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); CALDERON DAZA, LIDIA - Kansas State University; CRUPPE, GIOVANA - Kansas State University; TEMBO, BATISEBA - Zambia Agricultural Research Institute; SINGH, PAWAN,K - International Maize & Wheat Improvement Center (CIMMYT); COOK, DAVID - Kansas State University; Pedley, Kerry; VALENT, BARBARA - Kansas State University

Submitted to: New Phytologist
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/27/2023
Publication Date: 11/20/2023
Citation: Liu, S., Lin, G., Ramachandran, S.R., Calderon Daza, L., Cruppe, G., Tembo, B., Singh, P., Cook, D., Pedley, K.F., Valent, B. 2023. Rapid mini-chromosome divergence among fungal isolates causing wheat blast outbreaks in Bangladesh and Zambia. New Phytologist. 241:1266-1276. https://doi.org/10.1111/nph.19402.
DOI: https://doi.org/10.1111/nph.19402

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 lineage exemplified by a field isolate collected in Bolivia (termed B71). However, we found strong evidence to support that distinct 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 that belong 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 in efforts to control the disease in areas where it already occurs.

Technical Abstract: The fungal pathogen, Magnaporthe oryzae Triticum pathotype, causing wheat blast disease was first identified in South America and recently spread across continents to Bangladesh (South Asia) and Zambia (South-central Africa). Here, we studied the genetic relationship among isolates found on the three continents. M. oryzae strains closely related with a South American field isolate B71 were found to have caused the wheat blast outbreaks in South Asia and Africa. Genomic variation among isolates from the three continents was examined using an improved B71 reference genome and short- and long-read whole genome sequences. We found strong evidence to support that the outbreaks in Bangladesh and Zambia were caused by the introductions of genetically separated isolates, although they were all close to B71 and, therefore, collectively referred to as the B71 branch. In addition, B71 branch strains carried at least one supernumerary mini-chromosome. De novo genome assembly of a Zambian strain and genome comparison revealed that its mini-chromosome was similar to the B71 mini-chromosome but with a high level of structural variation. 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 and rapid genomic changes suggest the mini-chromosomes may serve important virulence or niche adaptation roles under diverse environmental conditions.