Musa balbisiana genome reveals subgenome evolution and functional divergence.

Zhuo Wang, Hongxia Miao, Juhua Liu, Biyu Xu, Xiaoming Yao, Chunyan Xu, Shancen Zhao, Xiaodong Fang, Caihong Jia, Jingyi Wang, Jianbin Zhang, Jingyang Li, Yi Xu, Jiashui Wang, Weihong Ma, Zhangyan Wu, Lili Yu, Yulan Yang, Chun Liu, Yu Guo, Silong Sun, Franc-Christophe Baurens, Guillaume Martin, Frederic Salmon, Olivier Garsmeur, Nabila Yahiaoui, Catherine Hervouet, Mathieu Rouard, Nathalie Laboureau, Remy Habas, Sebastien Ricci, Ming Peng, Anping Guo, Jianghui Xie, Yin Li, Zehong Ding, Yan Yan, Weiwei Tie, Angélique D'Hont, Wei Hu, Zhiqiang Jin
Author Information
  1. Zhuo Wang: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  2. Hongxia Miao: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  3. Juhua Liu: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  4. Biyu Xu: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  5. Xiaoming Yao: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  6. Chunyan Xu: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  7. Shancen Zhao: BGI Institute of Applied Agriculture, BGI-Shenzhen, Shenzhen, China.
  8. Xiaodong Fang: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  9. Caihong Jia: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  10. Jingyi Wang: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  11. Jianbin Zhang: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  12. Jingyang Li: Key Laboratory of Genetic Improvement of Bananas, Hainan province, Haikou Experimental Station, China Academy of Tropical Agricultural Sciences, Haikou, China.
  13. Yi Xu: Key Laboratory of Genetic Improvement of Bananas, Hainan province, Haikou Experimental Station, China Academy of Tropical Agricultural Sciences, Haikou, China.
  14. Jiashui Wang: Key Laboratory of Genetic Improvement of Bananas, Hainan province, Haikou Experimental Station, China Academy of Tropical Agricultural Sciences, Haikou, China.
  15. Weihong Ma: Key Laboratory of Genetic Improvement of Bananas, Hainan province, Haikou Experimental Station, China Academy of Tropical Agricultural Sciences, Haikou, China.
  16. Zhangyan Wu: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  17. Lili Yu: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  18. Yulan Yang: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  19. Chun Liu: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  20. Yu Guo: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  21. Silong Sun: BGI Genomics, BGI-Shenzhen, Shenzhen, China.
  22. Franc-Christophe Baurens: CIRAD, UMR AGAP, Montpellier, France.
  23. Guillaume Martin: CIRAD, UMR AGAP, Montpellier, France. ORCID
  24. Frederic Salmon: AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
  25. Olivier Garsmeur: CIRAD, UMR AGAP, Montpellier, France.
  26. Nabila Yahiaoui: CIRAD, UMR AGAP, Montpellier, France.
  27. Catherine Hervouet: CIRAD, UMR AGAP, Montpellier, France.
  28. Mathieu Rouard: Bioversity International, Montpellier, France. ORCID
  29. Nathalie Laboureau: CIRAD, UMR BGPI, Montpellier, France.
  30. Remy Habas: CIRAD, UMR BGPI, Montpellier, France.
  31. Sebastien Ricci: AGAP, Univ Montpellier, CIRAD, INRA, Montpellier SupAgro, Montpellier, France.
  32. Ming Peng: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  33. Anping Guo: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  34. Jianghui Xie: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  35. Yin Li: Waksman Institute of Microbiology, Rutgers, The State University of New Jersey, Piscataway, NJ, USA. ORCID
  36. Zehong Ding: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  37. Yan Yan: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  38. Weiwei Tie: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China.
  39. Angélique D'Hont: CIRAD, UMR AGAP, Montpellier, France. dhont@cirad.fr. ORCID
  40. Wei Hu: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China. huwei2010916@126.com. ORCID
  41. Zhiqiang Jin: Key Laboratory of Biology and Genetic Resources of Tropical Crops, Institute of Tropical Bioscience and Biotechnology, Chinese Academy of Tropical Agricultural Sciences, Haikou, China. 18689846976@163.com. ORCID

