Population structure and migration of the witches’ broom pathogen Moniliophthora perniciosa from cacao and cultivated and wild solanaceous hosts in southeastern Brazil

Abstract

Moniliophthora perniciosa, causal agent of witches' broom disease in cacao plantations in South America and the Caribbean Islands, has co-evolved with its host cacao, but the pathogen has also emerged in many solanaceous hosts in Brazil, including economically important food crops and wild species. This study was carried out to: (i) determine the existence of host subpopulations of M. perniciosa in Brazil; (ii) estimate gene and genotypic diversity of M. perniciosa host subpopulations infecting solanaceous hosts in southeastern Bahia and Minas Gerais states, Brazil; and (iii) estimate the amount and directionality of historical migration of M. perniciosa subpopulations. Up to 203 M. perniciosa isolates collected from solanaceous hosts with symptoms from Bahia and Minas Gerais states in Brazil and from Theobroma spp. (cacao) and Herrania spp. were characterized with 11 microsatellite markers. Factorial correspondence analyses, minimum-spanning network and Bayesian clustering revealed genetic clusters associated with their host of origin. Significant subpopulation differentiation was evident (Φ ST = 0.30, P ≤ 0.05) among M. perniciosa host subpopulations. Most of the multilocus microsatellite genotypes (MLMGs) were host-specific, with few MLMGs shared among subpopulations. Pairwise comparisons among M. perniciosa host subpopulations were significant, except between jurubeba (Solanum paniculatum) and cultivated solanaceous subpopulations. The combined analyses rejected the null hypothesis that M. perniciosa in Brazil is a single genetic population not structured by host. These findings support a scenario of introduction and subsequent adaptation to solanaceous hosts that should be taken into consideration to improve mitigation and management of M. perniciosa.

Genome sequence and effectorome of Moniliophthora perniciosa and Moniliophthora roreri subpopulations

“…Moniliophthora perniciosa can infect more than five species, both horticultural and wild solanaceas, which is a rather unusual feature for this fungus that is highly efficient to cause disease in cacao [ 21 , 48 ]. In contrast, M. roreri is a highly specialized pathogen of cacao plants, infecting only pods.…”

“…Each isolate is specific of subpopulation: Mp4145 (CEPLAC/CEPEC, Bahia, Brazil accession number 4145) and Mp1441 (CEPLAC/CEPEC, Bahia, accession number 1441) isolated from a susceptible cacao genotype collected in 2003 and 2012, respectively, and represents two separate incursions of M. perniciosa in Bahia [ 20 ]. Mp178 (CEPLAC/CEPEC, Bahia, accession number 4413) and Mp4071 (CEPLAC/CEPEC, Bahia, accession number 4071) were derived from the wild solanaceous hosts lobeira in Minas Gerais and Caiçara in Bahia (both from Brazil); that do not infect cacao [ 21 ]. Mp4124 (INIAP/Ecuador, accession number 404) is a representative isolate from M. perniciosa population’s from Ecuador [ 22 ], and MrPeru (Peru/ICT, accession number 05) is a representative of one of the major groups of M. roreri (the Bolívar group) established by Phillips-Mora et al [ 19 ] in a global diversity study.…”

“…The concentration and quality of the DNA obtained were checked in Qubit and NanoDrop™ 8000 Spectrophotometer (Therm Fisher Scientific) in 1% agarose gel. The identities of the isolates were validated using the highly conserved fungal rRNA gene primers (ITS1F and ITS4) as previously described [ 21 , 24 ].…”

Fungi associated with a dry invasive white patches on trunks of economic fruit trees in south-west Nigeria

“…(Mvondo et al, 2017) and Moniliophthora spp. (Patrocínio et al, 2017), which are established host-specific pathogens of woody plants, are generally found in a saprophytic or endophytic relationship with the plant hosts (Busby et al, 2016;Deng and Cao, 2017). Nevertheless, their phytopathogenic potential can manifest in plants with age-induced stress or nutrient deficiency condition (Sánchez-Hervás et al, 2008;Bartoszewska et al, 2011).…”

Distribución potencial y nicho fundamental de Moniliophthora spp en cacao de América y África

“…La escoba de bruja se originó en Brasil. Se considera que la región amazónica occidental del país es el centro endémico de Mp y los estados de Acre y el Amazonas occidental contienen las poblaciones con mayor diversidad genética del patógeno (Purdy y Schmidt, 1996;Artero et al, 2017;Patrocínio et al, 2017), con un posible primer registro del hongo en 1785 (Silva, 1987). El biotipo C de la especie es endémico de la Amazonía (Purdy y Schmidt, 1996), zona desde la cual se ha dispersado, invadiendo y causando grandes pérdidas en los cultivos de las regiones locales del Brasil, principalmente hacia el estado de Bahía llegando a la región en 1989 (Artero et al, 2017).…”