Population genetic analysis of Fusarium decemcellulare, a guaraná pathogen, reveals high genetic diversity in the Amazonas state, Brazil

Authors: QUEIROZ, CLAUDIA - Federal University Of Amazonas (UFAM); CANIATO, FERNANDA - Federal University Of Amazonas (UFAM); SIQUEIRA, VANESSA - Instituto Nacional De Pesquisas Da Amazonia (INPA); DE MORAES CATARINO, ARICLEIA - Instituto Nacional De Pesquisas Da Amazonia (INPA); HANADA, ROGERIO - Instituto Nacional De Pesquisas Da Amazonia (INPA); O Donnell, Kerry; LARABA, IMANE - Orise Fellow; Rehner, Stephen; SOUSA, NELCIMAR - Embrapa; SILVA, GILVAN - Embrapa

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/4/2022
Publication Date: 5/18/2023
Citation: Queiroz, C.A., Caniato, F.F., Siqueira, V.K.S., de Moraes Catarino, A., Hanada, R.E., O'Donnell, K., Laraba, I., Rehner, S.A., Sousa, N.R., Silva, G.F. 2023. Population genetic analysis of Fusarium decemcellulare, a guaraná pathogen, reveals high genetic diversity in the Amazonas state, Brazil. Plant Disease. 107(5):1343-1354. https://doi.org/10.1094/PDIS-01-22-0083-RE.
DOI: https://doi.org/10.1094/PDIS-01-22-0083-RE

Interpretive Summary: Guaraná (Paullinia cupana var. sorbilis) is an economically important plant native to the Amazon basin in the Brazilian State of Amazonas. Guaraná seeds are used by the beverage industry in the production of soft and energy drinks due to the high concentration of caffeine. Brazil is the only country where guaraná is grown on a commercial scale. During pathogen surveys in the Brazilian Amazon, diseased guaraná displaying variable symptoms including abnormal flowers, stem galls, and oversprouting of vegetative buds was observed in eight different commercial sites. The pathogen was tentatively identified as Fusarium decemcellulare, which is increasingly becoming a constraint to guaraná production in the Brazilian Amazon. The objectives of this research were to characterize the genetic diversity and population structure of this pathogen. Population genetic analysis identified two populations designated C1 and C2 within the F. decemcellulare collection from the eight sites. The results suggests that movement of seedlings by humans may have played a role in shaping how F. decemcellulare genetic diversity is distributed in the Brazilian Amazon. Understanding the population genetics of the pathogen is crucial to formulate breeding strategies needed to develop durable resistant varieties and aid plant disease specialists’ efforts to develop robust disease control strategies.

Technical Abstract: Fusarium decemcellulare is one of the most important pathogens affecting guaraná crops in the Brazilian Amazon. Disease symptoms include floral hypertrophy and hyperplasia, stem galls, and oversprouting of vegetative buds. To date, no study has been conducted characterizing the genetic diversity and population structure of this pathogen. Here, a total of 224 isolates from eight guaraná production areas of the Brazilian Amazon were genotyped using a set of 10 ISSR markers. Although gene diversity metrics indicated gene composition at the eight sites sampled was relatively homogeneous (Nei’s gene diversity = 0.212 to 0.315), a total of 223 multilocus genotypes were identified among the 224 isolates. High genetic diversity was also found based on other indices (Stoddard and Taylor’s index = 0.91 to 1, Evenness index = 0.97 to 1). Population genetic analysis of the 10 ISSR marker fragments for the clone-corrected dataset with STRUCTURE software identified two populations designated C1 and C2 within the F. decemcellulare collection from the eight sites. Likewise, UPGMA hierarchical clustering and discriminant analysis of principal components (DAPC) of the strains from guaraná resolved these same two groups. Analysis of molecular variance demonstrated that 71% of genetic diversity occurred within the C1 and C2 populations. A pairwise comparison of sampling sites of two genetic population revealed that 59 of 66 were differentiated from one another (P <0.05) and high and significant gene flow was detected only between sampling sites assigned to the same genetic population. The presence of MAT1-1 and MAT1-2 strains at four of the five and seven of the eight sites, respectively, where the C1 and C2 populations were present, coupled with the high genetic diversity suggested that F. decemcellulare might be undergoing sexual reproduction. Isolation by distance was not observed (R2 = 0.02885, P > 0.05), which suggests that movement of seedlings by humans may have played a role in shaping how F. decemcellulare genetic diversity is distributed in the Brazilian Amazon.