Maternal mitochondrial inheritance in two Fusarium pathogens of prickly ash (Zanthoxylum bungeanum) in northern China

Authors: XUE, ZHOU - Northwest Agricultural & Forestry University; CAO, ZHI-MIN - Northwest Agricultural & Forestry University; LIU, XIN - Northwest Agricultural & Forestry University; Kim, Hye-Seon; Proctor, Robert; O Donnell, Kerry

Submitted to: Mycologia
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/19/2018
Publication Date: 3/21/2019
Citation: Xue, Z., Cao, Z., Liu, X., Kim, H.-S., Proctor, R.H., O'Donnell, K. 2019. Maternal mitochondrial inheritance in two Fusarium pathogens of prickly ash (Zanthoxylum bungeanum) in northern China. Mycologia. 111(2):235-243. https://doi.org/10.1080/00275514.2018.1562269.
DOI: https://doi.org/10.1080/00275514.2018.1562269

Interpretive Summary: Portal Request Remove travelers from my Concur profile list Fusarium is arguably the most economically destructive group of toxin producing plant pathogenic fungi. Collectively they are responsible for multibillion dollar annual losses to the world’s agricultural economy. This is because they cause disease on virtually every economically important crop. In addition, the diverse toxins they produce, which include two select agents, pose a significant threat to food safety, agricultural biosecurity, and plant and human health. We recently discovered that two Fusarium pathogens were responsible for the widespread death of Szechuan pepper trees in northern China. This disease threatens the world’s supply of this peppery spice, which is highly valued in Asian cuisine. Due to the negative impact this disease has had on pepper production, the current study was initiated to characterize the genetic diversity of the pathogens using a comparative genomics approach. Because mitochondria are associated with many biological phenomenon such the ability of a pathogen to cause disease together with several inherited diseases, knowledge of a pathogen’s mitochondrial inheritance pattern might help inform disease control strategies. Towards this end, we developed several robust molecular diagnostic tests from the complete mitochondrial genomes of these two pathogens to investigate mitochondrial inheritance in Fusarium for the first time. Results of this study revealed that all mitochondria were inherited from the female parent and the mitochondrial genomes of the pathogens harbored considerable genetic diversity. The molecular diagnostics developed in this study provide plant quarantine officials and plant disease specialists with the only tools available for tracking the movement of these pathogens so that they are not inadvertently introduced into disease free areas.

Technical Abstract: Mitochondrial inheritance in Fusarium zanthoxyli and F. continuum, two canker-inducing pathogens of prickly ash (Zanthoxylum bungeanum) in northern China, was investigated by genotyping ascospore progeny obtained from laboratory crosses. Polymorphic regions of the mitogenomes that contained indels and SNPs were identified via comparative analyses of the complete mitogenomes of the parents used in the intraspecific crosses. A reciprocal genetic cross of F. zanthoxyli NRRL 66714 (MAT1-1) × NRRL 66285 (MAT1-2), and a separate cross of F. continuum female NRRL 66286 (MAT1-2) × male NRRL 66218 (MAT1-1), revealed that mitochondria were only inherited from the maternal parent. In addition, the reciprocal cross demonstrated that mitochondrial inheritance is not linked to mating-type. Gene order in the circular mitogenomes of the prickly ash pathogens was identical to that previously reported for other fusaria and members of the Hypocreales, except that the trnL tRNAs were duplicated in F. zanthoxyli NRRL 66714. The genomes contained 14 polypeptide-encoding genes involved in oxidative respiration, one intron-encoded ribosomal protein (rsp3) gene, two ribosomal RNA (rRNA) genes and 26-28 tRNA genes. The F. zanthoxyli mitogenomes were 80.9 and 98.7 kb in length whereas those of F. continuum were considerably shorter and nearly identical in length at 63.4 kb. The significant differences in mitogenome length was primarily due to variable numbers of introns and ORFs encoding hypothetical proteins.