Skip to main content
SpringerLink
Log in

Identification and characterization of SHORTENED UPPERMOST INTERNODE 1, a gene negatively regulating uppermost internode elongation in rice

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In rice, the elongated internodes are derived from the vegetative shoot apical meristem (SAM), and the transition of the SAM from the vegetative to the reproductive stage induces internode elongation. In this study, we characterize two shortened uppermost internode mutants (sui1-1 and sui1-2). During the seedling and tillering stages, sui1 plants are morphologically similar to wild-type plants. However, at the heading stage, the sui1-1 mutant exhibits a shortened uppermost internode and a partly sheathed panicle, and the sui1-2 mutant shows an extremely shortened uppermost internode and a fully sheathed panicle. Gibberellin treatment results in elongation of every internode, but the shortened uppermost internode phenotype remains unaltered. Microscopic analysis indicates that cell length of sui1-1 uppermost internode exhibits decreased. Map-based cloning revealed that SUI1 is located on Chromosome 1, and encodes a putative phosphatidyl serine synthase (PSS) family protein. Searches for matches in protein databases showed that OsSUI1 contains the InterPro domain IPR004277, which is conserved in both animal and plant kingdoms. Introduction of a wild-type SUI1 gene fully rescued the mutant phenotype of sui1-1 and sui1-2, confirming the identity of the cloned gene. Consistent with these results, the SUI1-RNAi transgenic plants displayed decreased elongation of the uppermost internode. Our results suggest that SUI1 plays an important role in regulating uppermost internode length by decreasing longitudinal cell length in rice.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Achard P, Genschik P (2009) Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J Exp Bot 60:1085–1092

    Article  PubMed  CAS  Google Scholar 

  • Asano K, Miyao A, Hirochika H, Kitano H, Matsuoka M, Ashikari M (2010) SSD1, which encodes a plant-specific novel protein, controls plant elongation by regulating cell division in rice. Proc Jpn Acad Ser B Phys Biol Sci 86:265–273

    Article  PubMed  CAS  Google Scholar 

  • Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412

    Article  PubMed  CAS  Google Scholar 

  • De Lucas M, Davière JM, Rodríguez-Falcón M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blázquez MA, Titarenko E, Prat S (2008) A molecular framework for light and gibberellin control of cell elongation. Nature 451(7177):480–484

    Article  PubMed  Google Scholar 

  • Delhaize E, Hebb DM, Richards KD, Lin JM, Ryan PR, Gardner RC (1999) Cloning and expression of a wheat (Triticum aestivum L.) phosphatidylserine synthase cDNA. Overexpression in plants alters the composition of phospholipids. J Biol Chem 274:7082–7088

    Article  PubMed  CAS  Google Scholar 

  • Fan HY, Chen J, Lü CM, Zhang CY, Sun Q (2007) Proteomic Analysis of F2 Generation of Cucumber Against the Cucumber Powdery Mildew Disease. Acta Horticulturae Sinica 34:349–354 (Article in Chinese, abstract in English)

    Google Scholar 

  • Gangashetti MG, Jena KK, Shenoy VV, Freeman WH (2004) Inheritance of elongated uppermost internode and identification of RAPD marker linked to eui gene in rice. Curr Sci 87:469–475

    CAS  Google Scholar 

  • Haubrick LL, Assmann SM (2006) Brassinosteroids and plant function: some clues, more puzzles. Plant Cell Environ 29:446–457

    Article  PubMed  CAS  Google Scholar 

  • 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 6:271–282

    Article  PubMed  CAS  Google Scholar 

  • Kanfer J, Kennedy EP (1964) Metabolism and function of bacterial lipids. II. Biosynthesis of phospholipids in Escherichia Coli. J Biol Chem 239:1720–1726

    PubMed  CAS  Google Scholar 

  • Kawakatsu T, Itoh J, Miyoshi K, Kurata N, Alvarez N, Veit B, Nagato Y (2006) PLASTOCHRON2 regulates leaf initiation and maturation in rice. Plant Cell 18:612–625

    Article  PubMed  CAS  Google Scholar 

  • Kuge O, Nishijima M (1997) Phosphatidylserine synthase I and II of mammalian cells. Biochim Biophys Acta 1348:151–156

    PubMed  CAS  Google Scholar 

  • Li J, Yuan L (2000) Hybrid rice: genetics, breeding and seed production. Plant Breed Rev 17:150–158

