Desert truffle genomes reveal their reproductive modes and new insights into plant–fungal interaction and ectendomycorrhizal lifestyle

Abstract

 Desert truffles are edible hypogeous fungi forming ectendomycorrhizal symbiosis with plants of Cistaceae family. Knowledge about the reproductive modes of these fungi and the molecular mechanisms driving the ectendomycorrhizal interaction is lacking.  Genomes of the highly appreciated edible desert truffles, Terfezia claveryi Chatin and Tirmania nivea Trappe, have been sequenced and compared to other Pezizomycetes. Transcriptomes of T. claveryi x Heliantemum almeriense mycorrhiza from well-watered and drought-stressed plants, when intracellular colonizations is promoted, were investigated.  We have identified the fungal genes related to sexual reproduction in desert truffles and desert truffles specific genomic and secretomic features with respect to other Pezizomycetes, such as the expansion of a large set of gene families with unknown Pfam domains and a number of species or desert truffle-specific small secreted proteins differentially regulated in symbiosis. A core set of plant genes, including carbohydrate, lipid metabolism and defence related genes, differentially expressed in mycorrhiza under both conditions was found.  Our results highlight the singularities of desert truffles with respect to other mycorrhizal fungi while providing a first glimpse on plant and fungal determinants involved in ecto to endo symbiotic switch that occurs in desert truffle under dry conditions.

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

“…In Agaricales, Russulales, Thelephorales, and Pezizales, the transition from saprotrophy to the symbiotic ecology coincided with the loss of most hydrolytic enzymes acting on lignocellulose (Kohler et al, 2015;Hess et al, 2018;Murat et al, 2018;Miyauchi et al, 2020;Looney et al, 2021;Marqu es-G alvez et al, 2021). Our analyses of the largest set of ectomycorrhizal Boletales genomes to date support the view that transitions from brownrot to symbiosis entailed the widespread losses of PCWDEs acting on lignin, cellulose, hemicellulose, and pectin.…”

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

“…In Agaricales, Russulales, Thelephorales and Pezizales the transition from saprotrophy to the symbiotic ecology coincided with the loss of most hydrolytic enzymes acting on lignocellulose (Kohler et al, 2015;Hess et al, 2018;Murat et al 2018;Miyauchi et al, 2020;Looney et al, 2021;Marqués-Gálvez et al, 2021). Our analyses of the largest set of ectomycorrhizal Boletales genomes to date support the view that transitions from brown-rot to symbiosis entailed the widespread losses of PCWDEs acting on lignin, cellulose, hemicellulose and pectins.…”

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

“…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.…”