YODA-HSP90 Module Regulates Phosphorylation-Dependent Inactivation of SPEECHLESS to Control Stomatal Development under Acute Heat Stress in Arabidopsis

Samakovli, Despina; Tichá, Tereza; Vavrdová, Tereza; Ovečka, Miroslav; Luptovčiak, Ivan; Zapletalová, Veronika; Kuchařová, Anna; Křenek, Pavel; Krasylenko, Yuliya; Margaritopoulou, Theoni; Roka, Loukia; Milioni, Dimitra; Komis, George; Hatzopoulos, Polydefkis; Šamaj, Jozef

doi:10.1016/j.molp.2020.01.001

Cited by 73 publications

(55 citation statements)

References 79 publications

(25 reference statements)

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“…Notably, among the upregulated DEGs in tomato AtCA-YDA lines, there is a relevant number of genes that belongs to a functional category related with translation and protein folding (38.6% of genes), suggesting that the constitutive expression of AtCA-YDA might have an impact on cells reprograming for efficient protein translation. These data might support a function of YDA in the control of translation initiation in plants under biotic stress conditions, as it has been recently described for heat stress through YDA interaction with HSP90.1 protein ( Samakovli et al, 2020 ). The transcriptional reprograming observed in tomato AtCA-YDA lines would explain the enhanced disease resistance observed in the transgenic tomato lines.…”

Section: Discussionsupporting

confidence: 83%

YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

et al. 2020

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Mitogen-activated protein kinases (MAPK) play pivotal roles in transducing developmental cues and environmental signals into cellular responses through pathways initiated by MAPK kinase kinases (MAP3K). AtYODA is a MAP3K of Arabidopsis thaliana that controls stomatal development and non-canonical immune responses. Arabidopsis plants overexpressing a constitutively active YODA protein ( AtCA-YDA ) show broad-spectrum disease resistance and constitutive expression of defensive genes. We tested YDA function in crops immunity by heterologously overexpressing AtCA-YDA in Solanum lycopersicum . We found that these tomato AtCA-YDA plants do not show developmental phenotypes and fitness alterations, except a reduction in stomatal index, as reported in Arabidopsis AtCA-YDA plants. Notably, AtCA-YDA tomato plants show enhanced resistance to the bacterial pathogen Pseudomonas syringae pv. tomato DC3000 and constitutive upregulation of defense-associated genes, corroborating the functionality of YDA in tomato immunity. This function was further supported by generating CRISPR/Cas9-edited tomato mutants impaired in the closest orthologs of AtYDA [ Solyc08g081210 ( SlYDA1 ) and Solyc03g025360 ( SlYDA2 )]. Slyda1 and Slyda2 mutants are highly susceptible to P. syringae pv. tomato DC3000 in comparison to wild-type plants but only Slyda2 shows altered stomatal index. These results indicate that tomato orthologs have specialized functions and support that YDA also regulates immune responses in tomato and may be a trait for breeding disease resistance.

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Section: Discussionsupporting

confidence: 83%

YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

et al. 2020

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“…KIN10 interacts with SPCH in vivo and in vitro. SPCH is a master regulator of stomatal development downstream of a wide range of environmental and hormonal signals [6][7][8][9] . We found that sucrose treatment and overexpression of KIN10 both resulted in the increased levels of SPCH ( Figs.…”

Section: Resultsmentioning

confidence: 99%

“…The prime regulator linked to the initiation and proliferation of stomatal precursors is the basic helix-loop-helix transcription factor SPEECHLESS (SPCH), which controls hundreds of downstream genes to promote cell division and fate transitions 4,5 . SPCH also integrates a wide range of environmental and hormonal signals to regulate stomatal development [6][7][8][9] .…”

mentioning

confidence: 99%

KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor

Han

Liu

et al. 2020

Nat Commun

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Stomata are epidermal structures that modulate gas exchanges between plants and the atmosphere. The formation of stomata is regulated by multiple developmental and environmental signals, but how these signals are coordinated to control this process remains unclear. Here, we showed that the conserved energy sensor kinase SnRK1 promotes stomatal development under short-day photoperiod or in liquid culture conditions. Mutation of KIN10, the catalytic α-subunit of SnRK1, results in the decreased stomatal index; while overexpression of KIN10 significantly induces stomatal development. KIN10 displays the cell-typespecific subcellular location pattern. The nuclear-localized KIN10 proteins are highly enriched in the stomatal lineage cells to phosphorylate and stabilize SPEECHLESS, a master regulator of stomatal formation, thereby promoting stomatal development. Our work identifies a module links connecting the energy signaling and stomatal development and reveals that multiple regulatory mechanisms are in place for SnRK1 to modulate stomatal development in response to changing environments.

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“…During heat-induced senescence, leaf cells undergo a series of cellular changes including reactive oxygen species (ROS) accumulation, photosynthetic apparatus impairment and cell death (Cui et al 2020;Ivanov et al 2017;Lee et al 2014). Accordingly, plants have developed complex biochemical regulatory mechanisms to response and adapt to heat stress (Samakovli et al 2020;Li et al 2020;Wu et al 2018). However, the underlying genetic and molecular mechanisms are largely unknown.…”

Section: Resultsmentioning

confidence: 99%

Premature Senescence Leaf 50 Promotes Heat Stress Tolerance in Rice (Oryza Sativa L.)

Zhang

Shí

et al. 2020

Preprint

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BackgroundHeat stress is a major environmental factor that could induce premature leaf senescence in plants. So far, few rice premature senescent leaf mutants have been reported to involve in heat tolerance.FindingsWe identified a premature senescence leaf 50 (psl50) mutant that exhibited a higher heat susceptibility with decreased survival rate, over-accumulated hydrogen peroxide (H2O2) content and increased cell death under heat stress compared with the wild-type. The causal gene PREMATURE SENESCENCE LEAF 50 (PSL50) was isolated by using initial map-based resequencing (IMBR) approach, and we found that PSL50 promoted heat tolerance probably by acting as a modulator of H2O2 signaling in response to heat stress in rice (Oryza sativa L.).ConclusionsPSL50 negatively regulates heat-induced premature leaf senescence in rice.

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YODA-HSP90 Module Regulates Phosphorylation-Dependent Inactivation of SPEECHLESS to Control Stomatal Development under Acute Heat Stress in Arabidopsis

Abstract: Stomatal ontogenesis is a key element of plant adaptation aiming to control photosynthetic efficiency and water management under fluctuating environments 1,2,3 . Development of stomata is guided by endogenous and environmental cues and is tightly coupled to overall plant growth 1,2,3 .

Cited by 73 publications

References 79 publications

YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

YODA Kinase Controls a Novel Immune Pathway of Tomato Conferring Enhanced Disease Resistance to the Bacterium Pseudomonas syringae

KIN10 promotes stomatal development through stabilization of the SPEECHLESS transcription factor

Premature Senescence Leaf 50 Promotes Heat Stress Tolerance in Rice (Oryza Sativa L.)

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