Overexpression of OsSWEET5 in Rice Causes Growth Retardation and Precocious Senescence

As a novel sugar transporter family, SWEETs play important roles in plant growth and development. Here, we characterized a SWEET gene named OsSWEET5 through its overexpression in rice. Heterologous expression assay indicated that OsSWEET5 encoded a galactose transporter in yeast. OsSWEET5-overexpressing plants displayed the phenotypes of growth retardation and precocious senescence at seedling stage. GC-MS analysis showed that the sugar levels were largely altered in the leaves of the OsSWEET5-overexpressing plants. Molecular analysis revealed that these phenotypes might be due to the transcriptional changes of the genes involved in sugar metabolism and transport. In addition, the transgenic plants showed a lower level of auxin with altered transcription of genes involved in auxin signaling and translocation pathways. However, no obvious phenotype was observed between the amiRNA-OsSWEET5 transgenic lines and WT plants, which could be a result of the functional redundancy of the galactose transporters in rice. Taken together, our findings suggest that OsSWEET5 plays a crucial role in regulating the crosstalk between sugar and auxin in rice.

[1]  A. Krapp,et al.  Overexpression of the Vacuolar Sugar Carrier AtSWEET16 Modifies Germination, Growth, and Stress Tolerance in Arabidopsis1[W] , 2013, Plant Physiology.

[2]  Shiping Wang,et al.  Rice MtN3/saliva/SWEET family genes and their homologs in cellular organisms. , 2013, Molecular plant.

[3]  O. Loudet,et al.  Leaf Fructose Content Is Controlled by the Vacuolar Transporter SWEET17 in Arabidopsis , 2013, Current Biology.

[4]  J. Pech,et al.  SlARF4, an Auxin Response Factor Involved in the Control of Sugar Metabolism during Tomato Fruit Development1[C][W] , 2013, Plant Physiology.

[5]  K. Ljung,et al.  Soluble Carbohydrates Regulate Auxin Biosynthesis via PIF Proteins in Arabidopsis[W][OA] , 2012, Plant Cell.

[6]  L. Xiong,et al.  A GH 3 family m mber , OsGH 3-2 , modulates auxin and abscisic acid levels and differentially affects drought and cold tolerance in rice , 2012 .

[7]  Y. Ruan.  Signaling role of sucrose metabolism in development. , 2012, Molecular plant.

[8]  D. Braun,et al.  SWEET as Sugar: New Sucrose Effluxers in Plants. , 2012, Molecular plant.

[9]  Yongjun Lin,et al.  Two novel positive cis-regulatory elements involved in green tissue-specific promoter activity in rice (Oryza sativa L ssp.) , 2012, Plant Cell Reports.

[10]  Yong Zhou,et al.  Expression profile analysis of the polygalacturonase-inhibiting protein genes in rice and their responses to phytohormones and fungal infection , 2012, Plant Cell Reports.

[11]  Ning Tang,et al.  Constitutive Activation of Transcription Factor OsbZIP46 Improves Drought Tolerance in Rice1[C][W][OA] , 2012, Plant Physiology.

[12]  Alisdair R Fernie,et al.  Sucrose Efflux Mediated by SWEET Proteins as a Key Step for Phloem Transport , 2012, Science.

[13]  D. Braun.  SWEET! The Pathway Is Complete , 2012, Science.

[14]  L. Xiong,et al.  Characterization of an inositol 1,3,4-trisphosphate 5/6-kinase gene that is essential for drought and salt stress responses in rice , 2011, Plant Molecular Biology.

[15]  Gynheung An,et al.  Impaired Function of the Tonoplast-Localized Sucrose Transporter in Rice, OsSUT2, Limits the Transport of Vacuolar Reserve Sucrose and Affects Plant Growth1[W] , 2011, Plant Physiology.

[16]  F. Zhang,et al.  A Rice Plastidial Nucleotide Sugar Epimerase Is Involved in Galactolipid Biosynthesis and Improves Photosynthetic Efficiency , 2011, PLoS genetics.

