The bracteatus pineapple genome and domestication of clonally propagated crops

Li Yu Chen ,Michael C Schatz,Jae Young Choi,Jianping Wang,Qingsong Wu,Jishan Lin,Shaoling Zhang,Zhenyang Liao,Lixian Huang,Mahpara Fatima,Shu Min Kao ,Jeffrey L Bennetzen,S Ramakrishnan ,Qingyi Yu,Hansong Yan,Juan Liu,Xingtan Zhang,Ching Man Wai,Robert E Paull,Zhicong Lin,Michael Alonge,John C Cushman,Song Jiang ,Shuai Chen,Hongye Zhou,Teh Yang Hwa ,Michael D Purugganan,Won Cheol Yim ,Jingjing Yue,Tracie K Matsumoto ,Yuan Qin,Christian Lexer,Géo Coppens D'eeckenbrugge ,Peter Boches,Jisen Zhang,Robert Vanburen,Hao Wang,Garth M Sanewski,Ming Li Wang ,Margot Paris,Jun Wu,Chih‐Wei Tung ,Lulu Wang,Anupma Sharma,Ray Ming

doi:10.1038/s41588-019-0506-8

Abstract

Domestication of clonally propagated crops such as pineapple from South America was hypothesized to be a ‘one-step operation’. We sequenced the genome of Ananas comosus var. bracteatus CB5 and assembled 513 Mb into 25 chromosomes with 29,412 genes. Comparison of the genomes of CB5, F153 and MD2 elucidated the genomic basis of fiber production, color formation, sugar accumulation and fruit maturation. We also resequenced 89 Ananas genomes. Cultivars ‘Smooth Cayenne’ and ‘Queen’ exhibited ancient and recent admixture, while ‘Singapore Spanish’ supported a one-step operation of domestication. We identified 25 selective sweeps, including a strong sweep containing a pair of tandemly duplicated bromelain inhibitors. Four candidate genes for self-incompatibility were linked in F153, but were not functional in self-compatible CB5. Our findings support the coexistence of sexual recombination and a one-step operation in the domestication of clonally propagated crops. This work guides the exploration of sexual and asexual domestication trajectories in other clonally propagated crops.

Highlights

Most grain crops, vegetables and ornamentals are produced sexually through seed propagation, whereas most fruit trees, tubers and some ornamentals are clonally propagated through grafting, tissue culture, divisions or cuttings
To eliminate redundant homozygous sequences, we developed a new algorithm, Pseudohaploid, that identifies and filters out heterozygous contigs based on whole-genome alignment
To overcome the problem of assembling a heterozygous genome, we have developed an algorithm, Pseudohaploid, that identifies and filters out heterozygous contigs by searching for redundant homologous sequences

Summary

Introduction

Vegetables and ornamentals are produced sexually through seed propagation, whereas most fruit trees, tubers and some ornamentals are clonally propagated through grafting, tissue culture, divisions or cuttings. Reproducing species undergo hundreds to thousands of generations of recombination during domestication; this recurrent selection leaves highly tractable signatures in the genome. Domestication of clonally propagated crops depends on both vegetative and sexual reproduction, the latter acting more sporadically on long-lived clones. It can even be a one-step operation, where selection is completed once a clone is selected[1]. Pineapple (Ananas comosus (L.) Merr.) is a fruit crop originated and domesticated in South America. We generated a second Ananas reference genome from the bracteatus accession CB5 and resequenced numerous leading pineapple cultivars and wild Ananas species to explore the diversity and domestication history of pineapple, patterns of clonal propagation and signatures of human selection

Methods

Results

Conclusion