期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2021
卷号：118
期号：49
DOI：10.1073/pnas.2111521118
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Understanding how host–microbe homeostasis is controlled and maintained in plant roots is key to enhance plant productivity. However, the factors that contribute to the maintenance of this equilibrium between plant roots and their multikingdom microbial communities remain largely unknown. Here, we observed a link between fungal load in roots and plant health, and we showed that modulation of fungal abundance is tightly controlled by a two-layer regulatory circuit involving the host innate immune system on one hand and bacterial root commensals on another hand. Our results shed a light into how host–microbe and microbe–microbe interactions act in concert to prevent dysbiosis in
Arabidopsis thaliana roots, thereby promoting plant health and maintaining growth-promoting activities of multikingdom microbial commensals.
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.
