Transcriptional and post‐transcriptional mechanisms regulating salt tolerance in plants

Abstract

Amid mounting global human population, particularly in the developing world, climate change continues to challenge food security and crop cultivation. Hence, mitigation strategies are needed to sustain and invigorate the crop resources needed for agriculture. Within the broad purview and compliance of sustainable development goals (SDG), it is also a compelling task to improve the way food is produced and, in this context, research advances should provide solutions. Among the different abiotic stresses, soil salinity is a critical threat for sustainable agriculture. Changing climatic scenario and the rising seawater levels have created undue pressure on new, novel strategies for developing plants with salinity tolerance. Soil salinity at ≥4 dS m−1 electrical conductivity creates a toxic environment for most plant species. By 2050, about 50% of arable land will become saline, from the current estimate of 45 million hectares of salt-affected land (Shrivastava & Kumar, 2015). Soil salinity is a key abiotic stress factor that affects crops plants both in terms of yield and quality of the crop produce (Munns & Tester, 2008). It is the need of the hour to combine notional model based on the present convention of salt stress responses with various multidisciplinary approaches for mitigating salinity stress in crop plants (Wani et al., 2020). Therefore, it has become a major challenge for agriculturists, plant breeders, and biotechnologists to develop innovative solutions to improve plant's tolerance to salinity stress. Salinity stress tolerance is a complex phenomenon that involves well-orchestrated plant responses, including defense against osmotic and oxidative stress, ionic homeostasis, membrane stability, and well-maintained key metabolic processes and phytohormones (Cabot et al., 2014; Isayenkov, 2019). The complex nature of salinity-induced perturbations at molecular, cellular, and whole plant physiological levels has necessitated a comprehensive understanding of the responsive physiological and molecular mechanisms plants adopt to offset the harmful effects of salt stress (Ismail & Horie, 2017; Zhang et al., 2020). Tolerant plants display a network of regulatory mechanisms, including reprogramming of the expression of several key genes at transcriptional and/or post-transcriptional levels (Tanveer & Shabala, 2018). These regulations are crucial for plants to restore and re-establish their cellular homeostasis during stress and the recovery phase. High-throughput sequencing methods, available databases, and in silico tools have facilitated the understanding of such regulatory mechanisms of salinity stress response and tolerance at transcriptional/post-transcriptional levels. Recent research has shown that there are several major players at transcriptional levels and post-transcriptional levels such as transcription factors (TFs), regulatory noncoding RNA species, including small and micro-RNAs with key regulatory roles in sensing and modulating the salinity stress impacts on major crop plants (Shriram et al., 2016). These regulatory elements are seen as major targets for engineering salinity tolerance in important crops. This special issue was initiated to bring together articles highlighting various transcriptional and post-transcriptional regulatory mechanisms underlying sensing, signaling, and responses to salinity stress in important crops and model plants using a wide variety of biological, analytical, and computational tools. The physiological, molecular, and biochemical cues to salinity stress have been very well addressed by several researchers. Several strategies, including melatonin, play an essential role in the regulation of plant growth, development, and stress responses (Costa et al., 2018). Several genomic and nongenomic strategies are being validated for gauging their potential for improving crop salt tolerance, which include stress-inducible promoters, protein post-translational modifications, halotolerant microbiome, and halophyte gene resources. State-of-the art approaches of plant phenotyping, next-generation sequencing, and molecular-assisted breeding have facilitated the generation of novel genetic resources for improving salt tolerance (Morton et al., 2019; Suprasanna, 2020). In the past few years, there has been a growing interest in gaining more molecular insights using genomic-assisted approaches for understanding the resilience mechanism of plants to changing environmental conditions. This special issue has articles presenting updated information on the regulatory short RNAs, miRNAs, transporters, late embryogenesis abundant (LEA) genes, Rab7 from Aeluropus lagopoides and WRKY18 TFs, RNA-binding bacterial chaperones and enhancers, which could be used as potential targets for engineering salinity stress tolerance. The epigenetic changes, including histone modifications and chromatin remodeling, play a crucial regulatory role in defense against salt stress environments. The recent upsurge in omics methods, such as metabolomics and proteomics, has created more interest as novel metabolites and proteomic signatures associated with salt stress responses are being unraveled. Studies conducted on transcriptome sequencing and transcriptome analyses in halophytes and woody species in this special issue have highlighted the need to explore salt tolerance traits in these species. Bansal et al. (2021) reported a draft genome as well as transcriptome analyses of halophyte rice Oryza coarctata, a wild relative of cultivated rice, in an attempt to provide potential resources for salinity and submergence stress response factors. Vita et al. (2021) compared the transcript profiling of two Quinoa genotypes with contrasting salt tolerance to identify the candidate genes involved in the differential early responses among genotypes. The transcriptome profiling, supported by in vitro physiological analyses, provides insights into the early-stage molecular mechanisms, both at the shoot and root level, based on the sensitive/tolerance traits in Quinoa, a halophytic annual pseudo-cereal species with high nutritional value. Basu and Roychoudhury (2021) reported the transcript profiling of stress-responsive genes and metabolic changes during salinity in indica and japonica rice cultivars with distinct varietal difference, which was attributed to their differential salinity tolerance abilities. Elnaggar et al. (2021) reported de novo transcriptome sequencing, assembly, and gene expression profiling of a salt-stressed halophyte (Salsola drummondii) from a saline habitat. The DNA polymorphisms via whole-genome sequencing and their functional relevance were investigated in salinity stress response in chickpea plants by Rajkumar et al. (2021). Frosi et al. (2021) reported the root transcriptome in Cenostigma pyramidale, a tolerant woody legume, and showed that early salt stress modulates ionic channels and transporters, the establishment of homeostasis of Na+ and K+, signaling by Ca2+, TFs, water transport, and oxidative stress. Reporting the first root transcriptome in this woody tree species, the authors suggested that the results provide clues on how ionic channels and transporters are modulated under salt stress tolerance. Salt-tolerant crop plants and halophytes offer ideal plant models to explore promising stress-responsive genes and metabolites to amend salt stress responses in crop plants. Using Pongamia pinnata (L.), Marriboina et al. (2021) showed effective apoplastic sodium sequestration in the roots, and strong correlation between phytohormones and metabolites such as mannitol, carbohydrates, fatty acids, and enhanced expression of transporters and signaling genes. Further, Skodra et al. (2021) highlighted the details of salt-responsive tissue-specific metabolic pathways in olive tree and constructed an interaction scheme of changes in metabolites and transcripts across olive tissues exposed to salinity stress. Cartagena et al. (2021) reported a comparative transcriptome analysis of root types in salt-tolerant and sensitive rice varieties subjected to salinity stress, and the results revealed important transcriptional regulation of stress responses. The study conducted by Chakraborty et al. (2021) hypothesized that well-developed constitutive aerenchyma provides an adaptive advantage during partial submergence due to saline water flooding in rice. In an interesting study, Tak et al., 2021 described the 5′-upstream regulatory region of the WRKY18 TF of banana and functionally analyzed its stress-meditated activation and strong guard cell-preferred activity. The fluorescent β-galactosidase assay demonstrated the higher stress-mediated induction profiles of PMusaWRKY18 at different time points in transgenic tobacco lines exposed to drought, high salinity, cold, and application of abscisic acid, salicylic acid, methyl jasmonate, and ethephon (Tak et al. (2021). Similarly, Guddimalli et al. (2021) overexpressed the RNA-binding bacterial chaperones in rice, resulting in the stay-green phenotype and improved yield and tolerance to salt and drought stresses. Divya et al. (2021) studied the functional characterization of late embryogenesis abundant genes and promoters in pearl millet and their role in abiotic stress tolerance. Naguib et al. (2021) reported that the raffinose accumulation and