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Invertebrate Microbiology | Spotlight

Two Photolyases Repair Distinct DNA Lesions and Reactivate UVB-Inactivated Conidia of an Insect Mycopathogen under Visible Light

Ding-Yi Wang, Bo Fu, Sen-Miao Tong, Sheng-Hua Ying, Ming-Guang Feng
Karyn N. Johnson, Editor
Ding-Yi Wang
Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China
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Bo Fu
College of Agricultural and Food Science, Zhejiang A&F University, Lin’an, Zhejiang, China
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Sen-Miao Tong
Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, ChinaCollege of Agricultural and Food Science, Zhejiang A&F University, Lin’an, Zhejiang, China
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Sheng-Hua Ying
Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China
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Ming-Guang Feng
Institute of Microbiology, College of Life Sciences, Zhejiang University, Hangzhou, Zhejiang, China
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  • ORCID record for Ming-Guang Feng
Karyn N. Johnson
University of Queensland
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DOI: 10.1128/AEM.02459-18
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ABSTRACT

Fungal conidia serve as active ingredients of fungal insecticides but are sensitive to solar UV irradiation, which impairs double-stranded DNA (dsDNA) by inducing the production of cytotoxic cyclobutane pyrimidine dimers (CPDs) and (6-4)-pyrimidine-pyrimidine photoproducts (6-4PPs). This study aims to elucidate how CPD photolyase (Phr1) and 6-4PP photolyase (Phr2) repair DNA damage and photoreactivate UVB-inactivated cells in Beauveria bassiana, a main source of fungal insecticides. Both Phr1 and Phr2 are proven to exclusively localize in the fungal nuclei. Despite little influence on growth, conidiation, and virulence, singular deletions of phr1 and phr2 resulted in respective reductions of 38% and 19% in conidial tolerance to UVB irradiation, a sunlight component most harmful to formulated conidia. CPDs and 6-4PPs accumulated significantly more in the cells of Δphr1 and Δphr2 mutants than in those of a wild-type strain under lethal UVB irradiation and were largely or completely repaired by Phr1 in the Δphr2 mutant and Phr2 in the Δphr1 mutant after optimal 5-h exposure to visible light. Consequently, UVB-inactivated conidia of the Δphr1 and Δphr2 mutants were much less efficiently photoreactivated than were the wild-type counterparts. In contrast, overexpression of either phr1 or phr2 in the wild-type strain resulted in marked increases in both conidial UVB resistance and photoreactivation efficiency. These findings indicate essential roles of Phr1 and Phr2 in photoprotection of B. bassiana from UVB damage and unveil exploitable values of both photolyase genes for improved UVB resistance and application strategy of fungal insecticides.

IMPORTANCE Protecting fungal cells from damage from solar UVB irradiation is critical for development and application of fungal insecticides but is mechanistically not understood in Beauveria bassiana, a classic insect pathogen. We unveil that two intranuclear photolyases, Phr1 and Phr2, play essential roles in repairing UVB-induced dsDNA lesions through respective decomposition of cytotoxic cyclobutane pyrimidine dimers and (6-4)-pyrimidine-pyrimidine photoproducts, hence reactivating UVB-inactivated cells effectively under visible light. Our findings shed light on the high potential of both photolyase genes for use in improving UVB resistance and application strategy of fungal insecticides.

FOOTNOTES

    • Received 7 October 2018.
    • Accepted 26 November 2018.
    • Accepted manuscript posted online 14 December 2018.
  • Supplemental material for this article may be found at https://doi.org/10.1128/AEM.02459-18.

  • Copyright © 2019 American Society for Microbiology.

All Rights Reserved.

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Two Photolyases Repair Distinct DNA Lesions and Reactivate UVB-Inactivated Conidia of an Insect Mycopathogen under Visible Light
Ding-Yi Wang, Bo Fu, Sen-Miao Tong, Sheng-Hua Ying, Ming-Guang Feng
Appl. Environ. Microbiol. Feb 2019, 85 (4) e02459-18; DOI: 10.1128/AEM.02459-18

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Two Photolyases Repair Distinct DNA Lesions and Reactivate UVB-Inactivated Conidia of an Insect Mycopathogen under Visible Light
Ding-Yi Wang, Bo Fu, Sen-Miao Tong, Sheng-Hua Ying, Ming-Guang Feng
Appl. Environ. Microbiol. Feb 2019, 85 (4) e02459-18; DOI: 10.1128/AEM.02459-18
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KEYWORDS

DNA damage repair
entomopathogenic fungi
UV resistance
biological control potential
gene expression and regulation
photolyase
photoreactivation

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