Reactive oxygen species

Tolerance of plants to abiotic stressors such as drought and salinity is triggered by complex multicomponent signaling pathways to restore cellular homeostasis and promote survival. Major plant transcription factor families such as bZIP, NAC, AP2/ERF, and MYB orchestrate regulatory networks underlying abiotic stress tolerance. Sucrose non-fermenting 1-related protein kinase 2 and mitogen-activated protein kinase pathways contribute to initiation of stress adaptive downstream responses and promote plant growth and development. As a convergent point of multiple abiotic cues, cellular effects of environmental stresses are not only imbalances of ionic and osmotic homeostasis but also impaired photosynthesis, cellular energy depletion, and redox imbalances. Recent evidence of regulatory systems that link sensing and signaling of environmental conditions and the intracellular redox status have shed light on interfaces of stress and energy signaling. ROS (reactive oxygen species) cause severe cellular damage by peroxidation and de-esterification of membrane-lipids, however, current models also define a pivotal signaling function of ROS in triggering tolerance against stress. Recent research advances suggest and support a regulatory role of ROS in the cross talks of stress triggered hormonal signaling such as the abscisic acid pathway and endogenously induced redox and metabolite signals. Here, we discuss and review the versatile molecular convergence in the abiotic stress responsive signaling networks in the context of ROS and lipid-derived signals and the specific role of stomatal signaling.

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Tolerance to drought and salt stress in plants: Unraveling the signaling networks.

BACKGROUND Pathogens cause agricultural devastation and huge economic losses. Up to 30% of our crops are lost before or after harvest to pathogens and pests, wasting water and human effort. Diseases and pests are major problems for sustainable agriculture in the face of population growth. Similarly, microbial infection remains a major cause of human mortality and morbidity, responsible for ~25% of deaths worldwide in 2012. We lack vaccines for several major infectious diseases, and antibiotic resistance is an ever- growing concern. Plant and animal innate immune systems respond to pathogen infection and regulate beneficial interactions with commensal and symbiotic microbes. Plants and animals use intracellular proteins of the nucleotide binding domain (NBD), leucine-rich repeat (NLR) superfamily to detect many kinds of pathogens. Plant and animal NLRs evolved from distinct derivatives of a common ancestral prokaryotic adenosine triphosphatase (ATPase): the NBD shared by APAF-1, plant NLR proteins, and CED-4 (NB-ARC) domain class and that shared by apoptosis inhibitory protein (NAIP), CIITA, HET-E, TP1 (NACHT) domain class, respectively. Animals and fungi can carry both NB-ARC and NACHT domain proteins, but NACHT domain proteins are absent from plants and several animal taxa, such as Drosophila and nematodes. Despite the vast evolutionary distance between plants and animals, we describe trans-kingdom principles of NLR activation. We propose that NLRs evolved for pathogen-sensing in diverse organisms because the flexible protein domain architecture surrounding the NB-ARC and NACHT domains facilitates evolution of “hair trigger” switches, into which a virtually limitless number of microbial detection platforms can be integrated. ADVANCES Structural biology is beginning to shed light on pre- and postactivation NLR architectures. Various detection and activation platforms have evolved in both plant and animal NLR surveillance systems. This spectrum ranges from direct NLR activation, through binding of microbial ligands, to indirect NLR activation after the modification of host cellular targets, or decoys of those targets, by microbial virulence factors. Homo- and heterotypic dimerization and oligomerization of NLRs add complexity to signaling responses and can enable signal amplification. NLR population genomics across the plant and animal kingdoms is increasing owing to application of new capture-based sequencing methods. A more complete catalog of NLR repertoires within and across species will provide an enhanced toolbox for exploiting NLRs to develop therapeutic interventions. OUTLOOK Despite breakthroughs in our molecular understanding of NLR activation, many important questions remain. Biochemical mechanisms of NLR activation remain obscure. Events downstream of plant NLR activation and outputs such as transcription of defense genes, changes in cell permeability, localized cell death, and systemic signaling remain opaque. We do not know whether activated plant NLRs oligomerize or, if they do, how this is achieved, given the diversity of subcellular sites of activation observed for various NLRs. It is not clear whether and how the different N-terminal domains of plant NLRs signal. We have increasing knowledge regarding how animal NLRs assemble and signal, although knowledge gaps remain. Therapeutic interventions in humans targeting NLRs remain on the horizon. Design of novel recognition capabilities and engineering of new or extended NLR functions to counter disease in animals and plants provides tantalizing future goals to address plant and animal health problems worldwide.

