Skip to main content
Log in

Genetic complementation analysis of rice sucrose transporter genes in Arabidopsis SUC2 mutant atsuc2

  • Original Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Sucrose transporters (SUTs) play a critical role on the phloem plasma membrane in loading sucrose into the phloem of source leaves for long-distance transport to sink organs. Rice has a small gene family of five SUTs, Oryza sativa SUT1 (OsSUT1) to OsSUT5. To identify rice SUTs that function as phloem loaders, we adopted a growth restoration assay of the severe growth retardation phenotype of atsuc2, a mutant of the best-characterized Arabidopsis phloem loader AtSUC2, by introducing OsSUTs. The rice SUT genes were expressed by two different promoters, the native phloem-specific promoter of AtSUC2 (pAtSUC2) and the constitutive Cauliflower Mosaic Virus 35S (pCaMV35S) promoter. Of all the transgenic atsuc2 plants, only pAtSUC2: OsSUT1 complemented the atsuc2 mutant phenotype in a comparable manner to wild type (WT), and consistent levels of soluble sugars and starch were recovered compared to those of WT. This suggests that OsSUT1 is a functional ortholog of the Arabidopsis AtSUC2 and functions as an apoplastic phloem loader. In addition, ossut1 mutants were produced via anther culture and their primary carbohydrate levels and growth phenotypes were indistinguishable from those of WT. This suggests that the rice phloem loader OsSUT1 function may not be essential for rice vegetative growth under normal conditions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Aoki N, Hirose T, Scofield GN, Whitfield PR, Furbank RT (2003) The sucrose transporter gene family in rice. Plant Cell Physiol 44:223–232

    Article  CAS  PubMed  Google Scholar 

  • Clough S, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • Dasgupta K, Khadilkar AS, Sulpice R, Pant B, Scheible WR, Fisahn J, Stitt M, Ayre BG (2014) Expression of sucrose transporter cDNAs specifically in companion cells enhances phloem loading and long-distance transport of sucrose but leads to an inhibition of growth and the perception of a phosphate limitation. Plant Physiol 165:715–731

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eom JS, Cho JI, Reinders A, Lee SW, Yoo Y, Tuan PQ, Choi SB, Bang G, Park YI, Cho MH, Bhoo SH, An G, Hahn TR, Ward JM, Jeon JS (2011) Impaired function of the tonoplast-localized sucrose transporter in rice, OsSUT2, limits the transport of vacuolar reserve sucrose and affects plant growth. Plant Physiol 157:109–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eom JS, Choi SB, Ward JM, Jeon JS (2012) The mechanism of phloem loading in rice (Oryza sativa). Mol Cells 33:431–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gottwald JR, Krysan PJ, Young JC, Evert RF, Sussman MR (2000) Genetic evidence for the in planta role of phloem-specific plasma membrane sucrose transporters. Proc Natl Acad Sci USA 97:13979–13984

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Herath HMI, Bandara DC, Samarajeewa PK (2007) Effect of culture media for anther culture of indica rice varieties and hybrids of indica and Japonica. TARE 10:17–22

    Google Scholar 

  • Ishimaru K, Hirose T, Aoki N, Takahashi S, Ono K, Yamamoto S, Wu J, Saji S, Baba T, Ugaki M, Matsumoto T, Ohsugi R (2001) Antisense expression of a rice sucrose transporter OsSUT1 in rice (Oryza sativa L). Plant Cell Physiol 42:1181–1185

    Article  CAS  PubMed  Google Scholar 

  • Jain M, Nijhawan A, Tyagi AK, Khurana JP (2006) Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR. Biochem Biophys Res Commun 345:645–651

    Article  Google Scholar 

  • Kühn C, Quick WP, Schulz A, Sonnewald U, Frommer WB (1996) Companion cell-specific inhibition of the potato sucrose transporter SUT1. Plant Cell Environ 19:1115–1123

    Article  Google Scholar 

  • Kühn C, Hajirezaei MR, Fernie AR, Roessner-Tunali U, Czechowski T, Hirner B, Frommer WB (2003) The sucrose transporter StSUT1 localizes to sieve elements in potato tuber phloem and influences tuber physiology and development. Plant Physiol 131:102–113

    Article  PubMed  PubMed Central  Google Scholar 

  • Kühn C and Grof CP (2010). Sucrose transporters of higher plants. Curr Opin Plant Biol 13:288–298

