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Effects of Strigolactones on Grain Yield and Seed Development in Rice

  • Yusuke Yamada
  • Mami Otake
  • Takuma Furukawa
  • Masato Shindo
  • Koichiro Shimomura
  • Shinjiro Yamaguchi
  • Mikihisa UmeharaEmail author
Article
  • 147 Downloads

Abstract

Strigolactones (SLs) are well known as a class of endogenous phytohormones that regulate tiller bud outgrowth. Reduction of inorganic phosphate (Pi) induces the accumulation of SLs, which inhibit tiller bud outgrowth in wild-type (WT) rice plants, but not in SL mutants. This suggests that SLs are important for plant adaptation to Pi-deficient conditions. Thus, we investigated the effects of SLs on grain yield and seed size in WT and dwarf (d) mutant rice plants treated with various Pi concentrations. In both WT and d mutants, plant growth, chlorophyll levels, panicle number, number of hulls, and total grain number decreased as Pi decreased, indicating that SL is not required to mediate these Pi responses. The d mutants produced more panicles than the WT control, but there was no increase in grain yield, and the seed-setting rate decreased. Removal of outgrowing tillers did not affect grain yield in d mutants. GR24 (a synthetic SL) treatment rescued grain yield in d mutants. The d3 and d53 mutants had the lowest grain yields among d mutants. Furthermore, the endosperm of d mutants was 25% smaller than that of WT plants; there were no significant differences in embryo length between WT and d mutant plants, but the endosperm cell area of the d mutants was approximately 30% smaller than that of WT plants. We propose that SLs control grain yield and rice endosperm development.

Keywords

Endosperm Inorganic phosphate Oryza sativa Productivity Strigolactone Tillering 

Notes

Acknowledgements

We thank Junko Kyozuka (Tohoku University, Japan) for providing the rice seeds, and Hanako Nakamura and Soya Furusawa (Toyo University, Japan) for their technical assistance. This study was supported by Grants-in-Aid for Scientific Research on Innovative Areas and for Scientific Research (C) from Japan’s Ministry of Education, Culture, Sports, Science and Technology (Nos. 23119523 and 26450144 to M.U.), by the Inoue Enryo Memorial Foundation for Promoting Sciences from Toyo University to Y.Y., and was in part supported by Research Center for Life and Environmental Sciences, Toyo University.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

344_2018_9887_MOESM1_ESM.pdf (33.5 mb)
Supplementary material 1 (PDF 34332 KB)

