Theobroma cacao, the source of chocolate, is affected by destructive diseases wherever it is grown. Some diseases are endemic; however, as cacao was disseminated from the Amazon rain forest to new cultivation sites it encountered new pathogens. Two well-established diseases cause the greatest losses: black pod rot, caused by several species of Phytophthora, and witches’ broom of cacao, caused by Moniliophthora perniciosa. Phytophthora megakarya causes the severest damage in the main cacao producing countries in West Africa, while P. palmivora causes significant losses globally. M. perniciosa is related to a sister basidiomycete species, M. roreri which causes frosty pod rot. These Moniliophthora species only occur in South and Central America, where they have significantly limited production since the beginnings of cacao cultivation. The basidiomycete Ceratobasidium theobromae causing vascular-streak dieback occurs only in South-East Asia and remains poorly understood. Cacao swollen shoot disease caused by Cacao swollen shoot virus is rapidly spreading in West Africa. This review presents contemporary research on the biology, taxonomy and genomics of what are often new-encounter pathogens, as well as the management of the diseases they cause.

Laurel wilt kills members of the Lauraceae plant family in the southeastern United States. It is caused by Raffaelea lauricola T.C. Harr., Fraedrich and Aghayeva, a nutritional fungal symbiont of an invasive Asian ambrosia beetle, Xyleborus glabratus Eichhoff, which was detected in Port Wentworth, Georgia, in 2002. The beetle is the primary vector of R. lauricola in forests along the southeastern coastal plain of the United States, but other ambrosia beetle species that obtained the pathogen after the initial introduction may play a role in the avocado (Persea americana Miller) pathosystem. Susceptible taxa are naïve (new-encounter) hosts that originated outside Asia. In the southeastern United States, over 300 million trees of redbay (P. borbonia (L.) Spreng.) have been lost, and other North American endemics, non-Asian ornamentals and avocado—an important crop that originated in MesoAmerica—are also affected. However, there are no reports of laurel wilt on the significant number of lauraceous endemics that occur in the Asian homeland of R. lauricola and X. glabratus; coevolved resistance to the disease in the region has been hypothesized. The rapid spread of laurel wilt in the United States is due to an efficient vector, X. glabratus, and the movement of wood infested with the insect and pathogen. These factors, the absence of fully resistant genotypes, and the paucity of effective control measures severely constrain the disease’s management in forest ecosystems and avocado production areas.

Lasiodiplodia theobromae (Pat.) Griffon & Maubl., a member of the family Botryosphaeriaceae, is becoming a significant threat to crops and woody plants in many parts of the world, including the major cacao growing areas. While attempting to isolate Ceratobasidium theobromae, a causal agent of vascular streak dieback (VSD), from symptomatic cacao stems, 74% of isolated fungi were Lasiodiplodia spp. Sequence-based identification of 52 putative isolates of L. theobromae indicated that diverse species of Lasiodiplodia were associated with cacao in the studied areas, and the isolates showed variation in aggressiveness when assayed using cacao leaf discs. The present study reports a 43.75 Mb de novo assembled genome of an isolate of L. theobromae from cacao. Ab initio gene prediction generated 13 061 protein-coding genes, of which 2862 are unique to L. theobromae, when compared with other closely related Botryosphaeriaceae. Transcriptome analysis revealed that 11 860 predicted genes were transcriptionally active and 1255 were more highly expressed in planta compared with cultured mycelia. The predicted genes differentially expressed during infection were mainly those involved in carbohydrate, pectin, and lignin catabolism, cytochrome P450, necrosis-inducing proteins, and putative effectors. These findings significantly expand our knowledge of the genome of L. theobromae and the genes involved in virulence and pathogenicity.

We summarize the information available on ambrosia beetle species that have been associated in Florida with Raffaelea lauricola T.C. Harr., Fraedrich & Aghayeva, the primary symbiont of Xyleborus glabratus Eichhoff and cause of laurel wilt. In total, 14 species in Ambrosiodmus, Euwallacea, Premnobius, Xyleborus, Xyleborinus, and Xylosandrus were either reared from laurel wilt-affected host trees or trapped in laurel wilt-affected stands of the same, and assayed for R. lauricola. In six collections from native species in the southeastern United States [Persea borbonia (L.), Persea palustris (Raf.) Sarg., and Persea humilis Nash] and four from avocado (Persea americana Mill.), extracted mycangia or heads (taxa with mandibular mycangia) or intact bodies (taxa with mycangia in other locations) were surface-disinfested before assays on a semi-selective medium for the isolation of Raffaelea (CSMA+). Raffaelea lauricola was identified based on its characteristic phenotype on CSMA+, and the identity of a random subset of isolates was confirmed with taxon-specific microsatellite markers. The pathogen was recovered from 34% (246 of 726) of the individuals that were associated with the native Persea spp., but only 6% (58 of 931) of those that were associated with avocado. Over all studies, R. lauricola was recovered from 10 of the ambrosia beetle species, but it was most prevalent in Xyleborus congeners. This is the first record of R. lauricola in Ambrosiodmus lecontei Hopkins, Xyleborinus andrewesi (Blandford), and Xyleborus bispinatus Eichhoff. The potential effects of R. lauricola’s promiscuity are discussed.