[17]  Thomas L. Slewinski,et al.  Diverse functional roles of monosaccharide transporters and their homologs in vascular plants: a physiological perspective. , 2011, Molecular plant.

[18]  Y. Xing,et al.  Two complementary recessive genes in duplicated segments control etiolation in rice , 2011, Theoretical and Applied Genetics.

[19]  W. Frommer,et al.  Sugar transporters for intercellular exchange and nutrition of pathogens , 2010, Nature.

[20]  Xianghua Li,et al.  Manipulating Broad-Spectrum Disease Resistance by Suppressing Pathogen-Induced Auxin Accumulation in Rice1[C][W][OA] , 2010, Plant Physiology.

[21]  F. White,et al.  Rice xa13 Recessive Resistance to Bacterial Blight Is Defeated by Induction of the Disease Susceptibility Gene Os-11N3[W][OA] , 2010, Plant Cell.

[22]  G. Poschet,et al.  Identification and characterization of AtSTP14, a novel galactose transporter from Arabidopsis. , 2010, Plant & cell physiology.

[23]  Thomas L. Slewinski,et al.  Maize SUT1 functions in phloem loading , 2010, Plant signaling & behavior.

[24]  Xianghua Li,et al.  Identification and Application of a Rice Senescence-Associated Promoter1[C][W][OA] , 2010, Plant Physiology.

[25]  P. Chourey,et al.  Sugar Levels Regulate Tryptophan-Dependent Auxin Biosynthesis in Developing Maize Kernels[C][W][OA] , 2010, Plant Physiology.

[26]  Hong Ma,et al.  Carbon Starved Anther Encodes a MYB Domain Protein That Regulates Sugar Partitioning Required for Rice Pollen Development[W][OA] , 2010, Plant Cell.

[27]  S. Rothstein,et al.  Auxin-responsive SAUR39 gene modulates auxin level in rice , 2009, Plant signaling & behavior.

[28]  Tong Zhu,et al.  SAUR39, a Small Auxin-Up RNA Gene, Acts as a Negative Regulator of Auxin Synthesis and Transport in Rice1[W] , 2009, Plant Physiology.

[29]  Ashverya Laxmi,et al.  Glucose and Auxin Signaling Interaction in Controlling Arabidopsis thaliana Seedlings Root Growth and Development , 2009, PloS one.

[30]  D. Brummell,et al.  Galactose metabolism in cell walls of opening and senescing petunia petals , 2009, Planta.

[31]  R. Meeley,et al.  Sucrose transporter1 functions in phloem loading in maize leaves , 2009 .

[32]  V. Germain,et al.  Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars: Monosaccharide/proton symporter function in Arabidopsis , 2008 .

[33]  Honglin Xu,et al.  Molecular cloning and expression analysis of a monosaccharide transporter gene OsMST4 from rice (Oryza sativa L.) , 2007, Plant Molecular Biology.

[34]  Jian Liu,et al.  Molecular cloning and function analysis of the stay green gene in rice. , 2007, The Plant journal : for cell and molecular biology.

[35]  N. Sauer.  Molecular physiology of higher plant sucrose transporters , 2007, FEBS letters.

[36]  H. Seo,et al.  The Senescence-Induced Staygreen Protein Regulates Chlorophyll Degradation[W] , 2007, The Plant Cell Online.

[37]  Eun-Jeong Lee,et al.  Glycosyl hydrolases of cell wall are induced by sugar starvation in Arabidopsis. , 2007, Plant & cell physiology.

[38]  M. Ohto,et al.  Involvement of HLS1 in sugar and auxin signaling in Arabidopsis leaves. , 2006, Plant & cell physiology.

[39]  J. Bennetzen,et al.  Promoter mutations of an essential gene for pollen development result in disease resistance in rice. , 2006, Genes & development.

[40]  E. Baena-González,et al.  Sugar sensing and signaling in plants: conserved and novel mechanisms. , 2006, Annual review of plant biology.

[41]  N. Sauer,et al.  AtSTP11, a pollen tube-specific monosaccharide transporter in Arabidopsis , 2005, Planta.

