Genomic Analysis of Diverse Members of the Fungal Genus Monosporascus Reveals Novel Lineages, Unique Genome Content and a Potential Bacterial Associate

Abstract

The genus Monosporascus represents an enigmatic group of fungi important in agriculture and widely distributed in natural arid ecosystems. Of the nine described species, two (M. cannonballus and M. eutypoides) are important pathogens on the roots of members of Cucurbitaceae in agricultural settings. The remaining seven species are capable of colonizing roots from a diverse host range without causing obvious disease symptoms. Recent molecular and culture studies have shown that members of the genus are nearly ubiquitous as root endophytes in arid environments of the Southwestern United States. Isolates have been obtained from apparently healthy roots of grasses, shrubs and herbaceous plants located in central New Mexico and other regions of the Southwest. Phylogenetic and genomic analyses reveal substantial diversity in these isolates. The New Mexico isolates include close relatives of M. cannonballus and M. ibericus, as well as isolates that represent previously unrecognized lineages. To explore evolutionary relationships within the genus and gain insights into potential ecological functions, we sequenced and assembled the genomes of three M. cannonballus isolates, one M. ibericus isolate, and six diverse New Mexico isolates. The assembled genomes were significantly larger than what is typical for the Sordariomycetes despite having predicted gene numbers similar to other members of the class. Differences in predicted genome content and organization were observed between endophytic and pathogenic lineages of Monosporascus. Several Monosporascus isolates appear to form associations with members of the bacterial genus Ralstonia (Burkholdariaceae).

Soil Origin and Plant Genotype Modulate Switchgrass Aboveground Productivity and Root Microbiome Assembly

“…Of these, Striaticonidium brachysporum and Monosporascus eutypoides may yield special interests since they were further selected in the linear regression model showing significant and positive association with switchgrass biomass. Interestingly, many closely related species or species in genera Striaticonidium and Monosporascus are known to be plant pathogens; however, many are plant endophytes, and their functional relationship with plants may differ between species or hosts ( 40 – 42 ). Further investigations with switchgrass isolates will allow for direct tests on beneficial effects and mechanisms of switchgrass biomass accumulation under different soil conditions, such as varied levels of microbial diversity or plant nutrients.…”

Characterization of Five New Monosporascus Species: Adaptation to Environmental Factors, Pathogenicity to Cucurbits and Sensitivity to Fungicides

“…Bruton [ 2 ] indicated that inadequate crop rotation contributes more than other factors to increase the inoculum of cucurbit soilborne pathogens, thus determining the emergence of new diseases or increasing disease incidence and severity of the already existing ones. Moreover, in the specific case of Monosporascus spp., Robinson et al [ 14 ] commented that there is no evidence that isolates of Monosporascus from the roots of plants in natural ecosystems cause disease symptoms, despite their broad host association, thus raising questions regarding whether presumed endophytic lineages differ from pathogenic lineages with respect to specific genes or groups of genes. These authors compared the genomes of endophytic and pathogenic isolates within the genus Monosporascus and also across genera within the Xylariales with respect to genes for carbohydrate-active enzymes, genes known to be involved in pathogenicity in certain fungi, and genes for effector proteins that facilitate the colonization of plant tissues.…”

“…semiaridus A. Negreiros, M. León, J. Armengol and R. Sales Júnior. Monosporascus has been also reported as a common root endophyte in surveys of grasses, shrubs and herbaceous plants located in the southwestern United States using both molecular and culturing methods [ 11 , 12 , 13 , 14 ].…”

The Sordariomycetes: an expanding resource with Big Data for mining in evolutionary genomics and transcriptomics

“…Some of these non-model species are emerging as “new” models and, unlike the classic models that have undergone intensive investigation in biology and genetics, established during the pre-genomics era, these species are often studied under a reverse approach, with investigation originating in genomics and then extending to genetics and the analysis of biological traits. For example, the genomes of a large number of species of Xylariale have recently been sequenced, and comparative genomics has revealed genetic changes that are probably associated with bioactivities, diverse lifestyles, environmental adaptations, and selective pressure in these “mystical”-looking fungi ( Robinson et al., 2020 ; Wibberg et al., 2020 ; Franco et al., 2022 ; Fricke et al., 2023 ). At the same time, the annotation of classic model genomes, such as those of Neurospora , Podospora , and Sordaria genomes, has undergone continuous improvement, in part on the basis of information obtained from newly sequenced genomes of the same or closely related species ( Teichert et al., 2014 ; Gladieux et al., 2015 ; Blank-Landeshammer et al., 2019 ; Teichert et al., 2020 ; Lelandais et al., 2022 ; Rodriguez et al., 2022 ; Vittorelli et al., 2023 ).…”