Optimization of rice panicle architecture by specifically suppressing ligand-receptor pairs.

Tao Guo, Zi-Qi Lu, Yehui Xiong, Jun-Xiang Shan, Wang-Wei Ye, Nai-Qian Dong, Yi Kan, Yi-Bing Yang, Huai-Yu Zhao, Hong-Xiao Yu, Shuang-Qin Guo, Jie-Jie Lei, Ben Liao, Jijie Chai, Hong-Xuan Lin
Author Information
  1. Tao Guo: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China. ORCID
  2. Zi-Qi Lu: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  3. Yehui Xiong: Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China.
  4. Jun-Xiang Shan: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China. ORCID
  5. Wang-Wei Ye: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  6. Nai-Qian Dong: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China. ORCID
  7. Yi Kan: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  8. Yi-Bing Yang: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  9. Huai-Yu Zhao: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  10. Hong-Xiao Yu: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  11. Shuang-Qin Guo: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  12. Jie-Jie Lei: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  13. Ben Liao: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China.
  14. Jijie Chai: Tsinghua-Peking Center for Life Sciences, School of Life Sciences, Tsinghua University, Beijing, 100084, China. chaijj@tsinghua.edu.cn. ORCID
  15. Hong-Xuan Lin: National Key Laboratory of Plant Molecular Genetics, CAS Centre for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, 200032, China. hxlin@cemps.ac.cn. ORCID

Abstract

Rice panicle architecture determines the grain number per panicle and therefore impacts grain yield. The OsER1-OsMKKK10-OsMKK4-OsMPK6 pathway shapes panicle architecture by regulating cytokinin metabolism. However, the specific upstream ligands perceived by the OsER1 receptor are unknown. Here, we report that the EPIDERMAL PATTERNING FACTOR (EPF)/EPF-LIKE (EPFL) small secreted peptide family members OsEPFL6, OsEPFL7, OsEPFL8, and OsEPFL9 synergistically contribute to rice panicle morphogenesis by recognizing the OsER1 receptor and activating the mitogen-activated protein kinase cascade. Notably, OsEPFL6, OsEPFL7, OsEPFL8, and OsEPFL9 negatively regulate spikelet number per panicle, but OsEPFL8 also controls rice spikelet fertility. A osepfl6 osepfl7 osepfl9 triple mutant had significantly enhanced grain yield without affecting spikelet fertility, suggesting that specifically suppressing the OsEPFL6-OsER1, OsEPFL7-OsER1, and OsEPFL9-OsER1 ligand-receptor pairs can optimize rice panicle architecture. These findings provide a framework for fundamental understanding of the role of ligand-receptor signaling in rice panicle development and demonstrate a potential method to overcome the trade-off between spikelet number and fertility.

