Of mushrooms and chocolate trees: aetiology and phylogeny of witches' broom and frosty pod diseases of cacao

Abstract

The troubled history of the two major diseases of the chocolate tree (Theobroma cacao) in South America, witches' broom and frosty pod, is reviewed, concentrating on critical aspects of the aetiology as well as the phylogeny of the causal agents. Both diseases are caused by sister species within the genus Moniliophthora, belonging to the Marasmiaceae family of mushrooms. The witches' broom pathogen, Moniliophthora perniciosa, evolved on the Amazonian side of the Andes and induces brooms not only in cacao and its relatives in the genera Theobroma and Herrania (Malvaceae), but also in species in the plant families Bignoniaceae, Malpighiaceae and Solanaceae, on which the mushrooms (basidiomata) are produced. Moniliophthora roreri, the type species of the genus, evolved as a pod pathogen on endemic Theobroma species on the western side of the northern Andean Cordillera. Because Moniliophthora was described originally as the asexual form of an unknown basidiomycete, the generic diagnosis is amended here to accommodate species with agaricoid basidiomata. In addition, the new variety M. roreri var. gileri is designated for the morphotype occurring on Theobroma gileri, in northwest Ecuador. Cytology studies indicate that the supposed conidia of M. roreri are, in fact, sexual spores (meiospores) and it is posited that the fruiting structure represents a much-modified mushroom. Finally, based on preliminary data from pathogenicity testing, it is hypothesized that the true causal agent of both diseases is an as yet unidentified infectious agent vectored into the host by the fungus.

How do Agaricomycetes shape their fruiting bodies? 1. Morphological aspects of development

“…The report by Cabrera-Ponce et al (2012) implies that U. maydis likely possesses basic gene sets for tissue formation and of basidiospore production in a manner as found in the majority of the Agaricomycetes. Contrariwise, the phragmobasidia-like structures observed in pseudotramal basidiomata of M. roreri (Evans et al 2002(Evans et al , 2003(Evans et al , 2013) might indicate that Agaricomycetes share with U. maydis the set of genes that the smut uses for phragmobasidia formation. It is indeed not excluded that genes being appointed in normal holobasidia formation in the Agaricomycetes are corresponding to genes being appointed in normal phragmobasidia formation in smuts and in rusts, respectively.…”

“…Close sister species in the agaric genus Moniliophthora produce typical agaricoid mushrooms with normal 4-spored undivided holobasidia (Moniliophthora perniciosa), respectively pseudostromal basidiomata (Moniliophthora roreri) with sporophores (interpreted as 'modified basidia') presenting chains of globose to subglobose thickwalled spores which can undergo stages of meiosis and germinate like probasidia of smuts and rusts into unusual four-celled cross-divided phragmobasidium-like structures (Delgado and Cook, 1976;Evans et al, 2002Evans et al, , 2003Evans et al, , 2013Aime and Phillips-Mora, 2005). Resupinate basidiomes, usually with undivided holobasidia, are actually found across all major lineages of the Agaricomycetes (Binder et al, 2005(Binder et al, , 2010Matheny et al, 2006;Miller et al, 2006;Larsson, 2007;Uehling et al, 2012a,b;Birkebak et al, 2013).…”

Moniliophthora roreri, causal agent of cacao frosty pod rot

“… †From type locality of host in Ecuador; earlier record on T . gileri in north‐west Colombia is now thought to be a different, closely related species (B. G. D. Bartley, personal communication, Lisbon, Portugal; Evans et al ., ).…”

“…Evans et al . () amended the description to include the agaric sexual morph or basidiocarp of Mp . In the interim, other mushroom‐forming species, with saprotrophic and, in some cases, endophytic lifestyles, rather than a pathogenic one, were added to the genus (Kerekes and Desjardin, ; Krupp and Albee‐Scott, ).…”

“…Pathol . 62 : 734 (). Basidiomycota (Phylum), Agaricomycetes (Class), Agaricales (Order), Marasmiaceae (Family).…”