References

  1. Abe S, Sado A, Tanaka K, Kisugi T, Asami K, Ota S, Kim HI, Yoneyama K, Xie X, Ohnishi T, Seto Y, Yamaguchi S, Akiyama K, Yoneyama K, Nomura T (2014) Carlactone is converted to carlactonoic acid by MAX1 in Arabidopsis and its methyl ester can directly interact with AtD14 in vitro. Proc Natl Acad Sci USA 111(50):18084–18089.  https://doi.org/10.1073/pnas.1410801111 CrossRefPubMedGoogle Scholar
  2. Agusti J, Herold S, Schwarz M, Sanchez P, Ljung K, Dun EA, Brewer PB, Beveridge CA, Sieberer T, Sehr EM, Greb T (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci USA 108(50):20242–20247.  https://doi.org/10.1073/pnas.1111902108 CrossRefPubMedGoogle Scholar
  3. Alder A, Jamil M, Marzorati M, Bruno M, Vermathen M, Bigler P, Ghisla S, Bouwmeester H, Beyer P, Al-Babili S (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335(6074):1348–1351.  https://doi.org/10.1126/science.1218094 CrossRefPubMedGoogle Scholar
  4. Arite T, Iwata H, Ohshima K, Maekawa M, Nakajima M, Kojima M, Sakakibara H, Kyozuka J (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51(6):1019–1029CrossRefGoogle Scholar
  5. Arite T, Umehara M, Ishikawa S, Hanada A, Maekawa M, Yamaguchi S, Kyozuka J (2009) d14, a strigolactone-insensitive mutant of rice, shows an accelerated outgrowth of tillers. Plant Cell Physiol 50(8):1416–1424.  https://doi.org/10.1093/pcp/pcp091 CrossRefPubMedGoogle Scholar
  6. Arite T, Kameoka H, Kyozuka J (2012) Strigolactone positively controls crown root elongation in rice. J Plant Growth Regul 31(2):165–172.  https://doi.org/10.1007/s00344-011-9228-6 CrossRefGoogle Scholar
  7. Booker J, Sieberer T, Wright W, Williamson L, Willett B, Stirnberg P, Turnbull C, Srinivasan M, Goddard P, Leyser O (2005) MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. Dev Cell 8(3):443–449CrossRefGoogle Scholar
  8. de Saint Germain A, Ligerot Y, Dun EA, Pillot JP, Ross JJ, Beveridge CA, Rameau C (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163(2):1012–1025.  https://doi.org/10.1104/pp.113.220541 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Gomez-Roldan V, Fermas S, Brewer PB, Puech-Pages V, Dun EA, Pillot JP, Letisse F, Matusova R, Danoun S, Portais JC, Bouwmeester H, Becard G, Beveridge CA, Rameau C, Rochange SF (2008) Strigolactone inhibition of shoot branching. Nature 455(7210):189–194CrossRefGoogle Scholar
  10. Hu ZY, Yan HF, Yang JH, Yamaguchi S, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51(7):1136–1142.  https://doi.org/10.1093/pcp/pcq075 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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(1):79–86CrossRefGoogle Scholar
  12. Jiang L, Liu X, Xiong G, Liu H, Chen F, Wang L, Meng X, Liu G, Yu H, Yuan Y, Yi W, Zhao L, Ma H, He Y, Wu Z, Melcher K, Qian Q, Xu HE, Wang Y, Li J (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504(7480):401–405.  https://doi.org/10.1038/nature12870 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kamachi K, Yamaya T, Mae T, Ojima K (1991) A role for glutamine-synthetase in the remobilization of leaf nitrogen during natural senescence in rice leaves. Plant Physiol 96(2):411–417CrossRefGoogle Scholar
  14. Kawamoto T (2003) Use of a new adhesive film for the preparation of multi-purpose fresh-frozen sections from hard tissues, whole-animals, insects and plants. Arch Histol Cytol 66(2):123–143CrossRefGoogle Scholar
  15. Kohlen W, Charnikhova T, Liu Q, Bours R, Domagalska MA, Beguerie S, Verstappen F, Leyser O, Bouwmeester H, Ruyter-Spira C (2011) Strigolactones are transported through the xylem and play a key role in shoot architectural response to phosphate deficiency in nonarbuscular mycorrhizal host Arabidopsis. Plant Physiol 155(2):974–987.  https://doi.org/10.1104/pp.110.164640 CrossRefPubMedGoogle Scholar
  16. Li N, Li Y (2016) Signaling pathways of seed size control in plants. Curr Opin Plant Biol 33:23–32.  https://doi.org/10.1016/j.pbi.2016.05.008 CrossRefPubMedGoogle Scholar
  17. Lin H, Wang RX, Qian Q, Yan MX, Meng XB, Fu ZM, Yan CY, Jiang B, Su Z, Li JY, Wang YH (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21(5):1512–1525CrossRefGoogle Scholar
  18. Lopez-Raez JA, Charnikhova T, Gomez-Roldan V, Matusova R, Kohlen W, De Vos R, Verstappen F, Puech-Pages V, Becard G, Mulder P, Bouwmeester H (2008) Tomato strigolactones are derived from carotenoids and their biosynthesis is promoted by phosphate starvation. New Phytol 178:863–874CrossRefGoogle Scholar
