Population genomic analysis reveals geographic structure and climatic diversification for Macrophomina phaseolina isolated from soybean and dry bean across the United States, Puerto Rico, and Colombia

Abstract

Macrophomina phaseolina causes charcoal rot, which can significantly reduce yield and seed quality of soybean and dry bean resulting from primarily environmental stressors. Although charcoal rot has been recognized as a warm climate-driven disease of increasing concern under global climate change, knowledge regarding population genetics and climatic variables contributing to the genetic diversity of M. phaseolina is limited. This study conducted genome sequencing for 95 M. phaseolina isolates from soybean and dry bean across the continental United States, Puerto Rico, and Colombia. Inference on the population structure using 76,981 single nucleotide polymorphisms (SNPs) revealed that the isolates exhibited a discrete genetic clustering at the continental level and a continuous genetic differentiation regionally. A majority of isolates from the United States (96%) grouped in a clade with a predominantly clonal genetic structure, while 88% of Puerto Rican and Colombian isolates from dry bean were assigned to a separate clade with higher genetic diversity. A redundancy analysis (RDA) was used to estimate the contributions of climate and spatial structure to genomic variation (11,421 unlinked SNPs). Climate significantly contributed to genomic variation at a continental level with temperature seasonality explaining the most variation while precipitation of warmest quarter explaining the most when spatial structure was accounted for. The loci significantly associated with multivariate climate were found closely to the genes related to fungal stress responses, including transmembrane transport, glycoside hydrolase activity and a heat-shock protein, which may mediate climatic adaptation for M. phaseolina. On the contrary, limited genome-wide differentiation among populations by hosts was observed. These findings highlight the importance of population genetics and identify candidate genes of M. phaseolina that can be used to elucidate the molecular mechanisms that underly climatic adaptation to the changing climate.

Rapid diversification of grey mangroves (Avicennia marina) driven by geographic isolation and extreme environmental conditions in the Arabian Peninsula

“…The genotyping quality filters employed here are commonly utilized in GEA studies based on RDA (e.g. Brauer et al, 2016;Chang et al, 2022;Faske et al, 2021;Friis et al, 2018Friis et al, , 2022Laporte et al, 2016;Ortiz et al, 2023;Ruiz Miñano et al, 2022;Vu et al, 2020). However, overly conservative quality filters may limit outlier detection analyses based on genotype-environment association analysis.…”

From the classroom to the farm: a lesson plan that promotes smallholder farmers’ education and training about plant pathology in the context of climate change

“…Although the extent of extreme weather events and pest and disease outbreaks had not been extensively quantified in Puerto Rico, modeling studies suggest an increased exposure and sensitivity to diseases and pests as temperatures rise ( 22 ). Similarly, population genomic analyses of Macrophomina phaseolina conducted in the United States, Puerto Rico, and Colombia showed the contributions of climate to the pathogen’s genetic variation that can contribute to the pathogen’s adaptive capacity ( 35 ).…”