Transcriptome analysis of wheat seedling and spike tissues in the hybrid Jingmai 8 uncovered genes involved in heterosis.

Yong-Jie Liu, Shi-Qing Gao, Yi-Miao Tang, Jie Gong, Xiao Zhang, Yong-Bo Wang, Li-Ping Zhang, Ren-Wei Sun, Quan Zhang, Zhao-Bo Chen, Xiang Wang, Cai-Juan Guo, Sheng-Quan Zhang, Feng-Ting Zhang, Jian-Gang Gao, Hui Sun, Wei-Bing Yang, Wei-Wei Wang, Chang-Ping Zhao
Author Information
  1. Yong-Jie Liu: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  2. Shi-Qing Gao: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China. gaoshiqing@baafs.net.cn.
  3. Yi-Miao Tang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  4. Jie Gong: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  5. Xiao Zhang: Hebei Normal University, Shijiazhuang, 050024, China.
  6. Yong-Bo Wang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  7. Li-Ping Zhang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  8. Ren-Wei Sun: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  9. Quan Zhang: Shandong Normal University, Jinan, 250014, China.
  10. Zhao-Bo Chen: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  11. Xiang Wang: Huazhong Agricultural University, Wuhan, 430070, China.
  12. Cai-Juan Guo: Yangtze University, Jingzhou, 434023, China.
  13. Sheng-Quan Zhang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  14. Feng-Ting Zhang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  15. Jian-Gang Gao: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  16. Hui Sun: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  17. Wei-Bing Yang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  18. Wei-Wei Wang: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China.
  19. Chang-Ping Zhao: Beijing Engineering Research Center for Hybrid Wheat, The Municipal Key Laboratory of the Molecular Genetics of Hybrid Wheat, Beijing Academy of Agriculture and Forestry Sciences, Beijing, 100097, China. zhaochangping@baafs.net.cn.

Abstract

MAIN CONCLUSION: Transcriptome analysis was carried out for wheat seedlings and spikes from hybrid Jingmai 8 and both inbred lines to unravel mechanisms underlying heterosis. Heterosis, known as one of the most successful strategies for increasing crop yield, has been widely exploited in plant breeding systems. Despite its great importance, the molecular mechanism underlying heterosis remains elusive. In the present study, RNA sequencing (RNA-seq) was performed on the seedling and spike tissues of the wheat (Triticum aestivum) hybrid Jingmai 8 (JM8) and its homozygous parents to unravel the underlying mechanisms of wheat heterosis. In total, 1686 and 2334 genes were identified as differentially expressed genes (DEGs) between the hybrid and the two inbred lines in seedling and spike tissues, respectively. Gene Ontology analysis revealed that DEGs from seedling tissues were significantly enriched in processes involved in photosynthesis and carbon fixation, and the majority of these DEGs expressed at a higher level in JM8 compared to both inbred lines. In addition, cell wall biogenesis and protein biosynthesis-related pathways were also significantly represented. These results confirmed that a combination of different pathways could contribute to heterosis. The DEGs between the hybrid and the two inbred progenitors from the spike tissues were significantly enriched in biological processes related to transcription, RNA biosynthesis and molecular function categories related to transcription factor activities. Furthermore, transcription factors such as NAC, ERF, and TIF-IIA were highly expressed in the hybrid JM8. These results may provide valuable insights into the molecular mechanisms underlying wheat heterosis.

