Alternative Splicing Plays a Critical Role in Maintaining Mineral Nutrient Homeostasis in Rice ().

Chunlan Dong, Fei He, Oliver Berkowitz, Jingxian Liu, Pengfei Cao, Min Tang, Huichao Shi, Wujian Wang, Qiaolu Li, Zhenguo Shen, James Whelan, Luqing Zheng
Author Information
  1. Chunlan Dong: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  2. Fei He: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  3. Oliver Berkowitz: ARC Centre of Excellence in Plant Energy Biology, Department of Animal, Plant, and Soil Sciences, School of Life Sciences, La Trobe University, Victoria 3086, Australia. ORCID
  4. Jingxian Liu: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  5. Pengfei Cao: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  6. Min Tang: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  7. Huichao Shi: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  8. Wujian Wang: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  9. Qiaolu Li: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  10. Zhenguo Shen: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China. ORCID
  11. James Whelan: ARC Centre of Excellence in Plant Energy Biology, Department of Animal, Plant, and Soil Sciences, School of Life Sciences, La Trobe University, Victoria 3086, Australia. ORCID
  12. Luqing Zheng: College of Life Sciences, Nanjing Agricultural University, Nanjing, Jiangsu 210095, P.R. China zhenglq@njau.edu.cn. ORCID

Abstract

Alternative splicing (AS) of pre-mRNAs promotes transcriptome and proteome diversity and plays important roles in a wide range of biological processes. However, the role of AS in maintaining mineral nutrient homeostasis in plants is largely unknown. To clarify this role, we obtained whole transcriptome RNA sequencing data from rice () roots grown in the presence or absence of several mineral nutrients (Fe, Zn, Cu, Mn, and P). Our systematic analysis revealed 13,291 alternatively spliced genes, representing ∼53.3% of the multiexon genes in the rice genome. As the overlap between differentially expressed genes and differentially alternatively spliced genes is small, a molecular understanding of the plant's response to mineral deficiency is limited by analyzing differentially expressed genes alone. We found that the targets of AS are highly nutrient-specific. To verify the role of AS in mineral nutrition, we characterized mutants in genes encoding Ser/Arg (SR) proteins that function in AS. We identified several SR proteins as critical regulators of Zn, Mn, and P nutrition and showed that three SR protein-encoding genes regulate P uptake and remobilization between leaves and shoots of rice, demonstrating that AS has a key role in regulating mineral nutrient homeostasis in rice.

