Department of Microbiology and Immunology, The University of British Columbia, Vancouver, BC, Canada.
Michael Smith Laboratories, The University of British Columbia, Vancouver, BC, Canada.
Mol Ecol. 2018 Apr;27(8):1833-1847. doi: 10.1111/mec.14400. Epub 2017 Nov 23.
Plant-associated soil microbes are important mediators of plant defence responses to diverse above-ground pathogen and insect challengers. For example, closely related strains of beneficial rhizosphere Pseudomonas spp. can induce systemic resistance (ISR), systemic susceptibility (ISS) or neither against the bacterial foliar pathogen Pseudomonas syringae pv. tomato DC3000 (Pto DC3000). Using a model system composed of root-associated Pseudomonas spp. strains, the foliar pathogen Pto DC3000 and the herbivore Trichoplusia ni (cabbage looper), we found that rhizosphere-associated Pseudomonas spp. that induce either ISS and ISR against Pto DC3000 all increased resistance to herbivory by T. ni. We found that resistance to T. ni and resistance to Pto DC3000 are quantitative metrics of the jasmonic acid (JA)/salicylic acid (SA) trade-off and distinct strains of rhizosphere-associated Pseudomonas spp. have distinct effects on the JA/SA trade-off. Using genetic analysis and transcriptional profiling, we provide evidence that treatment of Arabidopsis with Pseudomonas sp. CH267, which induces ISS against bacterial pathogens, tips the JA/SA trade-off towards JA-dependent defences against herbivores at the cost of a subset of SA-mediated defences against bacterial pathogens. In contrast, treatment of Arabidopsis with the ISR strain Pseudomonas sp. WCS417 disrupts JA/SA antagonism and simultaneously primes plants for both JA- and SA-mediated defences. Our findings show that ISS against the bacterial foliar pathogens triggered by Pseudomonas sp. CH267, which is a seemingly deleterious phenotype, may in fact be an adaptive consequence of increased resistance to herbivory. Our work shows that pleiotropic effects of microbiome modulation of plant defences are important to consider when using microbes to modify plant traits in agriculture.
植物相关的土壤微生物是植物防御反应的重要调节因子，可应对多种地上部病原体和昆虫侵害。例如，有益的根际假单胞菌（Pseudomonas spp.）近缘菌株可以诱导系统抗性（ISR）、系统易感性（ISS）或两者都不诱导细菌性叶部病原体丁香假单胞菌 pv.番茄 DC3000（Pto DC3000）。我们使用由根相关假单胞菌菌株、叶部病原体 Pto DC3000 和植食性小菜蛾（T. ni）组成的模型系统发现，诱导 Pto DC3000 产生 ISS 和 ISR 的根际相关假单胞菌均增加了对 T. ni 取食的抗性。我们发现，对 T. ni 的抗性和对 Pto DC3000 的抗性是茉莉酸（JA）/水杨酸（SA）权衡的定量指标，而根际相关假单胞菌的不同菌株对 JA/SA 权衡具有不同的影响。通过遗传分析和转录谱分析，我们提供的证据表明，用诱导细菌病原体 ISS 的假单胞菌 sp. CH267 处理拟南芥会使 JA/SA 权衡向 JA 依赖型防御转变，以牺牲部分 SA 介导的防御来抵御细菌病原体。相比之下，用 ISR 菌株假单胞菌 sp. WCS417 处理拟南芥会破坏 JA/SA 拮抗作用，并同时使植物对 JA 和 SA 介导的防御做好准备。我们的研究结果表明，由假单胞菌 sp. CH267 引发的对细菌性叶部病原体的 ISS 可能实际上是增加对取食抗性的适应性结果，因为这看似是一种有害表型。我们的工作表明，在农业中使用微生物来改变植物性状时，微生物对植物防御的多效性调节效应非常重要。
