Plant Hormone Cross Talk with a Focus on Strigolactone and Its Chemical Dissection in Rice

Chapter

Abstract

Plant hormones and several series of small molecules in plants play versatile roles in regulating plant growth and development. Since the finding of the first plant hormone auxin, the studies on both biosynthesis and signaling pathways of plant hormones have made a great progress because of the contribution of genomics and genetics. In rice, several dwarf (D) mutants that show dwarf phenotypes due to loss of functions or gain of functions in various genes have been determined to be involved in plant hormone biosynthesis or signaling pathways. Especially the studies on strigolactones (SLs) have greatly relied on D mutants including D27, D17, D10, D14, D3, and D53. Vice versa, SL studies deciphered how the genes regulate the phenotype and nutrition absorption in rice. In this chapter, we focus on summarizing the recent studies on the cross talk of SLs with other plant hormones to give an insight on the complexity of plant hormone signals. We also introduce and propose the combination of chemical regulators with genomics and genetics studies to drive the studies on plant forward.

Keywords

Plant hormone Cross talk Strigolactone Chemical regulator Dwarf mutant 

Notes

Acknowledgment

This work was supported in part by grants from the Core Research for Evolutional Science and Technology (CREST) and The Science and Technology Research Promotion Program for Agriculture, Fisheries, and Food Industry.

