Abiotic Stress Responses in Plants: Present and Future

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.

Understanding abiotic stress responses in plants is an important and challenging topic in plant research. Physiological and molecular biological analyses have allowed us to draw a picture of abiotic stress responses in various plants, and determination of the Arabidopsis genome sequence has had a great impact on this research field. The availability of the complete genome sequence has facilitated access to essential information for all genes, e.g. gene products and their function, transcript levels, putative cis-regulatory elements, and alternative splicing patterns. These data have been obtained from comprehensive transcriptome analyses and studies using full-length cDNA collections and T-DNA- or transposon-tagged mutant lines, which were also enhanced by genome sequence information. Moreover, studies on novel regulatory mechanisms involving use of small RNA molecules, chromatin modulation and genomic DNA modification have enabled us to recognize that plants have evolved complicated and sophisticated systems in response to complex abiotic stresses. Integrated data obtained with various 'omics' approaches have provided a more comprehensive picture of abiotic stress responses. In addition, research on stress responses in various plant species other than Arabidopsis has increased our knowledge regarding the mechanisms of plant stress tolerance in nature. Based on this progress, improvements in crop stress tolerance have been attempted by means of gene transfer and marker-assisted breeding. In this review, we summarize recent progress in abiotic stress studies, especially in the post-genomic era, and offer new perspectives on research directions for the next decade.

Transcription factors (TFs) are master regulators of abiotic stress responses in plants. This review focuses on TFs from seven major TF families, known to play functional roles in response to abiotic stresses, including drought, high salinity, high osmolarity, temperature extremes and the phytohormone ABA. Although ectopic expression of several TFs has improved abiotic stress tolerance in plants, fine-tuning of TF expression and protein levels remains a challenge to avoid crop yield loss. To further our understanding of TFs in abiotic stress responses, emerging gene regulatory networks based on TFs and their direct targets genes are presented. These revealed components shared between ABA-dependent and independent signaling as well as abiotic and biotic stress signaling. Protein structure analysis suggested that TFs hubs of large interactomes have extended regions with protein intrinsic disorder (ID), referring to their lack of fixed tertiary structures. ID is now an emerging topic in plant science. Furthermore, the importance of the ubiquitin-proteasome protein degradation systems and modification by sumoylation is also apparent from the interactomes. Therefore; TF interaction partners such as E3 ubiquitin ligases and TF regions with ID represent future targets for engineering improved abiotic stress tolerance in crops.

Intracellular changes in calcium ions (Ca2+) in response to different biotic and abiotic stimuli are detected by various sensor proteins in the plant cell. Calmodulin (CaM) is one of the most extensively studied Ca2+-sensing proteins and has been shown to be involved in transduction of Ca2+ signals. After interacting with Ca2+, CaM undergoes conformational change and influences the activities of a diverse range of CaM-binding proteins. A number of CaM-binding proteins have also been implicated in stress responses in plants, highlighting the central role played by CaM in adaptation to adverse environmental conditions. Stress adaptation in plants is a highly complex and multigenic response. Identification and characterization of CaM-modulated proteins in relation to different abiotic stresses could, therefore, prove to be essential for a deeper understanding of the molecular mechanisms involved in abiotic stress tolerance in plants. Various studies have revealed involvement of CaM in regulation of metal ions uptake, generation of reactive oxygen species and modulation of transcription factors such as CAMTA3, GTL1, and WRKY39. Activities of several kinases and phosphatases have also been shown to be modulated by CaM, thus providing further versatility to stress-associated signal transduction pathways. The results obtained from contemporary studies are consistent with the proposed role of CaM as an integrator of different stress signaling pathways, which allows plants to maintain homeostasis between different cellular processes. In this review, we have attempted to present the current state of understanding of the role of CaM in modulating different stress-regulated proteins and its implications in augmenting abiotic stress tolerance in plants.

