MAPKKKs in Plants: Multidimensional Regulators of Plant Growth and Stress Responses

Mitogen-activated protein kinase kinase kinase (MAPKKK, MAP3K) is located upstream of the mitogen-activated protein kinase (MAPK) cascade pathway and is responsible for receiving and transmitting external signals to the downstream MAPKKs. Although a large number of MAP3K genes play important roles in plant growth and development, and response to abiotic and biotic stresses, only a few members’ functions and cascade signaling pathways have been clarified, and the downstream MAPKKs and MAPKs of most MAP3Ks are still unknown. As more and more signaling pathways are discovered, the function and regulatory mechanism of MAP3K genes will become clearer. In this paper, the MAP3K genes in plants were classified and the members and basic characteristics of each subfamily of MAP3K were briefly described. Moreover, the roles of plant MAP3Ks in regulating plant growth and development and stress (abiotic and biotic) responses are described in detail. In addition, the roles of MAP3Ks involved in plant hormones signal transduction pathway were briefly introduced, and the future research focus was prospected.

[1]  Xiaosan Huang,et al.  Genome-wide identification of the mitogen-activated protein kinase kinase kinase (MAPKKK) in pear (Pyrus bretschneideri) and their functional analysis in response to black spot , 2022, Planta.

[2]  W. Shan,et al.  The Raf‐like kinase Raf36 negatively regulates plant resistance against the oomycete pathogen Phytophthora parasitica by targeting MKK2 , 2021, Molecular plant pathology.

[3]  Chenchen Wang,et al.  WIPK–NtLTP4 pathway confers resistance to Ralstonia solanacearum in tobacco , 2021, Plant Cell Reports.

[4]  Xianghua Li,et al.  The rice Raf-like MAPKKK OsILA1 confers broad-spectrum resistance to bacterial blight by suppressing the OsMAPKK4-OsMAPK6 cascade. , 2021, Journal of integrative plant biology.

[5]  L. Fu,et al.  Hydrogen Sulfide-linked Persulfidation of ABSCISIC INSENSITIVE 4 Controls Arabidopsis ABA Responses Through the Transactivation of Mitogen-Activated Protein Kinase Kinase Kinase 18. , 2021, Molecular plant.

[6]  C. Zheng,et al.  RING finger protein RGLG1 and RGLG2 negatively modulate MAPKKK18 mediated drought stress tolerance in Arabidopsis. , 2020, Journal of integrative plant biology.

[7]  T. Taji,et al.  Arabidopsis Raf‐like kinases act as positive regulators of subclass III SnRK2 in osmostress signaling , 2020, The Plant journal : for cell and molecular biology.

[8]  Xiyan Yang,et al.  Genome-wide identification of MAPK cascade genes reveals the GhMAP3K14–GhMKK11–GhMPK31 pathway is involved in the drought response in cotton , 2020, Plant Molecular Biology.

[9]  J. Šamaj,et al.  YODA-HSP90 module regulates phosphorylation-dependent inactivation of SPEECHLESS to control stomatal development under acute heat stress in Arabidopsis. , 2020, Molecular plant.

[10]  Zhiguo Liu,et al.  Genome-wide identification of MAPKKK genes and their responses to phytoplasma infection in Chinese jujube (Ziziphus jujuba Mill.) , 2019, BMC Genomics.

[11]  Zhiguo Liu.  Genome-wide identification of MAPKKK genes and their responses to phytoplasma infection in Chinese jujube , 2020 .

[12]  J. Carr,et al.  Inositol hexakisphosphate biosynthesis underpins PAMP‐triggered immunity to Pseudomonas syringae pv. tomato in Arabidopsis thaliana but is dispensable for establishment of systemic acquired resistance , 2019, Molecular plant pathology.

[13]  M. Yasuda,et al.  Arabidopsis MAPKKK δ-1 is required for full immunity against bacterial and fungal infection , 2019, Journal of experimental botany.

[14]  Liming Cao,et al.  OstMAPKKK5, a truncated mitogen-activated protein kinase kinase kinase 5, positively regulates plant height and yield in rice , 2019, The Crop Journal.

[15]  T. Janda,et al.  Pattern of changes in salicylic acid-induced protein kinase (SIPK) gene expression and salicylic acid accumulation in wheat under cadmium exposure. , 2019, Plant biology.

