RESEARCH-PGR: The Cytonuclear Dimension of Allopolyploidy

基因组学时代的一个关键认识是所有植物，包括我们的主要作物，都有基因组复制的历史，其中细胞内的DNA含量翻倍（多倍体）。尽管近年来人们对基因组加倍的后果已经了解了很多，但关于基因组复制如何促进植物生物学和作物生产力的许多基本问题仍然存在。基因组复制的一个重要方面是现在加倍的核基因组如何与植物细胞内发现的其他基因组区室（如线粒体和质体）相互作用。计划中的研究将调查基因组复制这一未被充分探索的方面，并揭示在生长、繁殖和产量中起关键作用的细胞能量学如何在基因组加倍事件发生后发生改变。这项研究将使用多种重要作物系统和最先进的基因组技术。项目资源、数据和人员将用于扩大推广和教育计划，包括基因组学国际研讨会系列，以及为高中教师提供实际研究和课程开发的沉浸式体验的长期努力。该项目将为研究和服务学习的各个教育和职业阶段的参与者创造培训机会。总而言之，本研究旨在为基因组相互作用和作物生物学提供基础见解，并扩大植物生物学研究的参与。异源多倍体事件需要两个不同谱系的基因组同时合并，并伴随着核基因组含量的加倍。由于细胞质基因组通常只从一个（母亲）亲本遗传，异源多倍体化预计会对细胞核和细胞质基因组的相对拷贝数（即化学计量）产生复杂的影响，并且还会产生新的、“未经测试的”细胞核和细胞质基因型配对。计划中的研究将揭示基因组反应的频谱，以减轻异源多倍体对细胞核相互作用的破坏性影响，并促进杂交/多倍体谱系的成功建立。生物信息学分析将测试细胞器靶核基因的预测代偿反应，这些基因解决了父系衍生的核亚基因组和母系衍生的细胞质基因组之间的不适应相互作用，包括：(1)母系偏倚基因转换；(2)选择压力改变对父系亚基因组序列进化的影响；(3)父本偏性假原化和基因丢失；(4)父本同源基因的优先下调。通过对600个棉花异源多倍体基因组的重新测序，该研究将扩展到群体基因组水平，以检测这些“实际”效应。最后，细胞核与细胞质基因组的相对拷贝数以及细胞核、线粒体和质体的相对表达水平将被精确量化，以区分对化学计量失衡的多种假设反应。总之，这些分析将为细胞核相互作用是否以及如何促进多倍体作物的形成和进化提供强有力的测试。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

One of the key realizations of the genomics era is that all plants, including our major crop plants, have histories of genome duplication in which the DNA content inside cells is doubled (polyploidy). Although much has been learned about the consequences of genome doubling in recent years, many fundamental questions remain regarding how genome duplication contributes to plant biology and crop productivity. An important dimension of genome duplication is how the now-doubled nuclear genome interacts with other genomic compartments found within the plant cell, such as the mitochondria and plastids. The planned research will investigate this underexplored aspect of genome duplications, with implications for how cellular energetics, which play a key role in growth, reproduction, and yield, are altered in the wake of genome doubling events. The research will use a diverse panel of important crop systems and state-of-the-art genomics techniques. Project resources, data, and personnel will be used to expand outreach and education programs, including an international workshop series on genomics and a long-term effort to provide high school teachers with an immersive experience in hands-on research and curricular development. The project will create training opportunities for participants across the full range of educational and career stages in both research and service-learning. In sum, this research aims to provide fundamental insights into genome interactions and crop biology and broaden participation in plant biological research.Allopolyploidy events entail the simultaneous merger of genomes from two divergent lineages combined with the doubling of nuclear genome content. Because cytoplasmic genomes are typically inherited from only a single (maternal) parent, allopolyploidization is expected to have complex effects on the relative copy number (i.e., stoichiometry) of nuclear and cytoplasmic genomes, and also create novel, "untested" pairings of nuclear and cytoplasmic genotypes. The planned research will reveal the spectrum of genomic responses that alleviate the disruptive effects of allopolyploidy on cytonuclear interactions and facilitate the successful establishment of hybrid/polyploid lineages. Bioinformatic analyses will test for predicted compensatory responses in organelle-targeted nuclear genes that resolve maladapted interactions between the paternally derived nuclear subgenome and maternally derived cytoplasmic genomes, including: (1) maternally biased gene conversion; (2) altered selection pressures on sequence evolution in the paternal subgenome; (3) paternally biased pseudogenization and gene loss; and (4) preferential down-regulation of paternal homoeologs. By taking advantage of 600 re-sequenced genomes from cotton allopolyploids, the proposed research will be extended to the population-genomic level to detect these effects "in action". Finally, the relative copy number of nuclear vs. cytoplasmic genomes and the relative expression levels in the nucleus, mitochondria, and plastids will be precisely quantified to differentiate among multiple hypothesized responses to stoichiometric imbalance. Together, these analyses will provide a powerful test of whether and how cytonuclear interactions contribute to the formation and evolution of polyploid crops.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.