Plant Biotechnology Reports

, Volume 7, Issue 1, pp 83–90 | Cite as

Transgenic overexpression of UIP1, an interactor of the 3′ untranslated region of the Rubisco small subunit mRNA, increases rice tolerance to drought

  • Su-Hyun Park
  • Jin Seo Jeong
  • Mark C. F. R. Redillas
  • Harin Jung
  • Seung Woon Bang
  • Youn Shic Kim
  • Ju-Kon Kim
Original Article

Abstract

Gene regulation at the post-transcriptional level is a well-organized process to adjust plants in response to environmental changes. Here, we identified a novel RNA-binding protein (RBP) possessing a CBS (cystathionine-β-synthase) domain through yeast three-hybrid screening. This RBP, 3′-UTR-interacting protein 1 (UIP1), interacts with 3′ untranslated region of the Rubisco small subunit mRNA (3′ RbcS)—the major mRNA element that mediates the stress-induced mRNA decay (SMD) under drought and salt stress conditions. Six deletion constructs were made to delineate the binding domain of the UIP1 protein. Co-transformation of yeast with these constructs together with three different hybrid RNAs in various combinations showed that deletion of 51 N-terminal amino acids resulted in a loss of sequence-specific binding affinity. Further deletion at the region between 52 and 212 amino acids revealed that the CBS domain of UIP1 is necessary for binding to 3′ RbcS. Transgenic overexpression of UIP1 in rice resulted in an increase in tolerance to drought stress at the vegetative stage of growth. Under drought, high salt and low temperature conditions, the maximum photochemical efficiency of photosystem II (F v /F m) of UIP1 plants was higher than those of the nontransgenic plants. Interestingly, the effect of UIP1 overexpression on tolerance to stress was much more pronounced under drought than under high salt and low temperature conditions. Taken together, our results demonstrate that UIP1 interacts with 3′ untranslated region of RbcS1 mRNA and increases tolerance of transgenic overexpressors to drought stress.

Keywords

UIP1 (3′-UTR-interacting protein 1) 3′RbcS Yeast three-hybrid Transgenic rice Drought tolerance SMD 

Notes

Acknowledgments

This study was supported by the Rural Development Administration under “Cooperative Research Program for Agriculture Science and Technology Development” (Project No. PJ906910), the Next generation BioGreen 21 Program (Project No. PJ007971 to J.-K.K. and PJ009022 to J.S.J), the Ministry of Education, Science and Technology under “Mid-career Researcher Program” (Project No. 20100026168).

