Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panamá: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes

Abstract

Colletotrichum interacts with numerous plant species overtly as symptomatic pathogens and cryptically as asymptomatic endophytes. It is not known whether these contrasting ecological modes are optional strategies expressed by individual Colletotrichum species or whether a species’ ecology is explicitly pathogenic or endophytic. We explored this question by inferring relationships among 77 C. gloeosporioides s.l. strains isolated from asymptomatic leaves and from anthracnose lesions on leaves and fruits of Theobroma cacao (cacao) and other plants from Panamá. ITS and 5′-tef1 were used to assess diversity and to delineate operational taxonomic units for multilocus phylogenetic analysis. The ITS and 5′-tef1 screens concordantly resolved four strongly supported lineages, clades A–D: Clade A includes the ex type of C. gloeosporioides, clade B includes the ex type ITS sequence of C. boninense, and clades C and D are unidentified. The ITS yielded limited resolution and support within all clades, in particular the C. gloeosporioides clade (A), the focal lineage dealt with in this study. In contrast the 5′-tef1 screen differentiated nine distinctive haplotype subgroups within the C. gloeosporioides clade that were concordant with phylogenetic terminals resolved in a five-locus nuclear phylogeny. Among these were two phylogenetic species associated with symptomatic infections specific to either cacao or mango and five phylogenetic species isolated principally as asymptomatic infections from cacao and other plant hosts. We formally describe two new species, C. tropicale and C. ignotum, that are frequent asymptomatic associates of cacao and other Neotropical plant species, and epitypify C. theobromicola, which is associated with foliar and fruit anthracnose lesions of cacao. Asymptomatic Colletotrichum strains isolated from cacao plants grown in China included six distinct C. gloeosporioides clade taxa, only one of which is known to occur in the Neotropics.

• anthracnose
• China
• endophyte
• multilocus
• Panamá
• pathogen

We are sincerely grateful for the help of Veronica Martins, Clare Whittaker and Adnan Ismaiel who provided invaluable laboratory support throughout this study. For help in the field and lab in Panamá we thank Luis Ramirez, Dora Alvarez, Zuleyka Maynard, Luis C. Mejía, Terri Shirshac, Jill Urriola, Clara Perez, Luciano Arauz, Kenman Concepción, Mirna Santana and Rohan Hebbar. We thank Kaoru Kitajima and S. Joseph Wright for letting us find samples in their common-garden plots and the Autoridad Nacional del Ambiente de Panamá for permitting collection and exportation of samples. The mention of trade products or company names or firm names does not imply that the U.S. Department of Agriculture recommends them over similar products or companies not mentioned.