Impacts of parental genomic divergence in non-syntenic regions on cotton heterosis,Journal of Advanced Research

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Impacts of parental genomic divergence in non-syntenic regions on cotton heterosis
Journal of Advanced Research ( IF 11.4 ) Pub Date : 2024-08-06 , DOI: 10.1016/j.jare.2024.08.010
Chujun Huang ₁ , Yu Cheng ₁ , Yan Hu ₂ , Xuemei Zhang ₃ , Jinwen Chen ₁ , Ting Zhao ₁ , Zhanfeng Si ₁ , Yiwen Cao ₂ , Yiqian Li ₁ , Lei Fang ₂ , Xueying Guan ₂ , Tianzhen Zhang ₂

Affiliation

Introduction

Heterosis has revolutionized crop breeding, enhancing global agricultural production. However, the mechanisms underlying heterosis remain obscure. Xiangzamian 2# (XZM2), a super hybrid upland cotton (Gossypium hirsutum L.) characterized by high-yield heterosis, has been developed and extensively planted in China.

Objectives

We conducted a systematic analysis of CRI12 and J8891, two parents of XZM2. We aimed to reveal the precise genetic information and the role of non-syntenic divergence in shaping heterosis, laying a foundation for advancing understanding of heterosis.

Methods

We de novo assembled high-quality genomes of CRI12 and J8891, and further uncovered abundant genetic variations and non-syntenic regions between the parents. Whole-genome comparison, association analysis, transcriptomic analysis and relative identity-by-descent (rIBD) estimation were conducted to identify structural variations (SVs) and introgressions within non-syntenic blocks and to analyze their impacts on promoting heterosis.

Results

Parental genetic divergence increased in non-syntenic regions. Furthermore, these regions, accounting for only 16.71% of the total genome, contained more loci with significantly higher heterotic effects, far exceeding the syntenic background. SVs covered 97.26% of non-syntenic sequences and caused widespread gene expression differences in these regions, driving dynamic complementation of gene expression in the hybrid. A set of SVs were responsible for trait improvement and had positive effects on heterosis, contributing larger heritability than short variations. We characterized numerous parental-specific introgressions from G. barbadense. Specifically, a functional introgression segment within non-syntenic blocks introduced an elite haplotype, which significantly increased lint yield and enhanced heterosis.

Conclusion

Our study clarified non-syntenic regions to harbor more loci with higher heterotic effects, revealed their importance in promoting heterosis and supported the crucial role of genetic complementation in heterosis. SVs and introgressions were identified as key factors responsible for non-syntenic divergence between the parents. They had important effects on gene expression and trait improvement, positively contributing to heterosis.

中文翻译：

非共丝区亲本基因组分化对棉花优势的影响

介绍

优势彻底改变了作物育种，促进了全球农业生产。然而，优势的潜在机制仍然不清楚。香杂棉 2# （XZM2）是一种以高产优势为特征的超级杂交陆地棉（Gossypium hirsutum L.），已在我国开发并广泛种植。

目标

我们对 XZM2 的两个亲本 CRI12 和 J8891 进行了系统分析。我们旨在揭示精确的遗传信息和非同线分歧在塑造优势中的作用，为促进对优势的理解奠定基础。

方法

我们从头组装了 CRI12 和 J8891 的高质量基因组，并进一步发现了亲本之间丰富的遗传变异和非共丝区域。进行全基因组比较、关联分析、转录组分析和相对同源鉴定（rIBD）估计，以确定非连线块内的结构变异（SVs）和渗入，并分析它们对促进优势的影响。

结果

亲本遗传分化在非同线区域增加。此外，这些区域仅占总基因组的 16.71%，包含更多的基因座，具有显著更高的效应，远超共线背景。SVs 覆盖了 97.26% 的非同线序列，并在这些区域引起了广泛的基因表达差异，从而推动了杂交种中基因表达的动态互补。一组 SVs 负责性状改善，对优势有积极影响，比短变异贡献更大的遗传力。我们表征了来自 G. barbadense 的许多亲本特异性渗入。具体来说，非共丝块中的功能性渗入片段引入了精英单倍型，这显着提高了棉绒产量并增强了优势。