Plant hormone regulation of abiotic stress responses

Abstract

Plant hormones are signalling compounds that regulate crucial aspects of growth, development and environmental stress responses. Abiotic stresses, such as drought, salinity, heat, cold and flooding, have profound effects on plant growth and survival. Adaptation and tolerance to such stresses require sophisticated sensing, signalling and stress response mechanisms. In this Review, we discuss recent advances in understanding how diverse plant hormones control abiotic stress responses in plants and highlight points of hormonal crosstalk during abiotic stress signalling. Control mechanisms and stress responses mediated by plant hormones including abscisic acid, auxin, brassinosteroids, cytokinins, ethylene and gibberellins are discussed. We discuss new insights into osmotic stress sensing and signalling mechanisms, hormonal control of gene regulation and plant development during stress, hormone-regulated submergence tolerance and stomatal movements. We further explore how innovative imaging approaches are providing insights into single-cell and tissue hormone dynamics. Understanding stress tolerance mechanisms opens new opportunities for agricultural applications.

Figure 1 |. Osmotic stress and salinity sensing and signaling in plants.

a | Mechanosensitive channels have been proposed to be involved in sensing the alterations of membrane tension caused by hypoosmotic stress and other abiotic stresses. MSL8 prevents bursting of pollen during hydration and germination. MSL10 potentiates hypoosmotic/cell swelling-induced [Ca²⁺]_cyt transient increases, ROS production, and programmed cell death. MSL1 and MSL2/3 control mitochondrial and plastidial osmotic pressure. MCA1 and MCA2 function in hypoosmotic and cold-induced [Ca²⁺]_cyt transients and regulate cold acclimation responses. Tonoplast-localized PIEZOs (PZO) are required for [Ca²⁺]_cyt oscillations in tip-growing cells, and mechanical-induced [Ca²⁺]_cyt increases in the root tip to regulate root penetration into denser barriers. b | Hyperosmotic stress-induced [Ca²⁺]_cyt increases have been reported to function in early hyperosmotic-stress signaling. OSCA1 is an osmotic/mechanical-sensitive channel required for hyperosmotic-induced [Ca²⁺]_cyt increases. Ca²⁺-responsive phospholipid-binding BONZAI (BON) proteins regulate hyperosmotic-induced [Ca²⁺]_cyt increases and suppress NLR immune signaling to trigger a hyperosmotic stress response. Drought induces ABA biosynthesis NCED3 gene expression, leading to ABA accumulation. Root-derived CLE25 peptides activate NCED3 gene expression in the shoot in response to dehydration likely through receptor-like kinases BAM1 and BAM3. NGATHA (NGA) transcription factors are responsible for the drought-induced transcriptional activation of NCED3. Hyperosmotic stress activates Raf-like M3Ks via phosphorylation through an unknown osmotic stress sensor-mediated signal transduction mechanism. Members of the B2 and B3 subgroups of Raf-like M3Ks mediate both the rapid osmotic stress-induced and slower, post-ABA synthesis, activation of SnRK2.2/2.3/2.6, whereas the B4 subgroup of Raf-like M3Ks only activate osmotic stress-responsive SnRK2.1/2.4/2.5/2.9/2.10^,–. c | A Salt-induced [Ca²⁺]_cyt increase triggers tolerance responses through the salt overly sensitive (SOS) pathway. Glycosyl inositol phosphorylceramide sphingolipids (GIPCs) synthesized by Inositol Phosphorylceramide Glucuronosyltransferase (MOCA1/IPUT1) are involved in Na⁺ sensing. The Annexin 4 (ANN4)-medicated [Ca²⁺]_cyt increase is feedback inhibited by the SOS pathway for fine-tuning salt tolerance. FERONIA (FER) is required for maintaining cell wall integrity under salt stress.

Figure 2 |. Hormonal crosstalk through transcriptional regulation.

Plant hormones control abiotic stress response by altering transcriptional programs. The ABA signaling system intersects with many other hormone pathways during transcription. This figure summarizes the relationships between ABA signaling and key transcriptional regulators during hormonal signaling. During ABA-responses, SUCROSE NONFERMENTING 1-RELATED PROTEIN KINASE 2 (SnRK2) protein kinases phosphorylate ABA-RESPONSIVE ELEMENT (ABRE)-binding proteins/ABRE-binding factors (AREBs/ABFs) and ABA-INSENSITIVE 5 (ABI5) transcription factors. AREBs/ABFs and ABI5 activate target genes with ABREs in their promotors to drive ABA responses. For instance, during drought stress AREBs/ABFs activate transcription of RESPONSE TO DESSICATION 26 (RD26), a transcription factor that can repress brassinosteroid signaling. Additionally, in dormant seeds, ABI5 target genes repress gibberellic acid (GA) biosynthesis and thereby block germination. Cytokinin signaling can repress ABA responses possibly by triggering the degradation of ABI5. ABA-activated SnRK2-type protein kinases promote transcriptional ABA responses by phosphorylating type-A ARABIDOPSIS RESPONSE REGULATOR5 (ARR5), a negative regulator of the cytokinin pathway. Finally, in unstressed conditions the protein kinase TARGET OF RAPAMYCIN (TOR) promotes plant growth by inhibiting SnRK2-type protein kinase-mediated ABA responses through phosphorylation of ABA receptors. Conversely, during stress SnRK2-type protein kinases phosphorylate and inhibit the TOR regulatory protein RAPTOR1B leading to growth repression. Note that not all mechanisms shown here are necessarily present at the same time or in the same cell/tissue.

