Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens

Eukaryotic translation initiation factor 4E (eIF4E) plays a key role in the infection of potyviruses in susceptible plants by interacting with viral genome-linked protein (VPg). Sugarcane (<i>Saccharum</i> spp.) production is threatened by mosaic disease caused by <i>Sugarcane mosa...

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Main Authors: Zongtao Yang, Meng Dong, Guangyuan Cheng, Shuxian Liu, Hai Zhang, Heyang Shang, Yingshuan Zhou, Guoqiang Huang, Muqing Zhang, Fengji Wang, Jingsheng Xu
Format: Article
Language:English
Published: MDPI AG 2021-03-01
Series:Viruses
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Online Access:https://www.mdpi.com/1999-4915/13/3/518
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author Zongtao Yang
Meng Dong
Guangyuan Cheng
Shuxian Liu
Hai Zhang
Heyang Shang
Yingshuan Zhou
Guoqiang Huang
Muqing Zhang
Fengji Wang
Jingsheng Xu
author_facet Zongtao Yang
Meng Dong
Guangyuan Cheng
Shuxian Liu
Hai Zhang
Heyang Shang
Yingshuan Zhou
Guoqiang Huang
Muqing Zhang
Fengji Wang
Jingsheng Xu
author_sort Zongtao Yang
collection DOAJ
description Eukaryotic translation initiation factor 4E (eIF4E) plays a key role in the infection of potyviruses in susceptible plants by interacting with viral genome-linked protein (VPg). Sugarcane (<i>Saccharum</i> spp.) production is threatened by mosaic disease caused by <i>Sugarcane mosaic virus</i> (SCMV), <i>Sorghum mosaic virus</i> (SrMV), and <i>Sugarcane streak mosaic virus</i> (SCSMV). In this study, two <i>eIF4Es</i> and their isoform <i>eIF(iso)4E</i> and 4E-binding protein coding genes were cloned from sugarcane cultivar <i>ROC22</i> and designated <i>SceIF4Ea</i>, <i>SceIF4Eb</i>, <i>SceIF(iso)4E,</i> and <i>ScnCBP</i>, respectively. Real-time quantitative PCR analysis showed different expression profiles of these four genes upon SCMV challenge. A subcellular localization assay showed that SceIF4Ea, SceIF4Eb, SceIF(iso)4E, and ScnCBP were distributed in the nucleus and cytoplasm. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays showed that SceIF4Ea/b and SceIF(iso)4E were selectively employed by different sugarcane mosaic pathogens, i.e., SCMV-VPg interacted with SceIF4Ea/b and SceIF(iso)4E, SrMV-VPg interacted with both SceIF4Eb and SceIF(iso)4E, and SCSMV-VPg interacted only with SceIF(iso)4E. Intriguingly, the BiFC assays, but not the Y2H assays, showed that ScnCBP interacted with the VPgs of SCMV, SrMV, and SCSMV. Competitive interaction assays showed that SCMV-VPg, SrMV-VPg, and SCMV-VPg did not compete with each other to interact with SceIF(iso)4E, and SceIF(iso)4E competed with SceIF4Eb to interact with SrMV-VPg but not SCMV-VPg. This study sheds light on the molecular mechanism of sugarcane mosaic pathogen infection of sugarcane plants and benefits sugarcane breeding against the sugarcane mosaic disease.
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spelling doaj.art-77d77fc2b92c458199539aec5c18aada2023-11-21T11:30:34ZengMDPI AGViruses1999-49152021-03-0113351810.3390/v13030518Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic PathogensZongtao Yang0Meng Dong1Guangyuan Cheng2Shuxian Liu3Hai Zhang4Heyang Shang5Yingshuan Zhou6Guoqiang Huang7Muqing Zhang8Fengji Wang9Jingsheng Xu10National Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaState Key Laboratory for Conservation and Utilization of Agro-Bioresources, Guangxi Key Laboratory for Sugarcane Biology, Guangxi University, Nanning 530005, ChinaKey Laboratory of Ministry of Education for Genetics, Breeding and Multiple Utilization of Crops, College of Crop Science, Fujian Agriculture and Forestry University, Jinshan, Fuzhou 350002, ChinaNational Engineering Research Center for Sugarcane & Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture and Rural Affairs, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaEukaryotic translation initiation factor 4E (eIF4E) plays a key role in the infection of potyviruses in susceptible plants by interacting with viral genome-linked protein (VPg). Sugarcane (<i>Saccharum</i> spp.) production is threatened by mosaic disease caused by <i>Sugarcane mosaic virus</i> (SCMV), <i>Sorghum mosaic virus</i> (SrMV), and <i>Sugarcane streak mosaic virus</i> (SCSMV). In this study, two <i>eIF4Es</i> and their isoform <i>eIF(iso)4E</i> and 4E-binding protein coding genes were cloned from sugarcane cultivar <i>ROC22</i> and designated <i>SceIF4Ea</i>, <i>SceIF4Eb</i>, <i>SceIF(iso)4E,</i> and <i>ScnCBP</i>, respectively. Real-time quantitative PCR analysis showed different expression profiles of these four genes upon SCMV challenge. A subcellular localization assay showed that SceIF4Ea, SceIF4Eb, SceIF(iso)4E, and ScnCBP were distributed in the nucleus and cytoplasm. Yeast two-hybrid (Y2H) and bimolecular fluorescence complementation (BiFC) assays showed that SceIF4Ea/b and SceIF(iso)4E were selectively employed by different sugarcane mosaic pathogens, i.e., SCMV-VPg interacted with SceIF4Ea/b and SceIF(iso)4E, SrMV-VPg interacted with both SceIF4Eb and SceIF(iso)4E, and SCSMV-VPg interacted only with SceIF(iso)4E. Intriguingly, the BiFC assays, but not the Y2H assays, showed that ScnCBP interacted with the VPgs of SCMV, SrMV, and SCSMV. Competitive interaction assays showed that SCMV-VPg, SrMV-VPg, and SCMV-VPg did not compete with each other to interact with SceIF(iso)4E, and SceIF(iso)4E competed with SceIF4Eb to interact with SrMV-VPg but not SCMV-VPg. This study sheds light on the molecular mechanism of sugarcane mosaic pathogen infection of sugarcane plants and benefits sugarcane breeding against the sugarcane mosaic disease.https://www.mdpi.com/1999-4915/13/3/518eIF4EVPgSCMVSrMVSCSMV
spellingShingle Zongtao Yang
Meng Dong
Guangyuan Cheng
Shuxian Liu
Hai Zhang
Heyang Shang
Yingshuan Zhou
Guoqiang Huang
Muqing Zhang
Fengji Wang
Jingsheng Xu
Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
Viruses
eIF4E
VPg
SCMV
SrMV
SCSMV
title Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
title_full Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
title_fullStr Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
title_full_unstemmed Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
title_short Selective Interaction of Sugarcane eIF4E with VPgs from Sugarcane Mosaic Pathogens
title_sort selective interaction of sugarcane eif4e with vpgs from sugarcane mosaic pathogens
topic eIF4E
VPg
SCMV
SrMV
SCSMV
url https://www.mdpi.com/1999-4915/13/3/518
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