References

  1. Agusti J, Herold S, Schwarz M et al (2011) Strigolactone signaling is required for auxin-dependent stimulation of secondary growth in plants. Proc Natl Acad Sci U S A 108:20242–20247.  https://doi.org/10.1073/pnas.1111902108 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Akiyama K, Matsuzaki K, Hayashi H (2005) Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–827.  https://doi.org/10.1038/nature03608 CrossRefPubMedGoogle Scholar
  3. Alder A, Jamil M, Marzorati M et al (2012) The path from β-carotene to carlactone, a strigolactone-like plant hormone. Science 335:1348–1351.  https://doi.org/10.1126/science.1218094 CrossRefPubMedGoogle Scholar
  4. Arite T, Iwata H, Ohshima K et al (2007) DWARF10, an RMS1/MAX4/DAD1 ortholog, controls lateral bud outgrowth in rice. Plant J 51:1019–1029.  https://doi.org/10.1111/j.1365-313X.2007.03210.x CrossRefPubMedGoogle Scholar
  5. Arite T, Kameoka H, Kyozuka J (2012) Strigolactone positively controls crown root elongation in Rice. J Plant Growth Regul 31:165–172.  https://doi.org/10.1007/s00344-011-9228-6 CrossRefGoogle Scholar
  6. Asahina M, Tamaki Y, Sakamoto T et al (2014) Blue light-promoted rice leaf bending and unrolling are due to up-regulated brassinosteroid biosynthesis genes accompanied by accumulation of castasterone. Phytochemistry 104:21–29.  https://doi.org/10.1016/j.phytochem.2014.04.017 CrossRefPubMedGoogle Scholar
  7. Blackwell HE, Zhao Y (2003) Chemical genetic approaches to plant biology. Plant Physiol 133:448–455, 173:825–835.  https://doi.org/10.1104/pp.103.031138
  8. Cheng X, Ruyter-Spira C, Bouwmeester H (2013) The interaction between strigolactones and other plant hormones in the regulation of plant development. Front Plant Sci 4:199.  https://doi.org/10.3389/fpls.2013.00199 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clouse SD, Sasse JM (1998) BRASSINOSTEROIDS: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451.  https://doi.org/10.1146/annurev.arplant.49.1.427 CrossRefPubMedGoogle Scholar
  10. de Saint Germain A, Ligerot Y, Dun EA et al (2013) Strigolactones stimulate internode elongation independently of gibberellins. Plant Physiol 163:1012–1025.  https://doi.org/10.1104/pp.113.220541 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164.  https://doi.org/10.1146/annurev.arplant.54.031902.134921 CrossRefPubMedGoogle Scholar
  12. Gomez-Roldan V, Fermas S, Brewer PB et al (2008) Strigolactone inhibition of shoot branching. Nature 455:189–194.  https://doi.org/10.1038/nature07271 CrossRefPubMedGoogle Scholar
  13. Hayashi K, Tan X, Zheng N et al (2008) Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proc Natl Acad Sci 105:5632–5637.  https://doi.org/10.1073/pnas.0711146105 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Hayashi K, Neve J, Hirose M et al (2012) Rational design of an auxin antagonist of the SCF TIR1 auxin receptor complex. ACS Chem Biol 7:590–598.  https://doi.org/10.1021/cb200404c CrossRefPubMedGoogle Scholar
  15. Holbrook-Smith D, Toh S, Tsuchiya Y, McCourt P (2016) Small-molecule antagonists of germination of the parasitic plant striga hermonthica. Nat Chem Biol 12:724–729.  https://doi.org/10.1038/nchembio.2129 CrossRefPubMedGoogle Scholar
  16. Hu Z, Yan H, Yang J et al (2010) Strigolactones negatively regulate mesocotyl elongation in rice during germination and growth in darkness. Plant Cell Physiol 51:1136–1142.  https://doi.org/10.1093/pcp/pcq075 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Hu Z, Yamauchi T, Yang J et al (2014) Strigolactone and cytokinin act antagonistically in regulating rice mesocotyl elongation in darkness. Plant Cell Physiol 55:30–41.  https://doi.org/10.1093/pcp/pct150 CrossRefPubMedGoogle Scholar
  18. Ishikawa S, Maekawa M, Arite T et al (2005) Suppression of tiller bud activity in Tillering dwarf mutants of Rice. Plant Cell Physiol 46:79–86.  https://doi.org/10.1093/pcp/pci022 CrossRefPubMedGoogle Scholar
  19. Ito S, Yamagami D, Umehara M et al (2017) Regulation of strigolactone biosynthesis by gibberellin signaling. Plant Physiol 174:1250–1259.  https://doi.org/10.1104/pp.17.00301 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Jiang L, Liu X, Xiong G et al (2013) DWARF 53 acts as a repressor of strigolactone signalling in rice. Nature 504:401–405.  https://doi.org/10.1038/nature12870 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Jiang K, Otani M, Shimotakahara H et al (2017a) Substituted Phthalimide AC94377 is a selective agonist of the gibberellin receptor GID1. Plant Physiol 173:825–835.  https://doi.org/10.1104/pp.16.00937 CrossRefPubMedGoogle Scholar
