The OPEN STOMATA1–SPIRAL1 module regulates microtubule stability during abscisic acid-induced stomatal closure in Arabidopsis

Abstract

Drought stress triggers abscisic acid (ABA) signaling in guard cells and induces stomatal closure to prevent water loss in land plants. Stomatal movement is accompanied by reorganization of the cytoskeleton. Cortical microtubules disassemble in response to ABA, which is required for stomatal closure. However, how ABA signaling regulates microtubule disassembly is unclear, and the microtubule-associated proteins (MAPs) involved in this process remain to be identified. In this study, we show that OPEN STOMATA 1 (OST1), a central component in ABA signaling, mediates microtubule disassembly during ABA-induced stomatal closure in Arabidopsis thaliana. We identified the MAP SPIRAL1 (SPR1) as the substrate of OST1. OST1 interacts with and phosphorylates SPR1 at Ser6, which promotes the disassociation of SPR1 from microtubules and facilitates microtubule disassembly. Compared to the wild type, the spr1 mutant exhibited significantly greater water loss and reduced ABA responses, including stomatal closure and microtubule disassembly in guard cells. These phenotypes were restored by introducing the phosphorylated active form of SPR1. Our findings demonstrate that SPR1 positively regulate microtubule disassembly during ABA-induced stomatal closure, which depends on OST1-mediated phosphorylation. These findings reveal a specific connection between a core component of ABA signaling and MAPs.

Time for a drought experiment: Do you know your plants’ water status?

“…Later experiments where soil water content was monitored and controlled found that chiq1-1 had reduced water usage because of its small size but did not differ in tolerance compared with the wild-type when both were exposed to the same severity of soil drying ( Ginzburg et al, 2022 ). Another example of the avoidance of water loss phenomenon is provided in this issue by Wang et al (2023) , who describe a component in ABA signaling, SPIRAL1 (SPR1), that mediates microtubule disassembly during ABA-induced stomatal closure in Arabidopsis. When subjected to water withholding experiments, spr1 mutant plants failed to close their stomata and therefore exhibited significantly greater water loss and lower survivability than the wild-type after a fixed time of water withholding.…”

Genome-Wide Identification, Characterization, and Expression Analysis of SPIRAL1 Family Genes in Legume Species

“…For instance, cortical MTs, which are anchored to the inner surface of a plasma membrane during interphase, played an important role in defining the final shape of differentiated plant cells by guiding cellulose microfibril deposition and controlling anisotropic cell expansion [ 2 , 3 , 4 , 5 , 6 , 7 , 8 ]. Similar to other eukaryotes, the structure of plant MTs is modulated not only by various developmental cues, but also by environmental signals and stress conditions [ 9 , 10 , 11 ]. Rearrangement of cortical MT arrays has been observed after pathogen attack or exposure to extreme temperature, dehydration, and hyper salinity, indicating the great importance of MTs in biotic and abiotic stresses [ 12 , 13 , 14 , 15 , 16 , 17 ].…”

“…The six SPR1 family genes in A. thaliana share high sequence similarity in the N- and C-terminal regions, and they act redundantly in maintaining anisotropic growth in rapidly elongating cells [ 18 ]. In addition to its roles in regulating plant development, SPR1 also plays a key role in the response to abiotic stress-induced MT disassembly [ 10 , 11 ]. SPR1 is degraded by the 26S proteasome, and its degradation rate is accelerated in response to salt stress, thus facilitating MT disassembly and new MT network formation for better survival in high salinity conditions [ 11 ].…”

Focus on climate change and plant abiotic stress biology

“… Lorenzo et al (2023) present a gene discovery pipeline in maize called BREEDIT, combining multiplex genome editing of whole gene families with crossing schemes to improve complex traits such as yield and drought tolerance. Two articles report on proteins that function in guard cells, one related to abscisic acid (ABA)-activated Ca 2+ signaling ( Tan et al, 2023 ) and the second describing a module that regulates microtubule disassembly ( Wang et al, 2023 ). Both of these articles highlight the critical role of stomatal regulation in controlling water loss, which is important both to avoid dehydration and also as a key determinant of water use efficiency (amount of water lost per amount of biomass gained).…”

“… Tan et al (2023) show that multiple CYCLIC NUCLEOTIDE-GATED CHANNEL proteins act as ABA-activated Ca 2+ channels essential for ABA regulation of cytosolic Ca2 + signaling and stomatal closure in Arabidopsis. Wang et al (2023) report that another central component in ABA signaling, the SNF-Related Kinase OPEN STOMATA1 (OST1/SnRK2.6), regulates microtubule disassembly through direct phosphorylation of the plant-specific microtubule-associated protein SPIRAL1 during ABA-induced stomatal closure. Another two articles describe new aspects of the salt overly sensitive (SOS) pathway, which is well-known to be a critical determinant of salt tolerance.…”