  19. Luquet D, Zhang BG, Dingkuhn M, Dexet A, Clement-Vidal A (2005) Phenotypic plasticity of rice seedlings: case of phosphorus deficiency. Plant Prod Sci 8(2):145–151CrossRefGoogle Scholar
  20. Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135(2):756–772.  https://doi.org/10.1104/pp.104.039826 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Nelson DC, Scaffidi A, Dun EA, Waters MT, Flematti GR, Dixon KW, Beveridge CA, Ghisalberti EL, Smith SM (2011) F-box protein MAX2 has dual roles in karrikin and strigolactone signaling in Arabidopsis thaliana. Proc Natl Acad Sci USA 108(21):8897–8902.  https://doi.org/10.1073/pnas.1100987108 CrossRefPubMedGoogle Scholar
  22. Ongaro V, Leyser O (2008) Hormonal control of shoot branching. J Exp Bot 59(1):67–74CrossRefGoogle Scholar
  23. Park MR, Baek SH, de Los Reyes BG, Yun SJ, Hasenstein KH (2012) Transcriptome profiling characterizes phosphate deficiency effects on carbohydrate metabolism in rice leaves. J Plant Physiol 169(2):193–205.  https://doi.org/10.1016/j.jplph.2011.09.002 CrossRefPubMedGoogle Scholar
  24. Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156(3):1006–1015.  https://doi.org/10.1104/pp.111.175281 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Ruyter-Spira C, Kohlen W, Charnikhova T, van Zeijl A, van Bezouwen L, de Ruijter N, Cardoso C, Lopez-Raez JA, Matusova R, Bours R, Verstappen F, Bouwmeester H (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155(2):721–734.  https://doi.org/10.1104/pp.110.166645 CrossRefPubMedGoogle Scholar
  26. Seto Y, Sado A, Asami K, Hanada A, Umehara M, Akiyama K, Yamaguchi S (2014) Carlactone is an endogenous biosynthetic precursor for strigolactones. Proc Natl Acad Sci USA 111(4):1640–1645.  https://doi.org/10.1073/pnas.1314805111 CrossRefPubMedGoogle Scholar
  27. Shindo M, Shimomura K, Yamaguchi S, Umehara M (2018) Upregulation of DWARF27 is associated with increased strigolactone levels under sulfur deficiency in rice. Plant Direct 2(4):e00050.  https://doi.org/10.1002/pld3.50 doiCrossRefGoogle Scholar
  28. Snowden KC, Simkin AJ, Janssen BJ, Templeton KR, Loucas HM, Simons JL, Karunairetnam S, Gleave AP, Clark DG, Klee HJ (2005) The Decreased apical dominance1/Petunia hybrida CAROTENOID CLEAVAGE DIOXYGENASE8 gene affects branch production and plays a role in leaf senescence, root growth, and flower development. Plant Cell 17(3):746–759CrossRefGoogle Scholar
  29. Sun H, Tao J, Liu S, Huang S, Chen S, Xie X, Yoneyama K, Zhang Y, Xu G (2014) Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot 65(22):6735–6746.  https://doi.org/10.1093/jxb/eru029 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Ueda H, Kusaba M (2015) Strigolactone regulates leaf senescence in concert with ethylene in Arabidopsis. Plant Physiol 169:138–147.  https://doi.org/10.1104/pp.15.00325 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Umehara M (2011) Strigolactone, a key regulator of nutrient allocation in plants. Plant Biotechnol 28(5):429–437.  https://doi.org/10.5511/plantbiotechnology.11.1109a CrossRefGoogle Scholar
  32. Umehara M, Hanada A, Yoshida S, Akiyama K, Arite T, Takeda-Kamiya N, Magome H, Kamiya Y, Shirasu K, Yoneyama K, Kyozuka J, Yamaguchi S (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455(7210):195–200CrossRefGoogle 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(7):1118–1126.  https://doi.org/10.1093/pcp/pcq084 CrossRefPubMedPubMedCentralGoogle Scholar
  34. Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195(2):306–320.  https://doi.org/10.1111/j.1469-8137.2012.04190.x CrossRefPubMedGoogle Scholar
  35. Wang Y, Li J (2011) Branching in rice. Curr Opin Plant Biol 14(1):94–99  https://doi.org/10.1016/j.pbi.2010.11.002 CrossRefPubMedPubMedCentralGoogle Scholar
  36. Wang Y, Sun S, Zhu W, Jia K, Yang H, Wang X (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27(6):681–688.  https://doi.org/10.1016/j.devcel.2013.11.010 CrossRefPubMedGoogle Scholar
  37. Waters MT, Smith SM (2013) KAI2- and MAX2-mediated responses to karrikins and strigolactones are largely independent of HY5 in Arabidopsis seedlings. Mol Plant 6(1):63–75.  https://doi.org/10.1093/mp/sss127 CrossRefPubMedGoogle Scholar
  38. Waters MT, Nelson DC, Scaffidi A, Flematti GR, Sun YK, Dixon KW, Smith SM (2012) Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis. Development 139:1285–1295.  https://doi.org/10.1242/dev.074567 CrossRefPubMedGoogle Scholar
  39. Woo HR, Chung KM, Park JH, Oh SA, Ahn T, Hong SH, Jang SK, Nam HG (2001) ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 13(8):1779–1790CrossRefGoogle Scholar
