Independent whole-genome duplications define the architecture of the genomes of the devastating West African cacao black pod pathogen Phytophthora megakarya and its close relative Phytophthora palmivora

Authors: MORALES-CRUZ, ABRAHAM - University Of California, Davis; ALI, SHAHIN - University Of California, Davis; MINIO, ANDREA - University Of California, Davis; FIGUEROA-BALDERAS, ROSA - University Of California, Davis; GARCIA, JADRAN - University Of California, Davis; Kasuga, Takao; Puig, Alina; MARELLI, JEAN-PHILIPPE - Mars, Inc; Bailey, Bryan; CANTU, DARIO - University Of California, Davis

Submitted to: G3, Genes/Genomes/Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/29/2020
Publication Date: 4/30/2020
Citation: Morales-Cruz, A., Ali, S.S., Minio, A., Figueroa-Balderas, R., Garcia, J.F., Kasuga, T., Puig, A.S., Marelli, J., Bailey, B.A., Cantu, D. 2020. Independent whole-genome duplications define the architecture of the genomes of the devastating West African cacao black pod pathogen Phytophthora megakarya and its close relative Phytophthora palmivora. G3, Genes/Genomes/Genetics. 10(6). https://doi.org/10.1534/g3.120.401014.
DOI: https://doi.org/10.1534/g3.120.401014

Interpretive Summary: Phytophthora megakarya (Pmeg) and P. palmivora (Ppal) cause black pod rot of cacao, the most economically important disease on cacao globally. While Ppal is a cosmopolitan pathogen, Pmeg, which is more aggressive on cacao than Ppal, has been reported only in West and Central Africa where it has been spreading and devastating cacao plantations since the 1950s. In this study, we sequenced the genomes of multiple isolates of both species. Thirty-one additional isolates were sequenced to analyze genomic diversity. These resources make it possible to better understand the biology and pathogenicity.

Technical Abstract: Phytophthora megakarya (Pmeg) and P. palmivora (Ppal) are oomycete pathogens that cause black pod rot of cacao (Theobroma cacao), the most economically important disease on cacao globally. While Ppal is a cosmopolitan pathogen, Pmeg, which is more aggressive on cacao than Ppal, has been reported only in West and Central Africa where it has been spreading and devastating cacao plantations since the 1950s. In this study, we reconstructed the complete diploid genomes of multiple isolates of both species using single-molecule sequencing. Thirty-one additional genotypes were sequenced to analyze inter- and intra-species genomic diversity. These resources make it possible to better understand the molecular basis of virulence differences in closely related and consequential pathogens and study their evolutionary history. The Pmeg genome is exceptionally large (222 Mbp) and nearly twice the size Ppal (135 Mbp) and most known Phytophthora species (~100 Mbp on average). We show that the genomes of both species recently expanded by independent whole-genome duplications (WGD). WGD and the dramatic expansion of a few gene families led to the exceptionally large genome of Pmeg and the diversification of virulence-related genes. We show that WGD and transposable elements, particularly long-terminal repeats, led to the massive expansion of disease-related gene families including secreted RxLR effectors. Finally, this study provides evidence of adaptive evolution among well-known effectors and discusses the implications of effector expansion and diversification.