[16]  Yuelin Zhang,et al.  Antagonistic interactions between two MAP kinase cascades in plant development and immune signaling , 2018, EMBO reports.

[17]  T. Nanmori,et al.  Control of plant growth and development by overexpressing MAP3K17, an ABA-inducible MAP3K, in Arabidopsis. , 2018, Plant biotechnology.

[18]  Shuqun Zhang.  Mitogen‐Activated Protein Kinase Cascades in Plant Signaling , 2018 .

[19]  Han Li,et al.  GhMAP3K65, a Cotton Raf-Like MAP3K Gene, Enhances Susceptibility to Pathogen Infection and Heat Stress by Negatively Modulating Growth and Development in Transgenic Nicotiana benthamiana , 2017, International journal of molecular sciences.

[20]  Huasen Wang,et al.  Global Identification, Classification, and Expression Analysis of MAPKKK genes: Functional Characterization of MdRaf5 Reveals Evolution and Drought-Responsive Profile in Apple , 2017, Scientific Reports.

[21]  B. Ellis,et al.  The Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase 20 (MKKK20) Acts Upstream of MKK3 and MPK18 in Two Separate Signaling Pathways Involved in Root Microtubule Functions , 2017, Front. Plant Sci..

[22]  Yan Yan,et al.  The MAPKKK and MAPKK gene families in banana: identification, phylogeny and expression during development, ripening and abiotic stress , 2017, Scientific Reports.

[23]  Yan Yan,et al.  A Raf-like MAPKKK gene, GhRaf19, negatively regulates tolerance to drought and salt and positively regulates resistance to cold stress by modulating reactive oxygen species in cotton. , 2016, Plant science : an international journal of experimental plant biology.

[24]  Jian‐Kang Zhu.  Abiotic Stress Signaling and Responses in Plants , 2016, Cell.

[25]  H. Hirt,et al.  The Role of MAPK Modules and ABA during Abiotic Stress Signaling. , 2016, Trends in plant science.

[26]  J. Šamaj,et al.  YODA and MPK6 have critical roles in postembryonic root development , 2016 .

[27]  D. Bartels,et al.  Lipid signalling in plant responses to abiotic stress. , 2016, Plant, cell & environment.

[28]  Ji Wang,et al.  A cotton Raf-like MAP3K gene, GhMAP3K40, mediates reduced tolerance to biotic and abiotic stress in Nicotiana benthamiana by negatively regulating growth and development. , 2015, Plant science : an international journal of experimental plant biology.

[29]  René Schneider,et al.  A Mechanism for Sustained Cellulose Synthesis during Salt Stress , 2015, Cell.

[30]  Dayong Li,et al.  Arabidopsis Raf-Like Mitogen-Activated Protein Kinase Kinase Kinase Gene Raf43 Is Required for Tolerance to Multiple Abiotic Stresses , 2015, PloS one.

[31]  Jian Wu,et al.  Genome-wide identification of MAPK, MAPKK, and MAPKKK gene families and transcriptional profiling analysis during development and stress response in cucumber , 2015, BMC Genomics.

[32]  H. Hirt,et al.  Identification and characterization of an ABA-activated MAP kinase cascade in Arabidopsis thaliana. , 2015, The Plant journal : for cell and molecular biology.

[33]  Shuqun Zhang,et al.  Mitogen-activated protein kinase cascades in signaling plant growth and development. , 2015, Trends in plant science.

[34]  Jian Wu,et al.  Genome-Wide Identification of MAPKK and MAPKKK Gene Families in Tomato and Transcriptional Profiling Analysis during Development and Stress Response , 2014, PloS one.

[35]  R. M. Rivero,et al.  Abiotic and biotic stress combinations. , 2014, The New phytologist.

[36]  W. Lukowitz,et al.  EDR1 Physically Interacts with MKK4/MKK5 and Negatively Regulates a MAP Kinase Cascade to Modulate Plant Innate Immunity , 2014, PLoS genetics.

[37]  Simon Gilroy,et al.  Salt stress-induced Ca2+ waves are associated with rapid, long-distance root-to-shoot signaling in plants , 2014, Proceedings of the National Academy of Sciences.

[38]  M. Deyholos,et al.  Identification and functional analysis of mitogen-activated protein kinase kinase kinase (MAPKKK) genes in canola (Brassica napus L.) , 2014, Journal of experimental botany.

