Seeing the unseen in characterizing RNA editome during rice endosperm development.

Ming Chen, Lin Xia, Xinyu Tan, Shenghan Gao, Sen Wang, Man Li, Yuansheng Zhang, Tianyi Xu, Yuanyuan Cheng, Yuan Chu, Songnian Hu, Shuangyang Wu, Zhang Zhang
Author Information
  1. Ming Chen: National Genomics Data Center, China National Center for Bioinformation, Beijing, China. ORCID
  2. Lin Xia: National Genomics Data Center, China National Center for Bioinformation, Beijing, China.
  3. Xinyu Tan: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  4. Shenghan Gao: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China. ORCID
  5. Sen Wang: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China.
  6. Man Li: National Genomics Data Center, China National Center for Bioinformation, Beijing, China.
  7. Yuansheng Zhang: National Genomics Data Center, China National Center for Bioinformation, Beijing, China.
  8. Tianyi Xu: National Genomics Data Center, China National Center for Bioinformation, Beijing, China. ORCID
  9. Yuanyuan Cheng: National Genomics Data Center, China National Center for Bioinformation, Beijing, China.
  10. Yuan Chu: National Genomics Data Center, China National Center for Bioinformation, Beijing, China.
  11. Songnian Hu: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China. husn@im.ac.cn. ORCID
  12. Shuangyang Wu: Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing, China. shuangyang.wu@gmi.oeaw.ac.at. ORCID
  13. Zhang Zhang: National Genomics Data Center, China National Center for Bioinformation, Beijing, China. zhangzhang@big.ac.cn. ORCID

Abstract

Rice (Oryza sativa L.) endosperm is essential to provide nutrients for seed germination and determine grain yield. RNA editing, a post-transcriptional modification essential for plant development, unfortunately, is not fully characterized during rice endosperm development. Here, we perform systematic analyses to characterize RNA editome during rice endosperm development. We find that most editing sites are C-to-U CDS-recoding in mitochondria, leading to increased hydrophobic amino acids and changed structures of mitochondrial proteins. Comparative analysis of RNA editome reveals that CDS-recoding sites present higher editing frequencies with lower variabilities and their resultant recoded amino acids tend to exhibit stronger evolutionary conservation across many land plants. Furthermore, we classify mitochondrial genes into three groups, presenting distinct patterns in terms of CDS-recoding events. Besides, we conduct genome-wide screening to detect pentatricopeptide repeat (PPR) proteins and construct PPR-RNA binding profiles, yielding candidate PPR editing factors related to rice endosperm development. Taken together, our findings provide valuable insights for deciphering fundamental mechanisms of rice endosperm development underlying RNA editing machinery.

