Genomics of sorghum local adaptation to a parasitic plant

First author: Emily S. Bellis; Affiliations: The Pennsylvania State University (宾夕法尼亚州立大学): Pennsylvania, USA

Corresponding author: Emily S. Bellis

Host–parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR–Cas9-edited sorghum further indicate that the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities.

寄主与寄生物之间的协同演化可以维持物种互作相关性状的高水平遗传多样性。在许多系统中，寄主中由寄生物利用的性状在其它功能方面会受到限制，因此导致了在时空上复杂的选择压力。本文中，作者研究了主食高粱全基因组水平上的变异以及与其寄生野草黄独脚金之间的相关性，玄参科植物黄独脚金是非洲粮食安全的主要限制性因素。作者假设沿寄生植物出现梯度上的地理选择模糊维持了高粱地方品种抗性的遗传多样性。作者发现高粱LGS1基因位点的功能缺失等位基因在不同的非洲地方品种中多次独立发生，并且地理上与黄独脚金的寄生相关，说明了局域适应于寄生压力的演化。然而，这些等位基因在黄独脚金寄生易发生地区的频率较低，而在其它地区则没有，说明了存在潜在的权衡机制限制了这些等位基因的固定。LGS1基因能够通过改变独脚金内酯的立体化学特性而产生抗性，而独脚金内酯是一类植物激素，在地上部分发挥调控植物结构的功能，而在地下可以传递信号给菌根，能够刺激寄生菌的发芽。通过分析与寄生分布相关的全基因关联分析，作者发现在LGS1基因位点以及其它候选基因周边存在平衡选择的信号，这与权衡机制的假设一致。利用CRISPR–Cas9编辑高粱的试验进一步确认了LGS1介导的抗性十分依赖于寄生植物的基因型和非生物环境，并且抗性越强，伴随着光系统基因表达下降的代价。本文的研究揭示了一个在小农农业生态系统中长期维持寄主植物抗性基因多样性的现象，为工业化农业系统与自然群体都提供了一个有价值的比较。

p.s. Geographic selection mosaics，指的是对于互作的自然选择在不同环境下是不同的。该变异发生的原因是不同环境下基因的表达不同，一个物种如何影响另一个物种的演化适应性取决于这两个物种互作发生的环境。（参考https://thompsonlab.sites.ucsc.edu/research/the-geographic-mosaic-of-coevolution/）

通讯：Emily S. Bellis (https://em-bellis.github.io)

个人简介：2006-2010年，德克萨斯A&M大学，学士；2011-2017年，俄勒冈州立大学，博士；2018-2019年，宾夕法尼亚州立大学，博士后。

研究方向：生物与生物/非生物环境的互作。

doi: https://doi.org/10.1073/pnas.1908707117

Journal: PNAS

Published online: February 07, 2020