  22. Jiang K, Shimotakahara H, Luo M et al (2017b) Chemical screening and development of novel gibberellin mimics. Bioorg Med Chem Lett.  https://doi.org/10.1016/j.bmcl.2017.07.012
  23. Kapulnik Y, Delaux P-M, Resnick N et al (2011) Strigolactones affect lateral root formation and root-hair elongation in Arabidopsis. Planta 233:209–216.  https://doi.org/10.1007/s00425-010-1310-y CrossRefPubMedGoogle Scholar
  24. Kitahata N, Asami T (2011) Chemical biology of abscisic acid. J Plant Res 124:549–557.  https://doi.org/10.1007/s10265-011-0415-0 CrossRefPubMedGoogle Scholar
  25. Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297.  https://doi.org/10.1007/s00344-003-0058-z CrossRefPubMedGoogle Scholar
  26. Li X, Sun S, Li C et al (2014) The strigolactone-related mutants have enhanced lamina joint inclination phenotype at the seedling stage. J Genet Genomics 41:605–608.  https://doi.org/10.1016/j.jgg.2014.09.004 CrossRefPubMedGoogle Scholar
  27. Lin H, Wang R, Qian Q et al (2009) DWARF27, an iron-containing protein required for the biosynthesis of strigolactones, regulates rice tiller bud outgrowth. Plant Cell 21:1512–1525.  https://doi.org/10.1105/tpc.109.065987 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lo S-F, Yang S-Y, Chen K-T et al (2008) A novel class of gibberellin 2-oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603–2618.  https://doi.org/10.1105/tpc.108.060913 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Mashita O, Koishihara H, Fukui K et al (2016) Discovery and identification of 2-methoxy-1-naphthaldehyde as a novel strigolactone-signaling inhibitor. J Pestic Sci 41:71–78.  https://doi.org/10.1584/jpestics.D16-028 CrossRefGoogle Scholar
  30. Minakuchi K, Kameoka H, Yasuno N et al (2010) FINE CULM1 (FC1) works downstream of Strigolactones to inhibit the outgrowth of axillary buds in rice. Plant Cell Physiol 51:1127–1135.  https://doi.org/10.1093/pcp/pcq083 CrossRefPubMedPubMedCentralGoogle Scholar
  31. Monte I, Hamberg M, Chini A et al (2014) Rational design of a ligand-based antagonist of jasmonate perception. Nat Chem Biol 10:671–676.  https://doi.org/10.1038/nchembio.1575 CrossRefPubMedGoogle Scholar
  32. Müssig C (2005) Brassinosteroid-promoted growth. Plant Biol 7:110–117.  https://doi.org/10.1055/s-2005-837493 CrossRefPubMedGoogle Scholar
  33. Nakamura H, Asami T (2014) Target sites for chemical regulation of strigolactone signaling. Front Plant Sci.  https://doi.org/10.3389/fpls.2014.00623
  34. Nakamura H, Xue YL, Miyakawa T et al (2013) Molecular mechanism of strigolactone perception by DWARF14. Nat Commun 4:2613.  https://doi.org/10.1038/ncomms3613 PubMedGoogle Scholar
  35. Parker C (2009) Observations on the current status of Orobanche and Striga problems worldwide. Pest Manag Sci 65:453–459.  https://doi.org/10.1002/ps.1713 CrossRefPubMedGoogle Scholar
  36. Ruyter-Spira C, Kohlen W, Charnikhova T et al (2011) Physiological effects of the synthetic strigolactone analog GR24 on root system architecture in Arabidopsis: another belowground role for strigolactones? Plant Physiol 155:721–734.  https://doi.org/10.1104/pp.110.166645 CrossRefPubMedGoogle Scholar
  37. Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288.  https://doi.org/10.1007/s00344-003-0062-3 CrossRefPubMedGoogle Scholar
  38. Singh I, Shono M (2005) Physiological and molecular effects of 24-epibrassinolide, a brassinosteroid on thermotolerance of tomato. Plant Growth Regul 47:111–119.  https://doi.org/10.1007/s10725-005-3252-0 CrossRefGoogle Scholar
  39. Sun H, Tao J, Liu S et al (2014) Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice. J Exp Bot 65:6735–6746.  https://doi.org/10.1093/jxb/eru029 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Sun H, Tao J, Hou M et al (2015) A strigolactone signal is required for adventitious root formation in rice. Ann Bot 115:1155–1162.  https://doi.org/10.1093/aob/mcv052 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Takeuchi J, Okamoto M, Akiyama T et al (2014) Designed abscisic acid analogs as antagonists of PYL-PP2C receptor interactions. Nat Chem Biol 10:477–482.  https://doi.org/10.1038/nchembio.1524 CrossRefPubMedGoogle Scholar