    Article  PubMed  Google Scholar 

  • Lim JD, Cho JI, Park YI, Hahn TR, Choi SB, Jeon JS (2006) Sucrose transport from source to sink seeds in rice. Physiol Planta 126:572–584

    Article  CAS  Google Scholar 

  • Ngampanya B, Takeda T, Sonoda Y, Narangajavana J, Yamaguchi J (2002) Characterization of OsSUT2 cDNA expressed before flowering stage. Rice Genet Newslett 19:49–51

    Google Scholar 

  • Oppenheimer DG, Haas N, Silflow CD, and Snustad DP (1988) The ß-tubulin gene family of Arabidopsis thaliana: Preferential accumulation of the B1 transcript in roots. Gene 63:87–102

    Article  CAS  PubMed  Google Scholar 

  • Reinders A, Sivitz AB, Ward JM (2012) Evolution of plant sucrose uptake transporters. Front Plant Sci 3:22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Riesmeier JW, Willmitzer L, Frommer WB (1994) Evidence for an essential role of the sucrose transporter in phloem loading and assimilate partitioning. EMBO J 13:1–7

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rosche E, Blackmore D, Tegeder M, Richardson T, Schroeder H, Higgins TJ, Frommer WB, Offler CE, Patrick JW (2002) Seedspecific overexpression of a potato sucrose transporter increases sucrose uptake and growth rates of developing pea cotyledons. Plant J 30:165–175

    Article  CAS  PubMed  Google Scholar 

  • 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 does not affect photosynthesis. Funct Plant Biol 29:815–826

    Article  CAS  Google Scholar 

  • Scofield GN, Aoki N, Hirose T, Takano M, Jenkins CL, 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

    Article  CAS  PubMed  Google Scholar 

  • 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 58:3155–169

    Article  CAS  PubMed  Google Scholar 

  • Slewinski TL, Meeley R, Braun1 DM (2009) Sucrose transporter1 functions in phloem loading in maize leaves. J Exp Bot 60:881–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava AC, Ganesan S, Ismail IO, Ayre BG (2008) Functional characterization of the Arabidopsis AtSUC2 Suc/H+ Symporter by tissue-specific complementation reveals an essential role in phloem loading but not in long-distance transport. Plant Physiol 148:200–211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Srivastava AC, Dasgupta K, Ajieren E, Costilla G, Mc Garry RC, Ayre BG (2009) AtSUC2, the predominant sucrose/proton symporter involved in phloem loading, is not an essential gene as plants harbouring a null allele are able to complete their life cycle and produce viable seed. Ann Bot 104:1121–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sun Y, Reinders A, La Fleur KR, Mori T, Ward JM (2010) Transporter activity of rice sucrose transporers OsSUT1 and OsSUT5. Plant Cell Physiol 51:114–122

    Article  CAS  PubMed  Google Scholar 

  • Takeda T, Toyofuku K, Matsukura C, Yamaguchi J (2001) Sugar transporters involved in flowering and grain development of rice. J Plant Physiol 158:465–470

    Article  CAS  Google Scholar 

  • Turgeon R (2010) The Role of Phloem Loading Reconsidered. Plant Physiol 152:1817–1823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang L, Lu Q, Wen X, Lu C (2015) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169:2848–2862

    CAS  PubMed  PubMed Central  Google Scholar 

  • Van Bel AJE (1993) The transport phloem. Specifics of its functioning. Prog Bot 54:134–150

    Google Scholar 

  • Weichert N, Saalbach I, Weichert H, Kohl S, Erban A, Kopka J, Hause B, Varshney A, Sreenivasulu N, Strickert M, Kumlehn J, Weschke W, Weber H (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol 152:698–710

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wippel K, Sauer N (2011) Arabidopsis SUC1 loads the phloem in suc2 mutants when expressed from the SUC2 promoter. J Exp Bot 63:669–679

    Article  PubMed  PubMed Central  Google Scholar 

  • Zakharov A, Giersberg M, Hosein F, Melzer M, Müntz K, Saalbach I (2004) Seed-specific promoters direct gene expression in nonseed tissue. J Exp Bot 55:1463–1471

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jong-Seong Jeon.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eom, JS., Nguyen, C.D., Lee, DW. et al. Genetic complementation analysis of rice sucrose transporter genes in Arabidopsis SUC2 mutant atsuc2 . J. Plant Biol. 59, 231–237 (2016). https://doi.org/10.1007/s12374-016-0015-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-016-0015-6

Keywords

Navigation