Advertisement

Planta

, Volume 228, Issue 1, pp 51–59 | Cite as

OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.)

  • Liqiang Jia
  • Botao Zhang
  • Chuanzao Mao
  • Jinhui Li
  • Yunrong Wu
  • Ping Wu
  • Zhongchang WuEmail author
Original Article

Abstract

A short root mutant was isolated from an EMS-generated rice mutant library. Under normal growth conditions, the mutant exhibited short root, delayed flowering, and partial sterility. Some sections of the roots revealed that the cell length along the longitudinal axis was reduced and the cell shape in the root elongation zone shrank. Genetic analysis indicated that the short root phenotype was controlled by a recessive gene. Map-based cloning revealed that a nucleotide substitution causing an amino acid change from Gly to Arg occurred in the predicted rice gene (Os02g0550600). It coded an alkaline/neutral invertase and was homologous to Arabidopsis gene AtCyt-inv1. This gene was designated as OsCyt-inv1. The results of carbohydrate analysis showed an accumulation of sucrose and reduction of hexose in the Oscyt-inv1 mutant. Exogenously supplying glucose could rescue the root growth defects of the Oscyt-inv1 mutant. These results indicated that OsCyt-inv1 played important roles in root cell development and reproductivity in rice.

Keywords

Map-based cloning Neutral invertase Oryza Short root 

Abbreviations

CAPS

Cleaved amplified polymorphic sequence

EMS

Ethylmethane sulfonate

STS

Sequence tagged site

Notes

Acknowledgments

We thank Dr. H.X. Shou from our institute for critical reading of the manuscript. This research was supported by the National Natural Science Foundation of China (30400021) and the Department of Science and Technology of Zhejiang Province, China.

