Independent Whole-Genome Duplications Define the Architecture of the Genomes of the Devastating West African Cacao Black Pod PathogenPhytophthora megakaryaand Its Close RelativePhytophthora palmivora

Abstract

<jats:p><jats:italic>Phytophthora megakarya</jats:italic> and <jats:italic>P. palmivora</jats:italic> are oomycete pathogens that cause black pod rot of cacao (<jats:italic>Theobroma cacao</jats:italic>), the most economically important disease on cacao globally. While <jats:italic>P. palmivora</jats:italic> is a cosmopolitan pathogen, <jats:italic>P. megakarya</jats:italic>, which is more aggressive on cacao than <jats:italic>P. palmivora</jats:italic>, has been reported only in West and Central Africa where it has been spreading and devastating cacao farms since the 1950s. In this study, we reconstructed the complete diploid genomes of multiple isolates of both species using single-molecule real-time sequencing. Thirty-one additional genotypes were sequenced to analyze inter- and intra-species genomic diversity. The <jats:italic>P. megakarya</jats:italic> genome is exceptionally large (222 Mbp) and nearly twice the size of <jats:italic>P. palmivora</jats:italic> (135 Mbp) and most known <jats:italic>Phytophthora</jats:italic> species (∼100 Mbp on average). Previous reports pointed toward a whole-genome duplication (WGD) in <jats:italic>P. palmivora</jats:italic>. In this study, we demonstrate that both species underwent independent and relatively recent WGD events. In <jats:italic>P. megakarya</jats:italic> we identified a unique combination of WGD and large-scale transposable element driven genome expansion, which places this genome in the upper range of <jats:italic>Phytophthora</jats:italic> genome sizes, as well as effector pools with 1,382 predicted RxLR effectors. Finally, this study provides evidence of adaptive evolution of effectors like RxLRs and Crinklers, and discusses the implications of effector expansion and diversification.</jats:p>

The Role of Fungi in the Cocoa Production Chain and the Challenge of Climate Change

“…Despite this, in a study conducted in six cocoa-growing regions in West Africa, where sixteen Phytophthora isolates were analysed, it was found that these isolates were more virulent and they reproduced faster than P. megakarya [ 20 ]. Recently, Morales-Cruz et al [ 21 ] demonstrated that P. megakarya genome is extensive (222 Mbp) and nearly twice the size of P. palmivora (135 Mbp) and most known Phytophthora species (∼100 Mbp on average). Ali et al [ 16 ] found that P. megakarya shows a different virulence-related gene complement, similar in size and potentially of greater diversity than P. palmivora .…”

Current status of plant pathogens of agricultural importance for Colombia. A review

“…Hence, the identification and characterisation of core effectors, which are deployed by P. palmivora in Colombia to surpass the immunity of cocoa plant varieties, could be extremely useful in deploying effector-aided resistant breeding that is less time consuming and more durable than conventional breeding strategies (Evangelisti et al, 2017). These effector studies could be aided by a recent study that redefined the genomic structure of P. palmivora, allowing for the identification of several new effectors from this pathogen (Morales-Cruz et al, 2020).…”

Phytophthora palmivora–Cocoa Interaction

“…Genome, transcriptome and secretome studies combined with RNA-sequencing and RT-PCR identified RXLR effectors and crinklers in Ppal and P. megakarya, which were differentially expressed in mycelia, zoospores, and in planta (infected pod husks) [ 106 ]. Furthermore, recent work by Morales–Cruz et al [ 136 ] predicted that Ppal had 717 RxLR effectors compared to P. megakarya, which had 1,382 effectors due to genome duplication and expansion in the latter. In addition, 251 “putative effectors” in Ppal had shared homology and often bordered RxLRs [ 136 ].…”

“…Furthermore, recent work by Morales–Cruz et al [ 136 ] predicted that Ppal had 717 RxLR effectors compared to P. megakarya, which had 1,382 effectors due to genome duplication and expansion in the latter. In addition, 251 “putative effectors” in Ppal had shared homology and often bordered RxLRs [ 136 ]. More work would be needed to understand the functions of these effectors in Ppal and how they aid in infection and in manipulating cocoa’s immunity to cause disease.…”