In nature, roots of healthy plants are colonized by multikingdom microbial communities that include bacteria, fungi, and oomycetes. A key question is how plants control the assembly of these diverse microbes in roots to maintain host–microbe homeostasis and health. Using microbiota reconstitution experiments with a set of immunocompromised Arabidopsis thaliana mutants and a multikingdom synthetic microbial community (SynCom) representative of the natural A. thaliana root microbiota, we observed that microbiota-mediated plant growth promotion was abolished in most of the tested immunocompromised mutants. Notably, more than 40% of between-genotype variation in these microbiota-induced growth differences was explained by fungal but not bacterial or oomycete load in roots. Extensive fungal overgrowth in roots and altered plant growth was evident at both vegetative and reproductive stages for a mutant impaired in the production of tryptophan-derived, specialized metabolites (cyp79b2/b3). Microbiota manipulation experiments with single- and multikingdom microbial SynComs further demonstrated that 1) the presence of fungi in the multikingdom SynCom was the direct cause of the dysbiotic phenotype in the cyp79b2/b3 mutant and 2) bacterial commensals and host tryptophan metabolism are both necessary to control fungal load, thereby promoting A. thaliana growth and survival. Our results indicate that protective activities of bacterial root commensals are as critical as the host tryptophan metabolic pathway in preventing fungal dysbiosis in the A. thaliana root endosphere.

在自然界中，健康植物的根部被包括细菌、真菌和卵菌在内的多界微生物群落定殖。一个关键问题是植物如何控制这些不同微生物在根部的组装以维持宿主-微生物的稳态和健康。使用一组免疫功能低下的拟南芥突变体和代表天然拟南芥的多界合成微生物群落 (SynCom) 进行微生物群重建实验根微生物群，我们观察到微生物群介导的植物生长促进在大多数测试的免疫受损突变体中被取消。值得注意的是，在这些微生物群诱导的生长差异中，超过 40% 的基因型间变异可以由根中的真菌而非细菌或卵菌负荷来解释。对于色氨酸衍生的特化代谢物 ( cyp79b2/b3 )产生受损的突变体，在营养和生殖阶段，根中广泛的真菌过度生长和改变的植物生长都很明显。单界和多界微生物 SynCom 的微生物群操作实验进一步证明：1) 多界 SynCom 中真菌的存在是cyp79b2/b3中菌群失调表型的直接原因突变体和2）细菌共生体和宿主色氨酸代谢都是控制真菌负荷所必需的，从而促进拟南芥的生长和存活。我们的研究结果表明，细菌根共生体的保护活性与宿主色氨酸代谢途径在预防拟南芥根内环境中的真菌生态失调方面同样重要。