Collaborative Research: Processes and Consequences of Somatic Mutation Accumulation in Plants

该项目将解决一个长期存在的问题，即植物茎生长过程中的突变（体细胞突变）是否在成年植物中进行自然选择，传递给后代，并影响后代的适应性。突变是进化和适应变异的最终来源，但除非突变遗传给下一代，否则它不会影响进化。在动物中，只有在精子和卵子发育过程中发生的突变才是可遗传的。然而，植物不同于动物，因为它们可以积累额外的体细胞突变。尽管植物中有这种额外的遗传变异来源，但植物和动物之间的总体突变率是相似的。对这一悖论的一种可能解释是，植物生长过程中，自然选择过滤了体细胞突变。预计这一过程将去除有害的突变，保留有益的突变，这些突变可能影响后代的植物活力。使用黄猴花（Mimulus guttatus），该项目将首次对这一过滤过程进行全面测试。该项目的成果也将在植物育种、农业和保护生物学等领域有重要应用。此外，该项目将涉及高中，本科生和研究生的实践研究经验。尽管体细胞突变有可能在植物种群中产生新的遗传变异，但它们在植物进化中的作用仍然几乎完全未被探索。初步研究结果表明，单个茎可以拥有独特的体细胞变异，体细胞突变可以对幼苗活力产生实质性影响。此外，模型预测，随着茎的生长，体细胞突变的数量将保持在中等水平，并不断发生突变。该项目将通过以下方式检验这些模型的假设和预测：1)检查生殖和营养组织中共有体细胞突变的分布，2)估计高盐和低盐胁迫下的突变周转率，3)确定与有益突变出现相关的基因组效应，以及4)评估体细胞突变对幼苗活力的影响。基因组测序将允许体细胞突变沿着单个茎的时间进行跟踪，以估计周转率并揭示有益突变的存在。最后，本项目将通过比较不同交配策略繁殖的选择系对压力的反应来测试体细胞突变对适应性进化的贡献。这项工作的结果将揭示植物体细胞突变的基因组和表型后果，并将提高我们对植物进化的理解。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。

This project will address the long-standing question of whether mutations during stem growth (somatic mutations) in plants undergo natural selection within the adult plant, are passed to offspring, and affect the fitness of those offspring. Mutation is the ultimate source of variation for evolution and adaptation, but unless a mutation is inherited in the next generation, it will not affect evolution. In animals, only mutations that occur during the development of the sperm and egg are heritable. However, plants differ from animals, because they can accumulate additional somatic mutations. Despite this extra source of genetic variation in plants, overall mutation rates are similar between plants and animals. One potential explanation for this paradox is that somatic mutations are filtered by natural selection as plants grow. This process is predicted to remove harmful mutations and to retain beneficial ones, which could affect plant vigor in subsequent generations. Using the yellow monkeyflower (Mimulus guttatus), this project will provide the first comprehensive tests of this filtering process. The results from this project will also have important applications for the fields of plant breeding, agriculture, and conservation biology. Additionally, this project will involve high school, undergraduate, and graduate students in hands-on research experiences.Despite the potential for somatic mutations to generate novel genetic variation in plant populations, their role in plant evolution remains almost entirely unexplored. Preliminary findings demonstrate that individual stems can possess unique complements of somatic variants, and that somatic mutations can have substantial effects on seedling vigor. Moreover, models predict the maintenance of moderate numbers and constant turnover of somatic mutations as stems grow. This project will test the assumptions and predictions of these models by: i) examining the distribution of shared somatic mutations in reproductive and vegetative tissues, ii) estimating rates of mutation turnover under high and low salinity stress, iii) identifying the genomic effects associated with the appearance of beneficial mutations, and iv) evaluating the consequences of somatic mutations on seedling vigor. Genomic sequencing will allow somatic mutations to be tracked through time along individual stems to estimate rates of turnover and to reveal the presence of beneficial mutations. Finally, this project will test the potential for somatic mutations to contribute to adaptive evolution by contrasting the responses to stress in selection lines propagated by different mating strategies. The outcomes of this work will reveal the genomic and phenotypic consequences of somatic mutations in plants and will improve our understanding of plant evolution.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.