Key Laboratory of Urban Environment and Health, Ningbo Urban Environment Observation and Research Station, Institute of Urban Environment, Chinese Academy of Sciences, Xiamen 361021, China.
Zhejiang Key Laboratory of Urban Environmental Processes and Pollution Control, CAS Haixi Industrial Technology Innovation Center in Beilun, Ningbo 315830, China.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae144.
Antibiotic resistance in plant-associated microbiomes poses significant risks for agricultural ecosystems and human health. Although accumulating evidence suggests a role for plant genotypes in shaping their microbiome, almost nothing is known about how the changes of plant genetic information affect the co-evolved plant microbiome carrying antibiotic resistance genes (ARGs). Here, we selected 16 wheat cultivars and experimentally explored the impact of host genetic variation on phyllosphere microbiome, ARGs, and metabolites. Our results demonstrated that host genetic variation significantly influenced the phyllosphere resistomes. Wheat genotypes exhibiting high phyllosphere ARGs were linked to elevated Pseudomonas populations, along with increased abundances of Pseudomonas aeruginosa biofilm formation genes. Further analysis of 350 Pseudomonas spp. genomes from diverse habitats at a global scale revealed that nearly all strains possess multiple ARGs, virulence factor genes (VFGs), and mobile genetic elements (MGEs) on their genomes, albeit with lower nucleotide diversity compared to other species. These findings suggested that the proliferation of Pseudomonas spp. in the phyllosphere significantly contributed to antibiotic resistance. We further observed direct links between the upregulated leaf metabolite DIMBOA-Glc, Pseudomonas spp., and enrichment of phyllosphere ARGs, which were corroborated by microcosm experiments demonstrating that DIMBOA-Glc significantly enhanced the relative abundance of Pseudomonas spp. Overall, alterations in leaf metabolites resulting from genetic variation throughout plant evolution may drive the development of highly specialized microbial communities capable of enriching phyllosphere ARGs. This study enhances our understanding of how plants actively shape microbial communities and clarifies the impact of host genetic variation on the plant resistomes.
植物相关微生物组中的抗生素耐药性对农业生态系统和人类健康构成了重大威胁。尽管越来越多的证据表明植物基因型在塑造其微生物组方面发挥了作用，但几乎不知道植物遗传信息的变化如何影响携带抗生素耐药基因（ARGs）的共进化植物微生物组。在这里，我们选择了 16 个小麦品种，实验探索了宿主遗传变异对叶际微生物组、ARGs 和代谢物的影响。我们的结果表明，宿主遗传变异显著影响了叶际抗性组。表现出高叶际 ARGs 的小麦基因型与假单胞菌种群的增加有关，同时与铜绿假单胞菌生物膜形成基因的丰度增加有关。进一步对来自全球不同生境的 350 个假单胞菌属基因组进行分析表明，尽管与其他物种相比，其基因组上的核苷酸多样性较低，但几乎所有菌株都拥有多种 ARGs、毒力因子基因（VFGs）和移动遗传元件（MGEs）。这些发现表明，假单胞菌属在叶际的增殖显著促进了抗生素耐药性的发展。我们进一步观察到上调的叶片代谢物 DIMBOA-Glc、假单胞菌属和叶际 ARGs 富集之间的直接联系，这些联系得到微宇宙实验的证实，表明 DIMBOA-Glc 显著增强了假单胞菌属的相对丰度。总的来说，植物进化过程中遗传变异导致的叶片代谢物的变化可能会促使高度专业化的微生物群落的发展，从而能够富集叶际 ARGs。本研究增进了我们对植物如何积极塑造微生物群落的理解，并阐明了宿主遗传变异对植物抗性组的影响。
