Transcriptome Analysis Reveals Photoperiod-Associated Genes Expressed in Rice Anthers.

Shiyu Sun, Duoxiang Wang, Jingbin Li, Yaqi Lei, Gang Li, WenGuo Cai, Xiangxiang Zhao, Wanqi Liang, Dabing Zhang
Author Information
  1. Shiyu Sun: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  2. Duoxiang Wang: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  3. Jingbin Li: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  4. Yaqi Lei: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  5. Gang Li: School of Agriculture, Food and Wine, University of Adelaide, Urrbrae, SA, Australia.
  6. WenGuo Cai: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  7. Xiangxiang Zhao: Jiangsu Collaborative Innovation Center of Regional Modern Agriculture and Environmental Protection, Huaiyin Normal University, Huai'an, China.
  8. Wanqi Liang: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.
  9. Dabing Zhang: Joint International Research Laboratory of Metabolic and Developmental Sciences, State Key Laboratory of Hybrid Rice, School of Life Sciences and Biotechnology, Shanghai Jiao Tong University, Shanghai, China.

Abstract

Environmental conditions, such as photoperiod and temperature, can affect male fertility in plants. While this feature is heavily exploited in rice to generate male-sterile lines for hybrid breeding, the underlying molecular mechanisms remain largely unknown. In this study, we use a transcriptomics approach to identify key genes and regulatory networks affecting pollen maturation in rice anthers in response to different day lengths. A total of 11,726 differentially expressed genes (DEGs) were revealed, of which 177 were differentially expressed at six time points over a 24-h period. GO enrichment analysis revealed that genes at all time points were enriched in transport, carbohydrate, and lipid metabolic processes, and signaling pathways, particularly phytohormone signaling. In addition, co-expression network analysis revealed four modules strongly correlated with photoperiod. Within these four modules, 496 hub genes were identified with a high degree of connectivity to other photoperiod-sensitive DEGs, including two previously reported photoperiod- and temperature-sensitive genes affecting male fertility, r and , respectively. This work provides a new understanding on photoperiod-sensitive pollen development in rice, and our gene expression data will provide a new, comprehensive resource to identify new environmentally sensitive genes regulating male fertility for use in crop improvement.

