Relationships between Sphaerulina musiva infection and the Populus microbiome and metabolome

Pathogenic fungal infection in plants may, in some cases, lead to downstream systematic impacts on the plant metabolome and microbiome that may inhibit or exacerbate the effects of fungal infection. While Sphaerulina musiva is a well-characterized fungal pathogen, which infects Populus species, important wood fiber and biofuel feedstock crops, little is known about its systematic effects on the metabolome and microbiome of Populus. Here, we investigate the microbiome and metabolome of P. trichocarpa and P. deltoides leaves and roots and the microbiome of their associated surfaces (i.e., phylloplane and rhizosphere, respectively) to understand the systematic impact of S. musiva abundance and infection on Populus species in a common garden field setting. We find that S. musiva is indeed present in both P. deltoides and P. trichocarpa, but S. musiva abundance is unrelated to stem canker onset and development. We also find that the leaf and root metabolomes significantly differ between the two Populus species and that certain leaf metabolites, particularly the phenolic glycosides salirepin and salireposide, are diminished in canker-infected P. trichocarpa trees compared to their uninfected counterparts. Furthermore, we found significant associations between the metabolome, S. musiva abundance and the microbiome, particularly in P. trichocarpa leaves. This suggests that the effects of S. musiva on P. trichocarpa trees are widespread and not confined to the site of canker infection.

植物病原真菌感染在部分情况下，可对植物代谢组（metabolome）与微生物组（microbiome）产生后续系统性影响，这类影响或抑制或加重真菌感染的病情进程。尽管球腔菌（Sphaerulina musiva）是一种特征明确的真菌病原菌，可侵染作为重要木纤维与生物燃料原料作物的杨属（Populus）植物，但目前学界对其引发的杨属植物代谢组与微生物组系统性影响仍知之甚少。本研究针对毛果杨（P. trichocarpa）与美洲黑杨（P. deltoides）的叶片、根系，及其关联生境（分别为叶围（phylloplane）与根际（rhizosphere））的微生物组与代谢组展开系统性分析，旨在探究共同花园田间试验环境下，球腔菌的丰度与侵染对杨属植物产生的系统性影响。研究结果显示，球腔菌确实可在美洲黑杨与毛果杨中检出，但该菌的丰度与杨树茎溃疡病的发生及发展并无显著关联。同时本研究发现，两种杨属植物的叶片与根系代谢组存在显著差异；与未感染溃疡病的毛果杨个体相比，感染溃疡病的毛果杨体内部分叶片代谢物（尤其是酚苷类（phenolic glycosides）化合物salirepin与salireposide）的含量显著降低。此外，本研究还发现代谢组、球腔菌丰度与微生物组三者之间存在显著关联，这一现象在毛果杨叶片中尤为突出。这表明球腔菌对毛果杨的影响具有广谱性，并非仅局限于溃疡病的侵染位点。