Role of small RNAs in abiotic stress responses in plants

SRO1 is an important regulator of stress and hormonal response in plants and functions by interacting with transcription factors and several other proteins involved in abiotic stress response. In the present study, we report OsRBD1, an RNA binding domain 1- containing protein as a novel interacting partner of OsSRO1a from rice. The interaction of OsSRO1a with OsRBD1 was shown in yeast as well as in planta. Domain–domain interaction study revealed that C-terminal RST domain of OsSRO1a interacts with the N-terminal RRM1 domain of OsRBD1 protein. Both the proteins were found to co-localize in nucleus. Transcript profiling under different stress conditions revealed co-regulation of OsSRO1a and OsRBD1 expression under some abiotic stress conditions. Further, co-transformation of both OsSRO1a and OsRBD1 in yeast conferred enhanced tolerance toward salinity, osmotic, and methylglyoxal treatments. Our study suggests that the interaction of OsSRO1a with OsRBD1 confers enhanced stress tolerance in yeast and may play an important role under abiotic stress responses in plants.

Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants

BackgroundThe immobile nature of plants means that they can be frequently confronted by various biotic and abiotic stresses during their lifecycle. Among the various abiotic stresses, water stress, temperature extremities, salinity, and heavy metal toxicity are the major abiotic stresses challenging overall plant growth. Plants have evolved complex molecular mechanisms to adapt under the given abiotic stresses. Long non-coding RNAs (lncRNAs)—a diverse class of RNAs that contain > 200 nucleotides(nt)—play an essential role in plant adaptation to various abiotic stresses.ResultsLncRNAs play a significant role as ‘biological regulators’ for various developmental processes and biotic and abiotic stress responses in animals and plants at the transcription, post-transcription, and epigenetic level, targeting various stress-responsive mRNAs, regulatory gene(s) encoding transcription factors, and numerous microRNAs (miRNAs) that regulate the expression of different genes. However, the mechanistic role of lncRNAs at the molecular level, and possible target gene(s) contributing to plant abiotic stress response and adaptation, remain largely unknown. Here, we review various types of lncRNAs found in different plant species, with a focus on understanding the complex molecular mechanisms that contribute to abiotic stress tolerance in plants. We start by discussing the biogenesis, type and function, phylogenetic relationships, and sequence conservation of lncRNAs. Next, we review the role of lncRNAs controlling various abiotic stresses, including drought, heat, cold, heavy metal toxicity, and nutrient deficiency, with relevant examples from various plant species. Lastly, we briefly discuss the various lncRNA databases and the role of bioinformatics for predicting the structural and functional annotation of novel lncRNAs.ConclusionsUnderstanding the intricate molecular mechanisms of stress-responsive lncRNAs is in its infancy. The availability of a comprehensive atlas of lncRNAs across whole genomes in crop plants, coupled with a comprehensive understanding of the complex molecular mechanisms that regulate various abiotic stress responses, will enable us to use lncRNAs as potential biomarkers for tailoring abiotic stress-tolerant plants in the future.

Abiotic stresses such as salinity, drought, nutrient defi ciency or toxicity, and fl ooding limit crop productivity world-wide. However, this situation becomes more problematic in developing countries, where they cause food insecurity for large populations and poverty, particularly in rural areas. For example, drought stress has affected more than 70 million hectares of rice-growing land world-wide. While salt stress and nutrient stress render more than 100 million hectares of agricultural land uncultivable thereby resulting in low outputs, poor human nutrition and reduced educational and employment opportunities. Thus, abiotic stresses are the major factors of poverty for millions of people. In this scenario, it is widely urged that strategies should be adopted which may be used to get maximum crop stand and economic returns from stressful environments. Major strategies include breeding of new crop varieties, screening and selection of the existing germ-plasm of potential crops, production of genetically modifi ed (GM) crops, exogenous use of osmoprotec-tants etc. In the last century, conventional selection and breeding program proved to be highly effective in improving crops against abiotic stresses. Therefore, breeding for abiotic stress tolerance in crop plants (for food supply) should be given high research priority. However, extent and rate of progress in improving stress tolerance in crops through conventional breeding program is limited. This is due to complex mechanism of abiotic stress tolerance, which is controlled by the expression of several minor genes. Furthermore, techniques employed for selecting tolerant plants are time consumable and consequently expensive. During the last decade, using advanced molecular biology techniques different researchers showed some promising results in understanding molecular mechanisms of abiotic stress tolerance as well as in inducing stress tolerance in some potential crops. These fi ndings emphasized that future research should focus on molecular, physiological and metabolic aspects of stress tolerance to facilitate the development of crops with an inherent capacity to withstand abiotic stresses. This would help stabilize the crop production, and signifi cantly contribute to food and nutritional security in developing countries and semi-arid tropical regions.