Intracellular innate immune surveillance devices in plants and animals

Plant hormones are small molecules that regulate plant growth and development, as well as responses to changing environmental conditions. By modifying the production, distribution or signal transduction of these hormones, plants are able to regulate and coordinate both growth and/or stress tolerance to promote survival or escape from environmental stress. A central role for the gibberellin (GA) class of growth hormones in the response to abiotic stress is becoming increasingly evident. Reduction of GA levels and signalling has been shown to contribute to plant growth restriction on exposure to several stresses, including cold, salt and osmotic stress. Conversely, increased GA biosynthesis and signalling promote growth in plant escape responses to shading and submergence. In several cases, GA signalling has also been linked to stress tolerance. The transcriptional regulation of GA metabolism appears to be a major point of regulation of the GA pathway, while emerging evidence for interaction of the GA-signalling molecule DELLA with components of the signalling pathway for the stress hormone jasmonic acid suggests additional mechanisms by which GA signalling may integrate multiple hormone signalling pathways in the response to stress. Here, we review the evidence for the role of GA in these processes, and the regulation of the GA signalling pathway on exposure to abiotic stress. The potential mechanisms by which GA signalling modulates stress tolerance are also discussed.

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The role of gibberellin signalling in plant responses to abiotic stress

Contents Summary 523 I. Introduction 523 II. Sensing salt stress 524 III. Ion homeostasis regulation 524 IV. Metabolite and cell activity responses to salt stress 527 V. Conclusions and perspectives 532 Acknowledgements 533 References 533 SUMMARY: Excess soluble salts in soil (saline soils) are harmful to most plants. Salt imposes osmotic, ionic, and secondary stresses on plants. Over the past two decades, many determinants of salt tolerance and their regulatory mechanisms have been identified and characterized using molecular genetics and genomics approaches. This review describes recent progress in deciphering the mechanisms controlling ion homeostasis, cell activity responses, and epigenetic regulation in plants under salt stress. Finally, we highlight research areas that require further research to reveal new determinants of salt tolerance in plants.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.14920

Elucidating the molecular mechanisms mediating plant salt-stress responses

Abiotic stresses and soil nutrient limitations are major environmental conditions that reduce plant growth, productivity and quality. Plants have evolved mechanisms to perceive these environmental challenges, transmit the stress signals within cells as well as between cells and tissues, and make appropriate adjustments in their growth and development in order to survive and reproduce. In recent years, significant progress has been made on many fronts of the stress signaling research, particularly in understanding the downstream signaling events that culminate at the activation of stress- and nutrient limitation-responsive genes, cellular ion homeostasis, and growth adjustment. However, the revelation of the early events of stress signaling, particularly the identification of primary stress sensors, still lags behind. In this review, we summarize recent work on the genetic and molecular mechanisms of plant abiotic stress and nutrient limitation sensing and signaling and discuss new directions for future studies.

Plant abiotic stress response and nutrient use efficiency.