Abstract

Banana cultivars (Musa ssp.) are diploid, triploid and tetraploid hybrids derived from Musa acuminata and Musa balbisiana. We presented a high-quality draft genome assembly of M. balbisiana with 430 Mb (87%) assembled into 11 chromosomes. We identified that the recent divergence of M. acuminata (A-genome) and M. balbisiana (B-genome) occurred after lineage-specific whole-genome duplication, and that the B-genome may be more sensitive to the fractionation process compared to the A-genome. Homoeologous exchanges occurred frequently between A- and B-subgenomes in allopolyploids. Genomic variation within progenitors resulted in functional divergence of subgenomes. Global homoeologue expression dominance occurred between subgenomes of the allotriploid. Gene families related to ethylene biosynthesis and starch metabolism exhibited significant expansion at the pathway level and wide homoeologue expression dominance in the B-subgenome of the allotriploid. The independent origin of 1-aminocyclopropane-1-carboxylic acid oxidase (ACO) homoeologue gene pairs and tandem duplication-driven expansion of ACO genes in the B-subgenome contributed to rapid and major ethylene production post-harvest in allotriploid banana fruits. The findings of this study provide greater context for understanding fruit biology, and aid the development of tools for breeding optimal banana cultivars.

References

  1. New Phytol. 1994 Aug;127(4):617-633 pubmed:33874382
  2. Proc Natl Acad Sci U S A. 2009 Sep 1;106(35):14908-13 pubmed:19706486
  3. Front Plant Sci. 2016 Dec 02;7:1778 pubmed:27994606
  4. Stat Appl Genet Mol Biol. 2005;4:Article17 pubmed:16646834
  5. Genome Biol. 2015 Dec 01;16:259 pubmed:26619908
  6. Nucleic Acids Res. 2004 Mar 19;32(5):1792-7 pubmed:15034147
  7. Bioinformatics. 2009 Jul 15;25(14):1754-60 pubmed:19451168
  8. Science. 2009 Oct 9;326(5950):289-93 pubmed:19815776
  9. BMC Genomics. 2008 Jan 30;9:58 pubmed:18234080
  10. New Phytol. 2018 Oct;220(1):87-93 pubmed:29882360
  11. BMC Plant Biol. 2013 Mar 12;13:41 pubmed:23497122
  12. Nat Methods. 2009 Sep;6(9):677-81 pubmed:19668202
  13. BMC Genomics. 2017 Jan 5;18(1):38 pubmed:28056785
  14. Bioinformatics. 2011 Feb 15;27(4):578-9 pubmed:21149342
  15. Genomics Proteomics Bioinformatics. 2010 Mar;8(1):77-80 pubmed:20451164
  16. J Mol Evol. 1985;22(2):160-74 pubmed:3934395
  17. Plant Physiol. 1999 Dec;121(4):1257-66 pubmed:10594112
  18. BMC Bioinformatics. 2003 Sep 11;4:41 pubmed:12969510
  19. Science. 2000 Nov 10;290(5494):1151-5 pubmed:11073452
  20. BMC Evol Biol. 2011 Apr 16;11:103 pubmed:21496296
  21. New Phytol. 2012 Dec;196(4):966-971 pubmed:23033870
  22. BMC Bioinformatics. 2013 Nov 12;14:321 pubmed:24219505
  23. Mol Biol Evol. 2019 Jan 1;36(1):97-111 pubmed:30403808
  24. J Exp Bot. 2014 Aug;65(16):4561-75 pubmed:25028558
  25. Nature. 2009 Jan 15;457(7227):327-31 pubmed:19029881
  26. Genome Res. 2010 Sep;20(9):1297-303 pubmed:20644199
  27. Proc Natl Acad Sci U S A. 1979 Jan;76(1):170-4 pubmed:16592605
  28. Brief Funct Genomics. 2014 Jul;13(4):296-307 pubmed:24907366
  29. Genetics. 1996 Apr;142(4):1349-55 pubmed:8846910