Black pod disease, caused by Phytophthora species, is among the main limiting factors of cacao (Theobroma cacao L.) production. High incidence levels of black pod disease have been reported in Brazil, being induced by Phytophthora capsici, Phytophthora citrophthora, Phytophthora heveae, and Phytophthora palmivora. To assess the diversity of Phytophthora species affecting cacao in Brazil, 40 new isolates were obtained from cacao pods exhibiting symptoms of black pod disease collected in different smallholder farms in 2017. Further, ten cacao-infecting isolates morphologically identified as P. citrophthora and P. palmivora were molecularly characterized. The genomic regions beta-tubulin, elongation factor 1 alpha, heat shock protein 90, and internal transcribed spacer, and the mitochondrially encoded cytochrome c oxidase I and II genes were PCR-amplified and Sanger-sequenced from the cacao-infecting Phytophthora isolates. The morphological characterization and evaluation of the mycelial growth rates for the Phytophthora isolates were performed in vitro. Based on the molecular analysis and morphological comparisons, 19 isolates were identified as P. palmivora (clade 4). Interestingly, 31 isolates grouped together in the phylogenetic tree and were placed apart from previously known species in Phytophthora clade 2. Therefore, these isolates are considered as a new species herein referred to as Phytophthora theobromicola sp. nov., which produced papillate, semipapillate, and persistent sporangia on simple sporangiophores. The P. palmivora isolates were identified as A1 mating type by pairing each isolate with known A1 and A2 tester strains of P. capsici, but no oogonia/antheridia were observed when P. theobromicola was paired with the different tester strains. The P. theobromicola and P. citrophthora isolates showed higher mycelial growth rates, when compared to P. palmivora, on different media at 10, 15, and 20°C, but similar values were observed when grown on clarified CA media at 25 and 30°C. The pathogenicity tests carried out on pods of four cacao clones (CCN51, PS1319, Cepec2004, and CP49) showed significant variability among the isolates of both Phytophthora species, with P. theobromicola inducing higher rates of necrotic lesion expansion, when compared to P. palmivora. Here, two Phytophthora species were found associated with black pod disease in the state of Bahia, Brazil, and the previously undescribed P. theobromicola seems to be prevalent in field conditions. This is the first report of P. theobromicola on T. cacao. Also, these findings are crucial to improve the disease control strategies, and for the development of cacao materials genetically resistant to Phytophthora.

Perennial agroecosystems often seek to optimize productivity by breeding nutrient-efficient, disease-resistant rootstocks. In cacao (Theobroma cacao L.), however, rootstock selection has traditionally relied on locally available open pollinated populations with limited data on performance. Furthermore, rootstock associations with the rhizobiome, or rhizosphere microbiome, have been neglected. Better understanding of rootstock and scion effects on cacao-specific traits, particularly those involved in root-microbe interactions and nutrient acquisition, could contribute to more efficient rootstock selection and breeding. A rootstock-scion interaction study was conducted using three scion genotypes and eight rootstock populations under greenhouse conditions to better understand the relationships among rootstock and scion identities, soil fertility, and rhizobiome composition and the impacts of these factors on plant uptake of macro- and micronutrients. We show that rootstock genotype has a stronger influence than scion on nutrient uptake, bacterial and fungal diversity, and rhizobiome composition, and that the relative contributions of rootstock and scion genotype to foliar nutrient status are dynamic over time. Correlation analysis and stepwise regression revealed complex relationships of soil physicochemical parameters and the rhizobiome to plant nutrition and emphasized strong impacts of microbial diversity and composition on specific nutrients. Linear discriminant analysis effect size estimation identified rootstock-responsive taxa potentially related to plant nutrition. This study highlights the importance of considering root-associated microbial communities as a factor in cacao rootstock breeding and the need for further investigation into mechanisms underlying nutrient acquisition and microbial interactions in grafted plants.