Autophagy-related protein PlAtg3 participates in vegetative growth, sporangial cleavage, autophagy and pathogenicity of Peronophythora litchii

doi:10.1016/j.jia.2024.01.009

Journal of Integrative Agriculture

2024, Vol. 23

Issue (11): 3788-3800 DOI: 10.1016/j.jia.2024.01.009

Plant Protection

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Autophagy-related protein PlAtg3 participates in vegetative growth, sporangial cleavage, autophagy and pathogenicity of Peronophythora litchii

Chengdong Yang^{1, 2, 3*}, Manfei Luo^{1, 2*}, Xue Zhang^{1, 2}, Linlin Ye^{1, 2}, Ge Yu^{1, 2}, Yi Lü^{1, 2}, Yi Chen^{1, 2}, Taixu Chen^{1, 2}, Xuejian Wang^{1, 2}, Wanzhen Feng^{1, 2#}, Qinghe Chen^{1, 2#}

¹ School of Breeding and Multiplication (Sanya Institute of Breeding and Multiplication), Hainan University, Sanya 572025, China

² Key Laboratory of Green Prevention and Control of Tropical Plant Diseases and Pests of Ministry of Education, School of Tropical Agriculture and Forestry, Hainan University, Haikou 570228, China

³ Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests, Fuzhou 350013, China

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摘要由植物病原卵菌荔枝霜疫霉引起的荔枝霜疫病是荔枝上最具破坏性的病害之一，它的发生会给荔枝的生产带来巨大经济损失。研究表明，细胞自噬在病原真菌的生长发育和致病过程中发挥至关重要作用。然而，植物病原卵菌中有关细胞自噬的功能尚不清楚。为了探究细胞自噬在荔枝霜疫霉生长发育和致病过程中的作用。在本研究中，通过生物信息学分析鉴定到了一个酵母自噬相关蛋白Atg3的同源蛋白，命名为PlAtg3。利用CRISPR/Cas9基因编辑技术对其敲除和原位回补发现，PlATG3的缺失削弱了荔枝霜疫霉的营养生长和有性/无性发育。通过特异性自噬体染料单丹黄酰戊二胺（monodansylcadaverine，MDC）对自噬体染色发现，PlATG3突变体中自噬体数量明显低于野生型菌株。FM4-64染料对细胞膜染色发现PlATG3的缺失影响了孢子囊细胞质割裂而导致游动孢子释放率显著降低。Atg8被认为是各种物种中的自噬标记蛋白。Western blot分析显示PlAtg8-PE在PlATG3突变体中的积累较野生型增多，表明PlAtg3参与了PlAtg8-PE的降解。但是，与酵母中ScAtg3能与ScAtg8互作相比，酵母双杂交（yeast two hybrid，Y2H）结果显示荔枝霜疫霉中PlAtg3无法与PlAtg8互作，可能是由于PlAtg3中缺乏Atg8家族相互作用基序（Atg8 family interacting motif，AIM）。此外，致病性实验表明PlATG3的缺失显著降低了荔枝霜疫霉对荔枝叶片和果实的致病力。综上所述，我们的数据揭示了PlAtg3在荔枝霜疫霉的菌丝生长、有性/无性发育、孢子囊割裂和游动孢子释放、自噬体形成和致病过程中发挥至关重要作用。这项研究有助于更好地理解荔枝霜疫霉的致病机制，并为开发更有效的控制卵菌类病害的策略提供见解。

Abstract

Litchi downy blight, caused by the plant pathogenic oomycete Peronophythora litchii, is one of the most devastating diseases on litchi and resulted in huge economic losses. Autophagy plays an essential role in the development and pathogenicity of the filamentous fungi. However, the function of autophagy in oomycetes remain elusive. Here, an autophagy-related protein Atg3 homolog PlAtg3 was identified and characterized in P. litchii. The absence of PlATG3 through the CRISPR/Cas9 gene replacement strategy compromised vegetative growth and sexual/asexual development. Cytological analyses revealed that the deletion of PlATG3 impaired autophagosome formation with monodansylcadaverine (MDC) staining and significantly disrupted zoospore release due to defects of sporangial cleavage with FM4-64 staining. Atg8 is considered to be an autophagy marker protein in various species. Western blot analysis indicated that PlAtg3 is involved in degradation of PlAtg8-PE. Interestingly, PlAtg3 was unable to interact with PlAtg8 in yeast two hybrid (Y2H) assays, possibly due to the absence of the Atg8 family interacting motif (AIM) in PlAtg3. Furthermore, pathogenicity assays revealed that the deletion of PlATG3 considerably reduced the virulence of P. litchii. Taken together, our data reveal that PlAtg3 plays an important role in radial growth, asexual/sexual development, sporangial cleavage and zoospore release, autophagosome formation, and pathogenicity in P. litchii. This study contributes to a better understanding of the pathogenicity mechanisms of P. litchii and provides insights for the development of more effective strategies to control oomycete diseases.

Keywords: PlAtg3 sporangial cleavage autophagy pathogenicity Peronophythora litchii

Received: 25 September 2023 Accepted: 09 November 2023

Fund: This work was supported by the grants from the Hainan Provincial Natural Science Foundation, China (321QN190 and 321CXTD437), the National Natural Science Foundation of China (32202246 and 32160614), the Open Project Program of Fujian Key Laboratory for Monitoring and Integrated Management of Crop Pests, China (MIMCP-202102), and the Scientific Research Foundation of Hainan University, China (KYQD(ZR)-21042 and KYQD(ZR)-20080).

About author: Chengdong Yang, E-mail: Chengdy@hainanu.edu.cn; #Correspondence Qinghe Chen, E-mail: qhchen@hainanu.edu.cn; Wanzhen Feng, E-mail: fwz@hainanu.edu.cn * These authors contributed equally to this study.

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	Chengdong Yang
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	Taixu Chen
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	Wanzhen Feng
	Qinghe Chen

Cite this article:

Chengdong Yang, Manfei Luo, Xue Zhang, Linlin Ye, Ge Yu, Yi Lü, Yi Chen, Taixu Chen, Xuejian Wang, Wanzhen Feng, Qinghe Chen. 2024. Autophagy-related protein PlAtg3 participates in vegetative growth, sporangial cleavage, autophagy and pathogenicity of Peronophythora litchii. Journal of Integrative Agriculture, 23(11): 3788-3800.

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