The cysteine-rich receptor-like kinase CRK4 contributes to the different drought stress response between Columbia and Landsberg erecta.

The natural variation between Arabidopsis (Arabidopsis thaliana) ecotypes Columbia (Col) and Landsberg erecta (Ler) strongly affects abscisic acid (ABA) signalling and drought tolerance. Here, we report that the cysteine-rich receptor-like protein kinase CRK4 is involved in regulating ABA signalling, which contributes to the differences in drought stress tolerance between Col-0 and Ler-0. Loss-of-function crk4 mutants in the Col-0 background were less drought tolerant than Col-0, whereas overexpressing CRK4 in the Ler-0 background partially to completely restored the drought-sensitive phenotype of Ler-0. F1 plants derived from a cross between the crk4 mutant and Ler-0 showed an ABA-insensitive phenotype with respect to stomatal movement, along with reduced drought tolerance like Ler-0. We demonstrate that CRK4 interacts with the U-box E3 ligase PUB13 and enhances its abundance, thus promoting the degradation of ABA-INSENSITIVE 1 (ABI1), a negative regulator of ABA signalling. Together, these findings reveal an important regulatory mechanism for modulating ABI1 levels by the CRK4-PUB13 module to fine-tune drought tolerance in Arabidopsis.

[1]  S. Karpiński,et al.  The CRK5 and WRKY53 Are Conditional Regulators of Senescence and Stomatal Conductance in Arabidopsis , 2022, Cells.

[2]  Jun Zhao,et al.  CYSTEINE-RICH RECEPTOR-LIKE KINASE5 (CRK5) and CRK22 regulate the response to Verticillium dahliae toxins. , 2022, Plant physiology.

[3]  H. Lee,et al.  Enhanced nitrate reductase activity offers Arabidopsis ecotype Landsberg erecta better salt stress resistance than Col-0. , 2022, Plant biology.

[4]  Zengyan Zhang,et al.  The cysteine-rich receptor-like kinase TaCRK3 contributes to defense against Rhizoctonia cerealis in wheat. , 2021, Journal of experimental botany.

[5]  M. Ishiura,et al.  Circadian clock in Arabidopsis thaliana determines flower opening time early in the morning and dominantly closes early in the afternoon. , 2021, Plant & cell physiology.

[6]  S. de Folter,et al.  Arabidopsis cysteine-rich receptor-like protein kinase CRK33 affects stomatal density and drought tolerance , 2021, Plant signaling & behavior.

[7]  Baoshan Wang,et al.  Arabidopsis U-box E3 ubiquitin ligase PUB11 negatively regulates drought tolerance by degrading the receptor-like protein kinases LRR1 and KIN7. , 2020, Journal of integrative plant biology.

[8]  Shan-Shan Zhao,et al.  The Anaerobic Product Ethanol Promotes Autophagy-Dependent Submergence Tolerance in Arabidopsis , 2020, International journal of molecular sciences.

[9]  M. Martin-Magniette,et al.  Landscape of the Noncoding Transcriptome Response of Two Arabidopsis Ecotypes to Phosphate Starvation1 , 2020, Plant Physiology.

[10]  Zhikang Li,et al.  A U-box E3 ubiquitin ligase OsPUB67 is positively involved in drought tolerance in rice , 2019, Plant Molecular Biology.

[11]  Jian-Min Zhou,et al.  PUB25 and PUB26 Promote Plant Freezing Tolerance by Degrading the Cold Signaling Negative Regulator MYB15. , 2019, Developmental cell.

[12]  M. Toyota,et al.  CRK2 Enhances Salt Tolerance by Regulating Callose Deposition in Connection with PLDα11[OPEN] , 2019, Plant Physiology.

[13]  D. Bar-Zvi,et al.  Overexpression of Arabidopsis ubiquitin ligase AtPUB46 enhances tolerance to drought and oxidative stress , 2018, bioRxiv.

[14]  Xiangzong Meng,et al.  The Monocot-Specific Receptor-like Kinase SDS2 Controls Cell Death and Immunity in Rice. , 2018, Cell host & microbe.

[15]  Honghui Lin,et al.  Transcription factor HAT1 is a substrate of SnRK2.3 kinase and negatively regulates ABA synthesis and signaling in Arabidopsis responding to drought , 2018, PLoS genetics.

[16]  Xiangzong Meng,et al.  Regulation of Arabidopsis brassinosteroid receptor BRI1 endocytosis and degradation by plant U-box PUB12/PUB13-mediated ubiquitination , 2018, Proceedings of the National Academy of Sciences.

[17]  L. Herrera-Estrella,et al.  The karrikin receptor KAI2 promotes drought resistance in Arabidopsis thaliana , 2017, PLoS genetics.

[18]  G. Stacey,et al.  Arabidopsis E3 ubiquitin ligase PLANT U-BOX13 (PUB13) regulates chitin receptor LYSIN MOTIF RECEPTOR KINASE5 (LYK5) protein abundance. , 2017, The New phytologist.

