Autophagy-related protein PlATG2 regulates the vegetative growth, sporangial cleavage, autophagosome formation, and pathogenicity of peronophythora litchii

ABSTRACT

Autophagy is an intracellular degradation process that is important for the development and pathogenicity of phytopathogenic fungi and for the defence response of plants. However, the molecular mechanisms underlying autophagy in the pathogenicity of the plant pathogenic oomycete Peronophythora litchii, the causal agent of litchi downy blight, have not been well characterized. In this study, the autophagy-related protein ATG2 homolog, PlATG2, was identified and characterized using a CRISPR/Cas9-mediated gene replacement strategy in P. litchii. A monodansylcadaverine (MDC) staining assay indicated that deletion of PlATG2 abolished autophagosome formation. Infection assays demonstrated that ΔPlatg2 mutants showed significantly impaired pathogenicity in litchi leaves and fruits. Further studies have revealed that PlATG2 participates in radial growth and asexual/sexual development of P. litchii. Moreover, zoospore release and cytoplasmic cleavage of sporangia were considerably lower in the ΔPlatg2 mutants than in the wild-type strain by FM4–64 staining. Taken together, our results revealed that PlATG2 plays a pivotal role in vegetative growth, sporangia and oospore production, zoospore release, sporangial cleavage, and plant infection of P. litchii. This study advances our understanding of the pathogenicity mechanisms of the phytopathogenic oomycete P. litchii and is conducive to the development of effective control strategies.

KEYWORDS:

• Autophagy
• PlATG2
• sporangial cleavage
• autophagosome formation
• pathogenicity
• peronophythora litchii

Disclosure statement

No potential conflict of interest was reported by the author(s).

Author contributions

Conceptualization: Qinghe Chen.

Funding acquisition: Qinghe Chen.

Investigation: Lin Lv, Chengdong Yang, Xue Zhang, Taixu Chen, Manfei Luo, and Ge Yu.

Methodology: Lin Lv, Chengdong Yang, Qinghe Chen.

Project administration: Qinghe Chen.

Resources: Chengdong Yang, Qinghe Chen.

Software: Lin Lv, Chengdong Yang, Xue Zhang.

Supervision: Qinghe Chen, Chengdong Yang.

Formal analysis: Chengdong Yang, Lin Lv, Xue Zhang, Taixu Chen, Manfei Luo, Ge Yu.

Writing – original draft: Chengdong Yang, Lin Lv.

Writing – review & editing: Qinghe Chen, Chengdong Yang.

Data Availability statement

All datasets presented in this study are included in the article/SupplementaryMaterial.

Supplemental data

Supplemental data for this article can be accessed online at https://doi.org/10.1080/21505594.2024.2322183

Additional information

Funding

This work was supported by the Hainan Provincial Natural Science Foundation of China (321CXTD437), National Natural Science Foundation of China (32160614), and Scientific Research Foundation of Hainan University [KYQD(ZR)-20080].