Submergence tolerance conferred by Sub1A is mediated by SLR1 and SLRL1 restriction of gibberellin responses in rice

Submergence-tolerant rice maintains viability during complete submergence by limiting underwater elongation until floodwaters recede. Acclimation responses to submergence are coordinated by the submergence-inducible Sub1A, which encodes an ethylene-responsive factor-type transcription factor (ERF). Sub1A is limited to tolerant genotypes and sufficient to confer submergence tolerance to intolerant accessions. Here we evaluated the role of Sub1A in the integration of ethylene, abscisic acid (ABA), and gibberellin (GA) signaling during submergence. The submergence-stimulated decrease in ABA content was Sub1A-independent, whereas GA-mediated underwater elongation was significantly restricted by Sub1A. Transgenics that ectopically express Sub1A displayed classical GA-insensitive phenotypes, leading to the hypothesis that Sub1A limits the response to GA. Notably Sub1A increased the accumulation of the GA signaling repressors Slender Rice-1 (SLR1) and SLR1 Like-1 (SLRL1) and concomitantly diminished GA-inducible gene expression under submerged conditions. In the Sub1A overexpression line, SLR1 protein levels declined under prolonged submergence but were accompanied by an increase in accumulation of SLRL1, which lacks the DELLA domain. In the presence of Sub1A, the increase in these GA signaling repressors and decrease in GA responsiveness were stimulated by ethylene, which promotes Sub1A expression. Conversely, ethylene promoted GA responsiveness and shoot elongation in submergence-intolerant lines. Together, these results demonstrate that Sub1A limits ethylene-promoted GA responsiveness during submergence by augmenting accumulation of the GA signaling repressors SLR1 and SLRL1.

[1]  M. Matsuoka,et al.  slender Rice, a Constitutive Gibberellin Response Mutant, Is Caused by a Null Mutation of the SLR1 Gene, an Ortholog of the Height-Regulating Gene GAI/RGA/RHT/D8 , 2001, Plant Cell.

[2]  N. Olszewski,et al.  Rice GIBBERELLIN INSENSITIVE DWARF1 Is a Gibberellin Receptor That Illuminates and Raises Questions about GA Signaling , 2006, The Plant Cell Online.

[3]  S. Swain,et al.  Gibberellin signal transduction presents …the SPY who O-GlcNAc'd me , 1999 .

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

[5]  J. Bailey-Serres,et al.  Ethylene—A key regulator of submergence responses in rice , 2008 .

[6]  R. K. Sarkar,et al.  Elongation ability and non-structural carbohydrate levels in relation to submergence tolerance in rice , 2005 .

[7]  X. Deng,et al.  Coordinated regulation of Arabidopsis thaliana development by light and gibberellins , 2008, Nature.

[8]  A. Cutler,et al.  Formation and breakdown of ABA. , 1999, Trends in plant science.

[9]  J. Benschop,et al.  Long-Term Submergence-Induced Elongation in Rumex palustris Requires Abscisic Acid-Dependent Biosynthesis of Gibberellin11 , 2006, Plant Physiology.

[10]  A. J. Williams,et al.  Regulated Phosphorylation of 40S Ribosomal Protein S6 in Root Tips of Maize1 , 2003, Plant Physiology.

[11]  M. Van Montagu,et al.  A comparative molecular-physiological study of submergence response in lowland and deepwater rice. , 2001, Plant physiology.

[12]  T. Sun,et al.  Gibberellin signal transduction. , 2000, Current opinion in plant biology.

[13]  Masatomo Kobayashi,et al.  Accumulation of Phosphorylated Repressor for Gibberellin Signaling in an F-box Mutant , 2003, Science.

[14]  Y. Kamiya,et al.  Ethylene promotes submergence-induced expression of OsABA8ox1, a gene that encodes ABA 8'-hydroxylase in rice. , 2006, Plant & cell physiology.

[15]  Xiangdong Fu,et al.  GA action: turning on de-DELLA repressing signaling. , 2007, Current opinion in plant biology.

[16]  K. Asano,et al.  Molecular Interactions of a Soluble Gibberellin Receptor, GID1, with a Rice DELLA Protein, SLR1, and Gibberellin[W] , 2007, The Plant Cell Online.

[17]  Cho,et al.  Deepwater rice: A model plant to study stem elongation , 1998, Plant physiology.

[18]  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.

[19]  T. Setter,et al.  The beneficial effect of reduced elongation growth on submergence tolerance of rice , 1996 .

[20]  C. Fankhauser,et al.  A molecular framework for light and gibberellin control of cell elongation , 2008, Nature.

[21]  P. C. Ram,et al.  Submergence tolerance of rainfed lowland rice: search for physiological marker traits , 2001 .

[22]  M. Matsuoka,et al.  The Gibberellin Signaling Pathway Is Regulated by the Appearance and Disappearance of SLENDER RICE1 in Nuclei Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010319. , 2002, The Plant Cell Online.

[23]  M. Matsuoka,et al.  Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. , 2005, The Plant journal : for cell and molecular biology.

[24]  S. J. Ambrose,et al.  The etr1-2 mutation in Arabidopsis thaliana affects the abscisic acid, auxin, cytokinin and gibberellin metabolic pathways during maintenance of seed dormancy, moist-chilling and germination. , 2005, The Plant journal : for cell and molecular biology.

[25]  S. Hoffmann-Benning,et al.  On the role of abscisic Acid and gibberellin in the regulation of growth in rice. , 1992, Plant physiology.

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

[27]  R. Pierik,et al.  How plants cope with complete submergence. , 2006, The New phytologist.

[28]  Masatomo Kobayashi,et al.  GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin , 2005, Nature.