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Journal of Plant Growth Regulation

, Volume 31, Issue 2, pp 165–172 | Cite as

Strigolactone Positively Controls Crown Root Elongation in Rice

  • Tomotsugu AriteEmail author
  • Hiromu Kameoka
  • Junko Kyozuka
Article

Abstract

Strigolactones are recently identified plant hormones that inhibit shoot branching. Pleiotropic defects in strigolactone-deficient or -insensitive mutants indicate that strigolactones control various aspects of plant growth and development. However, our understanding of the hormonal function of strigolactones in plants is very limited. In this study we demonstrate that rice dwarf mutants that are strigolactone-deficient or -insensitive exhibit a short crown root phenotype. Exogenous application of GR24, a synthetic strigolactone analog, complemented the crown root defect in strigolactone-deficient mutants but not in strigolactone-insensitive mutants. These observations imply that strigolactones positively regulate the length of crown roots. Histological observations revealed that the meristematic zone is shorter in dwarf mutants than in wild type, suggesting that strigolactones may exert their effect on roots via the control of cell division. We also show that crown roots of wild type, but not dwarf mutants, become longer under phosphate starvation.

Keywords

Cell division Oryza sativa Root development Phosphate starvation Strigolactone 

Notes

Acknowledgments

We thank Tadao Asami (University of Tokyo) for providing GR24, and Miho Takemura and Kanji Ohyama (Ishikawa Prefectural University) for providing T. Arite with facilities for carrying out the experiments.

