Genetic determinants of endophytism in the Arabidopsis root mycobiome

Abstract

The roots of Arabidopsis thaliana host diverse fungal communities that affect plant health and disease states. Here, we sequence the genomes of 41 fungal isolates representative of the A. thaliana root mycobiota for comparative analysis with other 79 plant-associated fungi. Our analyses indicate that root mycobiota members evolved from ancestors with diverse lifestyles and retain large repertoires of plant cell wall-degrading enzymes (PCWDEs) and effector-like small secreted proteins. We identify a set of 84 gene families associated with endophytism, including genes encoding PCWDEs acting on xylan (family GH10) and cellulose (family AA9). Transcripts encoding these enzymes are also part of a conserved transcriptional program activated by phylogenetically-distant mycobiota members upon host contact. Recolonization experiments with individual fungi indicate that strains with detrimental effects in mono-association with the host colonize roots more aggressively than those with beneficial activities, and dominate in natural root samples. Furthermore, we show that the pectin-degrading enzyme family PL1_7 links aggressiveness of endophytic colonization to plant health.

Lifestyle Transitions in Fusarioid Fungi are Frequent and Lack Clear Genomic Signatures

“…There is no single role that endophytes play in the plant host, as the endophytic lifestyle represents a functional range between pathogenicity and mutualism, which has been dubbed the “endophytic continuum” ( Schulz and Boyle 2005 ). The outcome of endophyte colonisation can be highly dependent on the context of the plant–fungal interaction, such as the status of the plant immune system and nutrient conditions ( Junker et al 2012 ; Lahrmann et al 2015 ; Hacquard et al 2016 ; Hiruma et al 2016 ), as well as the presence of other endophytes within the microbiome ( Redman et al 2001 ; Durán et al 2018 ; Mesny et al 2021 ; Wolinska et al 2021 ) and even light conditions ( Álvarez-Loayza et al 2011 ). The transient status of endophytism for many taxa is evident from observations of endophytes becoming decayers (saprotrophs) or pathogens following some change in host or abiotic conditions ( Slippers and Wingfield 2007 ; Arnold et al 2009 ; Promputtha et al 2010 ; Swett and Gordon 2015 ; Nelson et al 2020 ).…”

“…Another frequently studied group of proteins involved in the plant–fungal interaction are carbohydrate-active enzymes (CAZymes), many of which act as plant cell wall–degrading enzymes (PCWDEs) ( Kubicek et al 2014 ). CAZymes are often referred to as saprotrophic features ( Lebreton et al 2021 ), but are also abundant in plant pathogens and endophytes (e.g., Zhao et al 2013 ; Knapp et al 2018 ; Mesny et al 2021 ), and, although present in lower numbers in mycorrhizal fungi ( Kohler et al 2015 ; Peter et al 2016 ; Miyauchi et al 2020 ), certain CAZymes play key roles in the establishment and maintenance of the symbiosis ( Veneault-Fourrey et al 2014 ; Doré et al 2017 ; Marqués-Gálvez et al 2021 ). Comparing CSEP and CAZyme repertoires is therefore highly relevant to exploring genetic differences in plant associated lifestyles of fusarioid fungi.…”

Tryptophan metabolism and bacterial commensals prevent fungal dysbiosis in Arabidopsis roots

“…Therefore, an intact immune system is needed for the plant growth–promoting outcome of multikingdom microbial root commensals. A link between fungal load in roots and plant performance has been previously suggested in monoassociation experiments with fungal root endophytes ( 23 , 62 ). Inspection of a diverse set of A. thaliana root mycobiota members revealed that fungal colonization aggressiveness and detrimental effect on plant performance are correlated and suggested that the most beneficial fungi are less abundant than detrimental fungi in roots of natural A. thaliana populations ( 62 ).…”

“…A link between fungal load in roots and plant performance has been previously suggested in monoassociation experiments with fungal root endophytes ( 23 , 62 ). Inspection of a diverse set of A. thaliana root mycobiota members revealed that fungal colonization aggressiveness and detrimental effect on plant performance are correlated and suggested that the most beneficial fungi are less abundant than detrimental fungi in roots of natural A. thaliana populations ( 62 ). Furthermore, A. thaliana mutants impaired in Trp-derived, specialized metabolites were shown to be unable to control growth and accommodation of beneficial fungal root endophytes, which likely contributed to the altered plant growth phenotypes ( 23 , 24 , 66 ).…”

“…We speculate that the differential control of microbial load and assembly by the host immune system is relevant for the accommodation of multikingdom microbial consortia. This result might reflect the fact that phylogenetically diverse, A. thaliana root–colonizing fungi display higher pathogenic potential than that of root-derived bacteria in monoassociation with the host ( 27 , 39 , 61 – 63 ) and show more extensive, site-specific associations with A. thaliana roots than bacteria in nature ( 3 ). Furthermore, the reciprocal and complex interplay between bacterial root commensals and PTI reported recently corroborated that PTI outputs selectively modulate bacterial assembly, which in turn instructs the host immune system ( 13 , 14 , 64 , 65 ).…”