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Phylogenic analysis of adhesion related genes Mad1 revealed a positive selection for the evolution of trapping devices of nematode-trapping fungi.

ABSTRACT: Adhesions, the major components of the extracellular fibrillar polymers which accumulate on the outer surface of adhesive traps of nematode-trapping fungi, are thought to have played important roles during the evolution of trapping devices. Phylogenetic analyses based on the genes related to adhesive materials can be of great importance for understanding the evolution of trapping devices. Recently, AoMad1, one homologous gene of the entomopathogenic fungus Metarhizium anisopliae cell wall protein MAD1, has been functionally characterized as involved in the production of adhesions in the nematode-trapping fungus Arthrobotrys oligospora. In this study, we cloned Mad1 homologous genes from nematode-trapping fungi with various trapping devices. Phylogenetic analyses suggested that species which formed nonadhesive constricting ring (CR) traps more basally placed and species with adhesive traps evolved along two lineages. Likelihood ratio tests (LRT) revealed that significant positive selective pressure likely acted on the ancestral trapping devices including both adhesive and mechanical traps, indicating that the Mad1 genes likely played important roles during the evolution of nematode-trapping fungi. Our study provides new insights into the evolution of trapping devices of nematode-trapping fungi and also contributes to understanding the importance of adhesions during the evolution of nematode-trapping fungi.

SUBMITTER: Li J

PROVIDER: S-EPMC4778117 | biostudies-literature | 2016 Mar

REPOSITORIES: biostudies-literature

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Phylogenic analysis of adhesion related genes Mad1 revealed a positive selection for the evolution of trapping devices of nematode-trapping fungi.

Li Juan J Liu Yue Y Zhu Hongyan H Zhang Ke-Qin KQ

Scientific reports 20160304

Adhesions, the major components of the extracellular fibrillar polymers which accumulate on the outer surface of adhesive traps of nematode-trapping fungi, are thought to have played important roles during the evolution of trapping devices. Phylogenetic analyses based on the genes related to adhesive materials can be of great importance for understanding the evolution of trapping devices. Recently, AoMad1, one homologous gene of the entomopathogenic fungus Metarhizium anisopliae cell wall protei ...[more]

PMID: 26941065

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Project description:BackgroundNematode-trapping fungi are soil-living fungi that capture and kill nematodes using special hyphal structures called traps. They display a large diversity of trapping mechanisms and differ in their host preferences. To provide insights into the genetic basis for this variation, we compared the transcriptome expressed by three species of nematode-trapping fungi (Arthrobotrys oligospora, Monacrosporium cionopagum and Arthrobotrys dactyloides, which use adhesive nets, adhesive branches or constricting rings, respectively, to trap nematodes) during infection of two different plant-pathogenic nematode hosts (the root knot nematode Meloidogyne hapla and the sugar beet cyst nematode Heterodera schachtii).ResultsThe divergence in gene expression between the fungi was significantly larger than that related to the nematode species being infected. Transcripts predicted to encode secreted proteins and proteins with unknown function (orphans) were overrepresented among the highly expressed transcripts in all fungi. Genes that were highly expressed in all fungi encoded endopeptidases, such as subtilisins and aspartic proteases; cell-surface proteins containing the carbohydrate-binding domain WSC; stress response proteins; membrane transporters; transcription factors; and transcripts containing the Ricin-B lectin domain. Differentially expressed transcripts among the fungal species encoded various lectins, such as the fungal fruit-body lectin and the D-mannose binding lectin; transcription factors; cell-signaling components; proteins containing a WSC domain; and proteins containing a DUF3129 domain. A small set of transcripts were differentially expressed in infections of different host nematodes, including peptidases, WSC domain proteins, tyrosinases, and small secreted proteins with unknown function.ConclusionsThis is the first study on the variation of infection-related gene expression patterns in nematode-trapping fungi infecting different host species. A better understanding of these patterns will facilitate the improvements of these fungi in biological control programs, by providing molecular markers for screening programs and candidates for genetic manipulations of virulence and host preferences.

Project description:Orbiliomycetes is one of the earliest diverging branches of the filamentous ascomycetes. The class contains nematode-trapping fungi that form unique infection structures, called traps, to capture and kill free-living nematodes. The traps have evolved differently along several lineages and include adhesive traps (knobs, nets or branches) and constricting rings. We show, by genome sequencing of the knob-forming species Monacrosporium haptotylum and comparison with the net-forming species Arthrobotrys oligospora, that two genomic mechanisms are likely to have been important for the adaptation to parasitism in these fungi. Firstly, the expansion of protein domain families and the large number of species-specific genes indicated that gene duplication followed by functional diversification had a major role in the evolution of the nematode-trapping fungi. Gene expression indicated that many of these genes are important for pathogenicity. Secondly, gene expression of orthologs between the two fungi during infection indicated that differential regulation was an important mechanism for the evolution of parasitism in nematode-trapping fungi. Many of the highly expressed and highly upregulated M. haptotylum transcripts during the early stages of nematode infection were species-specific and encoded small secreted proteins (SSPs) that were affected by repeat-induced point mutations (RIP). An active RIP mechanism was revealed by lack of repeats, dinucleotide bias in repeats and genes, low proportion of recent gene duplicates, and reduction of recent gene family expansions. The high expression and rapid divergence of SSPs indicate a striking similarity in the infection mechanisms of nematode-trapping fungi and plant and insect pathogens from the crown groups of the filamentous ascomycetes (Pezizomycotina). The patterns of gene family expansions in the nematode-trapping fungi were more similar to plant pathogens than to insect and animal pathogens. The observation of RIP activity in the Orbiliomycetes suggested that this mechanism was present early in the evolution of the filamentous ascomycetes.

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Phylogenic analysis of adhesion related genes Mad1 revealed a positive selection for the evolution of trapping devices of nematode-trapping fungi.

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Phylogenic analysis of adhesion related genes Mad1 revealed a positive selection for the evolution of trapping devices of nematode-trapping fungi.

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