Nature Reviews: Plant Hormone Regulation in Abiotic stresss Responses

Abiotic stress, such as drought, salt, heat, cold, and flooding, exert profound effects on plant growth and survival. To adapt and survive, plants have developed intricate sensing, signaling, and stress response mechanisms. On May 6, 2022, the journal Nature Reviews Molecular Cell Biology published a review article titled "Plant hormone regulation of abiotic stress responses," authored by Professor Julian Schroeder from the University of California, a member of the National Academy of Sciences USA and the German Academy of Sciences. This comprehensive review delves into the latest advancements in understanding how various plant hormones regulate responses to abiotic stresss and underscores the crucial interactions between these hormones during abiotic stresss signal transduction.




The review comprehensively outline how plant hormones, alongside other signaling compounds, mediate plant responses to Abiotic stresss, including drought, osmotic stress, and flooding mechanisms.


1. Osmotic Stress Induction and Signaling Pathways

Plants have evolved adaptation mechanisms to cope with osmotic stress. These mechanisms involve the regulation of cell osmotic concentration, stomatal movement, and overall plant development through both ABA-dependent and ABA-independent pathways.


(1) Osmotic and Salt Stress Induction Mechanisms

Calcium signaling is considered pivotal in osmotic stress induction, as the cytosolic free calcium concentration ([Ca2+]cyt) in plant cells rapidly and transiently increases upon exposure to osmotic stress. Recent studies have highlighted the importance of OSCA1 as a potential osmotic pressure sensor and the positive regulatory role of the BON protein in osmotic stress responses. Notably, SnRK2-type protein kinases remain activated in the absence of OSCA and BON mutants, indicating additional osmotic stress sensing and signaling mechanisms.


(2) Osmotic Stress-Induced ABA Biosynthesis

Exposure to water-deficient environments for approximately 2.5-6 hours leads to an increase in endogenous ABA concentration. Stress induces the expression of NCED3, an enzyme catalyzing the rate-limiting step of ABA biosynthesis. To respond to root water deficit, water potential signals contribute to rapid ABA biosynthesis and stomatal closure in Arabidopsis leaves. Additionally, the peptide CLE25 is induced in the root stele during drought stress and moves to above-ground tissues to induce NCED3 expression.


(3) Emerging Roles of Raf-like M3K

A fast osmotic stress signal transduction pathway, independent of ABA, converges at the activation of SnRK2 protein kinases. Among the ten SnRK2 genes in Arabidopsis, SnRK2.9 is the exception, remaining inactive during osmotic stress, while SnRK2.2, SnRK2.3, and SnRK2.6 are significantly activated by ABA. Recent research indicates that Raf-like M3K kinases play a crucial role in the rapid activation of SnRK2 during osmotic stress, distinct from ABA-induced activation.




2. Gene Regulation Under Abiotic stresss

ABA-Mediated Transcriptional Regulation and Hormone Crosstalk

ABA-responsive elements (ABREs) in gene promoters are crucial for drought-induced gene expression. Transcription factors like AREB/ABF family members and ABI5 play key roles in ABA signal transduction. In the absence of abiotic stress, different hormone pathways interact to control various aspects of plant activities, indicating complex crosstalk. For example, ABA-induced transcription factor RD26 inhibits certain jasmonic acid-induced genes, and jasmonic acid-activated transcription factors suppress RD26 expression, revealing antagonistic crosstalk between ABA and jasmonic acid signals in drought stress response. Phosphorylation of ARR5 by SnRK2 negatively regulates the cytokinin signaling pathway, promoting protein stability and downregulating cytokinin responses during drought stress. Conversely, cytokinins trigger the degradation of ABI5 to promote seed germination. Furthermore, dehydration induces the expression of IAA5 and IAA19, suggesting that auxin responses are suppressed during drought stress.


3. Growth Regulation Under Abiotic stresss

(1) Interaction Between TOR and Abiotic stresss:

TOR (Target of Rapamycin) serves as a central regulator of development and metabolism in plants. Cross-regulation occurs between the ABA pathway and the TOR pathway, coordinating plant growth and Abiotic stresss responses. Under normal conditions, TOR phosphorylates PYL/RCAR to inhibit ABA signaling and promote growth. Conversely, under abiotic stresss conditions, ABA-activated SnRK2 kinases phosphorylate RAPTOR1B, inhibiting TOR kinase activity and suppressing growth.Hormonal_control_of_growth_and_development_during_abiotic_stress.

(2) Gibberellins, ABA, and Germination Determinants

Regulation of seed germination is vital for seedling survival in changing environmental conditions. During the process of seed maturation, a network of transcription factors, including ABI3, ABI4, and ABI5, regulated by ABA, orchestrates the induction of genes necessary for seed desiccation and ABA biosynthesis while concurrently suppressing genes related to gibberellin biosynthesis. Environmental cues such as cold and light act as signals to initiate seed dormancy release by shifting the hormonal equilibrium towards gibberellins. Moreover, the regulation of ABI5 expression emerges as a pivotal control point in modulating a range of environmental signals during germination. High salinity, on the other hand, hinders seed germination, with AGL21 and RSM1 transcription factors likely playing a role by intensifying ABI5 expression during exposure to NaCl.