[39]  Yiping Qi,et al.  SIS8, a putative mitogen-activated protein kinase kinase kinase, regulates sugar-resistant seedling development in Arabidopsis. , 2014, The Plant journal : for cell and molecular biology.

[40]  Xiao Hui Xu,et al.  Expression analysis of genes encoding mitogen-activated protein kinases in maize provides a key link between abiotic stress signaling and plant reproduction , 2014, Functional & Integrative Genomics.

[41]  W. Ye,et al.  The MAPKKK Gene Family in Gossypium raimondii: Genome-Wide Identification, Classification and Expression Analysis , 2013, International journal of molecular sciences.

[42]  S. Cutler,et al.  Glutamate signalling via a MEKK1 kinase-dependent pathway induces changes in Arabidopsis root architecture , 2013, The Plant journal : for cell and molecular biology.

[43]  Y. Machida,et al.  Regulation of organization and function of microtubules by the mitogen‐activated protein kinase cascade during plant cytokinesis , 2012, Cytoskeleton.

[44]  Alberto Paccanaro,et al.  Exploring the evolutionary path of plant MAPK networks. , 2012, Trends in plant science.

[45]  She Chen,et al.  The MEKK1-MKK1/MKK2-MPK4 Kinase Cascade Negatively Regulates Immunity Mediated by a Mitogen-Activated Protein Kinase Kinase Kinase in Arabidopsis[C][W] , 2012, Plant Cell.

[46]  T. Nanmori,et al.  MAP3Kδ4, an Arabidopsis Raf-like MAP3K, regulates plant growth and shoot branching , 2011 .

[47]  L. Xiong,et al.  Increased Leaf Angle1, a Raf-Like MAPKKK That Interacts with a Nuclear Protein Family, Regulates Mechanical Tissue Formation in the Lamina Joint of Rice[C][W] , 2011, Plant Cell.

[48]  R. Albert,et al.  Common and Unique Elements of the Aba-regulated Transcriptome of Arabidopsis Guard Cells , 2022 .

[49]  Cai-guo Xu,et al.  OsEDR1 negatively regulates rice bacterial resistance via activation of ethylene biosynthesis. , 2011, Plant, cell & environment.

[50]  Sun-Young Lee,et al.  Arabidopsis MKKK20 is involved in osmotic stress response via regulation of MPK6 activity , 2011, Plant Cell Reports.

[51]  G. Sessa,et al.  Tomato MAPKKKε is a positive regulator of cell-death signaling networks associated with plant immunity. , 2010, The Plant journal : for cell and molecular biology.

[52]  T. Soyano,et al.  HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana , 2010, Plant & cell physiology.

[53]  Kundan Kumar,et al.  In Silico Analysis Reveals 75 Members of Mitogen-Activated Protein Kinase Kinase Kinase Gene Family in Rice , 2010, DNA research : an international journal for rapid publication of reports on genes and genomes.

[54]  L. Xiong,et al.  A Raf-Like MAPKKK Gene DSM1 Mediates Drought Resistance through Reactive Oxygen Species Scavenging in Rice1[C][W][OA] , 2009, Plant Physiology.

[55]  Andrea Pitzschke,et al.  MAPK cascade signalling networks in plant defence. , 2009, Current opinion in plant biology.

[56]  Heribert Hirt,et al.  Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. , 2008, The Biochemical journal.

[57]  G. Hause,et al.  Haplo-Insufficiency of MPK3 in MPK6 Mutant Background Uncovers a Novel Function of These Two MAPKs in Arabidopsis Ovule Development[W] , 2008, The Plant Cell Online.

[58]  C. Xiang,et al.  The genetic locus At1g73660 encodes a putative MAPKKK and negatively regulates salt tolerance in Arabidopsis , 2008, Plant Molecular Biology.

[59]  Jianhua Zhu,et al.  Cold stress regulation of gene expression in plants. , 2007, Trends in plant science.

[60]  Y. Miao,et al.  Arabidopsis MEKK1 can take a short cut: it can directly interact with senescence-related WRKY53 transcription factor on the protein level and can bind to its promoter , 2007, Plant Molecular Biology.

[61]  P. Krysan,et al.  Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. , 2007, Journal of experimental botany.

