Rapid mini-chromosome divergence among fungal isolates causing wheat blast outbreaks in Bangladesh and Zambia

Authors: LIU, SANZHEN - Kansas State University; LIN, GUIFANG - Kansas State University; RAMACHANDRAN, SOWMYA - US Department Of Agriculture (USDA); CRUPPE, GIOVANA - Kansas State University; COOK, DAVID - Kansas State University; Pedley, Kerry; VALENT, BARBARA - Kansas State University

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 6/19/2022
Publication Date: 6/19/2022
Citation: Liu, S., Lin, G., Ramachandran, S.R., Cruppe, G., Cook, D.E., Pedley, K.F., Valent, B. 2022. Rapid mini-chromosome divergence among fungal isolates causing wheat blast outbreaks in Bangladesh and Zambia. bioRxiv. https://doi.org/10.1101/2022.06.18.496690.
DOI: https://doi.org/10.1101/2022.06.18.496690

Interpretive Summary: Wheat blast is an emerging fungal disease that threatens global wheat production and food security. The pathogen that causes wheat blast, a wheat-adapted lineage of Magnaporthe oryzae, was first identified in South America in the 1980s where it remained for several decades. In 2016 the pathogen was discovered in Bangladesh followed by its discovery in Zambia in 2017. The spread of the disease to South Asia and South-central Africa raised questions regarding the origin of the pathogen, and whether these outbreaks were caused by the same or similar strains. A molecular analysis of the strains collected in Bangladesh and Zambia revealed that they both belong to the same clonal lineage exemplified by a field isolate collected in Bolivia (termed B71). However, we found strong evidence to support that two major B71 sub-lineages separately caused the wheat blast outbreaks in Bangladesh and Zambia. We also demonstrate that in addition to the seven indispensable chromosomes that constitute the core genome of M. oryzae, all isolates from the B71 lineage maintain at least one extra “mini-chromosome.” Our findings show that while the core chromosomes of the Bangladesh and Zambia isolates are highly similar, their mini-chromosomes have undergone significant diversification. Since mini-chromosomes are hypothesized to be accelerators of pathogen adaptation to new hosts and environments, further investigation into the diversification of the mini-chromosomes among the populations in South America, Asia, and Africa may help prevent the spread of this devastating pathogen to new wheat production areas and controlling the disease in areas where it already occurs.

Technical Abstract: Global wheat production is seriously threatened by the filamentous fungal pathogen, Magnaporthe oryzae, causing wheat blast disease. The pathogen was first identified in South America and recently spread across continents to Bangladesh (South Asia) and Zambia (South-central Africa). M. oryzae strains closely related with a South American field isolate B71 was found to have caused the wheat blast outbreaks in South Asia and Africa. Here, we studied the genetic relationship among isolates found on the three continents. Using an improved reference genome for B71 and whole genome sequences of isolates from Bangladesh, Zambia, and South America, we found strong evidence to support that the outbreaks in Bangladesh and Zambia were caused by the introductions of genetically separated isolates. Structural variation analysis using whole genome short-read sequencing data indicate all isolates closely related to B71 maintained at least one supernumerary mini-chromosome and, interestingly, some Zambian isolates contain more than one mini-chromosome. Long-read sequencing and de novo genome assemblies of two Zambian isolates show that both contain a mini-chromosome similar to the B71 mini-chromosome, although pervasive structural variation exists among them. Genome assemblies also provide evidence that one Zambian isolate carries an additional mini-chromosome that is highly divergent from the B71 mini-chromosome. Our findings show that while the core genomes of the multiple introductions are highly similar, the mini-chromosomes have undergone marked diversification. The maintenance of the mini-chromosome during the multiple introductions, and the rapid sequence and structural variation suggests the mini-chromosomes may serve important virulence or niche adaptation roles under diverse environmental conditions.