Institute of Botany, Jiangsu Province and Chinese Academy of Sciences, Nanjing 210014, China.
Institute of Crop Germplasm and Biotechnology, Jiangsu Academy of Agricultural Sciences/The Jiangsu Provincial Platform for Conservation and Utilization of Agricultural Germplasm, Nanjing 210014, China.
Genetics. 2022 Apr 4;220(4). doi: 10.1093/genetics/iyac019.
In plants, large numbers of R genes, which segregate as loci with alternative alleles conferring different levels of disease resistance to pathogens, have been maintained over a long period of evolution. The reason why hosts harbor susceptible alleles in view of their null contribution to resistance is unclear. In rice, a single copy gene, Pi-ta, segregates for 2 expressed clades of alleles, 1 resistant and the other susceptible. We simulated loss-of-function of the Pi-ta susceptible allele using the CRISPR/Cas9 system to detect subsequent fitness changes and obtained insights into fitness effects related to the retention of the Pi-ta susceptible allele. Our creation of an artificial knockout of the Pi-ta susceptible allele suffered fitness-related trait declines of up to 49% in terms of filled grain yield upon the loss of Pi-ta function. The Pi-ta susceptible alleles might serve as an off-switch to downstream immune signaling, thus contributing to the fine-tuning of plant defense responses. The results demonstrated that the susceptible Pi-ta alleles should have evolved pleiotropic functions, facilitating their retention in populations. As Pi-ta is a single copy gene with no paralogs in the genome, its function cannot be compensated by an alternative gene; whereas most other R genes form gene clusters by tandem duplications, and the function could be compensated by paralogs with high sequence similarity. This attempt to evaluate the fitness effects of the R gene in crops indicates that not all disease resistance genes incur fitness costs, which also provides a plausible explanation for how host genomes can tolerate the possible genetic load associated with a vast repertoire of R genes.
在植物中，大量的 R 基因作为具有替代等位基因的基因座进行遗传，这些等位基因赋予了宿主对病原体不同程度的抗病性。然而，尽管这些等位基因对宿主的抗病性没有贡献，但它们在长期的进化过程中得以保留，其原因尚不清楚。在水稻中，单个拷贝的基因 Pi-ta 可分为两个表达的等位基因簇，一个是抗性的，另一个是敏感的。我们使用 CRISPR/Cas9 系统模拟 Pi-ta 敏感等位基因的功能丧失，以检测随后的适应性变化，并深入了解与保留 Pi-ta 敏感等位基因相关的适应性效应。我们创建了 Pi-ta 敏感等位基因的人工敲除体，发现当 Pi-ta 功能丧失时，其饱满粒产量的适应性相关性状下降了高达 49%。Pi-ta 敏感等位基因可能作为下游免疫信号的关闭开关，从而有助于植物防御反应的精细调控。研究结果表明，敏感的 Pi-ta 等位基因可能具有多效性的功能，这有助于它们在群体中的保留。由于 Pi-ta 是基因组中没有同源基因的单拷贝基因，其功能不能被替代基因所补偿；而大多数其他 R 基因通过串联重复形成基因簇，其功能可以被具有高度序列相似性的同源基因所补偿。这项评估作物中 R 基因适应性效应的尝试表明，并非所有的抗病基因都会带来适应性成本，这也为宿主基因组如何能够容忍与大量 R 基因相关的潜在遗传负荷提供了合理的解释。