[62]  A. Nantel,et al.  Loss of ovule identity induced by overexpression of the fertilization-related kinase 2 (ScFRK2), a MAPKKK from Solanum chacoense. , 2006, Journal of experimental botany.

[63]  P. Krysan,et al.  The protein kinase genes MAP3K ɛ 1 and MAP3K ɛ 2 are required for pollen viability in Arabidopsis thaliana , 2006 .

[64]  Andrea Pitzschke,et al.  Emerging MAP kinase pathways in plant stress signalling. , 2005, Trends in plant science.

[65]  H. Madhani,et al.  Principles of MAP kinase signaling specificity in Saccharomyces cerevisiae. , 2004, Annual review of genetics.

[66]  G. Martin,et al.  MAPKKKα is a positive regulator of cell death associated with both plant immunity and disease , 2004, The EMBO journal.

[67]  K. Shinozaki,et al.  The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. , 2004, Molecular cell.

[68]  H. Hirt,et al.  OMTK1, a Novel MAPKKK, Channels Oxidative Stress Signaling through Direct MAPK Interaction* , 2004, Journal of Biological Chemistry.

[69]  D. Anderson,et al.  Molecular cloning and expression of a MAP kinase homologue from pea , 1993, Plant Molecular Biology.

[70]  J. Kieber,et al.  Localization of the Raf-like Kinase CTR1 to the Endoplasmic Reticulum of Arabidopsis through Participation in Ethylene Receptor Signaling Complexes* , 2003, Journal of Biological Chemistry.

[71]  T. Mizuno,et al.  Cell autonomous circadian waves of the APRR1/TOC1 quintet in an established cell line of Arabidopsis thaliana. , 2003, Plant & cell physiology.

[72]  H. Hirt,et al.  Complexity, cross talk and integration of plant MAP kinase signalling. , 2002, Current opinion in plant biology.

[73]  M. Axtell,et al.  NPK1, an MEKK1-like mitogen-activated protein kinase kinase kinase, regulates innate immunity and development in plants. , 2002, Developmental cell.

[74]  Kazuo Shinozaki,et al.  Mitogen-activated protein kinase cascades in plants: a new nomenclature. , 2002, Trends in plant science.

[75]  M. Sussman,et al.  An Arabidopsis Mitogen-Activated Protein Kinase Kinase Kinase Gene Family Encodes Essential Positive Regulators of Cytokinesis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.001164. , 2002, The Plant Cell Online.

[76]  F. Ausubel,et al.  MAP kinase signalling cascade in Arabidopsis innate immunity , 2002, Nature.

[77]  Takeshi Mizuno,et al.  Compilation and Characterization of a Novel WNK Family of Protein Kinases in Arabiodpsis thaliana with Reference to Circadian Rhythms , 2002, Bioscience, biotechnology, and biochemistry.

[78]  Jian-Kang Zhu,et al.  Salt and drought stress signal transduction in plants. , 2002, Annual review of plant biology.

[79]  D. Scheel,et al.  Signal transmission in the plant immune response. , 2001, Trends in plant science.

[80]  P. Morris.  MAP kinase signal transduction pathways in plants. , 2001, The New phytologist.

[81]  Jonathan D. G. Jones,et al.  Plant pathogens and integrated defence responses to infection , 2001, Nature.

[82]  T. Meindl,et al.  The Bacterial Elicitor Flagellin Activates Its Receptor in Tomato Cells According to the Address–Message Concept , 2000, Plant Cell.

[83]  R. Nishihama,et al.  The MAP kinase cascade that includes MAPKKK-related protein kinase NPK1 controls a mitotic proces in plant cells. , 2000, Results and problems in cell differentiation.

[84]  D. Hardie.  PLANT PROTEIN SERINE/THREONINE KINASES: Classification and Functions. , 1999, Annual review of plant physiology and plant molecular biology.

[85]  T. Boller,et al.  Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. , 1999, The Plant journal : for cell and molecular biology.

[86]  T. Hunter,et al.  The protein kinases of budding yeast: six score and more. , 1997, Trends in biochemical sciences.

[87]  K. Irie,et al.  NPK1, a tobacco gene that encodes a protein with a domain homologous to yeast BCK1, STE11, and Byr2 protein kinases , 1993, Molecular and cellular biology.

[88]  T. Jacobs,et al.  MsERK1: a mitogen-activated protein kinase from a flowering plant. , 1993, The Plant cell.