Influence of temperature on the expression of the rice sucrose transporter 4 gene, OsSUT4, in germinating embryos and maturing pollen

• Autorzy: Chung P. , Hsiao H.-H. , Chen H.-J. , Chang C.-W. , Wang S.-J.
• Języki publikacji: EN

Abstrakty

EN

Rice (Oryza sativa L.) sucrose transporter 4 (OsSUT4) is a rice sucrose transporter family gene. During the early seed germination stage, OsSUT4 was substantially expressed in seed aleurone layer, scutellum, and embryonic vascular bundle. The OsSUT4 mRNA level in the embryos of seeds that were germinated at 30°C was higher than that of seeds germinated at 20°C. The temperature effect on the changes of OsSUT4 promoter activities was consistent with that on OsSUT4 mRNA levels. The OsSUT4 gene expression that occurs in response to temperature might be mediated by soluble sugars as signals that are transported from endosperms. The tissue-specific expression patterns of OsSUT4 found in spikelets were dependent on the developmental stages of rice panicles. The OsSUT4 transcript level in anthers during the post-heading stage was higher than that during the pre-heading stage, and the developmental expression pattern of the OsSUT4 gene in anthers was highly correlated with that of genes encoded sucrose metabolism and starch synthesis enzymes. The OsSUT4 promoter activity was also detected in mature and germinating pollen. Furthermore, the OsSUT4 expression in anthers was down-regulated at low temperature (i.e., 15/13°C) compared with that at 30/25 and 35/30°C. In conclusion, the levels of OsSUT4 expressions in germinating embryos and maturing pollen were regulated by temperature, and the expressions of OsSUT4 in embryos and pollen at higher temperature (i.e., 30 and 35°C) were stronger than that at lower temperature condition (i.e., 15 and 20°C).

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2014
• Tom: 36
• Numer: 01
• Opis fizyczny: p.217-229,fig.,ref.

Twórcy

autor

Chung P.

• Department of Agronomy, National Taiwan University, No.1, Section 4, Roosevelt Rd., Taipei 106, Taiwan, Republic of China

autor

Hsiao H.-H.

• Department of Agronomy, National Taiwan University, No.1, Section 4, Roosevelt Rd., Taipei 106, Taiwan, Republic of China

autor

Chen H.-J.

• Department of Agronomy, National Taiwan University, No.1, Section 4, Roosevelt Rd., Taipei 106, Taiwan, Republic of China

autor

Chang C.-W.

• Department of Agronomy, National Taiwan University, No.1, Section 4, Roosevelt Rd., Taipei 106, Taiwan, Republic of China

autor

Wang S.-J.

• Department of Agronomy, National Taiwan University, No.1, Section 4, Roosevelt Rd., Taipei 106, Taiwan, Republic of China