References

  1. Bateman A, Birney E, Cerruti L, Durbin R, Etwiller L, Eddy SR, Griffiths-Jones S, Howe KL, Marshall M, Sonnhammer ELL (2004) The Pfam protein families database. Nucleic Acids Res 32:D138–D141PubMedCrossRefGoogle Scholar
  2. Beemster GT, Fiorani F, Inze D (2003) Cell cycle: the key to plant growth control? Trends Plant Sci 8:154–158PubMedCrossRefGoogle Scholar
  3. Dorion S, Lalonde S, Saini HS (1996) Induction of male sterility in wheat by meiotic-stage water deficit is receded by a decline in invertase activity and changes in carbohydrate metabolism in anthers. Plant Physiol 111:137–145PubMedGoogle Scholar
  4. Gallagher JA, Pollock CJ (1998) Isolation and characterization of a cDNA clone from Lolium termulentum L. encoding for a sucrose hydrolytic enzyme which shows alkaline/neutral invertase activity. J Exp Bot 49:789–795CrossRefGoogle Scholar
  5. Goetz M, Godt EE, Guivarc’h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98:6522–6527PubMedCrossRefGoogle Scholar
  6. Ji X, Van den Ende W, Van Laere A, Cheng S, Benett J (2005) Structure, evolution, and expression of the two invertase gene families of rice. J Mol Evol 60:615–634PubMedCrossRefGoogle Scholar
  7. Jiang HW, Wang SM, Dang L, Wang SF, Chen HM, Wu YR, Jiang XH, Wu P (2005) A novel short-root gene encodes a glucosamine-6-phosphate acetyltransferase required for maintaining normal root cell shape in rice. Plant Physiol 138:232–242PubMedCrossRefGoogle Scholar
  8. Kim JY, Mahe A, Brangeon J, Prioul JL (2000) A maize vacuolar invertase, IVR2, is induced by water stress organ/tissue specificity and diurnal modulation of expression. Plant Physiol 124:71–84PubMedCrossRefGoogle Scholar
  9. Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato fruit. Plant Physiol 103:863–870PubMedGoogle Scholar
  10. Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540PubMedCrossRefGoogle Scholar
  11. Koch KE (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7:235–246PubMedCrossRefGoogle Scholar
  12. Koonjul P K, Minhas JS, Nunes C, Sheoran I S, Saini HS (2005) Selective transcriptional down-regulation of anther invertases precedes the failure of pollen development in water-stressed wheat. J Exp Bot 56:179–190PubMedGoogle Scholar
  13. Lalonde S, Beebe D, Saini HS (1997a) Early signs of disruption of wheat anther development associated with the induction of male sterility by meiotic-stage water deficit. Sex Plant Reprod 10:40–48CrossRefGoogle Scholar
  14. Lee HS, Sturm A (1996) Purification and characterization of neutral and alkaline invertase from carrot. Plant Physiol 112:1513–1522PubMedCrossRefGoogle Scholar
  15. Li J, Zhu SH, Song XW, Shen Y, Chen HM, Yu J, Yi KK, Liu YF, Karplus VJ, Wu P, Deng XW (2006) A rice glutamater receptor-like gene is critical for the division and survival of individual cells in the root apical meristem. Plant Cell 18:340–349PubMedCrossRefGoogle Scholar
  16. Lou Y, Gou JY, Xue HW (2007) PIP5K9, an Arabidopsis phosphatidylinositl monophosphate kinase, interacts with a cytosolic invertase to negatively regulate sugar-mediated root growth. Plant Cell 19:163–181PubMedCrossRefGoogle Scholar
  17. Lynch J (1995) Root architecture and plant productivity. Plant Physiol 109:7–13PubMedGoogle Scholar
  18. Maddison AL, Hedley PE, Meyer RC, Aziz N, Davidson D, Machray GC (1999) Expression of tandem invertase genes associated with sexual and vegetative growth cycles in potato. Plant Mol Biol 41:741–751PubMedCrossRefGoogle Scholar
  19. Morris DA, Arthur ED (1985) Invertase activity, carbohydrate metabolism and cell expansion in the stem of Phaseolus vulgaris L. J Exp Bot 36:623–633CrossRefGoogle Scholar
  20. Mouchel CF, Briggs GC, Hardtke CS (2004) Natural genetic variation in Arabidopsis identifies BREVIS RADIX, a novel regulator of cell proliferation and elongation in the root. Genes Dev 18:700–714PubMedCrossRefGoogle Scholar
  21. Murayama S, Handa H (2007) Genes for alkaline/neutral invertase in rice: alkaline/neutral invertases are located in plant mitochondria and also in plastids. Planta 225:1193–1203PubMedCrossRefGoogle Scholar
  22. Qi XP, Wu ZC, Mo XR, Li JH, Wu SH, Chu J, Wu P (2007) AtCYT-INV1, a neutral invertase, is involved in osmotic stress-induced inhibition on lateral root growth in Arabidopsis. Plant Mol Biol 64:575–587PubMedCrossRefGoogle Scholar
  23. Ricardo CPP, Ap RT (1970) Invertase activity during the development of carrot roots. Phytochemistry 9:239–247CrossRefGoogle Scholar
  24. Roitsch T, Bittner M, Godt DE (1995) Induction of apoplastic invertases of Chenopodium rubrum by D-glucose and a glucose analog and tissue-specific expression suggest a role in sink-source regulation. Plant Physiol 108:285–294PubMedCrossRefGoogle Scholar
  25. Sergeeva LI, Keurentjes JB, Bentsink L, Vonk J, Plas LH, Koornneef M, Vreugdenhil D (2006) Vacuolar ivertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc Natl Acad Sci USA 103:2994–2999PubMedCrossRefGoogle Scholar
  26. Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9:161–169CrossRefGoogle Scholar
  27. Sturm A, Chrispeels MJ (1990) cDNA cloning of carrot extracellular β-furactosidase and its expression in response to wounding and bacterial infection. Plant Cell 2:1107–1119PubMedCrossRefGoogle Scholar
  28. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121:1–8PubMedCrossRefGoogle Scholar
  29. Vargas W, Cumino A, Salerno GL (2003) Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol. Planta 216:951–960PubMedGoogle Scholar
  30. Viola R, Roberts AG, Haupt S, Gazzani S, Hancock RD, Marmiroli N, Machray GC, Oparka KJ (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. Plant Cell 13:385–398PubMedCrossRefGoogle Scholar
  31. Weber H, Heim U, Golombek S, Borisjuk L, Manteuffel R, Wobus U (1998) Expression of a yeast-derived invertase in developing cotyledons of Vicia narbonensis alters the carbohydrate state and affects storage functions. Plant J 16:163–172PubMedCrossRefGoogle Scholar
  32. Yao SG, Taketa S, Ichii M (2002) A novel short-root gene that affects specifically early root development in rice (Oryza sativa L.). Plant Sci 163:207–215CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Liqiang Jia
    • 1
  • Botao Zhang
    • 1
  • Chuanzao Mao
    • 1
  • Jinhui Li
    • 1
  • Yunrong Wu
    • 1
  • Ping Wu
    • 1
  • Zhongchang Wu
    • 1
    Email author
  1. 1.The State Key Laboratory of Plant Physiology and Biochemistry, College of Life ScienceZhejiang UniversityHangzhouChina

Personalised recommendations