is apparent that FBS1 is required for elevated expression of many jasmonic acid (JA) genes that have established roles in combatting environmental stresses, and that it also controls a subset of JA biosynthesis genes. FBS1 also significantly impacts abscisic acid (ABA) regulated genes, but this interaction is more complex, as FBS1 has both positive and negative effects on ABA-inducible and ABA-repressible gene modules. One noteworthy effect of FBS1 on ABA-related stress processes, however, is the restraint it imposes on the expression of multiple class I LIPID TRANSFER PROTEIN (LTP) gene family members that have demonstrated protective effects in water deficit-related stresses.ConclusionFBS1 impacts plant stress responses by regulating hundreds of genes that respond to the plant stress hormones JA and ABA. The positive effect that FBS1 has on JA processes and the negative effect it has on at least some ABA processes indicates that it in part regulates cellular responses balanced between these two important stress hormones. More broadly then, FBS1 may aid plant cells in switching between certain biotic (JA) and abiotic (ABA) stress responses. Finally, because FBS1 regulates a subset of JA biosynthesis and response genes, we conclude that it might have a role in tuning hormone responses to particular circumstances at the transcriptional level.

Agricultural productivity depends on increasingly extreme weather phenomena, and the use of germplasm that has to be continuously improved by plant breeders to become tolerant to various biotic and abiotic stresses. Molecular plant biologists try to understand the mechanisms associated with stress responses and provide knowledge that could be used in breeding programs. To provide a partial overview about our current understanding about molecular and physiological stress responses, and how this knowledge can be used in agriculture, we have edited a special issue on “Biotic and Abiotic Stress Responses in Crop Plants”. Contributions are from different fields including heat stress responses, stress responses during drought and salinity, as well as during flooding, and resistance and susceptibility to pathogenetic stresses and about the role of plant functional metabolites in biotic stress responses. Future research demand in particular areas of crop stress physiology is discussed, as well as the importance of translational research and investigations directly in elite crop plants and in the genetic resources available for breeding.

Histone acetylation is a dynamic modification process co-regulated by histone acetyltransferases (HATs) and histone deacetylases (HDACs). Although HDACs play vital roles in abiotic or biotic stress responses, their members in Triticumaestivum and their response to plant viruses remain unknown. Here, we identified and characterized 49 T. aestivumHDACs (TaHDACs) at the whole-genome level. Based on phylogenetic analyses, TaHDACs could be divided into 5 clades, and their protein spatial structure was integral and conserved. Chromosomal location and synteny analyses showed that TaHDACs were widely distributed on wheat chromosomes, and gene duplication has accelerated the TaHDAC gene family evolution. The cis-acting element analysis indicated that TaHDACs were involved in hormone response, light response, abiotic stress, growth, and development. Heatmaps analysis of RNA-sequencing data showed that TaHDAC genes were involved in biotic or abiotic stress response. Selected TaHDACs were differentially expressed in diverse tissues or under varying temperature conditions. All selected TaHDACs were significantly upregulated following infection with the barley stripe mosaic virus (BSMV), Chinese wheat mosaic virus (CWMV), and wheat yellow mosaic virus (WYMV), suggesting their involvement in response to viral infections. Furthermore, TaSRT1-silenced contributed to increasing wheat resistance against CWMV infection. In summary, these findings could help deepen the understanding of the structure and characteristics of the HDAC gene family in wheat and lay the foundation for exploring the function of TaHDACs in plants resistant to viral infections.

