Wu Xiaojun, Chen Xiangdong, Wang Ren, Wang Haoquan, Hu Xigui, Wang Yuquan, Li Gan, Dong Na, Hu Tiezhu, Ru Zhengang
Wheat Research Center, Henan Institute of Science and Technology, Xinxiang, 453000, China.
State Key Laboratory of High-Efficiency Production of Wheat-Maize Double Cropping, Xinxiang, 453000, China.
BMC Genomics. 2025 Sep 2;26(1):798. doi: 10.1186/s12864-025-11983-2.
As wheat is a globally important staple crop, the molecular regulatory network underlying heterosis in wheat remains incompletely understood. The flag leaf is the primary source of photoassimilates during grain filling and plays a crucial role in yield formation. However, the genetic mechanisms linking flag leaf development to heterosis are still unclear.
Transcriptomic analysis revealed dynamic transcriptional reprogramming during the anthesis to grain-filling transition, with a pronounced expression bias toward superior parental alleles in hybrids. Anthesis-stage non-additive dominance and grain-filling-stage additive enhancement synergistically orchestrated the temporal regulatory shift underlying heterosis. The dominant alleles from the superior parent accounted for more than 60% of the non-additive genes, and the superior parent bias in allele-specific expression ratios progressively increased during development. This highlighted the role of the superior parent as an allelic reservoir. Cis-regulatory variations primarily contributed to additive effects, whereas cis×trans interactions were the primary regulatory driver of positive overdominance. Notably, weighted co-expression network analysis identified HSP90.2-B as a putative heterosis-related gene, whose coordinated overexpression with AP2/ERF transcription factors provides valuable insights for elucidating the molecular basis of yield heterosis.
This study establishes two complementary models to decode the molecular regulation of heterosis in wheat. The "dual-engine" model demonstrates stage-specific gene expression patterns: non-additive effects predominantly drive early growth vigor during the anthesis stage, whereas additive expression patterns stabilize grain development and yield-related traits at the grain-filling stage. The "two-phase regulatory shift" model captures the dynamic temporal progression of heterotic regulation, evolving from trans-regulation-driven plastic responses at the anthesis stage to cis-regulation-mediated homeostatic control at the grain-filling stage. Importantly, the preferential coupling between cis-regulation/additive and trans-regulation/non-additive expression provides molecular evidence supporting the complementary nature of the models. We further identified developmentally specific modules (the anthesis-stage Red module and grain-filling-stage Brown module) with their core regulatory networks through weighted gene co-expression network analysis. These findings preliminarily characterize the multi-layered cooperative networks regulating heterosis development, potentially offering valuable theoretical clues for deciphering the molecular mechanisms underlying wheat heterosis.
由于小麦是全球重要的主食作物，小麦杂种优势的分子调控网络仍未完全了解。旗叶是籽粒灌浆期间光合产物的主要来源，在产量形成中起关键作用。然而，将旗叶发育与杂种优势联系起来的遗传机制仍不清楚。
转录组分析揭示了从开花到籽粒灌浆转变过程中的动态转录重编程，杂种中明显偏向于优势亲本等位基因的表达。开花期非加性显性和籽粒灌浆期加性增强协同协调了杂种优势的时间调控转变。优势亲本的显性等位基因占非加性基因的60%以上，等位基因特异性表达比率中的优势亲本偏向在发育过程中逐渐增加。这突出了优势亲本作为等位基因库的作用。顺式调控变异主要促成加性效应，而顺式×反式相互作用是正向超显性的主要调控驱动因素。值得注意的是，加权共表达网络分析确定HSP90.2-B为一个假定的杂种优势相关基因，其与AP2/ERF转录因子的协同过表达为阐明产量杂种优势的分子基础提供了有价值的见解。
本研究建立了两个互补模型来解码小麦杂种优势的分子调控。“双引擎”模型展示了阶段特异性基因表达模式：非加性效应在开花期主要驱动早期生长活力，而加性表达模式在籽粒灌浆期稳定籽粒发育和产量相关性状。“两阶段调控转变”模型捕捉了杂种优势调控的动态时间进程，从开花期反式调控驱动的可塑性反应演变为籽粒灌浆期顺式调控介导的稳态控制。重要的是，顺式调控/加性与反式调控/非加性表达之间的优先耦合提供了支持模型互补性的分子证据。我们通过加权基因共表达网络分析进一步鉴定了具有核心调控网络的发育特异性模块（开花期红色模块和籽粒灌浆期棕色模块）。这些发现初步表征了调控杂种优势发育的多层合作网络，可能为破译小麦杂种优势的分子机制提供有价值的理论线索。
