BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease

Pear ring rot disease is an important branch disease, caused by <i>Botryosphaeria dothidea</i>. With the discovery of fungal viruses, the use of their attenuated properties for biological control provides a new strategy for the biological control of fungal disease. RNA silencing is a maj...

Full description

Bibliographic Details
Main Authors: Shanshan Li, Haodong Zhu, Ying He, Ni Hong, Guoping Wang, Liping Wang
Format: Article
Language:English
Published: MDPI AG 2023-09-01
Series:Cells
Subjects:
Online Access:https://www.mdpi.com/2073-4409/12/19/2386
_version_ 1797576057829720064
author Shanshan Li
Haodong Zhu
Ying He
Ni Hong
Guoping Wang
Liping Wang
author_facet Shanshan Li
Haodong Zhu
Ying He
Ni Hong
Guoping Wang
Liping Wang
author_sort Shanshan Li
collection DOAJ
description Pear ring rot disease is an important branch disease, caused by <i>Botryosphaeria dothidea</i>. With the discovery of fungal viruses, the use of their attenuated properties for biological control provides a new strategy for the biological control of fungal disease. RNA silencing is a major antiviral defense mechanism in plants, insects, and fungi. Viruses encode and utilize RNA silencing suppressors to suppress host defenses. Previous studies revealed that Botryosphaeria dothidea chrysovirus 1 (BdCV1) exhibited weak pathogenicity and could activate host gene silencing by infecting <i>B. dothidea</i>. The aim of our study was to investigate whether BdCV1 can encode a silencing suppressor and what effect it has on the host. In this study, the capability of silencing inhibitory activity of four BdCV1-encoded proteins was analyzed, and the P3 protein was identified as a BdCV1 RNA silencing suppressor in the exotic host <i>Nicotiana benthamiana</i> line 16c. In addition, we demonstrated that P3 could inhibit local silencing, block systemic RNA silencing, and induce the necrosis reaction of tobacco leaves. Furthermore, overexpression of P3 could slow down the growth rate and reduce the pathogenicity of <i>B. dothidea</i>, and to some extent affect the expression level of RNA silencing components and virus-derived siRNAs (vsiRNAs). Combined with transcriptomic analysis, P3 had an effect on the gene expression and biological process of <i>B. dothidea</i>. The obtained results provide new theoretical information for further study of interaction between BdCV1 P3 as a potential silencing suppressor and <i>B. dothidea</i>.
first_indexed 2024-03-10T21:48:04Z
format Article
id doaj.art-d9affb09117b4de58af30d44e1454f9c
institution Directory Open Access Journal
issn 2073-4409
language English
last_indexed 2024-03-10T21:48:04Z
publishDate 2023-09-01
publisher MDPI AG
record_format Article
series Cells
spelling doaj.art-d9affb09117b4de58af30d44e1454f9c2023-11-19T14:13:05ZengMDPI AGCells2073-44092023-09-011219238610.3390/cells12192386BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot DiseaseShanshan Li0Haodong Zhu1Ying He2Ni Hong3Guoping Wang4Liping Wang5College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaCollege of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, ChinaPear ring rot disease is an important branch disease, caused by <i>Botryosphaeria dothidea</i>. With the discovery of fungal viruses, the use of their attenuated properties for biological control provides a new strategy for the biological control of fungal disease. RNA silencing is a major antiviral defense mechanism in plants, insects, and fungi. Viruses encode and utilize RNA silencing suppressors to suppress host defenses. Previous studies revealed that Botryosphaeria dothidea chrysovirus 1 (BdCV1) exhibited weak pathogenicity and could activate host gene silencing by infecting <i>B. dothidea</i>. The aim of our study was to investigate whether BdCV1 can encode a silencing suppressor and what effect it has on the host. In this study, the capability of silencing inhibitory activity of four BdCV1-encoded proteins was analyzed, and the P3 protein was identified as a BdCV1 RNA silencing suppressor in the exotic host <i>Nicotiana benthamiana</i> line 16c. In addition, we demonstrated that P3 could inhibit local silencing, block systemic RNA silencing, and induce the necrosis reaction of tobacco leaves. Furthermore, overexpression of P3 could slow down the growth rate and reduce the pathogenicity of <i>B. dothidea</i>, and to some extent affect the expression level of RNA silencing components and virus-derived siRNAs (vsiRNAs). Combined with transcriptomic analysis, P3 had an effect on the gene expression and biological process of <i>B. dothidea</i>. The obtained results provide new theoretical information for further study of interaction between BdCV1 P3 as a potential silencing suppressor and <i>B. dothidea</i>.https://www.mdpi.com/2073-4409/12/19/2386<i>Botryosphaeria dothidea</i>RNA silencingBdCV1RNA silencing suppressors
spellingShingle Shanshan Li
Haodong Zhu
Ying He
Ni Hong
Guoping Wang
Liping Wang
BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
Cells
<i>Botryosphaeria dothidea</i>
RNA silencing
BdCV1
RNA silencing suppressors
title BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
title_full BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
title_fullStr BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
title_full_unstemmed BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
title_short BdCV1-Encoded P3 Silencing Suppressor Identification and Its Roles in <i>Botryosphaeria dothidea</i>, Causing Pear Ring Rot Disease
title_sort bdcv1 encoded p3 silencing suppressor identification and its roles in i botryosphaeria dothidea i causing pear ring rot disease
topic <i>Botryosphaeria dothidea</i>
RNA silencing
BdCV1
RNA silencing suppressors
url https://www.mdpi.com/2073-4409/12/19/2386
work_keys_str_mv AT shanshanli bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease
AT haodongzhu bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease
AT yinghe bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease
AT nihong bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease
AT guopingwang bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease
AT lipingwang bdcv1encodedp3silencingsuppressoridentificationanditsrolesinibotryosphaeriadothideaicausingpearringrotdisease