Introduction

Numerous crops have transitioned to hybrid seed production to increase yields and yield stability through heterosis. However, the molecular mechanisms underlying heterosis and its stability across environments are not yet fully understood.

Objectives

This study aimed to (1) elucidate the genetic and molecular mechanisms underlying heterosis in sunflower, and (2) determine how heterosis is maintained under different environments.

Methods

Genome-wide association (GWA) analyses were employed to assess the effects of presence/absence variants (PAVs) and stop codons on 16 traits phenotyped in the sunflower association mapping population at three locations. To link the GWA results to transcriptomic variation, we sequenced the transcriptomes of two sunflower cultivars and their F₁ hybrid (INEDI) under both control and drought conditions and analyzed patterns of gene expression and alternative splicing.

Results

Thousands of PAVs were found to affect phenotypic variation using a relaxed significance threshold, and at most such loci the “absence” allele reduced values of heterotic traits, but not those of non-heterotic traits. This pattern was strengthened for PAVs that showed expression complementation in INEDI. Stop codons were much rarer than PAVs and less likely to reduce heterotic trait values. Hybrid expression patterns were enriched for the GO category, sensitivity to stimulus, but all genotypes responded to drought similarily – by up-regulating water stress response pathways and down-regulating metabolic pathways. Changes in alternative splicing were strongly negatively correlated with expression variation, implying that alternative splicing in this system largely acts to reinforce expression responses.

Conclusion

Our results imply that complementation of expression of PAVs in hybrids is a major contributor to heterosis in sunflower, consistent with the dominance model of heterosis. This mechanism can account for yield stability across different environments. Moreover, given the much larger numbers of PAVs in plant vs. animal genomes, it also offers an explanation for the stronger heterotic responses seen in the former.

中文翻译：

---

杂种中基因存在/缺失多态性的表达互补对向日葵的杂种优势有重要贡献

介绍

许多作物已经过渡到杂交种子生产，以通过杂种优势提高产量和产量稳定性。然而，杂种优势的分子机制及其跨环境稳定性尚未完全了解。

目标

本研究旨在 (1) 阐明向日葵杂种优势的遗传和分子机制，以及 (2) 确定如何在不同环境下维持杂种优势。

方法

全基因组关联 (GWA) 分析用于评估存在/不存在变异 (PAV) 和终止密码子对三个地点的向日葵关联作图群体中表型的 16 个性状的影响。为了将 GWA 结果与转录组变异联系起来，我们在对照和干旱条件下对两个向日葵品种及其 F ₁杂种 (INEDI) 的转录组进行了测序，并分析了基因表达和选择性剪接的模式。

结果

发现数以千计的 PAV 使用宽松的显着性阈值影响表型变异，并且在大多数此类基因座中，“缺失”等位基因会降低杂种优势性状的值，但不会降低非杂种优势性状的值。对于在 INEDI 中显示表达互补的 PAV，这种模式得到了加强。终止密码子比 PAV 少得多，并且不太可能降低杂种优势性状值。GO 类别、对刺激的敏感性丰富了混合表达模式，但所有基因型对干旱的反应相似——通过上调水分胁迫反应途径和下调代谢途径。可变剪接的变化与表达变异呈强烈负相关，这意味着该系统中的可变剪接主要用于加强表达反应。

结论

我们的结果表明，杂种中 PAV 表达的互补是向日葵杂种优势的主要贡献者，与杂种优势的优势模型一致。这种机制可以解释不同环境下的产量稳定性。此外，鉴于植物基因组与动物基因组中的 PAV 数量要多得多，它也解释了前者中出现的更强的杂种优势反应。