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Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens.

Morales-Cruz A, Amrine KC, Blanco-Ulate B, Lawrence DP, Travadon R, Rolshausen PE, Baumgartner K, Cantu D - BMC Genomics (2015)

Bottom Line: Phylogenetically-informed principal component analysis revealed more similar repertoires of expanded functions among species that cause similar symptoms, which in some cases did not reflect phylogenetic relationships, thereby suggesting patterns of convergent evolution.Gene families with significantly faster rates of gene gain can now provide a basis for further studies of in planta gene expression, diversity by genome re-sequencing, and targeted reverse genetic approaches.The functional validation of potential virulence factors will lead to a more comprehensive understanding of the mechanisms of pathogenesis and virulence, which ultimately will enable the development of accurate diagnostic tools and effective disease management.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California Davis, Davis, CA, 95616, USA. abmora@ucdavis.edu.

ABSTRACT

Background: Trunk diseases threaten the longevity and productivity of grapevines in all viticulture production systems. They are caused by distantly-related fungi that form chronic wood infections. Variation in wood-decay abilities and production of phytotoxic compounds are thought to contribute to their unique disease symptoms. We recently released the draft sequences of Eutypa lata, Neofusicoccum parvum and Togninia minima, causal agents of Eutypa dieback, Botryosphaeria dieback and Esca, respectively. In this work, we first expanded genomic resources to three important trunk pathogens, Diaporthe ampelina, Diplodia seriata, and Phaeomoniella chlamydospora, causal agents of Phomopsis dieback, Botryosphaeria dieback, and Esca, respectively. Then we integrated all currently-available information into a genome-wide comparative study to identify gene families potentially associated with host colonization and disease development.

Results: The integration of RNA-seq, comparative and ab initio approaches improved the protein-coding gene prediction in T. minima, whereas shotgun sequencing yielded nearly complete genome drafts of Dia. ampelina, Dip. seriata, and P. chlamydospora. The predicted proteomes of all sequenced trunk pathogens were annotated with a focus on functions likely associated with pathogenesis and virulence, namely (i) wood degradation, (ii) nutrient uptake, and (iii) toxin production. Specific patterns of gene family expansion were described using Computational Analysis of gene Family Evolution, which revealed lineage-specific evolution of distinct mechanisms of virulence, such as specific cell wall oxidative functions and secondary metabolic pathways in N. parvum, Dia. ampelina, and E. lata. Phylogenetically-informed principal component analysis revealed more similar repertoires of expanded functions among species that cause similar symptoms, which in some cases did not reflect phylogenetic relationships, thereby suggesting patterns of convergent evolution.

Conclusions: This study describes the repertoires of putative virulence functions in the genomes of ubiquitous grapevine trunk pathogens. Gene families with significantly faster rates of gene gain can now provide a basis for further studies of in planta gene expression, diversity by genome re-sequencing, and targeted reverse genetic approaches. The functional validation of potential virulence factors will lead to a more comprehensive understanding of the mechanisms of pathogenesis and virulence, which ultimately will enable the development of accurate diagnostic tools and effective disease management.

No MeSH data available.


Related in: MedlinePlus

Secondary metabolism related proteins in the 90 significantly expanded gene families of ascomycete trunk pathogens. (a) Bar graph of genes divided by secondary metabolism cluster types according to Antismash classification. t1PKS: type 1 Polyketide Synthase, TS: Terpene Synthase, NRPS: Non-Ribosomal Peptide Synthetases, t3PKS: type 3 Polyketide Synthase, uPKS: unusual Polyketide Synthase PKS, LS: Lantipeptide Synthase (LS). (b and c) Ascomycete trunk pathogens are projected on the first two principal components based on phylogenetic PCA of genes encoding (b) proteins involved in secondary metabolism and (c) P450s in the significantly expanded gene families. Only vectors of the largest loadings are shown
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Fig8: Secondary metabolism related proteins in the 90 significantly expanded gene families of ascomycete trunk pathogens. (a) Bar graph of genes divided by secondary metabolism cluster types according to Antismash classification. t1PKS: type 1 Polyketide Synthase, TS: Terpene Synthase, NRPS: Non-Ribosomal Peptide Synthetases, t3PKS: type 3 Polyketide Synthase, uPKS: unusual Polyketide Synthase PKS, LS: Lantipeptide Synthase (LS). (b and c) Ascomycete trunk pathogens are projected on the first two principal components based on phylogenetic PCA of genes encoding (b) proteins involved in secondary metabolism and (c) P450s in the significantly expanded gene families. Only vectors of the largest loadings are shown

Mentions: To visualize the diversity of significantly-expanded families of virulence functions in the ascomycete trunk pathogens and to identify similarities between species, a phylogenetically informed-principal components analysis (PCA) was applied. Members from the 90 expanded gene families in the ascomycete trunk pathogens were grouped into functional categories obtained from the specialized databases mentioned above (Table 3) and PCA was carried out using the Phyl.PCA function, part of the phytools R package [73]. Phyl.PCA takes into account correlations among species due to phylogenetic relatedness, while correcting the correlation matrices for non-independence among observations. Four separate analyses were conducted using the clock-calibrated tree described above and the matrices of the number of genes classified as Pfam (Fig. 6), CAZy (Fig. 7), secondary metabolism (Fig. 8), and P450s (Fig. 8).Fig. 6


Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens.

