Musa balbisiana genome reveals subgenome evolution and functional divergence

Zhuo Wang ,Silong Sun ,Sébastien Ricci ,Hongxia Miao ,Yi Xu ,Angélique D’hont ,Yulan Yang ,Catherine Hervouet ,Zhangyan Wu ,Juhua Liu ,Caihong Jia ,Jianhua Xie ,Zehong Ding ,Wei Hu ,Jianbin Zhang ,Jingyi Wang ,Jingyang Li ,Nathalie Laboureau ,Yu Guo ,Mathieu Rouard ,Anping Guo ,Xiaodong Fang ,Frédéric Salmon ,Guillaume Martin ,Olivier Garsmeur ,Xiaoming Yao ,Shancen Zhao ,Chun Liu ,Jiashui Wang ,Rémy Habas ,Yin Li ,Biao Xu ,Yan Yan ,Nabila Yahiaoui ,Franc-Christophe Baurens ,Ming Peng ,Lili Yu ,Wei Ma ,Chunyan Xu ,Weiwei Tie ,Zhiqiang Jin

doi:10.1038/s41477-019-0452-6

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.

Highlights

Banana cultivars (Musa ssp.) are diploid, triploid and tetraploid hybrids derived from Musa acuminata and Musa balbisiana
We identified that the recent divergence of M. acuminata (A-genome) and M. balbisiana (B-genome) occurred after lineagespecific whole-genome duplication, and that the B-genome may be more sensitive to the fractionation process compared to the A-genome
We found 9,038 gene families that were conserved in M. balbisiana, M. acuminata, Oryza sativa, Brachypodium distachyon and Vitis vinifera

Summary

Introduction

Banana cultivars (Musa ssp.) are diploid, triploid and tetraploid hybrids derived from Musa acuminata and Musa balbisiana. 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 duplicationdriven expansion of ACO genes in the B-subgenome contributed to rapid and major ethylene production post-harvest in allotriploid banana fruits. B ananas (Musa ssp.) are large herbaceous plants that are perennial but monocarpic. They originated in Southeast Asia and the Western Pacific and were one of the first crops to be domesticated, about 7,000 years ago, in Southeast Asia[1,2]. Bananas of this section are distinguished based on their genetic background as

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