  42. Tong H, Liu L, Jin Y et al (2012) DWARF AND LOW-TILLERING acts as a direct downstream target of a GSK3/SHAGGY-like kinase to mediate brassinosteroid responses in rice. Plant Cell 24:2562–2577.  https://doi.org/10.1105/tpc.112.097394 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Ueguchi-Tanaka M, Nakajima M, Motoyuki A, Matsuoka M (2007) Gibberellin receptor and its role in gibberellin signaling in plants. Annu Rev Plant Biol 58:183–198.  https://doi.org/10.1146/annurev.arplant.58.032806.103830 CrossRefPubMedGoogle Scholar
  44. Umehara M, Hanada A, Yoshida S et al (2008) Inhibition of shoot branching by new terpenoid plant hormones. Nature 455:195–200.  https://doi.org/10.1038/nature07272 CrossRefPubMedGoogle Scholar
  45. Umehara M, Hanada A, Magome H et al (2010) Contribution of strigolactones to the inhibition of tiller bud outgrowth under phosphate deficiency in rice. Plant Cell Physiol 51:1118–1126.  https://doi.org/10.1093/pcp/pcq084 CrossRefPubMedPubMedCentralGoogle Scholar
  46. Vanstraelen M, Benková E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487.  https://doi.org/10.1146/annurev-cellbio-101011-155741 CrossRefPubMedGoogle Scholar
  47. Wada K, Marumo S, Ikekawa N et al (1981) Brassinolide and homobrassinolide promotion of lamina inclination of rice seedlings. Plant Cell Physiol 22:323–325.  https://doi.org/10.1093/oxfordjournals.pcp.a076173 CrossRefGoogle Scholar
  48. Wang ZY, Nakano T, Gendron J et al (2002) Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Dev Cell 2:505–513.  https://doi.org/10.1016/S1534-5807(02)00153-3 CrossRefPubMedGoogle Scholar
  49. Wang Y, Sun S, Zhu W et al (2013) Strigolactone/MAX2-induced degradation of brassinosteroid transcriptional effector BES1 regulates shoot branching. Dev Cell 27:681–688.  https://doi.org/10.1016/j.devcel.2013.11.010 CrossRefPubMedGoogle Scholar
  50. Xu J, Zha M, Li Y et al (2015) The interaction between nitrogen availability and auxin, cytokinin, and strigolactone in the control of shoot branching in rice (Oryza sativa L.) Plant Cell Rep 34:1647–1662.  https://doi.org/10.1007/s00299-015-1815-8 CrossRefPubMedGoogle Scholar
  51. Yamada Y, Furusawa S, Nagasaka S et al (2014) Strigolactone signaling regulates rice leaf senescence in response to a phosphate deficiency. Planta 240:399–408.  https://doi.org/10.1007/s00425-014-2096-0 CrossRefPubMedGoogle Scholar
  52. Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu Rev Plant Biol 59:225–251.  https://doi.org/10.1146/annurev.arplant.59.032607.092804 CrossRefPubMedGoogle Scholar
  53. Yao R, Ming Z, Yan L et al (2016) DWARF14 is a non-canonical hormone receptor for strigolactone. Nature 536:469–473.  https://doi.org/10.1038/nature19073 CrossRefPubMedGoogle Scholar
  54. Yin Y, Wang ZY, Mora-Garcia S et al (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell 109:181–191.  https://doi.org/10.1016/S0092-8674(02)00721-3 CrossRefPubMedGoogle Scholar
  55. Zhang LY, Bai MY, Wu J et al (2010a) Antagonistic HLH/bHLH transcription factors mediate brassinosteroid regulation of cell elongation and plant development in rice and arabidopsis. Plant Cell 21:3767–3780. doi:  https://doi.org/10.1105/tpc.109.070441
  56. Zhang S, Li G, Fang J et al (2010b) The interactions among DWARF10, auxin and cytokinin underlie lateral bud outgrowth in rice. J Integr Plant Biol 52:626–638.  https://doi.org/10.1111/j.1744-7909.2010.00960.x PubMedGoogle Scholar
  57. Zhang Y, van Dijk ADJ, Scaffidi A et al (2014) Rice cytochrome P450 MAX1 homologs catalyze distinct steps in strigolactone biosynthesis. Nat Chem Biol 10:1028–1033.  https://doi.org/10.1038/nchembio.1660 CrossRefPubMedGoogle Scholar
  58. Zhou F, Lin Q, Zhu L et al (2013) D14–SCFD3-dependent degradation of D53 regulates strigolactone signalling. Nature 504:406–410.  https://doi.org/10.1038/nature12878 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Department of Bioscience, Faculty of Applied BioscienceTokyo University of AgricultureTokyoJapan
  2. 2.Department of Applied Biological Chemistry, Graduate School of Agricultural and Life SciencesThe University of TokyoTokyoJapan

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