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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

Estimation of gene family expansion and contraction using CAFE. (a) Clock calibrated phylogenetic tree showing the number of gene families significantly (P-value ≤ 0.01) expanded (red), contracted (blue) and their average pattern (black). (b) Venn diagram showing the number of proteins significantly expanded in each group of fungal species. (c) Bar plot showing the counts of genes annotated in each group of significantly expanded functional category. Only categories significantly overrepresented (P-value ≤ 0.01) in the 90 gene families expanded in the ascomycete trunk pathogens are shown
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Fig5: Estimation of gene family expansion and contraction using CAFE. (a) Clock calibrated phylogenetic tree showing the number of gene families significantly (P-value ≤ 0.01) expanded (red), contracted (blue) and their average pattern (black). (b) Venn diagram showing the number of proteins significantly expanded in each group of fungal species. (c) Bar plot showing the counts of genes annotated in each group of significantly expanded functional category. Only categories significantly overrepresented (P-value ≤ 0.01) in the 90 gene families expanded in the ascomycete trunk pathogens are shown

Mentions: The Computational Analysis of gene Family Evolution (CAFE; [65, 66]) computer program was utilized to identify gene families that had potentially undergone significant expansion or contraction in the genomes of the analyzed trunk pathogens. CAFE relies on a stochastic birth and death process to model the evolution of gene family sizes for a specified phylogenetic tree using the gene family sizes in the extant species. To apply CAFE, first a clock-calibrated phylogenetic tree was constructed (Fig. 5a) based on the multiple alignments of seventeen conserved peptides previously used to characterize phylogenic relationships across fungi (see Methods and [37]). To strengthen our analysis, 5 additional fungal species with known phylogenetic relationships were included (see Methods and [37]). After GBlocks parsing [67] of the concatenated alignments generated with MUSCLE [68], a total of 8,422 amino acid positions were imported into BEAUti [69]. Monophyletic partitions of data were specified and dated following [37] and [38] (see Methods). Branch-length estimation based on fossil records was carried out using the BEAST software package [69]. Branch lengths and tree topology were consistent with previous literature [38]. Our tree also confirmed the topology of recent divergence within the Dothideomycetes and Diaporthales, previously described [37, 38, 70], and the phylogenetically-distant relationship of P. chlamydospora and Dip. seriata, as described in [71].Fig. 5


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)

Estimation of gene family expansion and contraction using CAFE. (a) Clock calibrated phylogenetic tree showing the number of gene families significantly (P-value ≤ 0.01) expanded (red), contracted (blue) and their average pattern (black). (b) Venn diagram showing the number of proteins significantly expanded in each group of fungal species. (c) Bar plot showing the counts of genes annotated in each group of significantly expanded functional category. Only categories significantly overrepresented (P-value ≤ 0.01) in the 90 gene families expanded in the ascomycete trunk pathogens are shown
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Fig5: Estimation of gene family expansion and contraction using CAFE. (a) Clock calibrated phylogenetic tree showing the number of gene families significantly (P-value ≤ 0.01) expanded (red), contracted (blue) and their average pattern (black). (b) Venn diagram showing the number of proteins significantly expanded in each group of fungal species. (c) Bar plot showing the counts of genes annotated in each group of significantly expanded functional category. Only categories significantly overrepresented (P-value ≤ 0.01) in the 90 gene families expanded in the ascomycete trunk pathogens are shown
Mentions: The Computational Analysis of gene Family Evolution (CAFE; [65, 66]) computer program was utilized to identify gene families that had potentially undergone significant expansion or contraction in the genomes of the analyzed trunk pathogens. CAFE relies on a stochastic birth and death process to model the evolution of gene family sizes for a specified phylogenetic tree using the gene family sizes in the extant species. To apply CAFE, first a clock-calibrated phylogenetic tree was constructed (Fig. 5a) based on the multiple alignments of seventeen conserved peptides previously used to characterize phylogenic relationships across fungi (see Methods and [37]). To strengthen our analysis, 5 additional fungal species with known phylogenetic relationships were included (see Methods and [37]). After GBlocks parsing [67] of the concatenated alignments generated with MUSCLE [68], a total of 8,422 amino acid positions were imported into BEAUti [69]. Monophyletic partitions of data were specified and dated following [37] and [38] (see Methods). Branch-length estimation based on fossil records was carried out using the BEAST software package [69]. Branch lengths and tree topology were consistent with previous literature [38]. Our tree also confirmed the topology of recent divergence within the Dothideomycetes and Diaporthales, previously described [37, 38, 70], and the phylogenetically-distant relationship of P. chlamydospora and Dip. seriata, as described in [71].Fig. 5

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