The Amorphophallus konjac is an important specialty cash crop in China and is rich in konjac glucomannan (KGM); however, its long-term exposure to abiotic and biotic stresses has hindered the development of the industry. Lipoxygenase (LOX) is a key enzyme in plant fatty acid metabolism and stress response, playing a vital role in plant growth and development, regulation of secondary metabolism, and responses to biotic and abiotic stresses. To date, systematic studies on the LOX gene family in A. konjac remain lacking. This study aims to identify the A. konjac LOX gene family at the whole-genome level, analyze its sequence characteristics, evolutionary relationships, and expression patterns under various stresses, and provide candidate genes for stress-tolerant molecular breeding. Based on the LOX conserved domain, an HMM model was constructed, and 11 AkLOX family members were identified from the A. konjac genome. According to catalytic sites, the gene family was classified into three subfamilies: 9-LOX, 13-LOX Type I, and 13-LOX Type II, which were unevenly distributed on 4 chromosomes. The encoded proteins contained 848-945 amino acids with molecular weights ranging from 97,110.54Da to 102,962.26Da, all of which were unstable hydrophilic proteins. Phylogenetic and collinearity analyses revealed 6 homologous gene pairs between A. konjac and Amorphophallus albus, one pair between A. konjac and Cucumis sativus/Arabidopsis thaliana, and two pairs between A. konjac and Oryza sativa/Solanum tuberosum, indicating the phylogenetic conservation of the LOX family. Promoter cis-element analysis identified 23 types of cis-regulatory elements, most of which were related to plant growth and development, hormone responses, as well as biotic and abiotic stress responses. qRT-PCR results showed that the expression levels of AkLOX1/4/8 were significantly up-regulated under low temperature, drought, and MeJA treatments, supporting the reliability of the cis-element analysis. Under Pectobacterium carotovorum subsp. carotovorum (Pcc) stress, the expression levels of AkLOX2/3/11 were significantly up-regulated, showing an obvious stress-specific response pattern. This study performed genome-wide identification and expression analysis of the AkLOX gene family in A. konjac, and clarified their sequence characteristics, evolutionary relationships, and stress response patterns. It was confirmed that members of this gene family are widely involved in biotic and abiotic stress responses in A. konjac, providing candidate genes for subsequent research on A. konjac resistance to Pcc, low temperature, drought and other stresses.

Legumes are considered the second most important source of food after cereals, and their production can be affected by abiotic and biotic stresses. The incidence of biotic and abiotic stress conditions resulting from climate change is expected to increase in the future and may affect legume production drastically. Abiotic stresses could result in escalated biotic stress occurrence. Although responses to abiotic and biotic stress differ in most cases, combined abiotic and biotic stress responses could be expressed in synergistic or opposing forms. In view of the impending escalation in climate change, responses of legumes to stressful environments are expected to vary among crops. However, collective information on combined biotic and abiotic stress in legumes is not readily available. This paper seeks to gather available information on the responses of legumes to biotic, abiotic, and combined stress with a focus on physiological responses. This review will, therefore, help in providing information and encourage further research into combined stress factors in legumes

Plants have evolved with intricate mechanisms to cope with multiple environmental stresses. To adapt with biotic and abiotic stresses, plant responses involve changes at the cellular and molecular levels. The current study was designed to investigate the effects of combinations of different environmental stresses on the transcriptome level of Arabidopsis genome using public microarray databases. We investigated the role of cyclopentenones in mediating plant responses to environmental stress through TGA (TGACG motif-binding factor) transcription factor, independently from jasmonic acid. Candidate genes were identified by comparing plants inoculated with Botrytis cinerea or treated with heat, salt or osmotic stress with non-inoculated or non-treated tissues. About 2.5% heat-, 19% salinity- and 41% osmotic stress-induced genes were commonly upregulated by B. cinerea-treatment; and 7.6%, 19% and 48% of genes were commonly downregulated by B. cinerea-treatment, respectively. Our results indicate that plant responses to biotic and abiotic stresses are mediated by several common regulatory genes. Comparisons between transcriptome data from Arabidopsis stressed-plants support our hypothesis that some molecular and biological processes involved in biotic and abiotic stress response are conserved. Thirteen of the common regulated genes to abiotic and biotic stresses were studied in detail to determine their role in plant resistance to B. cinerea. Moreover, a T-DNA insertion mutant of the Responsive to Dehydration gene (rd20), encoding for a member of the caleosin (lipid surface protein) family, showed an enhanced sensitivity to B. cinerea infection and drought. Overall, the overlapping of plant responses to abiotic and biotic stresses, coupled with the sensitivity of the rd20 mutant, may provide new interesting programs for increased plant resistance to multiple environmental stresses, and ultimately increases its chances to survive. Future research directions towards a better dissection of the potential crosstalk between B. cinerea, abiotic stress, and oxylipin signaling are of our particular interest.