In the chestnut blight fungus Cryphonectria parasitica, as in most fungi, l
ittle is known about the efficiency of the asexual transmission of optional
mitochondrial plasmids, vertically through conidia, and horizontally throu
gh hyphal anastomoses. In this paper, we show that pCRY1, a circular mitoch
ondrial plasmid, is transmitted vertically with 100%-efficiency through con
idia. Moreover, the plasmid is transmitted horizontally through hyphal cont
act from donor strains to vegetatively compatible and most incompatible str
ains. An allelic difference between the donor and recipient strain, at only
one of the five nuclear incompatibility genes that were tested strongly in
hibited, but did not absolutely prevent, the transfer of pCRY1 through hyph
al fusions. In contrast, allelic differences in any one or several of the o
ther four heterokaryon-compatibility loci suppressed the transmission of th
e plasmid only partially or not at all. The plasmid was also transmitted am
ong incompatible strains by protoplast fusion without the concomitant trans
fer of mitochondrial DNA (mtDNA). A comparison of plasmid-bearing with plas
mid-free isogenic strains revealed that pCRY1 significantly diminishes the
pathogenic potency of some strains of the fungus, but does not affect the v
irulence of others. Collectively, the observations indicate that the introd
uction of deleterious mitochondrial genetic elements into natural populatio
ns may be a means for managing fungal pathogens.