Keywords

References

  1. Plant Cell. 2012 Jun;24(6):2562-77 [PMID: 22685166]
  2. Science. 2007 Oct 12;318(5848):261-5 [PMID: 17872410]
  3. Proc Natl Acad Sci U S A. 2014 Jul 8;111(27):10013-8 [PMID: 24951508]
  4. Nature. 2017 Jan 5;541(7635):92-95 [PMID: 28002408]
  5. Curr Biol. 2005 Jan 11;15(1):47-54 [PMID: 15649364]
  6. Plant Cell. 2007 Aug;19(8):2624-35 [PMID: 17675406]
  7. Plant Physiol. 2003 Sep;133(1):73-83 [PMID: 12970476]
  8. Transgenic Res. 2000 Dec;9(6):453-62 [PMID: 11206974]
  9. Ann Bot. 2007 Nov;100(5):959-66 [PMID: 17704538]
  10. Mol Plant. 2012 Nov;5(6):1210-6 [PMID: 23024213]
  11. Planta. 2006 Aug;224(3):598-611 [PMID: 16552590]
  12. J Exp Bot. 2020 Feb 19;71(4):1294-1305 [PMID: 31701134]
  13. J Zhejiang Univ Sci B. 2011 Jun;12(6):436-47 [PMID: 21634036]
  14. Plant Cell. 2008 Oct;20(10):2603-18 [PMID: 18952778]
  15. Nucleic Acids Res. 2018 Jan 4;46(D1):D1229-D1236 [PMID: 28977518]
  16. Planta. 2011 Feb;233(2):309-23 [PMID: 21046148]
  17. Trends Plant Sci. 2014 Apr;19(4):240-9 [PMID: 24373845]
  18. Nat Rev Genet. 2001 Oct;2(10):815-22 [PMID: 11584298]
  19. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8675-9 [PMID: 7915844]
  20. OMICS. 2012 May;16(5):284-7 [PMID: 22455463]
  21. Plant Cell. 2017 Jan;29(1):70-89 [PMID: 28082384]
  22. J Genet Genomics. 2011 Sep 20;38(9):379-90 [PMID: 21930097]
  23. Plant Cell Physiol. 2009 Mar;50(3):644-51 [PMID: 19208695]
  24. Trends Plant Sci. 2018 Jan;23(1):53-65 [PMID: 29126789]
  25. Nat Commun. 2014 Sep 11;5:4884 [PMID: 25208476]
  26. Cell Res. 2012 Apr;22(4):649-60 [PMID: 22349461]
  27. Plant Cell Physiol. 2017 Jul 1;58(7):1238-1248 [PMID: 28838125]
  28. Plant Mol Biol. 2007 Nov;65(4):439-51 [PMID: 17874189]
  29. BMC Plant Biol. 2016 Jan 19;16:22 [PMID: 26786707]
  30. Biosci Biotechnol Biochem. 2003 Mar;67(3):556-62 [PMID: 12723603]
  31. Proc Natl Acad Sci U S A. 2013 Jan 2;110(1):76-81 [PMID: 23256151]
  32. J Integr Plant Biol. 2020 Jul;62(7):1034-1056 [PMID: 31486580]
  33. J Integr Plant Biol. 2016 Feb;58(2):127-35 [PMID: 25951042]
  34. Nature. 2003 Apr 17;422(6933):719-22 [PMID: 12700762]
  35. Plant Cell Physiol. 2013 Dec;54(12):2011-9 [PMID: 24068795]
  36. Plant Cell Physiol. 2003 Nov;44(11):1229-36 [PMID: 14634161]
  37. Plant Physiol. 2009 Aug;150(4):1955-71 [PMID: 19482918]
  38. Plant Cell. 2006 Nov;18(11):3015-32 [PMID: 17138699]
  39. PLoS Genet. 2016 Jul 22;12(7):e1006085 [PMID: 27447945]
  40. Plant Cell Rep. 2017 Jun;36(6):919-931 [PMID: 28299429]
  41. Plant Cell. 2005 Dec;17(12):3311-25 [PMID: 16278346]
  42. Genome Res. 2003 Nov;13(11):2498-504 [PMID: 14597658]
  43. Plant Physiol. 2015 Nov;169(3):2064-79 [PMID: 26392263]
  44. Rice (N Y). 2017 Dec 28;10(1):53 [PMID: 29282604]
  45. Plant Cell Physiol. 2007 Jan;48(1):110-21 [PMID: 17132630]
  46. J Exp Bot. 2010 Aug;61(13):3639-46 [PMID: 20603282]
  47. Genome Res. 1997 Oct;7(10):986-95 [PMID: 9331369]
  48. Plant Cell Physiol. 2015 Mar;56(3):497-509 [PMID: 25520407]
  49. Plant J. 2001 Jun;26(6):607-15 [PMID: 11489174]
  50. Plant Physiol. 2013 Jun;162(2):858-71 [PMID: 23629836]
  51. Rice (N Y). 2013 Feb 06;6(1):4 [PMID: 24280374]
  52. Genes Dev. 2002 Aug 1;16(15):2006-20 [PMID: 12154129]
  53. Plant Physiol. 2009 Jan;149(1):297-305 [PMID: 19011004]
  54. Proc Natl Acad Sci U S A. 2001 Jul 3;98(14):7922-7 [PMID: 11416158]
  55. Plant Cell. 2010 Mar;22(3):672-89 [PMID: 20305120]
  56. Plant Signal Behav. 2012 Feb;7(2):170-3 [PMID: 22307044]
  57. Plant Cell Physiol. 2016 Jul;57(7):1530-1543 [PMID: 27903806]
  58. Nucleic Acids Res. 2013 Jan;41(Database issue):D1206-13 [PMID: 23180765]
  59. Proc Natl Acad Sci U S A. 2017 Nov 14;114(46):12327-12332 [PMID: 29087306]
  60. Nucleic Acids Res. 2010 Oct;38(18):e178 [PMID: 20802226]
  61. Methods. 2001 Dec;25(4):402-8 [PMID: 11846609]
  62. BMC Bioinformatics. 2008 Dec 29;9:559 [PMID: 19114008]
  63. J Biol Chem. 2016 Sep 16;291(38):19994-20007 [PMID: 27502283]
  64. Int J Mol Sci. 2020 Mar 23;21(6): [PMID: 32209971]
  65. Plant Physiol. 2002 Oct;130(2):784-95 [PMID: 12376644]
  66. Nucleic Acids Res. 2000 Jan 1;28(1):27-30 [PMID: 10592173]
  67. Dev Cell. 2013 Oct 14;27(1):113-22 [PMID: 24094741]
  68. Nat Plants. 2018 Aug;4(8):530-533 [PMID: 29988153]
  69. Proc Natl Acad Sci U S A. 2012 Feb 14;109(7):2654-9 [PMID: 22308482]
  70. Plant Cell. 2007 Mar;19(3):847-61 [PMID: 17400897]
  71. Proc Natl Acad Sci U S A. 2016 Dec 27;113(52):15144-15149 [PMID: 27965387]
  72. Plant Physiol. 2009 Feb;149(2):745-59 [PMID: 19010999]
  73. Plant Cell Rep. 2014 Nov;33(11):1881-99 [PMID: 25138437]
  74. Plant Mol Biol. 1999 Dec;41(6):753-64 [PMID: 10737140]
  75. Nucleic Acids Res. 2017 Jul 3;45(W1):W122-W129 [PMID: 28472432]
  76. J Exp Bot. 2016 Oct;67(18):5485-5494 [PMID: 27555544]
  77. Plant Physiol. 2014 Apr;164(4):2011-9 [PMID: 24569847]
  78. Biosci Biotechnol Biochem. 2005 Feb;69(2):410-4 [PMID: 15725670]
  79. BMC Plant Biol. 2014 May 17;14:133 [PMID: 24884869]
  80. New Phytol. 2020 Mar;225(5):2077-2093 [PMID: 31663135]
  81. J Exp Bot. 2006;57(5):1149-60 [PMID: 16449373]
  82. PLoS Comput Biol. 2008 Aug 15;4(8):e1000117 [PMID: 18704157]