The phytohormone ethylene regulates multiple aspects of plant growth and development and responses to environmental stress. However, the exact role of ethylene in freezing stress remains unclear. Here, we report that ethylene negatively regulates plant responses to freezing stress in Arabidopsis thaliana. Freezing tolerance was decreased in ethylene overproducer1 and by the application of the ethylene precursor 1-aminocyclopropane-1-carboxylic acid but increased by the addition of the ethylene biosynthesis inhibitor aminoethoxyvinyl glycine or the perception antagonist Ag+. Furthermore, ethylene-insensitive mutants, including etr1-1, ein4-1, ein2-5, ein3-1, and ein3 eil1, displayed enhanced freezing tolerance. By contrast, the constitutive ethylene response mutant ctr1-1 and EIN3-overexpressing plants exhibited reduced freezing tolerance. Genetic and biochemical analyses revealed that EIN3 negatively regulates the expression of CBFs and type-A Arabidopsis response regulator5 (ARR5), ARR7, and ARR15 by binding to specific elements in their promoters. Overexpression of these ARR genes enhanced the freezing tolerance of plants. Thus, our study demonstrates that ethylene negatively regulates cold signaling at least partially through the direct transcriptional control of cold-regulated CBFs and type-A ARR genes by EIN3. Our study also provides evidence that type-A ARRs function as key nodes to integrate ethylene and cytokinin signaling in regulation of plant responses to environmental stress.

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Ethylene Signaling Negatively Regulates Freezing Tolerance by Repressing Expression of CBF and Type-A ARR Genes in Arabidopsis

Contents Summary I. Introduction II. Cold stress and physiological responses in plants III. Sensing of cold signals in plants IV. Messenger molecules involved in cold signal transduction V. Cold signal transduction in plants VI. Conclusions and perspectives Acknowledgements References SUMMARY: Cold stress is a major environmental factor that seriously affects plant growth and development, and influences crop productivity. Plants have evolved a series of mechanisms that allow them to adapt to cold stress at both the physiological and molecular levels. Over the past two decades, much progress has been made in identifying crucial components involved in cold-stress tolerance and dissecting their regulatory mechanisms. In this review, we summarize recent major advances in our understanding of cold signalling and put forward open questions in the field of plant cold-stress responses. Answering these questions should help elucidate the molecular mechanisms underlying plant tolerance to cold stress.

https://nph.onlinelibrary.wiley.com/doi/pdf/10.1111/nph.15696

Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants.

https://www.cell.com/trends/plant-science/pdf/S1360-1385(18)30086-4.pdf

Molecular Regulation of CBF Signaling in Cold Acclimation.

Summary
In Arabidopsis, the C-repeat binding factors (CBFs) have been extensively studied as key transcription factors in the cold stress response. However, their exact functions in the cold response remains unclear due to the lack of a null cbf triple mutant.
In this study, we used CRISPR/Cas9 technology to mutate CBF1 or CBF1/CBF2 in a cbf3 T-DNA insertion mutant to generate cbf1,3 double and cbf1 cbf2 cbf3 (cbfs) triple mutants.
The response of the cbfs triple mutants to chilling stress is impaired. Furthermore, no significant difference in freezing tolerance was observed between the wild-type and the cbf1,3 and cbfs mutants without cold acclimation. However, the cbfs mutants were extremely sensitive to freezing stress after cold acclimation, and freezing sensitivity ranking was cbfs > cbf1,3 > cbf3. RNA-Seq analysis showed that 134 genes were CBF regulated, of which 112 were regulated positively and 22 negatively by CBFs.
Our study reveals the essential functions of CBFs in chilling stress response and cold acclimation, as well as defines a set of genes as CBF regulon. It also provides materials for the genetic dissection of components in CBF-dependent cold signaling.

Yiting Shi

Papers

Plant abiotic stress response and nutrient use efficiency.

Ethylene Signaling Negatively Regulates Freezing Tolerance by Repressing Expression of CBF and Type-A ARR Genes in Arabidopsis

Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants.

Molecular Regulation of CBF Signaling in Cold Acclimation.

The cbfs triple mutants reveal the essential functions of CBFs in cold acclimation and allow the definition of CBF regulons in Arabidopsis.