Comparative Genomics of Smut Pathogens: Insights From Orphans and Positively Selected Genes Into Host Specialization

Author(s)

Benevenuto, Juliana ^[1] ; Teixeira-Silva, Natalia S. ^[1] ; Kuramae, Eiko E. ^[2] ; Croll, Daniel ^[3] ; Monteiro-Vitorello, Claudia B. ^[1]

Affiliation

^[1] Univ Sao Paulo, Luiz de Queiroz Coll Agr USP ESALQ, Dept Genet, Microbial Genet Lab, Piracicaba - Brazil

^[2] Netherlands Inst Ecol NIOO KNAW, Dept Microbial Ecol, Wageningen - Netherlands

^[3] Univ Neuchatel UNINE, Inst Biol, Lab Evolutionary Genet, Neuchatel - Switzerland

• Document type: Journal article
• Source: FRONTIERS IN MICROBIOLOGY; v. 9, APR 6 2018.
• Web of Science Citations: 5

Abstract

Host specialization is a key evolutionary process for the diversification and emergence of new pathogens. However, the molecular determinants of host range are poorly understood. Smut fungi are biotrophic pathogens that have distinct and narrow host ranges based on largely unknown genetic determinants. Hence, we aimed to expand comparative genomics analyses of smut fungi by including more species infecting different hosts and to define orphans and positively selected genes to gain further insights into the genetics basis of host specialization. We analyzed nine lineages of smut fungi isolated from eight crop and non-crop hosts: maize, barley, sugarcane, wheat, oats, Zizania latifolia (Manchurian rice), Echinochloa colona (a wild grass), and Persicaria sp. (a wild dicot plant). We assembled two new genomes: Ustilago hordei (strain Uhor01) isolated from oats and U. tritici (strain CBS 119.19) isolated from wheat. The smut genomes were of small sizes, ranging from 18.38 to 24.63 Mb. U. hordei species experienced genome expansions due to the proliferation of transposable elements and the amount of these elements varied among the two strains. Phylogenetic analysis confirmed that Ustilago is not a monophyletic genus and, furthermore, detected misclassification of the U. tritici specimen. The comparison between smut pathogens of crop and non-crop hosts did not reveal distinct signatures, suggesting that host domestication did not play a dominant role in shaping the evolution of smuts. We found that host specialization in smut fungi likely has a complex genetic basis: different functional categories were enriched in orphans and lineage-specific selected genes. The diversification and gain/loss of effector genes are probably the most important determinants of host specificity. (AU)

• FAPESP's process: 17/13268-2 - Genomic and functional studies of the interaction Sporisorium scitamineum-cana and other smut fungi: advances and challenges
• Grantee: Claudia Barros Monteiro Vitorello
• Support Opportunities: Regular Research Grants
• FAPESP's process: 16/03768-5 - Comparative genomics perspective of host specialization by smut fungi
• Grantee: Juliana Benevenuto
• Support Opportunities: Scholarships abroad - Research Internship - Doctorate
• FAPESP's process: 16/16376-8 - Functional analysis of candidate effector proteins during Sporisorium scitamineum x sugarcane interaction
• Grantee: Natália de Sousa Teixeira e Silva
• Support Opportunities: Scholarships in Brazil - Doctorate
• FAPESP's process: 16/17545-8 - Genes, genomes & transposable elements contribution to plant-microbe interaction: a sugarcane study case
• Grantee: Marie-Anne Van Sluys
• Support Opportunities: Program for Research on Bioenergy (BIOEN) - Thematic Grants
• FAPESP's process: 14/21802-0 - Comparative genomics perspective of host specialization by smut fungi and genetic diversity of Sporisorium scitamineum isolates (sugarcane smut agent)
• Grantee: Juliana Benevenuto
• Support Opportunities: Scholarships in Brazil - Doctorate