Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>

Quinone outside inhibitor fungicides (QoIs) are crucial fungicides for controlling plant diseases, but resistance, mainly caused by G143A, has been widely reported with the high and widespread use of QoIs. However, two phenotypes of <i>Corynespora casiicola</i> (RI and RII) with the same...

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Main Authors: Bingxue Sun, Rongjia Zhou, Guangxue Zhu, Xuewen Xie, Ali Chai, Lei Li, Tengfei Fan, Baoju Li, Yanxia Shi
Format: Article
Language:English
Published: MDPI AG 2023-11-01
Series:Microorganisms
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Online Access:https://www.mdpi.com/2076-2607/11/12/2849
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author Bingxue Sun
Rongjia Zhou
Guangxue Zhu
Xuewen Xie
Ali Chai
Lei Li
Tengfei Fan
Baoju Li
Yanxia Shi
author_facet Bingxue Sun
Rongjia Zhou
Guangxue Zhu
Xuewen Xie
Ali Chai
Lei Li
Tengfei Fan
Baoju Li
Yanxia Shi
author_sort Bingxue Sun
collection DOAJ
description Quinone outside inhibitor fungicides (QoIs) are crucial fungicides for controlling plant diseases, but resistance, mainly caused by G143A, has been widely reported with the high and widespread use of QoIs. However, two phenotypes of <i>Corynespora casiicola</i> (RI and RII) with the same G143A showed significantly different resistance to QoIs in our previous study, which did not match the reported mechanisms. Therefore, transcriptome analysis of RI and RII strains after trifloxystrobin treatment was used to explore the new resistance mechanism in this study. The results show that 332 differentially expressed genes (DEGs) were significantly up-regulated and 448 DEGs were significantly down-regulated. The results of GO and KEGG enrichment showed that DEGs were most enriched in ribosomes, while also having enrichment in peroxide, endocytosis, the lysosome, autophagy, and mitophagy. In particular, mitophagy and peroxisome have been reported in medicine as the main mechanisms of reactive oxygen species (ROS) scavenging, while the lysosome and endocytosis are an important organelle and physiological process, respectively, that assist mitophagy. The oxidative stress experiments showed that the oxidative stress resistance of the RII strains was significantly higher than that of the RI strains: specifically, it was more than 1.8-fold higher at a concentration of 0.12% H<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mrow></mrow><mn>2</mn></msub></semantics></math></inline-formula>O<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mrow></mrow><mn>2</mn></msub></semantics></math></inline-formula>. This indicates that there is indeed a significant difference in the scavenging capacity of ROS between the two phenotypic strains. Therefore, we suggest that QoIs’ action caused a high production of ROS, and that scavenging mechanisms such as mitophagy and peroxisomes functioned in RII strains to prevent oxidative stress, whereas RI strains were less capable of resisting oxidative stress, resulting in different resistance to QoIs. In this study, it was first revealed that mitophagy and peroxisome mechanisms available for ROS scavenging are involved in the resistance of pathogens to fungicides.
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spelling doaj.art-d3855f17833c44788d7b8df45c1627ae2023-12-22T14:25:43ZengMDPI AGMicroorganisms2076-26072023-11-011112284910.3390/microorganisms11122849Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>Bingxue Sun0Rongjia Zhou1Guangxue Zhu2Xuewen Xie3Ali Chai4Lei Li5Tengfei Fan6Baoju Li7Yanxia Shi8State Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaState Key Laboratory of Vegetable Biobreeding, Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing 100081, ChinaQuinone outside inhibitor fungicides (QoIs) are crucial fungicides for controlling plant diseases, but resistance, mainly caused by G143A, has been widely reported with the high and widespread use of QoIs. However, two phenotypes of <i>Corynespora casiicola</i> (RI and RII) with the same G143A showed significantly different resistance to QoIs in our previous study, which did not match the reported mechanisms. Therefore, transcriptome analysis of RI and RII strains after trifloxystrobin treatment was used to explore the new resistance mechanism in this study. The results show that 332 differentially expressed genes (DEGs) were significantly up-regulated and 448 DEGs were significantly down-regulated. The results of GO and KEGG enrichment showed that DEGs were most enriched in ribosomes, while also having enrichment in peroxide, endocytosis, the lysosome, autophagy, and mitophagy. In particular, mitophagy and peroxisome have been reported in medicine as the main mechanisms of reactive oxygen species (ROS) scavenging, while the lysosome and endocytosis are an important organelle and physiological process, respectively, that assist mitophagy. The oxidative stress experiments showed that the oxidative stress resistance of the RII strains was significantly higher than that of the RI strains: specifically, it was more than 1.8-fold higher at a concentration of 0.12% H<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mrow></mrow><mn>2</mn></msub></semantics></math></inline-formula>O<inline-formula><math xmlns="http://www.w3.org/1998/Math/MathML" display="inline"><semantics><msub><mrow></mrow><mn>2</mn></msub></semantics></math></inline-formula>. This indicates that there is indeed a significant difference in the scavenging capacity of ROS between the two phenotypic strains. Therefore, we suggest that QoIs’ action caused a high production of ROS, and that scavenging mechanisms such as mitophagy and peroxisomes functioned in RII strains to prevent oxidative stress, whereas RI strains were less capable of resisting oxidative stress, resulting in different resistance to QoIs. In this study, it was first revealed that mitophagy and peroxisome mechanisms available for ROS scavenging are involved in the resistance of pathogens to fungicides.https://www.mdpi.com/2076-2607/11/12/2849mitophagyperoxisomereactive oxygen species
spellingShingle Bingxue Sun
Rongjia Zhou
Guangxue Zhu
Xuewen Xie
Ali Chai
Lei Li
Tengfei Fan
Baoju Li
Yanxia Shi
Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
Microorganisms
mitophagy
peroxisome
reactive oxygen species
title Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
title_full Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
title_fullStr Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
title_full_unstemmed Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
title_short Transcriptome Analysis Reveals the Involvement of Mitophagy and Peroxisome in the Resistance to QoIs in <i>Corynespora cassiicola</i>
title_sort transcriptome analysis reveals the involvement of mitophagy and peroxisome in the resistance to qois in i corynespora cassiicola i
topic mitophagy
peroxisome
reactive oxygen species
url https://www.mdpi.com/2076-2607/11/12/2849
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