Ceratocystis fimbriata Employs a Unique Infection Strategy Targeting Peltate Glandular Trichomes of Sweetpotato (Ipomoea batatas) Plants

Author:

Sun Yong1,Li Mengqiu1,Wang Yansu1,Li Lianwei1,Wang Meng1,Li Xintong1,Xu Mengke1,Loake Gary J.23,Guo Ming1ORCID,Jiang Jihong12

Affiliation:

1. The Key Laboratory of Biotechnology for Medicinal Plants of Jiangsu Province, Jiangsu Normal University, Xuzhou 221116, Jiangsu, P.R. China

2. Jiangsu Normal University−Edinburgh University, Centre for Transformative Biotechnology of Medicinal and Food Plants, Jiangsu Normal University, 101 Shanghai Road, Xuzhou, P.R. China

3. Institute of Molecular Plant Sciences, School of Biological Sciences, Edinburgh University, King’s Buildings, Mayfield Road, Edinburgh EH9 3JR, U.K.

Abstract

The infection processes of Ceratocystis fimbriata BMPZ13 (BMPZ13) was elucidated on vegetative tissues of sweetpotato plants employing light and scanning electron microscopy. Vegetative tissues infected with C. fimbriata BMPZ13 by either wounding or nonwounding 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 C. fimbriata BMPZ13 formed from germinated conidia were able to directly penetrate the epidermal cuticle for initial infection and invade sweetpotato peltate glandular trichomes, specialized secretory structures to store and secrete metabolites. A two-step biotrophic phase was observed with nonwounding inoculation on leaves and stems, featuring both intercellular and intracellular invasive hyphae, 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 C. fimbriata 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.

Funder

National Natural Science Foundation of China

Natural Science Foundation of Jiangsu Province

Publisher

Scientific Societies

Subject

Plant Science,Agronomy and Crop Science

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