References

  1. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827PubMedCrossRefGoogle Scholar
  2. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S et al (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50:1416–1424PubMedCrossRefGoogle Scholar
  3. Bar-Yosef B (1991) Root excretion and their environmental effects: influence on availability of phosphorus. In: Weisel Y, Eschel A, Kafkafi U (eds) Plant roots, the hidden half. C.H.I.P.S, New York, pp 529–557Google Scholar
  4. Beveridge CA, Kyozuka J (2010) New genes in the strigolactone-related shoot branching pathway. Curr Opin Plant Biol 13:34–39PubMedCrossRefGoogle Scholar
  5. Bouwmeester HJ, Matusova R, Zhongkui S, Beale MH (2003) Secondary metabolite signalling in host-parasitic plant interactions. Curr Opin Plant Biol 6:358–364PubMedCrossRefGoogle Scholar
  6. Gao Z, Qian Q, Liu X, Yan M, Feng Q, Dong G (2009) Dwarf 88, a novel putative esterase gene affecting architecture of rice plant. Plant Mol Biol 71:265–276PubMedCrossRefGoogle Scholar
  7. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pagès V, Dun EA, Pillot JP et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194PubMedCrossRefGoogle Scholar
  8. Heyward A, Stirnberg P, Beveridge C, Leyser O (2009) Interactions between auxin and strigolactone in shoot branching control. Plant Physiol 151:400–412CrossRefGoogle Scholar
  9. Hoshikawa K (1989) Growing rice plant—an anatomical monograph. Nosan Gyoson Bunka Kyokai, NobunkyoGoogle Scholar
  10. Hoshikawa K, Shoji K (1990) Nursling seedlings, their optimum ages for good rooting and the mechanism of rooting. Jpn J Crop Sci 59:173–174 (In Japanese)CrossRefGoogle Scholar
  11. Hu Z, Yan H, Yang J, Yamaguchi S, Maekawa M, Takamure I et al (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51:1136–1142PubMedCrossRefGoogle Scholar
  12. Ishikawa H, Evans ML (1995) Specialized zones of development in roots. Plant Physiol 109:725–727PubMedGoogle Scholar
  13. Ishikawa S, Maekawa M, Arite T, Onishi K, Takamure I, Kyozuka J (2005) Suppression of tiller bud activity in tillering dwarf mutants of rice. Plant Cell Physiol 46:79–86PubMedCrossRefGoogle Scholar
  14. Isobe K, Tsuboki Y (1998) The relationship between growth promotion by arbuscular mycorrhizal fungi and root morphology and phosphorus absorption in gramineous and leguminous crops. Jpn J Crop Sci 67:347–352CrossRefGoogle Scholar
  15. Kapulnik Y, Delaux PM, Resnik N, Mayzlish-Gati E, Wininger S, Bhattachaya C et al (2010) Strigolactones affect lateral root formation and root hair elongation in Arabidopsis. Planta 233:209–216PubMedCrossRefGoogle Scholar
  16. Koltai H, Dor E, Hershenhorn J, Joel DM, Weininger S, Lekalla S et al (2010) Strigolactones effect on root growth and root-hair elongation may be mediated by auxin-efflux carriers. J. Plant Growth Regul 29:129–136CrossRefGoogle Scholar
  17. Lin H, Wang R, Qian Q, Yan M, Meng X, Fu Z et al (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525PubMedCrossRefGoogle Scholar
  18. Linkohr BI, Williamson LC, Fitter AH, Leyser HM (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. Plant J 29:751–760PubMedCrossRefGoogle Scholar
  19. Liu W, Wu C, Fu Y, Hu G, Si H, Li Z et al (2009) Identification and characterization of HTD2: a novel gene negatively regulating tiller bud outgrowth in rice. Planta 230:649–658PubMedCrossRefGoogle Scholar
  20. López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256PubMedCrossRefGoogle Scholar
  21. López-Bucio J, Hernandez-Abreu E, Sanchez-Calderon L, Perez-Torres A, Rampey RA, Bartel B et al (2005) An auxin transport independent pathway is involved in phosphate stress-induced root architectural alterations in Arabidopsis. Identification of BIG as a mediator of auxin in pericycle cell activation. Plant Physiol 137:681–691PubMedCrossRefGoogle Scholar
  22. López-Ráez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R et al (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874PubMedCrossRefGoogle Scholar
  23. Minakuchi K, Kameoka H, Yasuno N, Umehara M, Luo L, Kobayashi K et al (2010) FINE CULM1 (FC1) works downstream of strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135PubMedCrossRefGoogle Scholar
  24. Pérez-Torres CA, López-Bucioa J, Cruz-Ramírezb A, Ibarra-Lacletteb E, Dharmasiric S et al (2008) Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–3272PubMedCrossRefGoogle Scholar
  25. Raghothama KG (1999) Phosphate acquisition. Ann Rev Plant Physiol Mol Biol 50:665–693CrossRefGoogle Scholar
  26. Ruyter-Spira C, Kohlen W, Charnikhova T, Zeijl A, Bezouwen L, Ruijter N et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: Another below-ground role for strigolactones? Plant Physiol 155:721–734PubMedCrossRefGoogle Scholar
  27. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J et al (1999) An auxin-dependent distal organizer of pattern and polarity in the arabidopsis root. Cell 99:463–472PubMedCrossRefGoogle Scholar
  28. Sasaki R, Hoshikawa K (1997) The role of crown roots from coleoptilar node in the rooting and development of transplanted rice nursling seedlings. Jpn J Crop Sci 66:259–267CrossRefGoogle Scholar
  29. Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL et al (2005) The decreased apical dominance 1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17:746–759PubMedCrossRefGoogle Scholar
  30. St. John TV (1980) Root size, root hairs and mycorrhizal infection: A re-examination of baylis shypothesis with tropical trees. New Phytol 84:483–487CrossRefGoogle Scholar
  31. Stirnberg P, van de Sande K, Leyser HMO (2002) MAX1 and MAX2 control shoot lateral branching in Arabidopsis. Development 129:1131–1141PubMedGoogle Scholar
  32. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200PubMedCrossRefGoogle Scholar
  33. Umehara M, Hanada A, Magome H, Takeda-Kamiya N, Yamaguchi S (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126PubMedCrossRefGoogle Scholar
  34. Williamson LC, Ribrioux SP, Fitter AH, Leyser HM (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol 126:875–882PubMedCrossRefGoogle Scholar
  35. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH et al (2001) ORE9, an F-Box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13:1779–1790PubMedCrossRefGoogle Scholar
  36. Yan H, Saika H, Maekawa M, Takemure I, Tsutsumi N, Kyozuka J et al (2007) Rice tillering dwarf mutant dwarf3 has increased leaf longevity during darkness-induced senescence or hydrogen peroxide-induced cell death. Genes Genet Syst 82:361–366PubMedCrossRefGoogle Scholar
  37. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225:1031–1038PubMedCrossRefGoogle Scholar
  38. Yoneyama K, Xie X, Sekimoto H, Takeuchi Y, Ogasawara S, Akiyama K et al (2008) Strigolactones, host recognition signals for root parasitic plants and arbuscular mycorrhizal fungi, from Fabaceae plants. New Phytol 179:484–494PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Tomotsugu Arite
    • 1
    • 2
    Email author
  • Hiromu Kameoka
    • 3
  • Junko Kyozuka
    • 3
  1. 1.Ishikawa Prefectural UniversityNonoichiJapan
  2. 2.Industrial Research Institute of IshikawaKanazawaJapan
  3. 3.Graduate School of Agriculture and Life SciencesUniversity of TokyoBunkyoJapan

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