References

  1. Plant Cell. 2016 Nov;28(11):2805-2829 [PMID: 27760804]
  2. Mol Cell. 2003 Aug;12(2):321-8 [PMID: 14536072]
  3. Bioinformatics. 2014 Aug 1;30(15):2114-20 [PMID: 24695404]
  4. Rice (N Y). 2013 Feb 06;6(1):4 [PMID: 24280374]
  5. Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 [PMID: 7984417]
  6. Plant Cell. 2006 Sep;18(9):2341-55 [PMID: 16920781]
  7. Plant J. 2014 Sep;79(5):797-809 [PMID: 24923534]
  8. Int J Mol Sci. 2022 Mar 11;23(6): [PMID: 35328469]
  9. ACS Synth Biol. 2022 Feb 18;11(2):1004-1008 [PMID: 35044750]
  10. Plant Cell. 2001 Jan;13(1):207-18 [PMID: 11158540]
  11. J Integr Plant Biol. 2023 Jul;65(7):1687-1702 [PMID: 36897026]
  12. Plant Commun. 2024 May 13;5(5):100836 [PMID: 38327059]
  13. Mol Genet Genomics. 2002 Dec;268(4):434-45 [PMID: 12471441]
  14. J Mol Biol. 2000 Jul 21;300(4):1005-16 [PMID: 10891285]
  15. Plant Cell. 2012 Feb;24(2):676-91 [PMID: 22319053]
  16. Cell Res. 2015 May;25(5):621-33 [PMID: 25906995]
  17. Plant J. 2020 Aug;103(5):1767-1782 [PMID: 32559332]
  18. J Exp Bot. 2021 Jun 22;72(13):4809-4821 [PMID: 33929512]
  19. Nucleic Acids Res. 2023 Jan 6;51(D1):D523-D531 [PMID: 36408920]
  20. Nucleic Acids Res. 2019 Apr 23;47(7):3728-3738 [PMID: 30753696]
  21. EMBO J. 1997 May 15;16(10):2945-54 [PMID: 9184238]
  22. Wiley Interdiscip Rev RNA. 2022 Jan;13(1):e1666 [PMID: 33998151]
  23. Plant J. 2021 Nov;108(4):912-959 [PMID: 34528296]
  24. Curr Opin Plant Biol. 2013 May;16(2):236-46 [PMID: 23582455]
  25. Int J Mol Sci. 2022 Jan 08;23(2): [PMID: 35054870]
  26. Nat Methods. 2022 Jun;19(6):679-682 [PMID: 35637307]
  27. Rice (N Y). 2021 May 22;14(1):46 [PMID: 34021837]
  28. Mol Biol Evol. 2022 Dec 5;39(12): [PMID: 36227729]
  29. New Phytol. 2017 Apr;214(2):782-795 [PMID: 28121385]
  30. Plant J. 2009 Sep;59(5):738-49 [PMID: 19453459]
  31. Plant Physiol. 2023 May 31;192(2):728-747 [PMID: 36806687]
  32. Sci China Life Sci. 2018 Feb;61(2):162-169 [PMID: 29075943]
  33. Plant J. 2016 Feb;85(4):532-47 [PMID: 26764122]
  34. Photosynth Res. 2015 Dec;126(2-3):311-21 [PMID: 26123918]
  35. Cells. 2021 Feb 22;10(2): [PMID: 33671598]
  36. Nucleic Acids Res. 2000 Jan 1;28(1):235-42 [PMID: 10592235]
  37. Proteomics. 2004 Jun;4(6):1581-90 [PMID: 15174128]
  38. Front Plant Sci. 2014 Jul 28;5:366 [PMID: 25120551]
  39. Front Plant Sci. 2021 Dec 09;12:781734 [PMID: 34956279]
  40. J Genet Genomics. 2020 Apr 20;47(4):201-212 [PMID: 32505546]
  41. Front Plant Sci. 2020 Nov 30;11:587641 [PMID: 33424883]
  42. J Integr Plant Biol. 2016 Sep;58(9):786-98 [PMID: 27449987]
  43. Science. 1989 Dec 22;246(4937):1632-4 [PMID: 2480644]
  44. RNA Biol. 2016 Jun 2;13(6):593-604 [PMID: 27149614]
  45. Mol Gen Genet. 1989 Jun;217(2-3):185-94 [PMID: 2770692]
  46. Nucleic Acids Res. 2019 Jan 8;47(D1):D170-D174 [PMID: 30364952]
  47. J Plant Physiol. 2019 Sep;240:152992 [PMID: 31234031]
  48. Plant Cell. 2004 Aug;16(8):2089-103 [PMID: 15269332]
  49. Planta. 2016 Oct;244(4):893-9 [PMID: 27306450]
  50. New Phytol. 2017 Jun;214(4):1563-1578 [PMID: 28277611]
  51. Plant J. 2014 Dec;80(5):870-82 [PMID: 25279799]
  52. Plant Cell. 2013 Mar;25(3):868-83 [PMID: 23463776]
  53. Plant Physiol Biochem. 2019 Feb;135:310-321 [PMID: 30599308]
  54. Plant Physiol. 2013 Dec;163(4):1844-58 [PMID: 24144791]
  55. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  56. Nucleic Acids Res. 2003 Jul 1;31(13):3406-15 [PMID: 12824337]