References

  1. Nucleic Acids Res. 2014 Apr;42(6):4019-30 [PMID: 24442672]
  2. Plant Cell. 2015 Aug;27(8):2083-7 [PMID: 26286536]
  3. Proc Natl Acad Sci U S A. 1977 Aug;74(8):3171-5 [PMID: 269380]
  4. Proc Natl Acad Sci U S A. 2014 Dec 23;111(51):E5593-601 [PMID: 25480548]
  5. Mol Plant. 2014 May;7(5):829-40 [PMID: 24398628]
  6. Plant Cell. 2010 Sep;22(9):2926-9 [PMID: 20884799]
  7. Proc Natl Acad Sci U S A. 2009 Dec 8;106(49):20978-83 [PMID: 19923426]
  8. Plant Physiol. 2009 Sep;151(1):262-74 [PMID: 19605549]
  9. New Phytol. 2012 Oct;196(1):139-48 [PMID: 22803610]
  10. Plant Cell. 2006 Jan;18(1):146-58 [PMID: 16339852]
  11. Plant Physiol. 2006 Jul;141(3):1000-11 [PMID: 16679417]
  12. Genomics. 2010 Nov;96(5):259-65 [PMID: 20688152]
  13. Biochem Biophys Res Commun. 2014 Dec 12;455(3-4):312-7 [PMID: 25446093]
  14. Genome Biol. 2010;11(10):R106 [PMID: 20979621]
  15. Nat Rev Genet. 2014 Oct;15(10):689-701 [PMID: 25112293]
  16. Bioinformatics. 2013 Jan 1;29(1):15-21 [PMID: 23104886]
  17. Nat Biotechnol. 2015 Mar;33(3):290-5 [PMID: 25690850]
  18. Genetics. 2011 May;188(1):11-20 [PMID: 21546547]
  19. Front Plant Sci. 2013 Oct 02;4:357 [PMID: 24106494]
  20. Trends Plant Sci. 2018 Feb;23(2):140-150 [PMID: 29074233]
  21. Genome Res. 2012 Jun;22(6):1184-95 [PMID: 22391557]
  22. Plant J. 2006 Jan;45(1):123-32 [PMID: 16367959]
  23. Nucleic Acids Res. 2006 Jan 1;34(Database issue):D745-8 [PMID: 16381972]
  24. Plant Cell Physiol. 2007 Aug;48(8):1170-81 [PMID: 17602187]
  25. Genome Biol. 2004;5(10):R80 [PMID: 15461798]
  26. Plant Cell. 2015 Dec;27(12):3294-308 [PMID: 26603559]
  27. J Exp Bot. 2008;59(12):3453-64 [PMID: 18772308]
  28. Plant Cell. 2013 Oct;25(10):3640-56 [PMID: 24179132]
  29. Genome Res. 2010 May;20(5):646-54 [PMID: 20305017]
  30. Plant Cell. 2014 Sep;26(9):3472-87 [PMID: 25248552]
  31. Plant J. 2012 Dec;72(6):935-46 [PMID: 22913769]
  32. Mol Plant. 2013 Nov;6(6):1975-83 [PMID: 23956122]
  33. Plant Cell. 2013 Oct;25(10):3657-83 [PMID: 24179125]
  34. Plant Cell Physiol. 2014 Dec;55(12):2027-36 [PMID: 25378690]
  35. PLoS Genet. 2013;9(10):e1003875 [PMID: 24146632]
  36. BMC Mol Biol. 2006 Jan 31;7:3 [PMID: 16448564]
  37. Nucleic Acids Res. 2017 Jan 4;45(D1):D190-D199 [PMID: 27899635]
  38. Plant Physiol. 2010 Oct;154(2):772-83 [PMID: 20699397]
  39. Plant J. 2017 Aug;91(4):741-753 [PMID: 28586097]
  40. J Exp Bot. 2005 Dec;56(422):3207-14 [PMID: 16263903]
  41. Plant Cell Physiol. 2004 Apr;45(4):460-9 [PMID: 15111721]
  42. Annu Rev Plant Biol. 2012;63:131-52 [PMID: 22404471]
  43. Annu Rev Biochem. 1987;56:467-95 [PMID: 3304142]
  44. Nature. 2008 Nov 27;456(7221):470-6 [PMID: 18978772]
  45. Genes Dev. 2010 Jun 1;24(11):1073-4 [PMID: 20516191]
  46. Int J Mol Sci. 2014 Sep 29;15(10):17541-64 [PMID: 25268622]
  47. Cell. 1977 Sep;12(1):1-8 [PMID: 902310]
  48. Curr Opin Plant Biol. 2015 Apr;24:125-35 [PMID: 25835141]
  49. Annu Rev Plant Biol. 2011;62:185-206 [PMID: 21370979]
  50. Elife. 2015 Jul 21;4:null [PMID: 26196146]
  51. Sci Rep. 2016 Nov 02;6:35846 [PMID: 27804982]
  52. Nat Protoc. 2012 Mar 01;7(3):562-78 [PMID: 22383036]
  53. Plant Cell. 2013 Nov;25(11):4285-304 [PMID: 24249833]
  54. Biomolecules. 2015 Jul 24;5(3):1717-40 [PMID: 26213982]
  55. Front Plant Sci. 2016 Aug 15;7:1198 [PMID: 27574525]
  56. Nature. 2011 Apr 14;472(7342):159-61 [PMID: 21478874]
  57. Plant Physiol. 2006 Jul;141(3):988-99 [PMID: 16679424]
  58. PLoS Genet. 2017 Mar 8;13(3):e1006663 [PMID: 28273088]
  59. New Phytol. 2016 Aug;211(3):926-39 [PMID: 27110682]
  60. BMC Genomics. 2014 Jun 02;15:419 [PMID: 24888378]
  61. Nat Methods. 2017 Jan;14(1):68-70 [PMID: 27869815]
  62. Plant Physiol. 2011 Jul;156(3):1149-63 [PMID: 21628630]
  63. Plant Physiol. 2013 Jul;162(3):1750-63 [PMID: 23735510]
  64. J Biol Chem. 2003 Nov 28;278(48):47644-53 [PMID: 13129917]
  65. Curr Opin Plant Biol. 2013 May;16(2):205-12 [PMID: 23566853]
  66. Plant Cell. 2014 Mar;26(3):996-1008 [PMID: 24681622]
  67. Front Plant Sci. 2011 Nov 30;2:83 [PMID: 22645553]
  68. Genome Biol. 2014;15(12):550 [PMID: 25516281]

MeSH Term

Alternative Splicing
Gene Expression Regulation, Plant
Homeostasis
Minerals
Mutation
Oryza
Phosphates
Phosphorus
Plant Proteins
Serine-Arginine Splicing Factors

Chemicals

Minerals
Phosphates
Plant Proteins
Serine-Arginine Splicing Factors
Phosphorus

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