Complex Evolutionary Origins of Specialized Metabolite Gene Cluster Diversity among the Plant Pathogenic Fungi of the Fusarium graminearum Species Complex

Author(s)

Tralamazza, Sabina Moser ^{[1, 2]} ; Rocha, Liliana Oliveira ^[3] ; Oggenfuss, Ursula ^[2] ; Correa, Benedito ^[1] ; Croll, Daniel ^[2]

Affiliation

^[1] Univ Sao Paulo, Inst Biomed Sci, Dept Microbiol, Sao Paulo - Brazil

^[2] Univ Neuchatel, Inst Biol, Lab Evolutionary Genet, Neuchatel - Switzerland

^[3] Univ Estadual Campinas, Dept Food Sci, Food Engn Fac, Ave Monteiro Lobato, Campinas, SP - Brazil

• Document type: Journal article
• Source: GENOME BIOLOGY AND EVOLUTION; v. 11, n. 11, p. 3106-3122, NOV 2019.
• Web of Science Citations: 0

Abstract

Fungal genomes encode highly organized gene clusters that underlie the production of specialized (or secondary) metabolites. Gene clusters encode key functions to exploit plant hosts or environmental niches. Promiscuous exchange among species and frequent reconfigurations make gene clusters some of the most dynamic elements of fungal genomes. Despite evidence for high diversity in gene cluster content among closely related strains, the microevolutionary processes driving gene cluster gain, loss, and neofunctionalization are largely unknown. We analyzed the Fusarium graminearum species complex (FGSC) composed of plant pathogens producing potent mycotoxins and causing Fusarium head blight on cereals. We de novo assembled genomes of previously uncharacterized FGSC members (two strains of F. austroamericanum, F. cortaderiae, and F. meridionale). Our analyses of 8 species of the FGSC in addition to 15 other Fusarium species identified a pangenome of 54 gene clusters within FGSC. We found that multiple independent losses were a key factor generating extant cluster diversity within the FGSC and the Fusarium genus. We identified a modular gene cluster conserved among distantly related fungi, which was likely reconfigured to encode different functions. We also found strong evidence that a rare cluster in FGSC was gained through an ancient horizontal transfer between bacteria and fungi. Chromosomal rearrangements underlying cluster loss were often complex and were likely facilitated by an enrichment in specific transposable elements. Our findings identify important transitory stages in the birth and death process of specialized metabolism gene clusters among very closely related species. (AU)

• FAPESP's process: 16/04364-5 - Diversity of Fusarium graminearum Species Complex isolated from wheat and native grasses of Brazil.
• Grantee: Benedito Corrêa
• Support Opportunities: Regular Research Grants
• FAPESP's process: 17/22369-7 - Genome assembly and analysis of Fusarium graminearum Species Complex from Brazilian wheat
• Grantee: Sabina Moser Tralamazza
• Support Opportunities: Scholarships abroad - Research Internship - Post-doctor