Keywords

References

  1. Proc Natl Acad Sci U S A. 2006 May 2;103(18):6805-10 [PMID: 16641103]
  2. Plant Biotechnol J. 2006 Mar;4(2):145-67 [PMID: 17177793]
  3. Plant Physiol. 2005 Jul;138(3):1216-31 [PMID: 16009997]
  4. Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 [PMID: 9843981]
  5. Curr Opin Plant Biol. 2006 Dec;9(6):671-8 [PMID: 17011815]
  6. Annu Rev Cell Dev Biol. 2008;24:81-103 [PMID: 18616425]
  7. Plant Mol Biol. 2007 Jan;63(1):21-34 [PMID: 17006594]
  8. Bioinformatics. 2010 Jan 1;26(1):139-40 [PMID: 19910308]
  9. BMC Biol. 2009 May 01;7:18 [PMID: 19409075]
  10. Proc Natl Acad Sci U S A. 2006 Aug 29;103(35):12957-8 [PMID: 16938847]
  11. Proc Natl Acad Sci U S A. 1987 Jan;84(1):109-12 [PMID: 16593792]
  12. Plant Cell. 2004 Jul;16(7):1707-16 [PMID: 15194819]
  13. Heredity (Edinb). 2013 Feb;110(2):171-80 [PMID: 23169565]
  14. Plant Cell Environ. 2011 Mar;34(3):389-405 [PMID: 21062315]
  15. BMC Genomics. 2013 Jan 16;14:19 [PMID: 23324257]
  16. Proc Natl Acad Sci U S A. 2016 Oct 25;113(43):E6704-E6711 [PMID: 27791039]
  17. FEBS Lett. 1989 Jan 2;242(2):435-8 [PMID: 2644135]
  18. Genetics. 2006 Aug;173(4):2199-210 [PMID: 16702414]
  19. Genome Res. 2012 Dec;22(12):2445-54 [PMID: 23086286]
  20. BMC Plant Biol. 2007 Sep 19;7:49 [PMID: 17877838]
  21. PLoS One. 2013;8(3):e58453 [PMID: 23520511]
  22. BMC Plant Biol. 2009 Aug 13;9:107 [PMID: 19678936]
  23. Plant Cell. 2003 Oct;15(10):2236-9 [PMID: 14523245]
  24. BMC Plant Biol. 2013 Dec 21;13:221 [PMID: 24358981]
  25. Genetics. 1965 Jul;52(1):139-44 [PMID: 17248265]
  26. Nature. 2009 Jan 15;457(7227):327-31 [PMID: 19029881]
  27. Theor Appl Genet. 2010 Jan;120(2):341-53 [PMID: 19657617]
  28. Plant Physiol. 2016 Oct;172(2):1142-1153 [PMID: 27540108]
  29. BMC Genet. 2017 Apr 17;18(1):36 [PMID: 28415964]
  30. Nat Methods. 2015 Apr;12(4):357-60 [PMID: 25751142]
  31. Int J Genomics. 2016;2016:2587823 [PMID: 28101503]
  32. Mol Plant. 2008 Sep;1(5):720-31 [PMID: 19825576]
  33. Proc Natl Acad Sci U S A. 2012 May 1;109(18):7109-14 [PMID: 22493265]
  34. Sci China C Life Sci. 2002 Oct;45(5):468-76 [PMID: 18759034]
  35. Theor Appl Genet. 2014 Oct;127(10):2149-58 [PMID: 25104328]
  36. Plant Cell. 2014 May 16;26(5):1878-1900 [PMID: 24838975]
  37. Genome Res. 2007 Mar;17(3):264-75 [PMID: 17255553]
  38. Plant Cell. 2010 Jan;22(1):17-33 [PMID: 20086188]
  39. Proc Natl Acad Sci U S A. 2009 Oct 20;106(42):17835-40 [PMID: 19805056]
  40. Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):11823-8 [PMID: 26351684]
  41. Science. 1908 Oct 2;28(718):454-5 [PMID: 17771943]
  42. G3 (Bethesda). 2016 Oct 13;6(10 ):3373-3379 [PMID: 27565885]
  43. Nat Genet. 2000 May;25(1):25-9 [PMID: 10802651]
  44. Science. 2004 Dec 24;306(5705):2206-11 [PMID: 15618507]
  45. Proc Natl Acad Sci U S A. 2009 May 12;106(19):7695-701 [PMID: 19372371]
  46. Genetics. 2001 Aug;158(4):1737-53 [PMID: 11514459]
  47. Proc Natl Acad Sci U S A. 2016 Oct 11;113(41):E6026-E6035 [PMID: 27663737]

Grants

  1. 31571641/National Natural Science Foundation of China
  2. 31171172/National Natural Science Foundation of China
  3. 6162009/Beijing Municipal Natural Science Foundation
  4. KJCX20170421/Beijing Academy of Agriculture and Forestry Sciences Reserve Program (CN)

MeSH Term

Gene Expression Profiling
Gene Expression Regulation, Plant
Gene Ontology
Hybrid Vigor
Inbreeding
Inflorescence
Photosynthesis
Seedlings
Sequence Analysis, RNA
Transcriptome
Triticum

Word Cloud

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