Plants survive by deploying appropriate stress responses under rapidly changing environmental conditions. Vascular plants transmit environmental information among distant organs. Long-distance ...signaling plays a crucial role in plant adaptation and subsequent survival under severe environmental conditions. In model plants, the micrografting method has recently emerged as an important method to elucidate tissue-to-tissue communication via hormones, RNAs, and peptides. In this chapter, I describe a micrografting method for Arabidopsis thaliana to graft shoots onto roots of plants with different genotypes. This grafting method may facilitate further research investigating how vascular plants integrate environmental information among distant organs via long-distance signaling.
SNF1-related protein kinases 2 (SnRK2s) are key regulators governing the plant adaptive responses to osmotic stresses, such as drought and high salinity. Subclass III SnRK2s function as central ...regulators of abscisic acid (ABA) signalling and orchestrate ABA-regulated adaptive responses to osmotic stresses. Seed plants have acquired other types of osmotic stress-activated but ABA-unresponsive subclass I SnRK2s that regulate mRNA decay and promote plant growth under osmotic stresses. In contrast to subclass III SnRK2s, the regulatory mechanisms underlying the rapid activation of subclass I SnRK2s in response to osmotic stress remain elusive. Here, we report that three B4 Raf-like MAP kinase kinase kinases (MAPKKKs) phosphorylate and activate subclass I SnRK2s under osmotic stress. Transcriptome analyses reveal that genes downstream of these MAPKKKs largely overlap with subclass I SnRK2-regulated genes under osmotic stress, which indicates that these MAPKKKs are upstream factors of subclass I SnRK2 and are directly activated by osmotic stress.
In plants, cold temperatures0 trigger stress responses and long-term responses that result in cold tolerance. In Arabidopsis thaliana, three dehydration-responsive element (DRE) binding protein ...1/C-repeat binding factors (DREB1/CBFs) act as master switches in cold-responsive gene expression. Induction of DREB1 genes triggers the cold stress-inducible transcriptional cascade, followed by the induction of numerous genes that function in the cold stress response and cold tolerance. Many regulatory factors involved in DREB1 induction have been identified, but how these factors orchestrate the cold stressspecific expression of DREB1s has not yet been clarified. Here, we revealed that plants recognize cold stress as two different signals, rapid and gradual temperature decreases, and induce expression of the DREB1 genes. CALMODULIN BINDING TRANSCRIPTION ACTIVATOR3 (CAMTA3) and CAMTA5 respond to a rapid decrease in temperature and induce the expression of DREB1s, but these proteins do not respond to a gradual decrease in temperature. Moreover, they function during the day and night, in contrast to some key circadian components, including CIRCADIAN CLOCK ASSOCIATED1 and LATE ELONGATED HYPOCOTYL, which regulate cold-responsive DREB1 expression as transcriptional activators only during the day. Thus, plants efficiently control the acquisition of freezing tolerance using two different signaling pathways in response to a gradual temperature decrease during seasonal changes and a sudden temperature drop during the night.
The drought stress responses of vascular plants are complex regulatory mechanisms because they include various physiological responses from signal perception under water deficit conditions to the ...acquisition of drought stress resistance at the whole-plant level. It is thought that plants first recognize water deficit conditions in roots and that several molecular signals then move from roots to shoots. Finally, a phytohormone, abscisic acid (ABA) is synthesized mainly in leaves. However, the detailed molecular mechanisms of stress sensors and the regulators that initiate ABA biosynthesis in response to drought stress conditions are still unclear. Another important issue is how plants adjust ABA propagation, stress-mediated gene expression and metabolite composition to acquire drought stress resistance in different tissues throughout the whole plant. In this review, we summarize recent advances in research on drought stress responses, focusing on long-distance signaling from roots to shoots, ABA synthesis and transport, and metabolic regulation in both cellular and whole-plant levels of Arabidopsis and crops. We also discuss coordinated mechanisms for acquiring drought stress adaptations and resistance
via
tissue-to-tissue communication and long-distance signaling.
