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ARS Home » Northeast Area » Beltsville, Maryland (BARC) » Beltsville Agricultural Research Center » Sustainable Perennial Crops Laboratory » Research » Publications at this Location » Publication #332628

Title: Phytophthora megakarya and P. palmivora, closely related causal agents of cacao black pod rot, underwent increases in genome sizes and gene numbers by different mechanisms

item ALI, SHAHIN - Non ARS Employee
item Shao, Jonathan
item Strem, Mary
item AMOAKO-ATTAH, ISHMAEL - Cocoa Research Institute Of Ghana
item MELNICK, RACHEL - Former ARS Employee
item YAW AKROFI, ANDREW - Cocoa Research Institute Of Ghana
item COULIBALY, KLOTIOLOMA - National Center For Agricultural Research (CNRA)
item ISMAEL KEBE, KEBE - National Center For Agricultural Research (CNRA)
item GUILTINAN - Pennsylvania State University
item BEGOUDE, B.A. DIDIER - Institute Of Agricultural Research For Development (IRAD)
item TEN HOOPEN, G MARTIJIN - Cirad, France
item SHEN, DANYU - Nanjing Agricultural University
item LARY, DAVID - University Of Texas
item KRONMILLER, BRENT - Oregon State University
item TYLER, BRETT - Oregon State University
item Meinhardt, Lyndel
item Bailey, Bryan

Submitted to: Genome Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/7/2017
Publication Date: 3/1/2017
Citation: Ali, S., Shao, J.Y., Strem, M.D., Amoako-Attah, I., Melnick, R., Yaw Akrofi, A., Coulibaly, K., Ismael Kebe, K., Guiltinan, Begoude, B., Ten Hoopen, G., Shen, D., Lary, D.J., Kronmiller, B., Tyler, B., Meinhardt, L.W., Bailey, B.A. 2017. Phytophthora megakarya and P. palmivora, closely related causal agents of cacao black pod rot, underwent increases in genome sizes and gene numbers by different mechanisms. Genome Biology and Evolution. 9:536-557.

Interpretive Summary: Phytophthora palmivora and Phytophthora megakarya cause black pod rot on cacao, a devastating disease which destroys cacao yields and threatens chocolate industry supplies. P. palmivora is spread around the world where cacao is grown causing 15 to 30% reductions in yield. P. megakarya, on the other hand, is found only in Africa. Africa is a major cacao supplier, and P. megakarya is very aggressive on cacao causing complete yield losses if not managed. As with most disease situations, whether involving animals or plants, understanding the genetics of both the pathogen and disease host is critical to optimizing methods for managing disease. For the first time, we have sequenced the genomes of both P. megakarya and P. palmivora identifying the genes each possess and the proteins they produce. The two species are very closely related but have used unusual methods to increase their genome sizes. P. palmivora has essentially doubled everything in its genome while P. megakarya has specifically increased the number of genes involved in causing disease. As a result the two species still have similar gene numbers but have many more genes than other Phytophthora species. These genome characteristics undoubtedly influence the unique interaction of each species with cacao. With this knowledge, cacao scientists will be better able to direct their research toward developing disease management tools including the development of cacao genotypes more tolerant of disease. Ultimately, by managing black pod rot, supplies of cacao will be stabilized benefiting the chocolate industry and consumers of the many cacao based products.

Technical Abstract: Phytophthora megakarya (Pmeg) and P. palmivora (Ppal) are closely related species causing black pod rot of cacao. While Ppal is a cosmopolitan plant pathogen, cacao is the only known host of importance for Pmeg. Pmeg is more virulent on cacao than Ppal. Therefore, we have sequenced both the Pmeg and Ppal genomes and carried out a comparative study to identify virulence-related gene models (GeneM) that may be responsible for their host specificities and the increased damage on cacao caused by Pmeg. Pmeg and Ppal have estimated genome sizes of 126.88 and 151.23 Mb, respectively and GeneM numbers of 42,036 and 44,327, respectively. Despite the similarities in GeneM numbers, our findings suggest that the evolutionary histories of Pmeg and Ppal are quite different. Post-speciation, Ppal has undergone recent whole-genome duplication (WGD) whereas Pmeg has undergone selective increase of GeneM numbers, likely through accelerated transposable element driven duplications (TDD). Many of the GeneMs in both species failed to match transcripts and may represent pseudogenes or cryptic genetic reservoirs. Pmeg appears to have undergone amplification of specific gene families, some of which are clearly virulence-related. In addition, the virulence-related gene families (examples include lipases, proteases, elicitins, NPPs and RxLRs) in both species showed significantly higher rates of base substitution compared to some housekeeping gene families. Analysis of mycelium, zoospore and in planta transcriptome expression profiles using neural network self-organizing map analysis identified 24 multi-variate and non-linear self-organizing map (SOM) classes. Many members of the RxLR, NPP, and pectinase genes families were specifically induced in planta whereas other virulence-related gene families were less specific in their patterns of expression. Pmeg displays a diverse virulence-related gene complement similar in size to and potentially of greater diversity than Ppal but it remains likely that the specific functions of the genes determine each species’ unique characteristics as pathogens.