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Title: Transcriptome profiling identifies gene expression patterns and promoter motifs associated with post-penetration resistance to Phytophthora palmivora in pods of Theobroma cacao genotypes

item BARUAH, INDRANI - Oak Ridge Institute For Science And Education (ORISE)
item Shao, Jonathan
item ALI, SHAHIN - University Of California, Davis
item Schmidt, Martha
item Meinhardt, Lyndel
item Bailey, Bryan
item Cohen, Stephen

Submitted to: Scientific Reports
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/12/2024
Publication Date: 2/20/2024
Citation: Baruah, I., Shao, J.Y., Ali, S., Schmidt, M.E., Meinhardt, L.W., Bailey, B.A., Cohen, S.P. 2024. Transcriptome profiling identifies gene expression patterns and promoter motifs associated with post-penetration resistance to Phytophthora palmivora in pods of Theobroma cacao genotypes. Scientific Reports. 14:4175(2024).

Interpretive Summary: The chocolate industry relies on the harvest of cocoa beans from healthy cacao trees, but diseases, such as black pod rot, threaten the health of cacao trees worldwide. There is no treatment for black pod rot and the only strategy to control it is to develop new, immune cacao varieties through cacao breeding programs. Breeding programs require in-depth knowledge of how cacao defends itself against diseases, but this knowledge is lacking for black pod rot. In this study, we used a big data approach to study how seven cacao varieties regulate their genes to respond to early infection. This allowed us to determine how resistant varieties of cacao defend themselves against black pod rot during the early stages of infection. We developed several new genomics tools that can be used by cacao breeders, including the identification of candidate genes and regulatory DNA sequences. Release of this information will help cacao breeders use cutting edge breeding techniques to improve cacao rapidly and efficiently to be more resistant to black pod rot, protecting the chocolate industry.

Technical Abstract: The oomycete Phytophthora palmivora infects the fruit of cacao trees (Theobroma cacao) causing black pod rot and reducing yields. Cacao genotypes vary in their resistance levels to P. palmivora, yet our understanding of how cacao fruit respond to the pathogen at the molecular level during disease establishment is limited. To address this issue, a disease development and RNA-Seq study was conducted on pods of seven cacao genotypes (ICS1, WFT, Gu133, Spa9, CCN51, Sca6 and Pound7) to better understand their reactions to the post-penetration stage of P. palmivora infection. The pod tissue-P. palmivora pathogen assay resulted in the genotypes being classified as susceptible (ICS1, WFT, Gu133 and Spa9) or resistant (CCN51, Sca6 and Pound7). The number of differentially expressed genes (DEGs) ranged from 1,625 to 6,957 depending on genotype. A custom gene correlation approach identified 34 correlation groups. De novo motif analysis was conducted on upstream promoter sequences identifying 76 novel motifs, 31 of which were over-represented in the upstream sequences of correlation groups and associated with gene ontology terms related to oxidative stress response, defense against fungal pathogens, general metabolism and cell function. Genes in one correlation group (Group 6) were strongly induced in all genotypes and enriched in genes annotated with defense-responsive terms. Expression pattern profiling revealed that genes in Group 6 were induced to higher levels in the resistant genotypes. Additional analysis allowed the identification of 17 candidate cis-regulatory modules likely to be involved in cacao defense against P. palmivora. This study is a comprehensive exploration of the cacao pod response to P. palmivora spread after infection and identified cacao genes, promoter motifs, and promoter motif combinations associated with post-penetration resistance to P. palmivora in cacao pods.