Morales-Cruz A, Amrine KC, Blanco-Ulate B, Lawrence DP, Travadon R, Rolshausen PE, Baumgartner K, Cantu D - BMC Genomics (2015)

Secondary metabolism related proteins in the 90 significantly expanded gene families of ascomycete trunk pathogens. (a) Bar graph of genes divided by secondary metabolism cluster types according to Antismash classification. t1PKS: type 1 Polyketide Synthase, TS: Terpene Synthase, NRPS: Non-Ribosomal Peptide Synthetases, t3PKS: type 3 Polyketide Synthase, uPKS: unusual Polyketide Synthase PKS, LS: Lantipeptide Synthase (LS). (b and c) Ascomycete trunk pathogens are projected on the first two principal components based on phylogenetic PCA of genes encoding (b) proteins involved in secondary metabolism and (c) P450s in the significantly expanded gene families. Only vectors of the largest loadings are shown
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4472170&req=5

Fig8: Secondary metabolism related proteins in the 90 significantly expanded gene families of ascomycete trunk pathogens. (a) Bar graph of genes divided by secondary metabolism cluster types according to Antismash classification. t1PKS: type 1 Polyketide Synthase, TS: Terpene Synthase, NRPS: Non-Ribosomal Peptide Synthetases, t3PKS: type 3 Polyketide Synthase, uPKS: unusual Polyketide Synthase PKS, LS: Lantipeptide Synthase (LS). (b and c) Ascomycete trunk pathogens are projected on the first two principal components based on phylogenetic PCA of genes encoding (b) proteins involved in secondary metabolism and (c) P450s in the significantly expanded gene families. Only vectors of the largest loadings are shown
Mentions: To visualize the diversity of significantly-expanded families of virulence functions in the ascomycete trunk pathogens and to identify similarities between species, a phylogenetically informed-principal components analysis (PCA) was applied. Members from the 90 expanded gene families in the ascomycete trunk pathogens were grouped into functional categories obtained from the specialized databases mentioned above (Table 3) and PCA was carried out using the Phyl.PCA function, part of the phytools R package [73]. Phyl.PCA takes into account correlations among species due to phylogenetic relatedness, while correcting the correlation matrices for non-independence among observations. Four separate analyses were conducted using the clock-calibrated tree described above and the matrices of the number of genes classified as Pfam (Fig. 6), CAZy (Fig. 7), secondary metabolism (Fig. 8), and P450s (Fig. 8).Fig. 6

Bottom Line: Phylogenetically-informed principal component analysis revealed more similar repertoires of expanded functions among species that cause similar symptoms, which in some cases did not reflect phylogenetic relationships, thereby suggesting patterns of convergent evolution.Gene families with significantly faster rates of gene gain can now provide a basis for further studies of in planta gene expression, diversity by genome re-sequencing, and targeted reverse genetic approaches.The functional validation of potential virulence factors will lead to a more comprehensive understanding of the mechanisms of pathogenesis and virulence, which ultimately will enable the development of accurate diagnostic tools and effective disease management.

View Article: PubMed Central - PubMed

Affiliation: Department of Viticulture and Enology, University of California Davis, Davis, CA, 95616, USA. abmora@ucdavis.edu.

ABSTRACT

Background: Trunk diseases threaten the longevity and productivity of grapevines in all viticulture production systems. They are caused by distantly-related fungi that form chronic wood infections. Variation in wood-decay abilities and production of phytotoxic compounds are thought to contribute to their unique disease symptoms. We recently released the draft sequences of Eutypa lata, Neofusicoccum parvum and Togninia minima, causal agents of Eutypa dieback, Botryosphaeria dieback and Esca, respectively. In this work, we first expanded genomic resources to three important trunk pathogens, Diaporthe ampelina, Diplodia seriata, and Phaeomoniella chlamydospora, causal agents of Phomopsis dieback, Botryosphaeria dieback, and Esca, respectively. Then we integrated all currently-available information into a genome-wide comparative study to identify gene families potentially associated with host colonization and disease development.

Results: The integration of RNA-seq, comparative and ab initio approaches improved the protein-coding gene prediction in T. minima, whereas shotgun sequencing yielded nearly complete genome drafts of Dia. ampelina, Dip. seriata, and P. chlamydospora. The predicted proteomes of all sequenced trunk pathogens were annotated with a focus on functions likely associated with pathogenesis and virulence, namely (i) wood degradation, (ii) nutrient uptake, and (iii) toxin production. Specific patterns of gene family expansion were described using Computational Analysis of gene Family Evolution, which revealed lineage-specific evolution of distinct mechanisms of virulence, such as specific cell wall oxidative functions and secondary metabolic pathways in N. parvum, Dia. ampelina, and E. lata. Phylogenetically-informed principal component analysis revealed more similar repertoires of expanded functions among species that cause similar symptoms, which in some cases did not reflect phylogenetic relationships, thereby suggesting patterns of convergent evolution.

Conclusions: This study describes the repertoires of putative virulence functions in the genomes of ubiquitous grapevine trunk pathogens. Gene families with significantly faster rates of gene gain can now provide a basis for further studies of in planta gene expression, diversity by genome re-sequencing, and targeted reverse genetic approaches. The functional validation of potential virulence factors will lead to a more comprehensive understanding of the mechanisms of pathogenesis and virulence, which ultimately will enable the development of accurate diagnostic tools and effective disease management.

No MeSH data available.


Related in: MedlinePlus