Evolutionary innovations through gain and loss of genes in the ectomycorrhizal Boletales

Abstract

We aimed to identify genomic traits of transitions to ectomycorrhizal ecology within the Boletales by comparing the genomes of 21 symbiotrophic species with their saprotrophic brown-rot relatives.Gene duplication rate is constant along the backbone of Boletales phylogeny with large loss events in several lineages, while gene family expansion sharply increased in the late Miocene, mostly in the Boletaceae.Ectomycorrhizal Boletales have a reduced set of plant cell-wall-degrading enzymes (PCWDEs) compared with their brown-rot relatives. However, the various lineages retain distinct sets of PCWDEs, suggesting that, over their evolutionary history, symbiotic Boletales have become functionally diverse. A smaller PCWDE repertoire was found in Sclerodermatineae. The gene repertoire of several lignocellulose oxidoreductases (e.g. laccases) is similar in brown-rot and ectomycorrhizal species, suggesting that symbiotic Boletales are capable of mild lignocellulose decomposition. Transposable element (TE) proliferation contributed to the higher evolutionary rate of genes encoding effector-like small secreted proteins, proteases, and lipases. On the other hand, we showed that the loss of secreted CAZymes was not related to TE activity but to DNA decay.This study provides novel insights on our understanding of the mechanisms influencing the evolutionary diversification of symbiotic boletes.

Leveraging genomics to understand the broader role of fungal small secreted proteins in niche colonization and nutrition

“…This protein, part of a larger family found in both mutualistic and saprotrophic fungi, is potentially one of the first functionally characterized examples of a protein family that maintains an ancestral role in hyphal dynamics and fruiting body formation that has also gained a novel function in symbiosis through neofunctionalization. As more genomes become available, similar situations appear common throughout entire fungal families [ 7 , 8 ], divisions [ 41 ], and orders [ 5 ], whereby proteins initially characterized in pathogenic or mutualistic fungi as essential for host interactions also have homologs in saprotrophic fungi where they are hypothesized to have a more basal role pertaining to fungal physiology.…”

“…Typically, the genomes of biotrophic pathogens or mutualistic fungi, which require a living host niche throughout their lifecycle, have the lowest number of plant cell wall active enzymes. This is especially a hallmark in the evolution of ectomycorrhizal fungi where a strong reduction in the complement of CAZymes has been found in all genomes studied to date [ 5 , 7 , 8 ].…”

Boletaceae in China: Taxonomy and phylogeny reveal a new genus, two new species, and a new record

“…The ability that ectomycorrhizal fungi symbiosis with the host can enhance the utilization efficiency of soil nutrition in plants and their ability to resist pests, which consequently improves the survival rates of plants in the ecosystem ( Marx, 1972 ; Trappe, 1977 ). Meanwhile, competing with saprotrophic fungi in carbon recycling and other nutrients can dramatically influence the balance of forest ecosystems ( Tedersoo et al, 2010 ; Wu et al, 2022 ). As a species-rich family in the order Boletales E.-J.…”

“…This result was widely recognized by other researchers. Lately, Wu et al unveiled evolutionary innovations from the genomic respects in the ectomycorrhizal Boletales ( Wu et al, 2022 ). The conclusion similar to Kohler et al (2015) and Miyauchi et al (2020) showed that Boletales impressively reduced their plant cell wall-degrading enzymes (PCWDEs).…”

Exploring the Relationships between Four New Species of Boletoid Fungi from Northern China and Their Related Species

“…With the development of molecular biology, the method of genealogical concordance phylogenetic species recognition (GCPSR) [ 20 ] was used to identify species of fungi, resolved some doubts about the status of taxa, and contributed to a better understanding of the relationships of the genera in this family [ 5 , 21 , 22 ]. In the past two decades, new genera and new species have rapidly increased, and the evolution of ectomycorrhizas of Boletales was gradually disclosed [ 23 , 24 ].…”