A Positive Feedback Loop Governed by SUB1A1 Interaction with MITOGEN-ACTIVATED PROTEIN KINASE3 Imparts Submergence Tolerance in Rice

Under inundation of rice, the SUB1A1 gene is subject to posttranslational regulation by a mitogen-activated protein kinase, MPK3. Mitogen-activated protein kinase (MAPK) signal transduction networks have been extensively explored in plants; however, the connection between MAPK signaling cascades and submergence tolerance is currently unknown. The ethylene response factor-like protein SUB1A orchestrates a plethora of responses during submergence stress tolerance in rice (Oryza sativa). In this study, we report that MPK3 is activated by submergence in a SUB1A-dependent manner. MPK3 physically interacts with and phosphorylates SUB1A in a tolerant-allele-specific manner. Furthermore, the tolerant allele SUB1A1 binds to the MPK3 promoter and regulates its expression in a positive regulatory loop during submergence stress signaling. We present molecular and physiological evidence for the key role of the MPK3-SUB1A1 module in acclimation of rice seedlings to the adverse effects of submergence. Overall, the results provide a mechanistic understanding of submergence tolerance in rice.

[1]  J. Bailey-Serres,et al.  Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice , 2006, Nature.

[2]  J. Bailey-Serres,et al.  Submergence Tolerant Rice: SUB1’s Journey from Landrace to Modern Cultivar , 2010, Rice.

[3]  H. Hirt Connecting oxidative stress, auxin, and cell cycle regulation through a plant mitogen-activated protein kinase pathway. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Xian-Jun Song,et al.  The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water , 2009, Nature.

[5]  P. Ronald,et al.  SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway. , 2013, The New phytologist.

[6]  J. Kudla,et al.  Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. , 2008, The Plant journal : for cell and molecular biology.

[7]  J. Bailey-Serres,et al.  Waterproofing Crops: Effective Flooding Survival Strategies1 , 2012, Plant Physiology.

[8]  S. Raina,et al.  CrMPK3, a mitogen activated protein kinase from Catharanthus roseus and its possible role in stress induced biosynthesis of monoterpenoid indole alkaloids , 2012, BMC Plant Biology.

[9]  A. Sinha,et al.  Interaction between two rice mitogen activated protein kinases and its possible role in plant defense , 2013, BMC Plant Biology.

[10]  M. Shih,et al.  Plant defense after flooding , 2013, Plant signaling & behavior.

[11]  J. Thornton,et al.  AQUA and PROCHECK-NMR: Programs for checking the quality of protein structures solved by NMR , 1996, Journal of biomolecular NMR.

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

[13]  E. Septiningsih,et al.  Development of submergence-tolerant rice cultivars: the Sub1 locus and beyond. , 2009, Annals of botany.

[14]  K. Jung,et al.  The Submergence Tolerance Regulator Sub1A Mediates Stress-Responsive Expression of AP2/ERF Transcription Factors1[C][W][OA] , 2010, Plant Physiology.

[15]  D. Arnon COPPER ENZYMES IN ISOLATED CHLOROPLASTS. POLYPHENOLOXIDASE IN BETA VULGARIS. , 1949, Plant physiology.

[16]  Meetu Gupta,et al.  Arsenic stress activates MAP kinase in rice roots and leaves. , 2011, Archives of biochemistry and biophysics.

[17]  K. Asada,et al.  Hydrogen Peroxide is Scavenged by Ascorbate-specific Peroxidase in Spinach Chloroplasts , 1981 .

[18]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[19]  J. Bailey-Serres,et al.  A Variable Cluster of Ethylene Response Factor–Like Genes Regulates Metabolic and Developmental Acclimation Responses to Submergence in Rice[W] , 2006, The Plant Cell Online.

[20]  Stephen R. Comeau,et al.  PIPER: An FFT‐based protein docking program with pairwise potentials , 2006, Proteins.

[21]  H. Hirt,et al.  Improvement of stress tolerance in plants by genetic manipulation of mitogen-activated protein kinases. , 2013, Biotechnology advances.

[22]  J. Bailey-Serres,et al.  Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice , 2008, Proceedings of the National Academy of Sciences.

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

[24]  J. Mundy,et al.  Gene regulation by MAP kinase cascades. , 2009, Current opinion in plant biology.

[25]  H. Hirt,et al.  Disentangling the Complexity of Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling , 2008, Plant Physiology.

[26]  N. Gutterson,et al.  Regulation of disease resistance pathways by AP2/ERF transcription factors. , 2004, Current opinion in plant biology.

[27]  T. Yeates,et al.  Verification of protein structures: Patterns of nonbonded atomic interactions , 1993, Protein science : a publication of the Protein Society.

[28]  E. Septiningsih,et al.  A marker-assisted backcross approach for developing submergence-tolerant rice cultivars , 2007, Theoretical and Applied Genetics.

