Pollen mimicry during infection of blueberry flowers by conidia of Monilinia vaccinii-corymbosi

Abstract

Infection of blueberry flowers by Monilinia vaccinii-corymbosi, which causes mummy berry disease, occurs via the gynoecium and involves conidial germination on the stigmatic surface followed by hyphal ingress into the stylar canal and subsequent colonization of the ovary. The extent to which these events mimic pollen–pistil interactions during pollination was investigated. Similar to blueberry pollen tubes, conidial germ tubes of M. vaccinii-corymbosi adhered selectively to imprints of stylar transmitting tract tissue on nitrocellulose membrane, with adhesion in both cases occurring at the tips of the tubes. By contrast, hyphae of the related Monilinia fructicola, which is nonpathogenic on blueberry and does not cause gynoecial infection, adhered indiscriminately to the entire membrane. Using monoclonal antibodies, the presence of epitopes of esterified and unesterified pectins and of arabinogalactan proteins (AGPs), which have been implicated in adhesion and pollen tube guidance in other plant species, was documented on blueberry pollen tubes in vitro. Epitopes of certain AGPs, but not of pectins, were also localized on conidia and hyphae of M. vaccinii-corymbosi. However, such epitopes were also detected on M. fructicola, suggesting that they are unlikely to be a discriminatory factor between fungi capable or not capable of gynoecial infection. Microscopic observation of inoculated pistils showed that similar to pollen tubes, hyphae of M. vaccinii-corymbosi tracked the lobes of the stylar lumen, grew directionally (i.e. with very limited branching) in close proximity to cells of the stylar adaxial epidermis and to one another, and were surrounded by extracellular matrix. By contrast, hyphae of M. fructicola, while being able to ingress into the style, branched profusely within the stylar canal, showing no directional growth or affinity to specific regions of the lumen. We propose these results as evidence of specialized opportunism by M. vaccinii-corymbosi, whereby fungal hyphae appear to mimic host pollen tubes and take advantage of an infrastructure intended to support host reproduction in order to facilitate infection of the ovary.