References

  1. Bailey-Serres J, Sorenson R, Juntawong P (2009) Getting the message across: cytoplasmic ribonucleoprotein complexes. Trends Plant Sci 14:443–453PubMedCrossRefGoogle Scholar
  2. Bernstein DS, Buter N, Stumpf C, Wickens M (2002) Analyzing mRNA–protein complexes using a yeast three-hybrid system. Methods 26:123–141PubMedCrossRefGoogle Scholar
  3. Castiglioni P, Warner D, Bensen RJ, Anstrom DC, Harrison J, Stoecker M, Abad M, Kumar G, Salvador S, D’Ordine R, Navarro S, Back S, Fernandes M, Targolli J, Dasgupta S, Bonin C, Luethy MH, Heard JE (2008) Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions. Plant Physiol 147:446–455PubMedCrossRefGoogle Scholar
  4. Dreyfuss G, Kim VN, Kataoka N (2002) Messenger-RNA-binding proteins and the messages they carry. Nat Rev Mol Cell Biol 3:195–205PubMedCrossRefGoogle Scholar
  5. Estévez R, Pusch M, Ferrer-Costa C, Orozco M, Jentsch T (2004) Functional and structural conservation of CBS domains from CLC chloride channels. J Physiol 557:363–378PubMedCrossRefGoogle Scholar
  6. Gong Z, Dong C-H, Lee H, Zhu J, Xiong L, Gong D, Stevenson B, Zhu J-K (2005) A dead box RNA helicase is essential for mRNA export and important for development and stress responses in Arabidopsis. Plant Cell 17:256–267PubMedCrossRefGoogle Scholar
  7. Guthrie C, Steitz J (2005) Nucleus and gene expression: coordinated nuclear events regulate mRNA synthesis, processing, export and turnover. Curr Opin Cell Biol 17:239–241CrossRefGoogle Scholar
  8. Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785PubMedCrossRefGoogle Scholar
  9. Hedbacker K, Carlson M (2009) SNF1/AMPK pathways in yeast. Front Biosci 13:2408–2420CrossRefGoogle Scholar
  10. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282PubMedCrossRefGoogle Scholar
  11. Hook B, Bernstein D, Zhang B, Wickens M (2005) RNA–protein interactions in the yeast three-hybrid system: affinity, sensitivity, and enhanced library screening. RNA 11:227–233Google Scholar
  12. Jang I-C, Choi W-B, Lee K-H, Song SI, Nahm BH, Kim J-K (2002) High-Level and ubiquitous expression of the rice cytochrome c gene OsCc1 and its promoter activity in transgenic plants provides a useful promoter for transgenesis of monocots. Plant Physiol 129:1473–1481PubMedCrossRefGoogle Scholar
  13. Jeong JS, Kim YS, Baek K-H, Jung H, Ha SH, Choi YD, Kim M, Reuzeau C, Kim J-K (2010) Root specific expression of OsNAC10 improves drought tolerance and grain yield in rice under field drought conditions. Plant Physiol 153:185–197PubMedCrossRefGoogle Scholar
  14. Jung H, Kim J-K, Ha S-H (2011) Use of animal viral internal ribosome entry site sequence makes multiple truncated transcripts without mediating polycistronic expression in rice. J Korean Soc Appl Biol Chem 54:678–684Google Scholar
  15. Kim JY, Kim WY, Kwak KJ, Oh SH, Han YS, Kang H (2010) Glycine-rich RNA-binding proteins are functionally conserved in Arabidopsis thaliana and Oryza sativa during cold adaptation process. J Exp Bot 61:2317–2325PubMedCrossRefGoogle Scholar
  16. Kushwaha HR, Singh AK, Sopory SK, Singla-Pareek SL, Pareek A (2009) Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.) Heynh and Oryza sativa L. reveals their developmental and stress regulation. BMC Genomics 10:200. doi: 10.1186/1471-2164-10-200 PubMedCrossRefGoogle Scholar
  17. Lee BH, Kapoor A, Zhu J, Zhu J-K (2006) STABILIZED1, a stress upregulated nuclear protein, is required for pre-mRNA splicing, mRNA turnover, and stress tolerance in Arabidopsis. Plant Cell 18:1736–1749PubMedCrossRefGoogle Scholar
  18. Lejeune F, Maquat LE (2005) Mechanistic links between nonsense-mediated mRNA decay and pre-mRNA splicing in mammalian cells. Curr Opin Cell Biol 17:309–315PubMedCrossRefGoogle Scholar
  19. Lorković ZJ (2009) Role of plant RNA-binding proteins in development, stress response and genome organization. Trends Plant Sci 14:1360–1385Google Scholar
  20. Lorković ZJ, Barta A (2002) Genome analysis: RNA recognition motif (RRM) and K homology (KH) domain RNA-binding proteins from the flowering plant Arabidopsis thaliana. Nucl Acids Res 30:623–635PubMedCrossRefGoogle Scholar
  21. Matsumoto K, Minami M, Shinozaki F, Suzuki Y, Abe K, Zenno S, Matsumoto S, Minami Y (2011) Hsp90 is involved in the formation of P-bodies and stress granules. Biochem Biop Res Commun 407:720–724CrossRefGoogle Scholar
  22. Meyer S, Savaresi S, Forster IC, Dutzler R (2007) Nucleotide recognition by the cytoplasmic domain of the human chloride transporter ClC-5. Nat Struct Mol Biol 14:60–67. doi: 10.1038/nsmb1188 PubMedCrossRefGoogle Scholar
  23. Moore MJ (2005) From birth to death: the complex lives of mRNAs. Science 309:1514–1518PubMedCrossRefGoogle Scholar
  24. Morris RT, Doroshenkb KA, Croftsb AJ, Lewisa N, Okitab TW, Wyrick JJ (2011) RiceRBP: a database of experimentally identified RNA-binding proteins in Oryza sativa L. Plant Sci 180:204–211PubMedCrossRefGoogle Scholar
  25. Park S-H, Chung PJ, Juntawong P, Bailey-Serres J, Kim YS, Jung H, Bang SW, Kim Y-K, Choi YD, Kim J-K (2012) Post-transcriptional control of photosynthetic mRNA decay under stress conditions requires 3′ and 5′ untranslated regions and correlates with differential polysome association in rice. Plant Physiol. doi: 10.1104/pp.112.194928
  26. Redillas MCF, Jeong JS, Strasser RJ, Kim YS, Kim J-K (2011) JIP analysis on rice (Oryza sativa cv. Nipponbare) grown under limited nitrogen conditions. J Korean Soc Appl Biol Chem 54(5):827–832Google Scholar
  27. SenGupta DJ, Zhang B, Kraemer B, Pochart P, Fields S, Wickens M, Bernstein DS, Buter N, Stumpf C (1996) A three-hybrid system to detect RNA–protein interactions in vivo. Proc Natl Acad Sci USA 93:8496–8501PubMedCrossRefGoogle Scholar
  28. Wurth L (2012) Versatility of RNA-binding proteins in cancer. Comp Funct Genom. doi: 10.1155/2012/178525
  29. Xu J, Chua NH NH (2011) Processing bodies and plant development. Curr Opin Plant Biol 14:88–93PubMedCrossRefGoogle Scholar
  30. Zhu J, Dong C-H, Zhu J-K (2007) Interplay between cold-responsive gene regulation, metabolism and RNA processing during plant cold acclimation. Curr Opin Plant Biol 10:290–295PubMedCrossRefGoogle Scholar

Copyright information

© Korean Society for Plant Biotechnology and Springer 2012

Authors and Affiliations

  • Su-Hyun Park
    • 1
  • Jin Seo Jeong
    • 1
  • Mark C. F. R. Redillas
    • 1
  • Harin Jung
    • 1
  • Seung Woon Bang
    • 1
  • Youn Shic Kim
    • 1
  • Ju-Kon Kim
    • 1
  1. 1.School of Biotechnology and Environmental EngineeringMyongji UniversityYonginKorea

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