Ceratocystis cacaofunesta genome analysis reveals a large expansion of extracellular phosphatidylinositol-specific phospholipase-C genes (PI-PLC)

Abstract

BackgroundThe Ceratocystis genus harbors a large number of phytopathogenic fungi that cause xylem parenchyma degradation and vascular destruction on a broad range of economically important plants. Ceratocystis cacaofunesta is a necrotrophic fungus responsible for lethal wilt disease in cacao. The aim of this work is to analyze the genome of C. cacaofunesta through a comparative approach with genomes of other Sordariomycetes in order to better understand the molecular basis of pathogenicity in the Ceratocystis genus.ResultsWe present an analysis of the C. cacaofunesta genome focusing on secreted proteins that might constitute pathogenicity factors. Comparative genome analyses among five Ceratocystidaceae species and 23 other Sordariomycetes fungi showed a strong reduction in gene content of the Ceratocystis genus. However, some gene families displayed a remarkable expansion, in particular, the Phosphatidylinositol specific phospholipases-C (PI-PLC) family. Also, evolutionary rate calculations suggest that the evolution process of this family was guided by positive selection. Interestingly, among the 82 PI-PLCs genes identified in the C. cacaofunesta genome, 70 genes encoding extracellular PI-PLCs are grouped in eight small scaffolds surrounded by transposon fragments and scars that could be involved in the rapid evolution of the PI-PLC family. Experimental secretome using LC–MS/MS validated 24% (86 proteins) of the total predicted secretome (342 proteins), including four PI-PLCs and other important pathogenicity factors.ConclusionAnalysis of the Ceratocystis cacaofunesta genome provides evidence that PI-PLCs may play a role in pathogenicity. Subsequent functional studies will be aimed at evaluating this hypothesis. The observed genetic arsenals, together with the analysis of the PI-PLC family shown in this work, reveal significant differences in the Ceratocystis genome compared to the classical vascular fungi, Verticillium and Fusarium. Altogether, our analyses provide new insights into the evolution and the molecular basis of plant pathogenicity.Electronic supplementary materialThe online version of this article (10.1186/s12864-018-4440-4) contains supplementary material, which is available to authorized users.

Inheritance of phenotypic traits in the progeny of a Ceratocystis interspecific cross

“…Similar results were found for the related pathogen M. grisea that infects rice (Murakami et al 2003;Murakami et al 2000) and for the brown mustard plant pathogen Leptosphaeria maculans (Chen et al 1996). Since a low number of genes are likely involved in host specificity in Ceratocystis species, pathogen host interaction genes, such as avirulence or effector genes might play a role (Deng et al 2017;Molano et al 2018;Shirke et al 2016) but would need further investigation.…”

“…Knowledge of the factors associated with host specificity and aggressiveness in Ceratocystis species has been limited to studies focusing on host response during infection (Al-Sadi et al 2010; Kojima and Uritani 1976;Trang et al 2017) and studies on enzymes produced by Ceratocystis for the breakdown of host phenolics (Wadke et al 2016). A recent Ceratocystis genome comparison identified potential pathogenicity genes in C. cacaofunesta and C. fimbriata, including putative effectors and a highly expanded phosphatidylinositol-specific phospholipase-C gene family (Molano et al 2018). This provides various candidates for future functional studies.…”

Draft genome sequence of Annulohypoxylon stygium, Aspergillus mulundensis, Berkeleyomyces basicola (syn. Thielaviopsis basicola), Ceratocystis smalleyi, two Cercospora beticola strains, Coleophoma cylindrospora, Fusarium fracticaudum, Phialophora cf. hyalina, and Morchella septimelata

“…In this study, we aimed to produce a draft genome assembly for C. smalleyi . This assembly would be the seventh Ceratocystis species for which a genome sequence is published, and adds to the valuable genomic resource available for members of Ceratocystidaceae ( Molano et al 2018 , Van der Nest et al 2014a , b , 2015 , Vanderpool et al 2017 , Wilken et al 2013 , 2018 , Wingfield et al 2015a , b , 2016a , b ). Furthermore, the availability of a genome assembly will afford the opportunity in future to investigate aspects of the unique biology of C. smalleyi .…”

IMA Genome-F 11

“…For example, the head blight pathogen Fusarium graminearum (genome size: 36.5 Mb) has approximately 14 164 genes (King et al 2015), the pine needle blight pathogen Dothistroma septosporum (genome size: 31. Wingfield et al 2016a;Wingfield et al 2017;Molano et al 2018;Vanderpool et al 2018;Wingfield et al 2018a). The annotation of the C. fimbriata genome sequence presented in this study is the first manually curated genome including additional RNA evidence, for any species in the Ceratocystidaceae.…”