Figure 3 |. Hormonal control of growth and development during abiotic stress.

a | ABA and GA signaling pathways antagonistically control germination. In dormant seeds, DELLA proteins and ABI5 promote ABA signaling by stimulating expression of ABA biosynthesis genes and the ABI5 gene and inhibit GA responses by repressing GA biosynthesis. INDUCER OF CBF EXPRESSION1 (ICE1) antagonizes DELLA and ABI5 activity to promote germination. During germination, GA levels increase, and GA triggers the destruction of DELLA proteins leading to decreased ABA signaling. b | Water is unevenly distributed in soil and large air pockets form between soil particles. Primary roots display hydrotropism or biased growth towards areas of higher water. This process depends on SnRK2.2 protein kinase activity in cortex cells of the elongation zone. When roots enter air spaces lateral root formation is repressed (xerobranching), a process that depends on the ABA inhibition of auxin signaling. Roots growing in areas where water is asymmetrically distributed display a growth program known as hydropatterning, where lateral roots preferentially form on the water contacting side. In hydropatterning, the auxin response factor ARF7 stimulates preferential lateral root initiation. c | During prolonged drought, plants will accelerate flowering to reproduce in a process called drought escape. Under drought stress, the ABA-activated transcription factors ABF3/4 and the floral regulator GIGANTEA (GI) stimulate expression of the flowering inducers SUPRESSOR OF OVEREXPRESSION OF CO1 (SOC1) and FLOWERING LOCUS T (FT) to advance flowering. d | Submerged plant tissues experience hypoxia and elevated ethylene gas (C₂H₄). These cues activate transcription factors known as group VII ETHYLENE RESPONSE FACTORs (ERF-VIIs). ERF-VIIs initiate a conserved hypoxia-induced transcriptional program. In deepwater rice varieties, elevated ethylene activates the ERFs SNORKEL1 and 2 (SK1/2) which induce GA biosynthesis. GA signaling promotes a flood escape strategy where stems elongate to emerge into the air.

Figure 4 |. Guard cell signal transduction and stomatal responses to environmental stimuli.

a | Schematic model of abscisic acid (ABA) signal transduction in guard cells. ABA transporters mediate ABA import or export from guard cells. In the presence of ABA, the key regulator SNF1-RELATED PROTEIN KINASE 2.6/OPEN STOMATA 1 (SnRK2.6/OST1) phosphorylates and activates SLOW ANION CHANNEL-ASSOCIATED 1 (SLAC1), ALUMINUM-ACTIVATED MALATE TRANSPORTER 12/QUICK-ACTIVATING ANION CHANNEL 1 (ALMT12/QUAC1), and RESPIRATORY BURST OXIDASE HOMOLOGs (RBOHs). Activation of the S-type anion channel SLAC1 and the R-type anion channel ALMT12/QUAC1 leads to long-term plasma membrane depolarization, which causes K⁺ efflux through the voltage-dependent K⁺_out channel GUARD CELL OUTWARD RECTIFYING K⁺ CHANNEL (GORK). Activated RBOH NADPH oxidases produce ROS that mediate HYDROGEN-PEROXIDE-INDUCED Ca²⁺ INCREASES 1 (HPCA1) sensor-dependent activation of Ca²⁺-permeable I_Ca channels, resulting in the elevation of the cytosolic Ca²⁺ concentration ([Ca²⁺]_cyt). Elevated [Ca²⁺]_cyt activates Ca²⁺-sensor proteins including Ca²⁺-DEPENDENT PROTEIN KINASEs (CPKs) that phosphorylate and activate SLAC1. The (pseudo-)kinase GUARD CELL HYDROGEN PEROXIDE-RESISTANT 1 (GHR1) mediates the activation of I_Ca and SLAC1 channels through an unknown mechanism, possibly as scaffolding protein. SnRK2.6/OST1 inhibits the K⁺_in channel K⁺ CHANNEL IN ARABIDOPSIS THALIANA 1 (KAT1), that mediates K⁺ uptake, by direct phosphorylation. In addition, SnRK2.6/OST1 causes a long-term decrease of KAT1 expression by inhibition of ABA-RESPONSIVE KINASE SUBSTRATE (AKS) transcription factors. ABA also inhibits H⁺-ATPase activity through SnRK2.6/OST1, but the detailed mechanism is unknown. Dashed lines indicate steps that are inhibited in the presence of ABA. Note that only guard cell ABA signaling regulating ion transport across the plasma membrane is depicted in this figure. b | In addition to drought stress, several other environmental stimuli can be perceived by guard cells and affect stomatal aperture though sophisticated signaling crosstalk and integration.