    Google Scholar 

  • Liu Y, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Luo A, Qian Q, Yin H, Liu X, Yin C, Lan Y, Tang J, Tang Z, Cao S, Wang X, Xia K, Fu X, Luo D, Chu C (2006) EUI1, encoding a putative cytochrome P450 monooxygenase, regulates internode elongation by modulating gibberellin responses in rice. Plant Cell Physiol 47(2):181–191

    Article  PubMed  CAS  Google Scholar 

  • Miki D, Itoh R, Shimamoto K (2005) RNA silencing of single and multiple members in a gene family of rice. Plant Physiol 138:1903–1913

    Article  PubMed  CAS  Google Scholar 

  • Miyoshi K, Ahn BO, Kawakatsu T, Ito Y, Itoh J, Nagato Y, Kurata N (2004) PLASTOCHRON1, a timekeeper of leaf initiation in rice, encodes cytochrome P450. Proc Natl Acad Sci USA 101:875–880

    Article  PubMed  CAS  Google Scholar 

  • Qiao BJ, Wang YY, Zhu XB, Hong DL (2007) QTL analysis of the uppermost internode length in rice under different growing environments. Yi Chuan 29:1001–1007 (Article in Chinese, abstract in English)

    Google Scholar 

  • Rieu I, Eriksson S, Powers SJ, Gong F, Griffiths J, Woolley L, Benlloch R, Nilsson O, Thomas SG, Hedden P, Phillips AL (2008a) Genetic analysis reveals that C19-GA 2-oxidation is a major gibberellin inactivation pathway in Arabidopsis. Plant Cell 20(9):2420–2436

    Article  PubMed  CAS  Google Scholar 

  • Rieu I, Ruiz-Rivero O, Fernandez-Garcia N, Griffiths J, Powers SJ, Gong F, Linhartova T, Eriksson S, Nilsson O, Thomas SG, Phillips AL, Hedden P (2008b) The gibberellin biosynthetic genes AtGA20ox1 and AtGA20ox2 act, partially redundantly, to promote growth and development throughout the Arabidopsis life cycle. Plant J 53:488–504

    Article  PubMed  CAS  Google Scholar 

  • Rushton PJ, Somssich IE, Ringler P, Shen QJ (2010) WRKY transcription factors. Trends Plant Sci 15:247–258

    Article  PubMed  CAS  Google Scholar 

  • Sakamoto T, Miura K, Itoh H, Tatsumi T, Ueguchi-Tanaka M, Ishiyama K, Kobayashi M, Agrawal GK, Takeda S, Abe K, Miyao A, Hirochika H, Kitano H, Ashikari M, Matsuoka M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134(4):1642–1653

    Article  PubMed  CAS  Google Scholar 

  • Shen ZT, Yang CD, He ZH (1987) Studies on eliminating panicle enclosure in WA type MS line of rice Oryza sativa subsp. indica. Chin J Rice Sci 1:95–99 (Article in Chinese, abstract in English)

    Google Scholar 

  • Smith TK, Bütikofer P (2010) Lipid metabolism in Trypanosoma brucei. Mol Biochem Parasitol 172:66–79

    Article  PubMed  CAS  Google Scholar 

  • Takeda K (1977) Internode elongation and dwarfism in some gramineous plants. Gamma Field Symp 16:1–18

    Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci USA 98:5116–5121

    Article  PubMed  CAS  Google Scholar 

  • Vance JE, Steenbergen R (2005) Metabolism and functions of phosphatidylserine. Prog Lipid Res 44:207–234

    Article  PubMed  CAS  Google Scholar 

  • Vences-Guzmán MA, Geiger O, Sohlenkamp C (2008) Sinorhizobium meliloti mutants deficient in phosphatidylserine decarboxylase accumulate phosphatidylserine and are strongly affected during symbiosis with alfalfa. J Bacteriol 190:6846–6856

    Article  PubMed  Google Scholar 

  • Wang L, Yin H, Qian Q, Yang J, Huang C, Hu X, Luo D (2009) NECK LEAF 1, a GATA type transcription factor, modulates organogenesis by regulating the expression of multiple regulatory genes during reproductive development in rice. Cell Res 19:598–611