  30. Front Plant Sci. 2017 Apr 04;8:475 pubmed:28421102
  31. BMC Bioinformatics. 2003 Jun 23;4:25 pubmed:12820902
  32. Plant Physiol. 1990 Sep;94(1):201-8 pubmed:16667688
  33. Mol Biol Evol. 2007 Aug;24(8):1586-91 pubmed:17483113
  34. Bioinformatics. 2001 Aug;17(8):754-5 pubmed:11524383
  35. Nat Genet. 2017 Nov;49(11):1633-1641 pubmed:28991254
  36. CSH Protoc. 2007 Jul 01;2007:pdb.top17 pubmed:21357135
  37. Am J Bot. 2018 Nov;105(11):1888-1910 pubmed:30368769
  38. Science. 2014 Jul 18;345(6194):1251788 pubmed:25035500
  39. BMC Genomics. 2016 Mar 16;17:243 pubmed:26984673
  40. Front Plant Sci. 2017 Mar 30;8:454 pubmed:28424724
  41. Bioinformatics. 2015 Oct 1;31(19):3210-2 pubmed:26059717
  42. Plant Biotechnol J. 2017 Apr;15(4):520-532 pubmed:27734628
  43. Nat Genet. 2016 Oct;48(10):1225-32 pubmed:27595476
  44. Plant Physiol. 2008 Apr;146(4):1878-91 pubmed:18263778
  45. Plant Cell. 1995 Jul;7(7):971-85 pubmed:7640529
  46. Genome Res. 2003 Nov;13(11):2498-504 pubmed:14597658
  47. Nucleic Acids Res. 2000 Jan 1;28(1):45-8 pubmed:10592178
  48. Genome Res. 2003 Sep;13(9):2178-89 pubmed:12952885
  49. Mol Biol Evol. 2014 Feb;31(2):448-54 pubmed:24296661
  50. Am J Bot. 2016 Jul;103(7):1187-96 pubmed:27206460
  51. Genome Res. 1997 Oct;7(10):986-95 pubmed:9331369
  52. Curr Protoc Bioinformatics. 2014 Dec 12;48:4.11.1-4.11.39 pubmed:25501943
  53. Plant Biotechnol J. 2018 Jan;16(1):151-164 pubmed:28500777
  54. Plant Cell. 2002 Sep;14(9):2191-213 pubmed:12215515
  55. Science. 2014 Aug 22;345(6199):950-3 pubmed:25146293
  56. New Phytol. 2014 May;202(3):986-1000 pubmed:24716518
  57. Nat Genet. 2009 Dec;41(12):1275-81 pubmed:19881527
  58. Nucleic Acids Res. 1999 Jan 1;27(1):29-34 pubmed:9847135
  59. New Phytol. 2016 Jun;210(4):1453-65 pubmed:26832306
  60. Nucleic Acids Res. 2009 Jan;37(1):1-13 pubmed:19033363
  61. Genes (Basel). 2017 Dec 28;9(1): pubmed:29283420
  62. Nat Methods. 2008 Jul;5(7):621-8 pubmed:18516045
  63. Nature. 2012 May 30;485(7400):635-41 pubmed:22660326
  64. Genome Res. 2002 Apr;12(4):656-64 pubmed:11932250
  65. BMC Bioinformatics. 2008 Dec 29;9:559 pubmed:19114008
  66. Nature. 2012 Aug 9;488(7410):213-7 pubmed:22801500
  67. Genetics. 2004 Feb;166(2):935-45 pubmed:15020478
  68. Nat Biotechnol. 2015 May;33(5):531-7 pubmed:25893781
  69. Bioinformatics. 2006 May 15;22(10):1269-71 pubmed:16543274
  70. Mol Plant. 2016 Dec 5;9(12):1667-1670 pubmed:27717919
  71. Nat Biotechnol. 2013 Dec;31(12):1119-25 pubmed:24185095
  72. Nucleic Acids Res. 2010 Jan;38(Database issue):D822-7 pubmed:19858103
  73. Brief Bioinform. 2009 Nov;10(6):619-30 pubmed:19720678
  74. Plant Cell Rep. 2003 Feb;21(6):511-6 pubmed:12789424
  75. Bioinformatics. 2009 Aug 15;25(16):2078-9 pubmed:19505943
  76. Nucleic Acids Res. 2014 Jan;42(Database issue):D1182-7 pubmed:24174544
  77. Nucleic Acids Res. 1980 Oct 10;8(19):4321-5 pubmed:7433111
  78. BMC Genomics. 2013 Oct 05;14:683 pubmed:24094114
  79. Science. 2008 Apr 25;320(5875):486-8 pubmed:18436778

MeSH Term

Ethylenes
Evolution, Molecular
Genetic Variation
Genome, Plant
Molecular Sequence Annotation
Musa

Chemicals

Ethylenes
ethylene