Ceratocystis fimbriata employs a unique infection strategy targeting peltate glandular trichomes of sweetpotato (Ipomoea batatas) plants

The infection processes of Ceratocystis fimbriata BMPZ13 (Cf BMPZ13) was elucidated on vegetative tissues of sweetpotato plants employing light and scanning electron microscopy. Vegetative tissues infected with Cf BMPZ13 by either wounding or non-wounding inoculation methods developed typical disease symptoms, establishing black rot in stems and necrosis on buds, young leaves, and stems of sprouts, in addition to wilt on leaves and shoot cuttings, typical of vascular associated diseases. The runner hyphae of Cf BMPZ13 formed from germinated conidia were able to directly penetrate the epidermal cuticle for initial infection and invade sweetpotato peltate glandular trichomes (PGT), specialized secretory structures to store and secrete metabolites. A two-step biotrophic phase was observed with non-wounding inoculation on leaves and stems, featuring both intercellular and intracellular invasive hyphae (IH), with the latter found within living cells of the leaf epidermis. Subsequent to the biotrophic phase was a necrotrophic phase displaying cell death in infected leaves and veins. Additionally, this cell death was an iron-associated ferroptosis, supporting the notion that iron is involved in the necrotrophic phase of Cf BMPZ13 infection. Significantly, we establish that C. fimbriata employs a unique infection strategy: the targeting of peltate glandular trichomes. Collectively, our findings show that C. fimbriata is a plant fungal pathogen with a hemibiotrophic infection style in sweetpotato vegetative tissues.