Expansion of banana (Musa acuminata) gene families involved in ethylene biosynthesis and signalling after lineage‐specific whole‐genome duplications

• Published in: The New phytologist Vol. 202; no. 3; pp. 986 - 1000
• Main Authors: Jourda, Cyril, Cardi, Céline, Mbéguié‐A‐Mbéguié, Didier, Bocs, Stéphanie, Garsmeur, Olivier, D'Hont, Angélique, Yahiaoui, Nabila
• Format: Journal Article
• Language: English
• Published: England William Wesley and Son 01.05.2014; New Phytologist Trust; Wiley Subscription Services, Inc
• Subjects: Alkynes; Arabidopsis; banana; bananas; Biosynthesis; Branches; Conserved Sequence - genetics; Control; Ethene; Ethylene; ethylene production; Ethylenes - biosynthesis; Evolution; fruit ripening; Fruits; Gene Duplication; Gene expression; Gene Expression Profiling; Gene Expression Regulation, Plant; Gene families; Genes; Genes, Plant; Genomes; Genomics; Identifiers; Impact analysis; Likelihood Functions; Lyases - metabolism; major genes; Multigene Family; Musa; Musa - enzymology; Musa - genetics; Musa acuminata; Phylogenetics; Phylogeny; Plants; Proteins; Redundancy; Reproduction (copying); Rice; Ripening; Selection, Genetic; Signal transduction; Signal Transduction - genetics; Signaling; whole‐genome duplication; banana; Musa acuminata; gene families; fruit ripening; ethylene; whole-genome duplication
• ISSN: 0028-646X; 1469-8137
• DOI: 10.1111/nph.12710

Whole‐genome duplications (WGDs) are widespread in plants, and three lineage‐specific WGDs occurred in the banana (Musa acuminata) genome. Here, we analysed the impact of WGDs on the evolution of banana gene families involved in ethylene biosynthesis and signalling, a key pathway for banana fruit ripening. Banana ethylene pathway genes were identified using comparative genomics approaches and their duplication modes and expression profiles were analysed. Seven out of 10 banana ethylene gene families evolved through WGD and four of them (1‐aminocyclopropane‐1‐carboxylate synthase (ACS), ethylene‐insensitive 3‐like (EIL), ethylene‐insensitive 3‐binding F‐box (EBF) and ethylene response factor (ERF)) were preferentially retained. Banana orthologues of AtEIN3 and AtEIL1, two major genes for ethylene signalling in Arabidopsis, were particularly expanded. This expansion was paralleled by that of EBF genes which are responsible for control of EIL protein levels. Gene expression profiles in banana fruits suggested functional redundancy for several MaEBF and MaEIL genes derived from WGD and subfunctionalization for some of them. We propose that EIL and EBF genes were co‐retained after WGD in banana to maintain balanced control of EIL protein levels and thus avoid detrimental effects of constitutive ethylene signalling. In the course of evolution, subfunctionalization was favoured to promote finer control of ethylene signalling.