[19]  P. He,et al.  A Cysteine-Rich Protein Kinase Associates with a Membrane Immune Complex and the Cysteine Residues Are Required for Cell Death1[OPEN] , 2016, Plant Physiology.

[20]  Da-Peng Zhang,et al.  Overexpression of an Arabidopsis cysteine-rich receptor-like protein kinase, CRK5, enhances abscisic acid sensitivity and confers drought tolerance , 2016, Journal of experimental botany.

[21]  Wei Zhang,et al.  THI1, a Thiamine Thiazole Synthase, Interacts with Ca2+-Dependent Protein Kinase CPK33 and Modulates the S-Type Anion Channels and Stomatal Closure in Arabidopsis1[OPEN] , 2015, Plant Physiology.

[22]  Xiaofeng Cao,et al.  New players in ABA signaling: identification of PUB12/13 involved in degradation of ABA co-receptor ABI1 , 2015, Science China Life Sciences.

[23]  Jigang Li,et al.  Degradation of the ABA co-receptor ABI1 by PUB12/13 U-box E3 ligases , 2015, Nature Communications.

[24]  Jarkko Salojärvi,et al.  Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress , 2015, PLoS genetics.

[25]  N. Chua,et al.  PLANT U-BOX PROTEIN10 Regulates MYC2 Stability in Arabidopsis , 2015, Plant Cell.

[26]  L. Zimmerli,et al.  Enhanced Arabidopsis pattern-triggered immunity by overexpression of cysteine-rich receptor-like kinases , 2015, Front. Plant Sci..

[27]  Dongping Lu,et al.  The dominant negative ARM domain uncovers multiple functions of PUB13 in Arabidopsis immunity, flowering, and senescence , 2015, Journal of experimental botany.

[28]  Y. Miao,et al.  Behind the scenes: the roles of reactive oxygen species in guard cells. , 2014, The New phytologist.

[29]  A. Molina,et al.  Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs , 2013, Front. Plant Sci..

[30]  B. Thomas,et al.  Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. , 2013, Plant, cell & environment.

[31]  Wenzhi Lan,et al.  ABA signaling in guard cells entails a dynamic protein-protein interaction relay from the PYL-RCAR family receptors to ion channels. , 2013, Molecular plant.

[32]  W. Kim,et al.  Roles of Four Arabidopsis U-Box E3 Ubiquitin Ligases in Negative Regulation of Abscisic Acid-Mediated Drought Stress Responses1[C][W][OA] , 2012, Plant Physiology.

[33]  Hong Ma,et al.  Analysis of Arabidopsis genome-wide variations before and after meiosis and meiotic recombination by resequencing Landsberg erecta and all four products of a single meiosis. , 2012, Genome research.

[34]  Jian-Min Zhou,et al.  The U-Box/ARM E3 Ligase PUB13 Regulates Cell Death, Defense, and Flowering Time in Arabidopsis1[C][W][OA] , 2012, Plant Physiology.

[35]  M. J. Chalmers,et al.  Molecular Mimicry Regulates ABA Signaling by SnRK2 Kinases and PP2C Phosphatases , 2012, Science.

[36]  P. He,et al.  Direct Ubiquitination of Pattern Recognition Receptor FLS2 Attenuates Plant Innate Immunity , 2011, Science.

[37]  K. Shinozaki,et al.  Analysis of Cytokinin Mutants and Regulation of Cytokinin Metabolic Genes Reveals Important Regulatory Roles of Cytokinins in Drought, Salt and Abscisic Acid Responses, and Abscisic Acid Biosynthesis[C][W] , 2011, Plant Cell.

[38]  Q. Xie,et al.  AtPUB19, a U-Box E3 Ubiquitin Ligase, Negatively Regulates Abscisic Acid and Drought Responses in Arabidopsis thaliana , 2011, Molecular plant.

[39]  Wenzhi Lan,et al.  A protein kinase-phosphatase pair interacts with an ion channel to regulate ABA signaling in plant guard cells , 2009, Proceedings of the National Academy of Sciences.

[40]  Y. Fujita,et al.  Structural basis of abscisic acid signalling , 2009, Nature.

[41]  E. Grill,et al.  Regulators of PP2C Phosphatase Activity Function as Abscisic Acid Sensors , 2009, Science.

[42]  Zhen Su,et al.  DWARF27, an Iron-Containing Protein Required for the Biosynthesis of Strigolactones, Regulates Rice Tiller Bud Outgrowth[W][OA] , 2009, The Plant Cell Online.

[43]  L. Du,et al.  Activation of hypersensitive cell death by pathogen-induced receptor-like protein kinases from Arabidopsis , 2004, Plant Molecular Biology.

[44]  M. Koornneef,et al.  Naturally occurring genetic variation in Arabidopsis thaliana. , 2004, Annual review of plant biology.

[45]  Julian I. Schroeder,et al.  Guard cell abscisic acid signalling and engineering drought hardiness in plants , 2001, Nature.

[46]  J. Salojärvi,et al.  Open Access Research Article Transcriptional Regulation of the Crk/duf26 Group of Receptor-like Protein Kinases by Ozone and Plant Hormones in Arabidopsis , 2022 .