Comparative genomics provides insights into the lifestyle and reveals functional heterogeneity of dark septate endophytic fungi

Dániel G Knapp,Gábor M Kovács,Matt Nolan,Joseph W Spatafora,Anna Lipzen,Kerrie Barry,Robin A Ohm,László Tamás,Joanne Hui Ping Lim,László G Nagy,Julianna B Németh,Matthieu Hainaut,Alan Kuo,Igor V Grigoriev,Bernard Henrissat,Jenifer Johnson

doi:10.1038/s41598-018-24686-4

Abstract

Dark septate endophytes (DSE) are a form-group of root endophytic fungi with elusive functions. Here, the genomes of two common DSE of semiarid areas, Cadophora sp. and Periconia macrospinosa were sequenced and analyzed with another 32 ascomycetes of different lifestyles. Cadophora sp. (Helotiales) and P. macrospinosa (Pleosporales) have genomes of 70.46 Mb and 54.99 Mb with 22,766 and 18,750 gene models, respectively. The majority of DSE-specific protein clusters lack functional annotation with no similarity to characterized proteins, implying that they have evolved unique genetic innovations. Both DSE possess an expanded number of carbohydrate active enzymes (CAZymes), including plant cell wall degrading enzymes (PCWDEs). Those were similar in three other DSE, and contributed a signal for the separation of root endophytes in principal component analyses of CAZymes, indicating shared genomic traits of DSE fungi. Number of secreted proteases and lipases, aquaporins, and genes linked to melanin synthesis were also relatively high in our fungi. In spite of certain similarities between our two DSE, we observed low levels of convergence in their gene family evolution. This suggests that, despite originating from the same habitat, these two fungi evolved along different evolutionary trajectories and display considerable functional differences within the endophytic lifestyle.

Highlights

The presence of root endophytes with melanized and septated intraradical hyphae has been known for over a century[11]
Various degradative enzyme activities have been detected in DSEs22,23, which could indicate that they have a rich plant cell wall degrading enzyme (PCWDE) repertoire
These fungi – Cadophora sp. and Periconia macrospinosa – albeit from the same environment, represent taxonomically distant species with different host preferences[16,18]. As these species are common and widespread members of dark septate endophytes (DSE) communities of semiarid sandy grasslands[16,19,42], they likely play key roles in the functioning of such ecosystems. We analyze their repertoires of carbohydrate active enzymes (CAZymes), PCWDEs and other relevant gene families and compare these to that of other ascomycetes to understand whether independently evolved DSE lineages possess common genomic signatures and to gain insights into their lifestyle

Summary

Introduction

The presence of root endophytes with melanized and septated intraradical hyphae has been known for over a century[11]. Periconia macrospinosa – albeit from the same environment, represent taxonomically distant species with different host preferences[16,18] As these species are common and widespread members of DSE communities of semiarid sandy grasslands[16,19,42], they likely play key roles in the functioning of such ecosystems. We analyze their repertoires of CAZymes, PCWDEs and other relevant gene families and compare these to that of other ascomycetes to understand whether independently evolved DSE lineages possess common genomic signatures and to gain insights into their lifestyle. To the best of our knowledge, this is the first comparative genome analysis of two different fungal root endophytes that belong to the same habitat

Methods

Results

Conclusion