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

Authors: MORALES-CRUZ, ABRAHAM - University Of California; AMRINE, KATHERINE - University Of California; BLANCO-ULATE, BARBARA - University Of California; LAWRENCE, DANIEL - University Of California; TRAVADON, RENAUD - University Of California; ROLSHAUSEN, PHILIPPE - University Of California; Baumgartner, Kendra; CANTU, DARIO - University Of California

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/6/2015
Publication Date: 6/19/2015
Publication URL: http://www.biomedcentral.com/1471-2164/16/469
Citation: Morales-Cruz, A., Amrine, K.C., Blanco-Ulate, B., Lawrence, D.P., Travadon, R., Rolshausen, P., Baumgartner, K., Cantu, D. 2015. Distinctive expansion of gene families associated with plant cell wall degradation, secondary metabolism, and nutrient uptake in the genomes of grapevine trunk pathogens. Biomed Central (BMC) Genomics. 16:469.

Interpretive Summary: The trunk diseases Eutypa dieback, Botryosphaeria dieback, Phomopsis dieback, and Esca threaten the longevity and productivity of grapevines worldwide. They are caused by fungi that are genetically unrelated, but nonetheless form chronic wood infections. Variation in their abilities to decompose the wood as a food source and in their production of compounds toxic to the grapevine are thought to contribute to the unique disease symptoms these fungi cause. We sequenced the genomes of six trunk pathogens: Diaporthe ampelina, Diplodia seriata, Eutypa lata, Neofusicoccum parvum, Phaeomoniella chlamydospora, and Togninia minima. In comparing their genomes, we focused on gene families that are likely to enhance the pathogen’s ability to infect grapevine wood: wood degradation, (nutrient uptake, and toxin production. For these comparisons between the genomes of the trunk pathogens, we examined the number of genes per gene family, the similarities/differences of genes within gene families, and the evolution of gene families over time. In the genomes of N. parvum, D. ampelina, and E. lata, we found an increase in total gene numbers within gene families associated with cell wall oxidative functions and secondary metabolic pathways, whereas D. seriata, P. chlamydospora, and T. minima appear to have actually ‘lost’ genes with these functions over time. This finding suggests that N. parvum, D. ampelina, and E. lata may produce more enzymes or toxins, which is consistent with the fact that infections of these three species (more so than the other three) spread quickly within a grapevine. Gene families with significantly faster rates of gene gain can now provide a basis for further studies, to determine how the different trunk pathogens spread from one plant cell to the next and how resistant grape cultivars evade or tolerate the pathogens. In the short term, the genomes of the trunk pathogens are an important study tool for development of accurate diagnostic markers.

Technical Abstract: 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, but 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 expanded genomic resources to three additional trunk pathogens, Diaporthe ampelina, Diplodia seriata, and Phaeomoniella chlamydospora, causal agents of Phomopsis dieback, Botryosphaeria dieback, and Esca, respectively. The predicted proteomes 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, D. 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. 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 ultimately 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.