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Comparative Genomic Analysis of Plant Pathogenic Colletotrichum Fungi

津島, 綾子 東京大学 DOI:10.15083/0002004266

2022.06.22

概要

Plant pathogens secrete proteins called effectors to manipulate host cells and to promote infection. Recent studies have shown examples of effectors conserved across taxa, which are required for full pathogenicity. However, in some cases, effectors are perceived by host immune receptors resulting in strong immune responses against the invading pathogens. To avoid this recognition, effectors are generally under diversifying selection and differ even between strains within the same species. Colletotrichum fungi collectively cause anthracnose disease in a broad range of plants, although individual species have specialized in infecting limited host plants. The aim of my Ph.D. research was to understand how Colletotrichum fungi adapt to various niches by characterizing their effector gene sets.

Among Colletotrichum fungi, C. higginsianum has been widely used for scientific studies as it infects the model plant Arabidopsis thaliana. However, the first published genome assembly of this pathogen is fragmented and possibly contains missing or incorrect gene annotations. In order to overcome this problem, I generated a more contiguous assembly of the genome of C. higginsianum MAFF305635-RFP by sequencing it using PacBio RS II. This genome assembly comprises of 28 contigs and is estimated to include 99.0% of all coding genes. I analyzed the conservation patterns of effector candidates amongst 24 ascomycetes including C. higginsianum MAFF305635-RFP. This analysis revealed that seven effector candidate orthogroups are specifically conserved in all seven Colletotrichum species tested, but not in other ascomycetes (Figure 1). This analysis also identified species-specific effector candidates of Colletotrichum fungi that may contribute to host specificity.

As few sexual morphs have been described in the genus Colletotrichum, most members including C. higginsianum appear to proliferate clonally. To determine whether Colletotrichum species exhibit within-species genomic variations in the absence of a sexual cycle, I compared the two closelyrelated C. higginsianum strains MAFF305635-RFP and IMI 349063, which were sequenced by Zampounis et al. (2016). First, I performed whole-genome alignments between the two C. higginsianum strains. This analysis revealed the presence of 10 large-scale rearrangements between the two strains, including six inter-chromosomal translocations and four intra-chromosomal inversions (Figure 2). Whole-genome alignments also indicated that the two strains have strain-specific regions (< 99% identity, < 15 kb) that are variable in the other strain. In order to identify strain-specific variations in effectors of C. higginsianum, effector candidates from the two strains were compared. This analysis revealed that 8 out 582 candidates in MAFF305635-RFP and 18 out 576 candidates in IMI 349063 were highly variable between the two strains with ≤ 90% query coverage. Such effector candidates showed variable conservation patterns in Ascomycota possibly reflecting differences in their evolutionary history (e.g. de novo evolution, loss after speciation, and horizontal gene transfer) (Figure 3). Transposable elements (TEs) are known to often be involved in the generation of genomic variations. To examine whether TEs contribute to the generation of genomic variations in C. higginsianum, the association between TEs and strain-specific regions was investigated. In the genome of MAFF305635-RFP, 29.5% of strain-specific regions were found to overlap with TEs and this is significantly higher than the case if TEs were randomly distributed on the genome (Monte Carlo method, P < 0.001). Further, my results indicate that the genome of C. higginsianum is compartmentalized into regions harboring conserved genes which are gene-dense and TE-sparse, as well as regions with more effector candidate genes which are gene-sparse and TE-dense.

To further characterize the effector candidates identified, I conducted functional analysis of CCE1 (Colletotrichum Core Effector 1). Genus-wide comparative genomic analyses revealed that this effector candidate gene is highly conserved in the genus Colletotrichum. In addition, transient expression assays indicate that CCE1 homologs from three Colletotrichum species infecting different hosts induce cell death in Nicotiana benthamiana leaves. Furthermore, by performing in planta coimmunoprecipitation, I identified candidate interactors of CCE1 including cytoskeleton-related proteins such as actin and tubulin, the Golgi-targeted protein α1-COP, and the ER-targeted protein BIP2. These data suggest that CCE1 proteins may function in promoting host cell death during infection by targeting a host component found in various host plants.

In conclusion, in this thesis, I show the diversity of effector candidates and a potential mechanism for generating genomic variations in Colletotrichum fungi. Given that effectors play important roles in plant-microbe interaction, variations in effector complements may contribute to the fitness of this group of fungi.

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