(3) Growth Hormones, ABA, and Root Growth under Stress

While high concentrations of exogenous ABA hinder root growth, lower concentrations in the nanomolar range stimulate primary root growth. ABA-deficient mutants exhibit compromised hydrotropism, and ABA accumulation in root tissues occurs during water stress. Furthermore, for hydrotropism to take place, SnRK2.2 is indispensable for the cell elongation necessary to promote differential growth. In contrast, in high-salinity environments, lateral roots experience prolonged growth inhibition, necessitating ABA signaling in the endodermis.


(4) Gibberellins, ABA, and Ethylene in abiotic stress-Mediated Flowering

During extended periods of drought, many plant species accelerate their transition to the flowering stage to reproduce before succumbing to the adverse conditions, a phenomenon known as drought escape. Under long-day conditions, mutants with compromised ABA biosynthesis exhibit delayed flowering, while hypersensitive pp2c triple mutants show early flowering. In contrast to drought stress, salt stress delays flowering in Arabidopsis, and ethylene is implicated in this delay. Salt stress induces the expression of genes involved in ethylene biosynthesis, leading to ethylene accumulation. Although the underlying mechanisms remain somewhat unclear, ethylene interferes with gibberellin signaling, resulting in the accumulation of DELLA proteins. Subsequently, DELLA proteins can delay flowering by inhibiting the flowering-promoting transcription factor CONSTANS.


(5) Ethylene and Gibberellins Control Flooding Responses

The submergence of plant tissues impedes their access to O2 and CO2, severely disrupting metabolic processes. Moreover, restricted gas diffusion underwater leads to the accumulation of ethylene in submerged plant tissues. In rice, ethylene accumulates in submerged stem and leaf tissues, and this heightened ethylene concentration induces the expression of ERFs SNORKEL1 and SNORKEL2. These ERFs stimulate stem elongation by promoting gibberellin biosynthesis. Recent research also suggests that compacted soil can lead to ethylene accumulation in roots, inhibiting further growth, highlighting the elevated ethylene levels as a common and early signal for plants to adapt to hypoxic stress during growth.


4. Regulation of Stomatal Movement

(1) Stomatal Response to Drought Stress

00001. Drought stress triggers ABA synthesis in vascular tissues and guard cells. ABA signaling in guard cells regulates plasma membrane ion channels, leading to the long-term efflux of anions and K+, resulting in stomatal closure. The protein kinase SnRK2.6 plays a pivotal role as a positive regulator of ABA signaling in guard cells. SnRK2.6/OST1 phosphorylates and activates SLAC1 and ALMT12/QUAC1. A group of PP2C proteins serves as negative regulators of ABA signaling, dephosphorylating SnRK2.6/OST1 and inactivating SLAC1. ABA can induce an increase in cytoplasmic [Ca2+] in guard cells, potentially mediated by plasma membrane Ca2+ influx through hyperpolarization-activated Ca2+-permeable cationic ICa channels. Initially, SnRK2.6/OST1 triggers the production of extracellular reactive oxygen species. Reactive oxygen species, in turn, activate ICa channels in the plasma membrane through the hydrogen peroxide sensor kinases HPCA1 and GHR1.


(2) Integration of Non-biological Signals in Guard Cells

Guard cells possess the capability to perceive and integrate a myriad of environmental stimuli. Among these, light and CO2 emerge as major non-biological factors governing stomatal aperture. Light-induced stomatal opening is mediated by the activation of H+-ATPase and subsequent K+ uptake, facilitated by voltage-dependent inward-rectifying K+ (K+ in) channels in the guard cell plasma membrane. ABA inhibits light-induced stomatal opening by suppressing H+-ATPase and K+ uptake. High CO2 concentrations induce stomatal closure, while low CO2 concentrations induce stomatal opening. Stomatal closure mediated by high CO2 concentrations is rapid and reversible.


5. Monitoring Hormone Responses in Plants

To gain insights into the process of plant hormone signal transduction during abiotic stress, it is crucial to ascertain the specific stress conditions, cellular types or tissues, and temporal dynamics in which plant hormone responses manifest. Genetically encoded plant hormone indicators serve as remarkable biological sensors capable of monitoring cellular hormone responses with remarkable spatiotemporal precision across various levels within the organism. Up to this point, only ABA indicators, namely ABACUS1-2µ and ABAleon, based on Förster resonance energy transfer (FRET), have been employed in studies associated with abiotic stress. Furthermore, as a complementary tool to direct ABA indicators, FRET-based SNACS reporters track the activity of downstream SnRK2-type protein kinases.


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