Bibliografia

• Aoki N, Hirose T, Scofield GN, Whitfeld PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232.
• Barker L, Kühn C, Weise A, Schulz A, Gebhard C, Hirner B, Hellmann H, Schulze W, Ward JM, Frommer WB (2000) SUT2, a putative sucrose sensor in sieve elements. Plant Cell 12:1153–1164.
• Barth I, Meyer S, Sauer N (2003) PmSUC3: characterization of a SUT2/SUC3-type sucrose transporter from Plantago major. Plant Cell 15:1375–1385.
• Braun DM, Slewinski TL (2009) Genetic control of carbon partitioning in grasses: roles of sucrose transporters and tie-dyed loci in phloem loading. Plant Physiol 149:71–81.
• Chen HJ, Wang SJ (2008) Molecular regulation of sink-source transition in rice leaf sheaths during the heading period. Acta Physiol Plant 30:639–649.
• Chen JY, Liu SL, Siao W, Wang SJ (2010) Hormone and sugar effects on rice sucrose transporter OsSUT1 expression in germinating embryos. Acta Physiol Plant 32:749–756.
• Chinnusamy V, Ohta M, Kanrar S, Lee BH, Hong X, Agarwal M, Zhu JK (2003) ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:1043–1054.
• Chu C, Lee TM (1989) The relationship between ethylene biosynthesis and chilling tolerance in seedlings of rice (Oryza sativa L.). Bot Bull Acad Sinica 30:263–273.
• Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007) Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol Cell Proteomics 6:207–230.
• Datta R, Chamusco KC, Chourey PS (2002) Starch biosynthesis during pollen maturation is associated with altered patterns of gene expression in maize. Plant Physiol 130:1645–1656.
• Dubouzet JG, Sakuma Y, Ito Y, Kasuga M, Dubouzet EG, Miura S, Seki M, Shinozaki K, Yamaguchi-Shinozaki K (2003) OsDREB genes in rice, Oryza sativa L., encode transcription activators that function in drought-, high-salt- and cold-responsive gene expression. Plant J 33:751–763.
• Gibson SI (2005) Control of plant development and gene expression by sugar signaling. Curr Opin Plant Biol 8:93–102.
• Hackel A, Schauer N, Carrari F, Fernie AR, Grimm B, Kühn C (2006) Sucrose transporter LeSUT1 and LeSUT2 inhibition affects tomato fruit development in different ways. Plant J 45:180–192.
• Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database: 1999. Nuc Acids Res 27:297–300.
• Hirose T, Imaizumi N, Scofield GN, Furbank RT, Ohsugi R (1997) cDNA cloning and tissue specific expression of a gene for sucrose transporter from rice (Oryza sativa L.). Plant Cell Physiol 38:1389–1396.
• Hirose T, Zhang Z, Miyao A, Hirochika H, Ohsugi R, Terao T (2010) Disruption of a gene for rice sucrose transporter, OsSUT1, impairs pollen function but pollen maturation is unaffected. J Exp Bot 61:3639–3646.
• Hwang YS, Karrer EE, Thomas BR, Chen L, Rodriguez RL (1998) Three cis-elements required for rice alpha-amylase Amy3D expression during sugar starvation. Plant Mol Biol 36:331–341.
• Imin N, Kerim T, Rolfe BG, Weinman JJ (2004) Effect of early cold stress on the maturation of rice anthers. Proteomics 4:1873–1882.
• Ishimaru T, Horigane AK, Ida M, Iwasawa N, San-oh YA, Nakazono M, Nishizawa NK, Masumura T, Kondo M, Yoshida M (2009) Formation of grain chalkiness and changes in water distribution in developing rice caryopses grown under high-temperature stress. 50:166–174.
• Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces cor genes and enhances freezing tolerance. Science 280:104–106.
• Jefferson RA (1987) Assaying chimeric genes in plants: the GUS gene fusion system. Plant Mol Biol Rep 5:387–405.
• Kong J, Li Z, Tan YP, Wan CX, Li SQ, Zhu YG (2007) Different gene expression patterns of sucrose-starch metabolism during pollen maturation in cytoplasmic male-sterile and male-fertile lines of rice. Physiol Planta 130:136–147.
• Lauterbach C, Niedermeier M, Besenbeck R, Stadler R, Sauer N (2007) Immunolocalization of the PmSUC1 sucrose transporter in Plantago major flowers and reporter-gene analyses of the PmSUC1 promoter suggest a role in sucrose release from the inner integument. Plant Biol 9:357–365.
• Lemoine R, Bürkle L, Barker L, Sakr S, Kühn C, Regnacq M, Gaillard C, Delrot S, Frommer WB (1999) Identification of a pollen-specific sucrose transporter-like protein NtSUT3 from tobacco. FEBS Lett 454:325–330.
• Lin CJ, Li CY, Lin SK, Yang FH, Huang JJ, Liu YH, Lur HS (2010) Influence of high temperature during grain filling on the accumulation of storage proteins and grain quality in rice (Oryza sativa L.). J Agric Food Chem 58:10545–10552.
• Liu Q, Sakuma Y, Abe H, Kasuga M, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcriptional factors, DREB1 and DREB2, with an EREP/AP2 DNA binding domain, separate two cellular signal transduction pathways in drought- and low temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406.
• Liu SL, Siao W, Wang SJ (2010) Changing sink demand of developing shoot affects transitory starch biosynthesis in embryonic tissues of germinating rice seeds. Seed Sci Res 20:137–144.
• Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int 30:583–591.
• Mamun EA, Cantrill LC, Overall RL, Sutton BG (2010) Mechanism of low-temperature-induced pollen failure in rice. Cell Biol Int 34:469–476.
• Meyer S, Melzer M, Truernit E, Hümmer C, Besenbeck R, Stadler R, Sauer N (2000) AtSUC3, a gene encoding a new Arabidopsis sucrose transporter, is expressed in cells adjacent to the vascular tissue and in a carpel cell layer. Plant J 24:869–882.
• Meyer S, Lauterbach C, Niedermeier M, Barth I, Sjolund RD, Sauer N (2004) Wounding enhances expression of AtSUC3, a sucrose transporter from Arabidopsis sieve elements and sink tissues. Plant Physiol 134:684–693.
• Morita A, Umemura T, Kuroyanagi M, Futsuhara Y, Perata P, Yamaguchi J (1998) Functional dissection of a sugar-repressed alpha-amylase gene (Ramy1A) promoter in rice embryos. FEBS Lett 423:81–85.
• Oliver SN, van Dongen JT, Alfred SC, Mamun EA, Zhao X, Saini HS, Fernandes SF, Blanchard CL, Sutton BG, Geigenberger P, Dennis ES, Dolferus R (2005) Cold-induced repression of the rice anther-specific cell wall invertase gene OSINV4 is correlated with sucrose accumulation and pollen sterility. Plant Cell Environ 28:1534–1551.
• Phan TTT, Ishibashi Y, Miyazaki M, Tran HT, Okamura K, Tanaka S, Nakamura J, Yuasa T, Iwaya-Inoue M (2013) High temperature-induced repression of the rice sucrose transporter (OsSUT1) and starch synthesis-related genes in sink and source organs at milky ripening stage causes chalky grains. J Agro Crop Sci 199:178–188.
• Prestridge DS (1991) SIGNAL SCAN: a computer program that scans DNA sequences for eukaryotic transcriptional elements. CAB-IOS 7:203–206.
• Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709.
• Scofield GN, Hirose T, Gaudron JA, Upadhyaya NM, Ohsugi R, Furbank RT (2002) Antisense suppression of the rice sucrose transporter gene, OsSUT1, leads to impaired grain filling and germination but dose not affect photosynthesis. Funct Plant Biol 29:815–826.
• Scofield GN, Aoki N, Hirose T, Takano M, Jenkins CLD, Furbank RT (2007a) The role of the sucrose transporter, OsSUT1, in germination and early seedling growth and development of rice plants. J Exp Bot 58:483–495.
• Scofield GN, Hirose T, Aoki N, Furbank RT (2007b) Involvement of the sucrose transporter, OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot 58:3155–3169.
• Shi W, Muthurajan R, Rahman H, Selvam J, Peng S, Zou Y, Jagadish KS (2013) Source-sink dynamics and proteomic reprogramming under elevated night temperature and their impact on rice yield and grain quality. New Phytol 197:825–837.
• Siahpoosh MR, Sanchez DH, Schlereth A, Scofield GN, Furbank RT, van Dongen JT, Kopka J (2012) Modification of OsSUT1 gene expression modulates the salt response of rice Oryza sativa cv. Taipei 309. Plant Sci 182:101–111.
• Siao W, Chen JY, Hsiao HH, Chung P, Wang SJ (2011) Characterization of OsSUT2 expression and regulation in germinating embryos of rice seeds. Rice 4:39–49.
• Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. Plant J 19:269–278.
• Sun C, Palmqvist S, Olsson H, Borén M, Ahlandsberg S, Jansson C (2003) A novel WRKY transcription factor, SUSIBA2, participates in sugar signaling in barley by binding to the sugarresponsive elements of the iso1 promoter. Plant Cell 15:2076–2092.
• Svensson JT, Crosatti C, Campoli C, Bassi R, Stanca AM, Close TJ, Cattivelli L (2006) Transcriptome analysis of cold acclimation in barley albina and xantha mutants. Plant Physiol 141:257–270.
• Tanaka K, Onishi R, Miyazaki M, Ishibashi Y, Yuasa T, Iwaya-Inoue M (2009) Changes in NMR relaxation of rice grains, kernel quality and physicochemical properties in response to a high temperature after flowering in heat-tolerant and heat-sensitive rice cultivars. Plant Prod Sci 12:185–192.
• Thum KE, Shin MJ, Palenchar PM, Kouranov A, Coruzzi GM (2004) Genome-wide investigation of light and carbon signaling interactions in Arabidopsis. Genome Biol 5:R10.
• Ueno K, Miyoshi K (2005) Difference of optimum germination temperature of seeds of intact and dehusked japonica rice during seed development. Euphytica 143:271–275.
• Wang SJ, Liu LF, Chen CK, Chen LW (2006) Regulations of granulebound starch synthase I gene expression in rice leaves by temperature and drought stress. Biol Plant 50:537–541.
• Woonton BW, Sherkat F, Maharjan P (2005) The influence of barley storage on respiration and glucose-6-phosphate dehydrogenase during malting. J Inst Brew 111:388–395.
• Yamakawa H, Hakata M (2010) Atlas of rice grain filling-related metabolism under high temperature: joint analysis of metabolome and transcriptome demonstrated inhibition of starch accumulation and induction of amino acid accumulation. Plant Cell Physiol 51:795–809.
• Yamakawa H, Hirose Y, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling related genes under high temperature using DNA microarray. Plant Physiol 144:258–277.

Identyfikatory

DOI

10.1007/s11738-013-1403-x