SUMMARY
Plant response to drought stress includes systems for intracellular regulation of gene expression and signaling, as well as inter‐tissue and inter‐organ signaling, which helps entire plants ...acquire stress resistance. Plants sense water‐deficit conditions both via the stomata of leaves and roots, and transfer water‐deficit signals from roots to shoots via inter‐organ signaling. Abscisic acid is an important phytohormone involved in the drought stress response and adaptation, and is synthesized mainly in vascular tissues and guard cells of leaves. In leaves, stress‐induced abscisic acid is distributed to various tissues by transporters, which activates stomatal closure and expression of stress‐related genes to acquire drought stress resistance. Moreover, the stepwise stress response at the whole‐plant level is important for proper understanding of the physiological response to drought conditions. Drought stress is sensed by multiple types of sensors as molecular patterns of abiotic stress signals, which are transmitted via separate parallel signaling networks to induce downstream responses, including stomatal closure and synthesis of stress‐related proteins and metabolites. Peptide molecules play important roles in the inter‐organ signaling of dehydration from roots to shoots, as well as signaling of osmotic changes and reactive oxygen species/Ca2+. In this review, we have summarized recent advances in research on complex plant drought stress responses, focusing on inter‐tissue signaling in leaves and inter‐organ signaling from roots to shoots. We have discussed the mechanisms via which drought stress adaptations and resistance are acquired at the whole‐plant level, and have proposed the importance of quantitative phenotyping for measuring plant growth under drought conditions.
Significance Statement
This review focuses on inter‐tissue signaling, inter‐organ signaling, and stress sensing in complex drought stress responses and tolerance, in which molecular patterns of stress signals are sensed by different sensors and transmitted to other tissues and organs to induce stress responses in total. Recent progress in quantitative phenotyping under drought conditions is also discussed to understand the whole system of complex drought responses and tolerance.
Functional diversification of transcription factors allows the precise regulation of transcriptomic changes under different environmental conditions. The NUCLEAR FACTOR Y (NF-Y) transcription factor ...comprises three subunits, NF-YA, NF-YB, and NF-YC, and is broadly diversified in plant species, whereas Humans (
) have one protein for each subunit. However, there remains much to be learned about the diversified functions of each subunit in plants. Here, we found that NF-YB2 and NF-YB3, which have the greatest sequence similarity to each other among NF-YB family proteins in Arabidopsis (
), are functionally diversified and specifically activate dehydration-inducible and heat-inducible genes, according to environmental conditions. Overexpression of
and
specifically enhanced drought and heat stress tolerance, respectively, and each single knockout mutant showed adverse stress-sensitive phenotypes. Transcriptomic analyses confirmed that overexpression of
and
largely affected the transcriptomic changes under dehydration and heat stress conditions, respectively. The DNA-binding profiles of each protein in planta also suggested that dehydration and heat stress increased the DNA-binding activity of NF-YB2 and NF-YB3 to dehydration-inducible and heat stress-inducible target genes, respectively. Moreover, phylogenetic analysis suggested that the NF-YB proteins of angiosperm plants belong to divergent NF-YB2 and NF-YB3 subgroups. These results demonstrate the functional diversification of NF-Y through evolutionary processes and how plants adapt to various abiotic stresses under fluctuating environments.
Drought is a severe and complex abiotic stress that negatively affects plant growth and crop yields. Numerous genes with various functions are induced in response to drought stress to acquire drought ...stress tolerance. The phytohormone abscisic acid (ABA) accumulates mainly in the leaves in response to drought stress and then activates subclass III SNF1-related protein kinases 2 (SnRK2s), which are key phosphoregulators of ABA signaling. ABA mediates a wide variety of gene expression processes through stress-responsive transcription factors, including ABA-RESPONSIVE ELEMENT BINDING PROTEINS (AREBs)/ABRE-BINDING FACTORS (ABFs) and several other transcription factors. Seed plants have another type of SnRK2s, ABA-unresponsive subclass I SnRK2s, that mediates the stability of gene expression through the mRNA decay pathway and plant growth under drought stress in an ABA-independent manner. Recent research has elucidated the upstream regulators of SnRK2s, RAF-like protein kinases, involved in early responses to drought stress. ABA-independent transcriptional regulatory systems and ABA-responsive regulation function in drought-responsive gene expression. DEHYDRATION RESPONSIVE ELEMENT (DRE) is an important cis-acting element in ABA-independent transcription, whereas ABA-RESPONSIVE ELEMENT (ABRE) cis-acting element functions in ABA-responsive transcription. In this review article, we summarize recent advances in research on cellular and molecular drought stress responses and focus on phosphorylation signaling and transcription networks in
and crops. We also highlight gene networks of transcriptional regulation through two major regulatory pathways, ABA-dependent and ABA-independent pathways, that ABA-responsive subclass III SnRK2s and ABA-unresponsive subclass I SnRK2s mediate, respectively. We also discuss crosstalk in these regulatory systems under drought stress.
