Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions

Common and lifestyle‐specific traits of mycorrhizal root metabolome reflect ecological strategies of plant–mycorrhizal interactions
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菌根根代谢组的共同和生活方式特异性特征反映了植物-菌根相互作用的生态策略

DOI:
10.1111/1365-2745.14049
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发表时间:
2022-11
期刊:
影响因子:
5.5
通讯作者:
Mengxue Xia;V. Suseela;M. L. McCormack;P. Kennedy;N. Tharayil
Mengxue Xia;V. Suseela;M. L. McCormack;P. Kennedy;N. Tharayil
中科院分区:
环境科学与生态学1区
文献类型:
--
作者:
Mengxue Xia;V. Suseela;M. L. McCormack;P. Kennedy;N. Tharayil

文献摘要

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菌根是植物根系和土壤真菌之间形成的广泛的地下共生体。这种植物-真菌伙伴关系通过调节植物性能和生物地球化学过程来影响陆地生态系统。菌根对植物和生态系统功能的影响最终是由调节植物-菌根相互作用的生物过程驱动的。尽管菌根形态和遗传特征的收敛模式已得到充分证明,并反映了塑造菌根生物学的关键选择力,但与植物和生态系统功能更密切相关的菌根相关根代谢组的可概括特征仍未被探索。在这里,我们比较了多种植物-菌根真菌组合中与菌根相关的代谢组变化。具体来说,我们接种了一组不同的温带树种与丛枝菌根或外生菌根真菌(两个主要的菌根生活方式)。利用综合代谢组学方法,我们然后评估了菌根和非菌根根和相应叶片中的代谢组。在多个植物-菌根真菌组合之间进行比较,我们的数据显示了菌根生活方式所特有的代谢物改变以及与生活方式无关的植物-真菌组合中常见的代谢物改变。丛枝菌根真菌和外生菌根真菌的根积累了不同的碳水化合物,反映了独特的碳分配策略的菌根。丛枝菌根根积累的环状多元醇(如肌醇)无法访问他们的真菌合作伙伴,这表明严格的碳分配调节。这种积累在外生菌根定植的根中没有发生,而是积累了非环状多元醇(例如甘露醇和阿拉伯糖醇),这些多元醇在非菌根根中未检测到,可能是真菌来源。菌根还改变了专门的代谢,其特征是黄烷-3-醇(例如儿茶素,没食子儿茶素及其低聚物)的频繁增加,但黄烷醇的减少与菌根的生活方式无关,这表明专门的代谢物的战术重新配置,以促进和抑制共生体。这些特征性的代谢物变化主要是根特异性的,并没有反映在叶片中。合成.使用多个植物-菌根系统和代谢组学方法,我们的研究表明,在根-菌根相互作用过程中发生的部分代谢物改变在植物-菌根系统中相对常见,对成功共生的碳分配和组织保护策略都有重要意义。这些可概括的模式出现强大的宿主植物的系统发育史,因此可能是广泛的陆地植物。
Mycorrhizas are widespread below‐ground symbioses formed between plant roots and soil fungi. This plant–fungal partnership impacts terrestrial ecosystems by mediating plant performance and biogeochemical processes. The influence of mycorrhizas on plant and ecosystem functioning is ultimately driven by the biological processes that regulate plant–mycorrhizal interactions. Although convergent patterns in morphological and genetic traits of mycorrhizas have been well‐documented and reflect key selection forces that shape the biology of mycorrhizas, generalizable traits of mycorrhizal‐associated root metabolome, which are more intimately linked to plant and ecosystem functioning, remain unexplored. Here, we compared mycorrhizal‐associated metabolome alterations across multiple plant–mycorrhizal fungus combinations. Specifically, we inoculated a phylogenetically diverse set of temperate tree species with either arbuscular mycorrhizal or ectomycorrhizal fungi (the two major mycorrhizal lifestyles). Using comprehensive metabolomics approaches, we then assessed the metabolome in mycorrhizal and non‐mycorrhizal roots and the corresponding leaves. Comparing across multiple plant–mycorrhizal fungus combinations, our data revealed metabolite alterations unique to mycorrhizal lifestyle as well as those common across plant–fungus combinations irrespective of lifestyles. Roots colonized by arbuscular mycorrhizal and ectomycorrhizal fungi accumulated different sets of carbohydrates, reflecting unique carbon allocation strategies for mycorrhizas. Arbuscular mycorrhizal roots accumulated cyclic polyols (e.g. inositols) inaccessible to their fungal partners, suggesting tight regulation of carbon partitioning. Such accumulation did not occur in ectomycorrhizal‐colonized roots, which instead accrued acyclic polyols (e.g. mannitol and arabitol) that were undetected in non‐mycorrhizal roots and likely of fungal origin. Mycorrhizas also altered specialized metabolism, featuring frequent increases in flavan‐3‐ols (e.g. catechins, gallocatechins, and their oligomers) but decreases in flavanols irrespective of mycorrhizal lifestyles, suggesting tactical reconfiguration of specialized metabolites to both facilitate and restrain the symbiont. These characteristic metabolite alterations were largely root specific and were not mirrored in leaves. Synthesis. Using multiple plant–mycorrhizal systems and metabolomics approaches, our study demonstrates that part of the metabolite alterations occurring during root–mycorrhizal interactions were relatively common across plant–mycorrhizal systems, with implications for both carbon partitioning and tissue protection strategies important for successful symbiosis. These generalizable patterns appear robust to the phylogenetic history of host plants and thus may be widespread in land plants.