  57. Curr Opin Plant Biol. 2013 May;16(2):247-54 [PMID: 23706659]
  58. BMC Genomics. 2018 Oct 1;19(1):720 [PMID: 30285603]
  59. Front Plant Sci. 2014 Mar 05;5:79 [PMID: 24634672]
  60. Bioinformatics. 2005 Mar 1;21(5):650-9 [PMID: 15388519]
  61. Nucleic Acids Res. 2024 Jan 5;52(D1):D18-D32 [PMID: 38018256]
  62. Physiol Plant. 2010 Apr;138(4):447-62 [PMID: 20059731]
  63. Nucleic Acids Res. 2013 Jan;41(Database issue):D36-42 [PMID: 23193287]
  64. J Exp Bot. 2020 Sep 19;71(18):5495-5505 [PMID: 32531050]
  65. J Exp Bot. 2020 Oct 22;71(20):6246-6261 [PMID: 32710615]
  66. Plant J. 2020 Mar;101(5):1040-1056 [PMID: 31630458]
  67. Bioinformatics. 2013 Jul 15;29(14):1813-4 [PMID: 23742983]
  68. Plant J. 2021 Apr;106(1):74-85 [PMID: 33354856]
  69. EMBO J. 1995 Mar 15;14(6):1276-85 [PMID: 7720718]
  70. BMC Plant Biol. 2008 Jul 16;8:79 [PMID: 18631376]
  71. Genomics Proteomics Bioinformatics. 2021 Aug;19(4):578-583 [PMID: 34400360]
  72. Proc Natl Acad Sci U S A. 2017 Aug 15;114(33):8883-8888 [PMID: 28761003]
  73. J Exp Bot. 2019 Nov 18;70(21):6163-6179 [PMID: 31598687]
  74. Plant Cell. 2023 May 29;35(6):1888-1900 [PMID: 36342219]
  75. BMC Plant Biol. 2020 Dec 9;20(1):553 [PMID: 33297963]
  76. Plant J. 2022 Sep;111(6):1676-1687 [PMID: 35877596]
  77. Mol Biol Evol. 2021 Jun 25;38(7):3022-3027 [PMID: 33892491]
  78. Bioinformatics. 2002 Feb;18(2):298-305 [PMID: 11847077]
  79. Nature. 1989 Oct 19;341(6243):662-6 [PMID: 2552326]
  80. Proc Natl Acad Sci U S A. 2017 Aug 15;114(33):8877-8882 [PMID: 28760958]
  81. RNA Biol. 2010 Mar-Apr;7(2):213-9 [PMID: 20473038]
  82. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  83. Plant J. 2024 Apr;118(2):345-357 [PMID: 38149801]
  84. Proc Natl Acad Sci U S A. 2022 Sep 27;119(39):e2210978119 [PMID: 36122211]
  85. Nucleic Acids Res. 2004 Jul 1;32(Web Server issue):W590-4 [PMID: 15215457]
  86. Genes (Basel). 2016 Dec 23;8(1): [PMID: 28025543]
  87. Mitochondrion. 2008 Jan;8(1):61-73 [PMID: 18033741]
  88. PLoS One. 2010 Jun 28;5(6):e11335 [PMID: 20596258]
  89. J Integr Plant Biol. 2023 Mar;65(3):755-771 [PMID: 36333887]
  90. Plant J. 2015 Oct;84(2):283-95 [PMID: 26303363]
  91. Plant Physiol. 2024 Feb 29;194(3):1593-1610 [PMID: 37956067]
  92. Mol Plant. 2020 Feb 3;13(2):215-230 [PMID: 31760160]
  93. Nucleic Acids Res. 2007 Jul;35(Web Server issue):W585-7 [PMID: 17517783]
  94. Nucleic Acids Res. 2016 Jan 4;44(D1):D733-45 [PMID: 26553804]
  95. Life Sci Alliance. 2019 Sep 30;2(5): [PMID: 31570514]
  96. Nature. 2014 Oct 09;514(7521):193-7 [PMID: 25252982]
  97. Plant Cell Physiol. 2020 Dec 23;61(11):1954-1966 [PMID: 32818255]
  98. New Phytol. 2022 May;234(4):1237-1248 [PMID: 35243635]
  99. Theor Appl Genet. 2020 May;133(5):1397-1413 [PMID: 31915876]
  100. BMC Bioinformatics. 2009 Dec 15;10:421 [PMID: 20003500]
  101. Plant Cell. 2023 Jan 2;35(1):529-551 [PMID: 36200865]
  102. PLoS Genet. 2019 Aug 2;15(8):e1008305 [PMID: 31374076]
  103. New Phytol. 2021 May;230(3):943-956 [PMID: 33341945]
  104. Front Plant Sci. 2014 Feb 18;5:35 [PMID: 24600456]

Grants

  1. 32030021/National Natural Science Foundation of China (National Science Foundation of China)

MeSH Term

Oryza
Endosperm
RNA Editing
RNA, Plant
Gene Expression Regulation, Plant
Plant Proteins
Mitochondria

Chemicals

RNA, Plant
Plant Proteins

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