[29]  L. Voesenek,et al.  Flooding stress: acclimations and genetic diversity. , 2008, Annual review of plant biology.

[30]  E. Septiningsih,et al.  Comparison of phenotypic versus marker-assisted background selection for the SUB1 QTL during backcrossing in rice , 2012, Breeding science.

[31]  Sandor Vajda,et al.  ClusPro: a fully automated algorithm for protein-protein docking , 2004, Nucleic Acids Res..

[32]  Keehyoung Joo,et al.  Improving physical realism, stereochemistry, and side‐chain accuracy in homology modeling: Four approaches that performed well in CASP8 , 2009, Proteins.

[33]  Insuk Lee,et al.  Towards Establishment of a Rice Stress Response Interactome , 2011, PLoS genetics.

[34]  H. Aebi,et al.  Catalase in vitro. , 1984, Methods in enzymology.

[35]  A. Sinha,et al.  Regulation of MAP kinase signaling cascade by microRNAs in Oryza sativa. , 2014, Plant signaling & behavior.

[36]  Erik Andreasson,et al.  Convergence and specificity in the Arabidopsis MAPK nexus. , 2010, Trends in plant science.

[37]  Philip R. Cohen,et al.  PD 098059 Is a Specific Inhibitor of the Activation of Mitogen-activated Protein Kinase Kinase in Vitro and in Vivo(*) , 1995, The Journal of Biological Chemistry.

[38]  N. Tuteja,et al.  Mitogen-activated protein kinase signaling in plants under abiotic stress , 2011, Plant signaling & behavior.

[39]  I. Rebay,et al.  Post‐translational modifications influence transcription factor activity: A view from the ETS superfamily , 2005, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  P. Gegenheimer Preparation of extracts from plants. , 1990, Methods in enzymology.

[41]  B. Mueller‐Roeber,et al.  SALT-RESPONSIVE ERF1 Regulates Reactive Oxygen Species–Dependent Signaling during the Initial Response to Salt Stress in Rice[W] , 2013, Plant Cell.

[42]  Thomas L. Madden,et al.  Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. , 1997, Nucleic acids research.

[43]  Santosh Kumar,et al.  Overexpression of an apoplastic peroxidase gene CrPrx in transgenic hairy root lines of Catharanthus roseus , 2011, Applied Microbiology and Biotechnology.

[44]  M. Shih,et al.  Submergence Confers Immunity Mediated by the WRKY22 Transcription Factor in Arabidopsis[W] , 2013, Plant Cell.

[45]  L. Packer,et al.  Photoperoxidation in isolated chloroplasts. I. Kinetics and stoichiometry of fatty acid peroxidation. , 1968, Archives of biochemistry and biophysics.

[46]  J. Mundy,et al.  Ancient signals: comparative genomics of plant MAPK and MAPKK gene families. , 2006, Trends in plant science.

[47]  A. Sinha,et al.  Rice Mitogen Activated Protein Kinase Kinase and Mitogen Activated Protein Kinase Interaction Network Revealed by In-Silico Docking and Yeast Two-Hybrid Approaches , 2013, PloS one.

[48]  Shweta Sharma,et al.  Virus-induced gene silencing in rice using a vector derived from a DNA virus , 2010, Planta.

[49]  Jo Campling,et al.  Analysis of Variance (ANOVA) , 2002 .

[50]  H. Hirt,et al.  A major role of the MEKK1-MKK1/2-MPK4 pathway in ROS signalling. , 2009, Molecular plant.

[51]  J. Bailey-Serres,et al.  The Submergence Tolerance Regulator SUB1A Mediates Crosstalk between Submergence and Drought Tolerance in Rice[W][OA] , 2010, Plant Cell.

[52]  H. Hirt,et al.  Reactive oxygen species signaling in plants. , 2006, Antioxidants & redox signaling.

[53]  Sandor Vajda,et al.  ClusPro: an automated docking and discrimination method for the prediction of protein complexes , 2004, Bioinform..

[54]  Sorina C. Popescu,et al.  MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. , 2009, Genes & development.

[55]  Dima Kozakov,et al.  How good is automated protein docking? , 2013, Proteins.

[56]  R. Dhindsa,et al.  Leaf Senescence: Correlated with Increased Levels of Membrane Permeability and Lipid Peroxidation, and Decreased Levels of Superoxide Dismutase and Catalase , 1981 .

[57]  Ronald V. Maier,et al.  Mitogen-activated protein kinases. , 2002, Critical care medicine.

[58]  Kevin W Eliceiri,et al.  NIH Image to ImageJ: 25 years of image analysis , 2012, Nature Methods.

[59]  J. Mundy,et al.  Mitogen-activated protein kinase signaling in plants. , 2010, Annual review of plant biology.