Feurtey Alice, Guitton Ellen, De Gracia Coquerel Marie, Duvaux Ludovic, Shiller Jason, Bellanger Marie-Noëlle, Expert Pascale, Sannier Mélanie, Caffier Valérie, Giraud Tatiana, Le Cam Bruno, Lemaire Christophe
Ecologie Systématique Evolution, CNRS, AgroParisTech, Université Paris-Saclay, Orsay, France.
Max Planck Institute for Evolutionary Biology, Plön, Germany.
Mol Ecol. 2020 Dec;29(24):4925-4941. doi: 10.1111/mec.15677. Epub 2020 Oct 27.
Secondary contact between crops and their wild relatives poses a threat to wild species, not only through gene flow between plants, but also through the dispersal of crop pathogens and genetic exchanges involving these pathogens, particularly those that have become more virulent by indirect selection on resistant crops, a phenomenon known as "pestification." Joint analyses of wild and domesticated hosts and their pathogens are essential to address this issue, but such analyses remain rare. We used population genetics approaches, demographic inference and pathogenicity tests on host-pathogen pairs of wild or domesticated apple trees from Central Asia and their main fungal pathogen, Venturia inaequalis, which itself has differentiated agricultural and wild-type populations. We confirmed the occurrence of gene flow from cultivated (Malus domestica) to wild (Malus sieversii) apple trees in Asian forests, potentially threatening the persistence of Asian wild apple trees. Pathogenicity tests demonstrated the pestification of V. inaequalis, the agricultural-type population being more virulent on both wild and domesticated trees. Single nucleotide polymorphism (SNP) markers and the demographic modelling of pathogen populations revealed hybridization following secondary contact between agricultural and wild-type fungal populations, and dispersal of the agricultural-type pathogen population in wild forests, increasing the threat of disease in the wild apple species. We detected an SNP potentially involved in pathogen pestification, generating an early stop codon in a gene encoding a small secreted protein in the agricultural-type fungal population. Our findings, based on joint analyses of paired host and pathogen data sets, highlight the threat posed by cultivating a crop near its centre of origin, in terms of pestified pathogen invasions in wild plant populations and introgression in the wild-type pathogen population.
作物与其野生近缘种之间的二次接触对野生物种构成了威胁，不仅通过植物间的基因流动，还通过作物病原体的传播以及涉及这些病原体的基因交换，特别是那些通过对抗性作物的间接选择而变得更具毒性的病原体，这一现象被称为“有害生物化”。对野生和驯化宿主及其病原体进行联合分析对于解决这一问题至关重要，但此类分析仍然很少见。我们采用群体遗传学方法、种群统计学推断以及对来自中亚的野生或驯化苹果树与其主要真菌病原体苹果黑星病菌（Venturia inaequalis）的宿主 - 病原体对进行致病性测试，该病菌本身已分化出农业型和野生型种群。我们证实了在亚洲森林中存在从栽培苹果（Malus domestica）到野生苹果（Malus sieversii）的基因流动，这可能威胁到亚洲野生苹果树的存续。致病性测试表明苹果黑星病菌出现了有害生物化现象，农业型种群对野生和驯化树木的毒性都更强。单核苷酸多态性（SNP）标记和病原体种群的种群统计学建模揭示了农业型和野生型真菌种群二次接触后的杂交现象，以及农业型病原体种群在野生森林中的扩散，增加了野生苹果物种患病的威胁。我们检测到一个可能与病原体有害生物化有关的SNP，它在农业型真菌种群中一个编码小分泌蛋白的基因中产生了一个提前终止密码子。我们基于对配对宿主和病原体数据集的联合分析得出的结果，突出了在作物起源中心附近种植作物所带来的威胁，即在野生植物种群中有害病原体的入侵以及野生型病原体种群中的基因渗入。
