Resequencing of 388 cassava accessions identifies valuable loci and selection for variation in heterozygosity

Wei Hu,Wenquan Wang,Xiaoying Yang,Liming Ma,Qingyun Leng,Jianhua Xie ,Biao Xu ,Jie Zhang,Zhiqiang Jin,Yin Li,Ruoxi Li,Songbi Chen,Xia Xiao ,Weiwei Tie,Mingcheng Wang,Gang Zhou,Jinghao Yang,Ming Peng,Yang Zhou,Xiaolong Li,Zehong Ding,Haitao Shi,Feifei An,Jiao Guo ,Ray Ming,Jianqiu Ye,Changmian Ji,Wenjun Ou,Yan Yan,Yunxie Wei,Zhongqing Wan,Zhe Liang,Anping Guo,Kaimian Li

doi:10.1186/s13059-021-02524-7

Abstract

BackgroundHeterozygous genomes are widespread in outcrossing and clonally propagated crops. However, the variation in heterozygosity underlying key agronomic traits and crop domestication remains largely unknown. Cassava is a staple crop in Africa and other tropical regions and has a highly heterozygous genome.ResultsWe describe a genomic variation map from 388 resequenced genomes of cassava cultivars and wild accessions. We identify 52 loci for 23 agronomic traits through a genome-wide association study. Eighteen allelic variations in heterozygosity for nine candidate genes are significantly associated with seven key agronomic traits. We detect 81 selective sweeps with decreasing heterozygosity and nucleotide diversity, harboring 548 genes, which are enriched in multiple biological processes including growth, development, hormone metabolisms and responses, and immune-related processes. Artificial selection for decreased heterozygosity has contributed to the domestication of the large starchy storage root of cassava. Selection for homozygous GG allele in MeTIR1 during domestication contributes to increased starch content. Selection of homozygous AA allele in MeAHL17 is associated with increased storage root weight and cassava bacterial blight (CBB) susceptibility. We have verified the positive roles of MeTIR1 in increasing starch content and MeAHL17 in resistance to CBB by transient overexpression and silencing analysis. The allelic combinations in MeTIR1 and MeAHL17 may result in high starch content and resistance to CBB.ConclusionsThis study provides insights into allelic variation in heterozygosity associated with key agronomic traits and cassava domestication. It also offers valuable resources for the improvement of cassava and other highly heterozygous crops.

Highlights

Heterozygous genomes are widespread in outcrossing and clonally propagated crops
This study identified valuable loci with variation in heterozygosity associated with key agronomic traits and offered insights into variation in heterozygosity during cassava domestication, which provides a large amount of new genomic resources for utilization of heterozygosity to accelerate cassava improvement
This study provided a variation map of 388 cassava accessions, identified 52 loci for 23 agronomic traits, and revealed allelic variation in heterozygosity associated with key agronomic traits and cassava domestication

Summary

Introduction

The variation in heterozygosity underlying key agronomic traits and crop domestication remains largely unknown. Associations between genotypes and phenotypes in populations have revealed homozygous allelic variations that are significantly associated with key agronomic traits in many crops, including rice [3], maize [4], tomato [2], and cotton [5], thereby accelerating the breeding process. We can track crop domestication and breeding history, and thereby better understand how human selection shaped crop genomes, as shown in tomato [2], cotton [9], rice [10], maize [11], soybean [12], peach [13], melon [14], watermelon [15], and pineapple [16]. The variation in heterozygosity underlying crop domestication remains largely unknown

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Conclusion