Abscisic acid: A key regulator of abiotic stress tolerance in plants

One of the most interesting signaling molecules that regulates a wide array of adaptive stress responses in plants are the micro RNAs (miRNAs) that are a unique class of non-coding RNAs constituting novel mechanisms of post-transcriptional gene regulation. Recent studies revealed the role of miRNAs in several biotic and abiotic stresses by regulating various phytohormone signaling pathways as well as by targeting a number of transcription factors (TFs) and defense related genes. Phytohormones are signal molecules modulating the plant growth and developmental processes by regulating gene expression. Studies concerning miRNAs in abiotic stress response also show their vital roles in abiotic stress signaling. Current research indicates that miRNAs may act as possible candidates to create abiotic stress tolerant crop plants by genetic engineering. Yet, the detailed mechanism governing the dynamic expression networks of miRNAs in response to stress tolerance remains unclear. In this review, we provide recent updates on miRNA-mediated regulation of phytohormones combating various stress and its role in adaptive stress response in crop plants.

Modulation of gene expression is one of the most significant molecular mechanisms of abiotic stress response in plants. Via altering DNA accessibility, histone chaperones affect the transcriptional competence of genomic loci. However, in contrast to other factors affecting chromatin dynamics, the role of plant histone chaperones in abiotic stress response and adaptation remains elusive. Here, we studied the physiological function of a stress-responsive putative rice (Oryza sativa) histone chaperone of the NAP superfamily: OsNAPL6. We show that OsNAPL6 is a nuclear-localized H3/H4 histone chaperone capable of assembling a nucleosome-like structure. Utilizing overexpression and knockdown approaches, we found a positive correlation between OsNAPL6 expression levels and adaptation to multiple abiotic stresses. Results of comparative transcriptome profiling and promoter-recruitment studies indicate that OsNAPL6 functions during stress response via modulation of expression of various genes involved in diverse functions. For instance, we show that OsNAPL6 is recruited to OsRad51 promoter, activating its expression and leading to more efficient DNA repair and abrogation of programmed cell death under salinity and genotoxic stress conditions. These results suggest that the histone chaperone OsNAPL6 may serve a regulatory role in abiotic stress physiology possibly via modulating nucleosome dynamics at various stress-associated genomic loci. Taken together, our findings establish a hitherto unknown link between histone chaperones and abiotic stress response in plants.

Environmental stresses such as drought, high salinity, and low temperature can adversely modulate the field crop’s ability by altering the morphological, physiological, and biochemical processes of the plants. It is estimated that about 50% + of the productivity of several crops is limited due to various types of abiotic stresses either presence alone or in combination (s). However, there are two ways plants can survive against these abiotic stresses; a) through management practices and b) through adaptive mechanisms to tolerate plants. These adaptive mechanisms of tolerant plants are mostly linked to their signalling transduction pathway, triggering the action of plant transcription factors and controlling the expression of various stress-regulated genes. In recent times, several studies found that Zn-finger motifs have a significant function during abiotic stress response in plants. In the first report, a wide range of Zn-binding motifs has been recognized and termed Zn-fingers. Since the zinc finger motifs regulate the function of stress-responsive genes. The Zn-finger was first reported as a repeated Zn-binding motif, comprising conserved cysteine (Cys) and histidine (His) ligands, in Xenopus laevis oocytes as a transcription factor (TF) IIIA (or TFIIIA). In the proteins where Zn2+ is mainly attached to amino acid residues and thus espousing a tetrahedral coordination geometry. The physical nature of Zn-proteins, defining the attraction of Zn-proteins for Zn2+, is crucial for having an in-depth knowledge of how a Zn2+ facilitates their characteristic function and how proteins control its mobility (intra and intercellular) as well as cellular availability. The current review summarized the concept, importance and mechanisms of Zn-finger motifs during abiotic stress response in plants.

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.

The ubiquitin-proteasome system in the plant response to abiotic stress: Potential role in crop resilience improvement