preferential allocation of carbon (14C) to developing leaves impart salinity tolerance in sugar beet. Sugar profile of leaves and roots confirmed the accumulation of raffinose in leaves, indicating a plausible role in imparting salinity tolerance by serving as an osmolyte. Further molecular analysis of the genes responsible for raffinose synthesis revealed an 18-fold increase in the expression of BvRS2 in the tolerant genotype, indicating its involvement in raffinose synthesis. The overexpression of AlRab7, a vesicle trafficking gene from A. lagopoides, resulted in an increase in germination and growth and curtailment in ionic and oxidative stress in transgenics (Agarwal et al., 2021). The authors concluded that the AlRab7 transgenic tobacco mitigates ionic stress by helping in differential and selective ion transport at the vacuole, regulating hormone signaling, ROS homeostasis, stomatal development, and movement. Two of the articles reported the exogenous use of melatonin to enhance salinity stress tolerance in Phaseolus vulgaris L. (ElSayed et al., 2021) and Olive plants (Zahedi et al., 2021), which was attributed to alleviated oxidative damages and induced antioxidant defense. Besides, this special issue also features reviews on important allied themes. Saddhe et al. (2021) reviewed the current understanding and updates on the molecular insights into the role of plant transporters in salt stress response, besides post-transcriptional and epigenetic regulation of ion transport in the plants. Jain and Garg (2021) discussed the enhancers (noncoding regulatory regions of the genome located distantly from their target genes) and how they regulate the gene expression programs in a context-specific manner via interacting with promoters of one or more target genes. They are generally associated with TF-binding sites and epi(genomic)/chromatin features, and they can be explored as potent targets for engineering salinity stress tolerance in plants. Negi et al. (2021) reviewed the regulatory short RNAs and important developments in recent years toward their use for manipulating salt tolerance in plants. Singh and Roychoudhury (2021) presented important insights into the gene regulation at transcriptional and post-transcriptional levels, including microRNA-mediated regulation, genome editing and alternative splicing, to combat salt stress in plants. Bhakta et al. (2020) presented an overview on the diverse roles of micro RNAs in banana, especially in abiotic stress responses like salinity, plant immune responses, fruit ripening and storage. A review by Choudhary et al. (2021) deliberated on the mechanisms of hormonal crosstalk that mediate the salinity stress response and adaptation in plants, with special emphasis on Graminaceous crops. Yung et al. (2021) has shown different epigenetic modifications of effector genes and how chromatin modifiers play important roles in regulating salt tolerance, besides crosstalk between epigenetic modifications and hormone signaling pathways. Such information is crucial for designing strategies using genome editing aimed at tailoring salt tolerance in crop plants. Another review by Roy et al. (2021) outlined the key roles played by plant growth-promoting rhizobacteria, endophytes, and mycorrhiza, and the inherent mechanisms associated with salt stress alleviation, suggesting that the rhizosphere microbiome could be designed to enhance the growth and productivity of salt-susceptible plants. Summing up, it is hoped that all the information that has been presented in the articles will further enhance our understanding on the genomics of resilience to salinity stress, with an emphasis on plants' improvement using precise target genes, salt-responsive tissue-specific pathways and metabolic pathways to produce better yield under changing climate conditions. Fine-tuning of salt-adaptive traits for use in breeding for salt tolerance will undoubtedly depend on future advances in crop genomics, phenomics, and stress-metabolite profiling. Continued research in these areas is expected to bring in potential strategies for developing climate-resilient crops with higher productivity as required for meeting the SDGs. VK and AKS acknowledge the financial support by the Department of Atomic Energy, Board of Research in Nuclear Sciences (DAE-BRNS), Government of India [37(1)/14/30/2018-BRNS]. VK acknowledges the financial support under DST-FIST (SR/ FST/COLLEGE-/19/568), DBT Star Status (BT/HRD/11/030/ 2012) and DBT-BUILDER Schemes implemented at Modern College of Arts, Science and Commerce, Ganeshkhind, Pune, India. All the authors / editors contributed substantially for this special issue.

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