Karyotype evolution in Fusarium

Authors: WAALWIJK, CEES - Wageningen University And Research Center; TAGA, MASATOKI - Okayama University; ZHENG, SONG-LIN - Okayama University; Proctor, Robert; Vaughan, Martha; O Donnell, Kerry

Submitted to: IMA Fungus
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/14/2018
Publication Date: 2/26/2018
Citation: Waalwijk, C., Taga, M., Zheng, S.-L., Proctor, R.H., Vaughan, M.M., O'Donnell, K. 2018. Karyotype evolution in Fusarium. IMA Fungus. 9(1):13-26. doi:10.5598/imafungus.2018.09.01.02
DOI: https://doi.org/10.5598/imafungus.2018.09.01.02

Interpretive Summary: The genus Fusarium contains over 300 genetically distinct species that occupy a broad array of ecological niches worldwide. Many of these species are plant pathogens, causing serious diseases on agriculturally important plants. Fusaria are responsible for multi-billion annual losses to the world’s economy. In addition, they produce a plethora of toxins, such as trichothecenes, fumonisins, and zearalenone, which pose a significant threat to food safety and human health. Comparative genetic studies have begun to revolutionize our understanding of species limits, evolutionary relationships, and mycotoxin potential in Fusarium. Such foundational information is essential for developing novel control strategies aimed at minimizing the threat that fusaria and their toxins pose to agricultural biosecurity. To assist full genome assembling, prior knowledge of chromosome number (CN) of the organism at hand is invaluable. In support of these efforts, the present study was initiated to determine CN for a broad set of Fusarium species, including representatives of 11 species complexes that span the phylogenetic breadth of the genus. The results indicate that karyotype evolution in Fusarium appears to have been dominated by a gradual reduction in core CN. The results provide a valuable framework for future comparative genomic research on the genus and will be of interest to a broad range of agricultural scientists.

Technical Abstract: The germ tube burst method (GTBM) was employed to examine karyotypes of 33 Fusarium species representative of 11 species complexes that span the phylogenetic breadth of the genus. The karyotypes revealed that the nucleolar organizing region (NOR), which includes the ribosomal rDNA region, was telomeric in the species where it was discernible. Variable karyotypes were detected in eight species due to variation in numbers of putative core and/or supernumerary chromosomes. The putative core chromosome number (CN) was most variable in the F. solani (CN = 9'12) and F. buharicum (CN = 9+1 and 18-20) species complexes. Quantitative real-time PCR and genome sequence analysis rejected the hypothesis that the latter variation in CN was due to diploidization. The core CN in six other species complexes where two or more karyotypes were obtained was less variable or fixed. Karyotypes of 10 species in the sambucinum species complex, which is the most derived lineage of Fusarium, revealed that members of this complex possess the lowest CN in the genus. When viewed in context of the species phylogeny, karyotype evolution in Fusarium appears to have been dominated by a reduction in core CN in five closely related complexes that share a most recent common ancestor (tricinctum and incarnatum-equiseti CN = 8-9, chlamydosporum CN = 8, heterosporum CN = 7, sambucinum CN = 4-5) but not in the sister to these complexes (nisikadoi CN = 11, oxysporum CN = 11 and fujikuroi CN = 10-12). CN stability is best illustrated by the F. sambucinum subclade, where the only changes observed since it diverged from other fusaria appear to have involved two independent putative telomere to telomere fusions that reduced the core CN from five to four, once each in the sambucinum and graminearum subclades. Results of the present study indicate a core CN of 4 may be fixed in the latter subclade, which is further distinguished by the absence of putative supernumerary chromosomes. Karyotyping of fusaria in the not too distant future will be done by whole-genome sequencing such that each scaffold represents a complete chromosome from telomere to telomere. The CN data presented here should be of value to assist such full genome assembling.