References

  1. J Integr Plant Biol. 2020 May;62(5):581-600 [PMID: 31081210]
  2. iScience. 2021 Aug 10;24(9):102965 [PMID: 34466788]
  3. Nature. 2003 Apr 10;422(6932):618-21 [PMID: 12687001]
  4. Nat Rev Genet. 2018 Jan;19(1):21-33 [PMID: 29109524]
  5. Mol Plant. 2021 Jun 7;14(6):997-1011 [PMID: 33741527]
  6. Science. 2005 Jul 29;309(5735):741-5 [PMID: 15976269]
  7. Nat Commun. 2017 Nov 14;8(1):1497 [PMID: 29133783]
  8. Plant Physiol. 2022 Aug 29;190(1):516-531 [PMID: 35689635]
  9. Cell Res. 2017 Sep;27(9):1142-1156 [PMID: 28776570]
  10. Plant Cell. 2011 Sep;23(9):3276-87 [PMID: 21963665]
  11. Nat Genet. 2010 Jun;42(6):541-4 [PMID: 20495565]
  12. Development. 2004 Nov;131(22):5649-57 [PMID: 15509765]
  13. Plant Cell. 2008 Apr;20(4):934-46 [PMID: 18381924]
  14. Plant Cell. 2016 Oct;28(10):2453-2463 [PMID: 27634315]
  15. Plant Physiol. 2013 Jun;162(2):872-84 [PMID: 23629832]
  16. Hortic Res. 2021 Jun 1;8(1):130 [PMID: 34059650]
  17. Plant Physiol. 2022 Jan 20;188(1):460-476 [PMID: 34730827]
  18. Nat Genet. 2009 Apr;41(4):494-7 [PMID: 19305410]
  19. J Plant Physiol. 2019 Mar - Apr;234-235:18-27 [PMID: 30660943]
  20. Plant Biotechnol J. 2020 Feb;18(2):415-428 [PMID: 31301098]
  21. Plant J. 2007 Jan;49(1):64-78 [PMID: 17144896]
  22. Plant Physiol. 2020 Mar;182(3):1346-1358 [PMID: 31882455]
  23. Plant Cell. 2018 Apr;30(4):871-888 [PMID: 29588389]
  24. Science. 2008 Jan 18;319(5861):294 [PMID: 18202283]
  25. Proc Natl Acad Sci U S A. 2013 Feb 19;110(8):3167-72 [PMID: 23382237]
  26. Nature. 2014 Sep 11;513(7517):246-50 [PMID: 25043023]
  27. Nature. 2015 Jun 25;522(7557):439-43 [PMID: 26083750]
  28. Nat Plants. 2017 Nov;3(11):885-893 [PMID: 29085070]
  29. Nature. 2010 Jan 14;463(7278):241-4 [PMID: 20010603]
  30. Plant Cell. 2020 Sep;32(9):2763-2779 [PMID: 32616661]
  31. J Exp Bot. 2013 Dec;64(17):5335-43 [PMID: 23881395]
  32. Science. 2016 Dec 23;354(6319):1594-1597 [PMID: 27940581]
  33. Plant Cell. 2008 Aug;20(8):2049-58 [PMID: 18676878]
  34. Plant Cell. 2021 May 31;33(4):1212-1228 [PMID: 33693937]
  35. Cell. 1997 May 16;89(4):575-85 [PMID: 9160749]
  36. J Exp Bot. 2017 Jan;68(1):45-53 [PMID: 27965367]
  37. Mol Plant. 2015 Aug;8(8):1274-84 [PMID: 25917172]
  38. Proc Natl Acad Sci U S A. 2013 Jan 8;110(2):767-72 [PMID: 23267064]
  39. Plant Biotechnol J. 2019 Jun;17(6):1007-1009 [PMID: 30677211]
  40. Annu Rev Plant Biol. 2014;65:385-413 [PMID: 24779997]
  41. Nat Biotechnol. 2022 Sep;40(9):1403-1411 [PMID: 35449414]
  42. Annu Rev Plant Biol. 2014;65:553-78 [PMID: 24471834]
  43. Genes Dev. 2012 Jan 15;26(2):126-36 [PMID: 22241782]
  44. Proc Natl Acad Sci U S A. 2016 Aug 9;113(32):8969-74 [PMID: 27466405]
  45. New Phytol. 2023 Apr;238(1):186-201 [PMID: 36564978]
  46. Genes Dev. 2017 May 1;31(9):927-938 [PMID: 28536146]
  47. Annu Rev Plant Biol. 2010;61:421-42 [PMID: 20192739]
  48. Proc Natl Acad Sci U S A. 2012 Apr 17;109(16):6337-42 [PMID: 22474391]
  49. Proc Natl Acad Sci U S A. 2022 Apr 19;119(16):e2201195119 [PMID: 35412898]
  50. Proc Natl Acad Sci U S A. 2009 Nov 24;106(47):20103-8 [PMID: 19901325]
  51. Science. 1999 Mar 19;283(5409):1911-4 [PMID: 10082464]
  52. Plant Physiol. 2019 Jan;179(1):265-279 [PMID: 30409857]
  53. Plant Cell. 2009 Apr;21(4):1095-108 [PMID: 19346465]
  54. Plant Physiol. 2006 Nov;142(3):1039-52 [PMID: 17012407]
  55. Plant Biotechnol J. 2022 Jan;20(1):158-167 [PMID: 34498389]
  56. Plant Cell Environ. 2023 Feb;46(2):451-463 [PMID: 36419209]

MeSH Term

Plant Proteins
Oryza
Ligands
Edible Grain
Biological Transport

Chemicals

Plant Proteins
Ligands

Word Cloud

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