The Green Revolution shaped the population structure of the rice pathogen Xanthomonas oryzae pv. oryzae

First author: Ian Lorenzo Quibod; Affiliations: International Rice Research Institute (国际水稻研究所): Metro Manila, Philippines

Corresponding author: Ricardo Oliva 

The impact of modern agriculture on the evolutionary trajectory of plant pathogens is a central question for crop sustainability. The Green Revolution replaced traditional rice landraces with high-yielding varieties, creating a uniform selection pressure that allows measuring the effect of such intervention. In this study, we analyzed a unique historical pathogen record to assess the impact of a major resistance gene, Xa4, in the population structure of Xanthomonas oryzae pv. oryzae (Xoo) collected in the Philippines in a span of 40 years. After the deployment of Xa4 in the early 1960s, the emergence of virulent pathogen groups was associated with the increasing adoption of rice varieties carrying Xa4, which reached 80% of the total planted area. Whole genomes analysis of a representative sample suggested six major pathogen groups with distinctive signatures of selection in genes related to secretion system, cell-wall degradation, lipopolysaccharide production, and detoxification of host defense components. Association genetics also suggested that each population might evolve different mechanisms to adapt to Xa4. Interestingly, we found evidence of strong selective sweep affecting several populations in the mid-1980s, suggesting a major bottleneck that coincides with the peak of Xa4 deployment in the archipelago. Our study highlights how modern agricultural practices facilitate the adaptation of pathogens to overcome the effects of standard crop improvement efforts.

现代农业对植物病原体演化轨迹的影响是作物可持续性的核心问题。绿色革命用高产品种取代了传统的水稻地方品种，使得选择压力变得均一化，可以衡量这种干预的效果。本文中，作者分析了菲律宾收集到的横跨40年的独特历史病原体记录，以评估主要抗性基因Xa4对水稻黄单胞菌水稻致病变种Xoo种群结构的影响。在1960年代初Xa4使用之后，具有毒力的病原体群的出现与携带Xa4的水稻品种的采用增加有关，该品种达到了总种植面积的80％。对代表样品的全基因组分析表明，六个主要病原体群组在与分泌系统、细胞壁降解、脂多糖产生和宿主防御成分排毒相关的基因中具有明显不同的选择特征。关联遗传学还显示，每个群体可能演化出了不同的机制来适应Xa4。有趣的是，作者发现了在1980年代中期强烈的选择性清除影响了一些群体的证据，这表明该病原菌群体的一个群体瓶颈与Xa4的使用高峰相吻合。本文的研究突出了现代农业实践如何促进了病原体的适应性，以克服标准化作物改良对其的影响。

通讯：Ricardo Oliva (https://www.irri.org/about-us/our-people/ricardo-oliva)

研究方向：作物育种改良。

doi: https://doi.org/10.1038/s41396-019-0545-2

Journal: The ISME Journal

Published date: October 30, 2019