[42]  F. Rojo-Callejas,et al.  Optimization of carbohydrate silylation for gas chromatography. , 2004, Journal of chromatography. A.

[43]  R. Hedrich,et al.  Diurnal and Light-Regulated Expression of AtSTP1 in Guard Cells of Arabidopsis1 , 2003, Plant Physiology.

[44]  Filip Rolland,et al.  Role of the Arabidopsis Glucose Sensor HXK1 in Nutrient, Light, and Hormonal Signaling , 2003, Science.

[45]  P. León,et al.  Sugar and hormone connections. , 2003, Trends in plant science.

[46]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[47]  M. Paul,et al.  Sink regulation of photosynthesis. , 2001, Journal of experimental botany.

[48]  A. Krogh,et al.  Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. , 2001, Journal of molecular biology.

[49]  V. Germain,et al.  Monosaccharide/proton symporter AtSTP1 plays a major role in uptake and response of Arabidopsis seeds and seedlings to sugars. , 2000, The Plant journal : for cell and molecular biology.

[50]  L. Williams,et al.  Sugar transporters in higher plants--a diversity of roles and complex regulation. , 2000, Trends in plant science.

[51]  N. Sauer,et al.  Monosaccharide transporters in plants: structure, function and physiology. , 2000, Biochimica et biophysica acta.

[52]  C. Hollenberg,et al.  Concurrent knock‐out of at least 20 transporter genes is required to block uptake of hexoses in Saccharomyces cerevisiae , 1999, FEBS letters.

[53]  W. Frommer,et al.  The Dual Function of Sugar Carriers: Transport and Sugar Sensing , 1999, Plant Cell.

[54]  P. Gamas,et al.  Use of a subtractive hybridization approach to identify new Medicago truncatula genes induced during root nodule development. , 1996, Molecular plant-microbe interactions : MPMI.

[55]  P. Frey.  The Leloir pathway: a mechanistic imperative for three enzymes to change the stereochemical configuration of a single carbon in galactose , 1996, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[56]  R. Müller,et al.  Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. , 1995, Gene.

[57]  N. Sauer,et al.  Subcellular Localization of the Inducible Chlorella HUP1 Monosaccharide-H+ Symporter and Cloning of a Co-Induced Galactose-H+ Symporter , 1995, Plant physiology.

[58]  N. Sauer,et al.  Primary structure, genomic organization and heterologous expression of a glucose transporter from Arabidopsis thaliana. , 1990, The EMBO journal.

[59]  M. Inouhe,et al.  Galactose inhibition of auxin-induced growth of mono- and dicotyledonous plants. , 1988, Plant physiology.

[60]  N. Sakurai,et al.  Inhibition of auxin‐induced cell elongation by galactose , 1981 .

[61]  G. C. Colclasure,et al.  Effect of Galactose and Other Monosaccharides on IAA Movement in Bean Hypocotyl Segments , 1977 .

[62]  L. Anker.  AUXIN-SYNTHESIS INHIBITION BY SUGARS, NOTABLY BY GALACTOSE , 1974 .

[63]  R. Roberts,et al.  Growth Inhibition and Metabolite Pool Levels in Plant Tissues Fed d-Glucosamine and d-Galactose. , 1971, Plant physiology.

[64]  L. Leloir.  The enzymatic transformation of uridine diphosphate glucose into a galactose derivative. , 1951, Archives of biochemistry and biophysics.

[65]  E. Truernit,et al.  A male gametophyte-specific monosaccharide transporter in Arabidopsis. , 1999, The Plant journal : for cell and molecular biology.

[66]  Shigeki Mitaku,et al.  SOSUI: classification and secondary structure prediction system for membrane proteins , 1998, Bioinform..

[67]  R. Cleland,et al.  Galactose inhibits auxin-induced growth of Avena coleoptiles by two mechanisms. , 1991, Plant & cell physiology.

[68]  R. Severson,et al.  Maintenance carbon cycle in crassulacean Acid metabolism plant leaves : source and compartmentation of carbon for nocturnal malate synthesis. , 1985, Plant physiology.