Plants have evolved complex systems to rapidly respond to severe stress conditions, such as heat, cold, and dehydration. Dehydration-responsive element-binding protein 2A (DREB2A) is a key ...transcriptional activator that induces many heat- and drought-responsive genes, increases tolerance to both heat and drought stress, and suppresses plant growth in Arabidopsis thaliana. DREB2A expression is induced by stress, but stabilization of the DREB2A protein in response to stress is essential for activating the expression of downstream stress-inducible genes. Under nonstress growth conditions, an integral negative regulatory domain (NRD) destabilizes DREB2A, but the mechanism by which DREB2A is stabilized in response to stress remains unclear. Here, based on bioinformatics, mutational, MS, and biochemical analyses, we report that Ser/Thr residues in the NRD are phosphorylated under nonstress growth conditions and that their phosphorylation decreases in response to heat. Furthermore, we found that this phosphorylation is likely mediated by casein kinase 1 and is essential for the NRD-dependent, proteasomal degradation of DREB2A under nonstress conditions. These observations suggest that inhibition of NRD phosphorylation stabilizes and activates DREB2A in response to heat stress to enhance plant thermotolerance. Our study reveals the molecular basis for the coordination of stress tolerance and plant growth through stress-dependent transcriptional regulation, which may allow the plants to rapidly respond to fluctuating environmental conditions.
Summary
Leaf senescence is the terminal phenotype of plant leaf development, and ethylene is a major plant hormone inducing leaf senescence. Recent studies have shown that abscisic acid (ABA) also ...induces leaf senescence. However, the detailed mechanisms of ABA‐induced leaf senescence remain unclear. We focused on the A subfamily of stress‐responsive NAC (SNAC‐A) transcription factors, the expression of which is induced by abiotic stresses, particularly ABA. Gene expression analysis revealed that seven SNAC‐A genes including ANAC055, ANAC019, ANAC072/RD26, ANAC002/ATAF1, ANAC081/ATAF2, ANAC102 and ANAC032 were induced by long‐term treatment with ABA and/or during age‐dependent senescence. The SNAC‐A septuple mutant clearly showed retardation of ABA‐inducible leaf senescence. Microarray analysis indicated that SNAC‐As induce ABA‐ and senescence‐inducible genes. In addition, comparison of the expression profiles of the downstream genes of SNAC‐As and ABA‐responsive element (ABRE)‐binding protein (AREB)/ABRE‐binding factor (ABF) (AREB/ABFs) indicates that SNAC‐As induce a different set of ABA‐inducible genes from those mediated by AREB/ABFs. These results suggest that SNAC‐As play crucial roles in ABA‐induced leaf senescence signaling. We also discuss the function of SNAC‐As in the transcriptional change of leaf senescence as well as in ABA response under abiotic stress conditions.
Significance Statement
Leaf senescence is induced by plant hormones such as ethylene and ABA, but the mechanism for ABA‐induced senescence was still unclear. Here we show that a septuple mutant of SNAC‐A type transcription factors exhibit delayed leaf senescence after ABA treatment, suggesting a critical role in transcriptional control of leaf senescence under abiotic stress.
Group A1 heat shock transcription factors (HsfA1s) are the master regulators of the heat stress response (HSR) in plants. Upon heat shock, HsfA1s trigger a transcriptional cascade that is composed of ...many transcription factors. Despite the importance of HsfA1s and their downstream transcriptional cascade in the acquisition of thermotolerance in plants, the molecular basis of their activation remains poorly understood. Here, domain analysis of HsfA1d, one of several HsfA1s in Arabidopsis thaliana, demonstrated that the central region of HsfA1d is a key regulatory domain that represses HsfA1d transactivation activity through interaction with HEAT SHOCK PROTEIN70 (HSP70) and HSP90. We designated this region as the temperature-dependent repression (TDR) domain. We found that HSP70 dissociates from HsfA1d in response to heat shock and that the dissociation is likely regulated by an as yet unknown activation mechanism, such as HsfA1d phosphorylation. Overexpression of constitutively active HsfA1d that lacked the TDR domain induced expression of heat shock proteins in the absence of heat stress, thereby conferring potent thermotolerance on the overexpressors. However, transcriptome analysis of the overexpressors demonstrated that the constitutively active HsfA1d could not trigger the complete transcriptional cascade under normal conditions, thereby indicating that other factors are necessary to fully induce the HSR. These complex regulatory mechanisms related to the transcriptional cascade may enable plants to respond resiliently to various heat stress conditions.
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