    Article  PubMed  CAS  Google Scholar 

  • Xu ZS, Liu L, Ni ZY, Liu P, Chen M, Li LC, Chen YF, Ma YZ (2009) W55a encodes a novel protein kinase that is involved in multiple stress responses. J Integr Plant Biol 51:58–66

    Article  PubMed  CAS  Google Scholar 

  • Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12:1591–1606

    Article  PubMed  CAS  Google Scholar 

  • Yamaoka Y, Yu Y, Mizoi J, Fujiki Y, Saito K, Nishijima M, Lee Y, Nishida I (2011) PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Plant J 67(4):648–661

    Google Scholar 

  • Yang RC, Huang RH, Zhang QQ, Zhang SB, Liang KJ (2000) Developing eui-cytoplasmic male sterile lines and applying them in hybrid rice breeding. Int Rice Res Newsl 25:11–12

    Google Scholar 

  • Yang SL, Yang RC, Qu XP, Zhang QQ, Huang RH, Wang B (2001) Genetic and microsatellite analyses of a new elongated uppermost internode gene eui2 of rice. Acta Botanica Sinica 43:67–71 (Article in Chinese, abstract in English)

    Google Scholar 

  • Yang RC, Zhang SB, Huang RH, Yang SL Zhang QQ (2002) Breeding technology of eui hybrids of rice. Sci Agric Sin 35:233–237 (Article in Chinese, abstract in English)

    Google Scholar 

  • Yin C, Gan L, Ng D, Zhou X, Xia K (2007) Decreased panicle-derived indole-3-acetic acid reduces gibberellin A1 level in the uppermost internode, causing panicle enclosure in male sterile rice Zhenshan 97A. J Exp Bot 58(10):2441–2449

    Article  PubMed  CAS  Google Scholar 

  • Zhang LY, Bai MY, Wu J, Zhu JY, Wang H, Zhang Z, Wang W, Sun Y, Zhao J, Sun X, Yang H, Xu Y, Kim SH, Fujioka S, Lin WH, Chong K, Lu T, Wang ZY (2009) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and Arabidopsis. Plant Cell. 21(12):3767–3780

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Nomura T, Xu Y, Zhang Y, Peng Y, Mao B, Hanada A, Zhou H, Wang R, Li P, Zhu X, Mander LN, Kamiya Y, Yamaguchi S, He Z (2006) ELONGATED UPPERMOST INTERNODE encodes a cytochrome P450 monooxygenase that epoxidizes gibberellins in a novel deactivation reaction in rice. Plant Cell 18:442–456

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Jianru Zuo at the Institute of Genetics and Developmental Biology, Chinese Academy of Sciences for the critical reading of the manuscript, Dr. Bin Han (National Center for Gene Research and Institute of Plant Physiology and Ecology, Chinese Academy of Sciences) for providing BAC clones, and Honglan Yan for photography. This work was supported by grants from the National Natural Science Foundation of China (Grant Nos. 30921140408; 30710103903; 31171532), the Zhejiang Natural Science Foundation (Grant Nos. Y3100357, Y308044), and the Transgenic Plant Research and Commercialization Project of the Ministry of Agriculture of China (Grant No. 2008ZX08011-001, 2008ZX08001-002).

Author information

Authors and Affiliations

  1. State Key Laboratory of Rice Biology, China National Rice Research Institute, Chinese Academy of Agricultural Sciences, 359 Tiyuchang Road, Hangzhou, 310006, China

    Li Zhu, Jiang Hu, Keming Zhu, Yunxia Fang, Zhenyu Gao, Yinghong He, Guangheng Zhang, Longbiao Guo, Dali Zeng, Guojun Dong, Meixian Yan, Jian Liu & Qian Qian

Authors
  1. Li Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jiang Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Keming Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunxia Fang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zhenyu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yinghong He
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Guangheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Longbiao Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Dali Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Guojun Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Meixian Yan
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jian Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Qian Qian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Qian Qian.

Additional information

Li Zhu, Jiang Hu and Keming Zhu have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhu, L., Hu, J., Zhu, K. et al. Identification and characterization of SHORTENED UPPERMOST INTERNODE 1, a gene negatively regulating uppermost internode elongation in rice. Plant Mol Biol 77, 475 (2011). https://doi.org/10.1007/s11103-011-9825-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11103-011-9825-6

Keywords

Search

Navigation