  40. Yamada Y, Furusawa S, Nagasaka S, Shimomura K, Yamaguchi S, Umehara M (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240(2):399–408.  https://doi.org/10.1007/s00425-014-2096-0 CrossRefPubMedGoogle Scholar
  41. Yan H, Saika H, Maekawa M, Takamure I, Tsutsumi N, Kyozuka J, Nakazono M (2007) Rice tillering dwarf mutant dwarf3 has increased leaf longevity during darkness-induced senescence or hydrogen peroxide-induced cell death. Genes Genet Syst 82(4):361–366CrossRefGoogle Scholar
  42. Yao R, Ming Z, Yan L, Li S, Wang F, Ma S, Yu C, Yang M, Chen L, Chen L, Li Y, Yan C, Miao D, Sun Z, Yan J, Sun Y, Wang L, Chu J, Fan S, He W, Deng H, Nan F, Li J, Rao Z, Lou Z, Xie D (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536(7617):469–473.  https://doi.org/10.1038/nature19073 CrossRefPubMedGoogle Scholar
  43. Yoneyama K, Xie X, Kusumoto D, Sekimoto H, Sugimoto Y, Takeuchi Y, Yoneyama K (2007a) Nitrogen deficiency as well as phosphorus deficiency in sorghum promotes the production and exudation of 5-deoxystrigol, the host recognition signal for arbuscular mycorrhizal fungi and root parasites. Planta 227(1):125–132CrossRefGoogle Scholar
  44. Yoneyama K, Yoneyama K, Takeuchi Y, Sekimoto H (2007b) Phosphorus deficiency in red clover promotes exudation of orobanchol, the signal for mycorrhizal symbionts and germination stimulant for root parasites. Planta 225(4):1031–1038.  https://doi.org/10.1007/s00425-006-0410-1 CrossRefPubMedGoogle Scholar
  45. Yoneyama K, Xie X, Kim HI, Kisugi T, Nomura T, Sekimoto H, Yokota T, Yoneyama K (2012) How do nitrogen and phosphorus deficiencies affect strigolactone production and exudation? Planta 235(6):1197–1207.  https://doi.org/10.1007/s00425-011-1568-8 CrossRefPubMedGoogle Scholar
  46. Yoneyama K, Xie X, Kisugi T, Nomura T, Yoneyama K (2013) Nitrogen and phosphorus fertilization negatively affects strigolactone production and exudation in sorghum. Planta 238:885–894.  https://doi.org/10.1007/s00425-013-1943-8 CrossRefPubMedGoogle Scholar
  47. Yoshida S, Kameoka H, Tempo M, Akiyama K, Umehara M, Yamaguchi S, Hayashi H, Kyozuka J, Shirasu K (2012) The D3 F-box protein is a key component in host strigolactone responses essential for arbuscular mycorrhizal symbiosis. New Phytol 196(4):1208–1216.  https://doi.org/10.1111/j.1469-8137.2012.04339.x CrossRefPubMedGoogle Scholar
  48. Yuan H, Liu D (2008) Signaling components involved in plant responses to phosphate starvation. J Integr Plant Biol 50(7):849–859.  https://doi.org/10.1111/j.1744-7909.2008.00709.x CrossRefPubMedPubMedCentralGoogle Scholar
  49. Zhang CQ, Xu Y, Lu Y, Yu HX, Gu MH, Liu QQ (2011) The WRKY transcription factor OsWRKY78 regulates stem elongation and seed development in rice. Planta 234(3):541–554.  https://doi.org/10.1007/s00425-011-1423-y CrossRefPubMedGoogle Scholar
  50. Zhang Y, van Dijk AD, Scaffidi A, Flematti GR, Hofmann M, Charnikhova T, Verstappen F, Hepworth J, van der Krol S, Leyser O, Smith SM, Zwanenburg B, Al-Babili S, Ruyter-Spira C, Bouwmeester HJ (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10(12):1028–1033.  https://doi.org/10.1038/nchembio.1660 CrossRefPubMedGoogle Scholar
  51. Zhang B, Ye W, Ren D, Tian P, Peng Y, Gao Y, Ruan B, Wang L, Zhang G, Guo L, Qian Q, Gao Z (2015) Genetic analysis of flag leaf size and candidate genes determination of a major QTL for flag leaf width in rice. Rice 8(1):39.  https://doi.org/10.1186/s12284-014-0039-9 CrossRefPubMedGoogle Scholar
  52. Zhou F, Lin Q, Zhu L, Ren Y, Zhou K, Shabek N, Wu F, Mao H, Dong W, Gan L, Ma W, Gao H, Chen J, Yang C, Wang D, Tan J, Zhang X, Guo X, Wang J, Jiang L, Liu X, Chen W, Chu J, Yan C, Ueno K, Ito S, Asami T, Cheng Z, Wang J, Lei C, Zhai H, Wu C, Wang H, Zheng N, Wan J (2013) D14-SCF(D3)-dependent degradation of D53 regulates strigolactone signalling. Nature 504(7480):406–410.  https://doi.org/10.1038/nature12878 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zou J, Zhang S, Zhang W, Li G, Chen Z, Zhai W, Zhao X, Pan X, Xie Q, Zhu L (2006) The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. Plant J 48(5):687–698CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Graduate School of Life SciencesToyo UniversityGunmaJapan
  2. 2.Department of Applied BiosciencesToyo UniversityGunmaJapan
  3. 3.Graduate School of Life SciencesTohoku UniversitySendaiJapan
  4. 4.Institute for Chemical ResearchKyoto UniversityKyotoJapan

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