Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus
Many of the recessive virus-resistance genes in plants encode eukaryotic translation initiation factors (eIFs), including eIF4E, eIF4G, and related proteins. Notably, eIF4E and its isoform eIF(iso)4E are pivotal for viral infection and act as recessive resistance genes against various potyviruses in...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-07-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fpls.2020.01098/full |
| _version_ | 1818445862115737600 |
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| author | Yoo-Joung Yoon Jelli Venkatesh Joung-Ho Lee Jinhee Kim Hye-Eun Lee Do-Sun Kim Byoung-Cheorl Kang |
| author_facet | Yoo-Joung Yoon Jelli Venkatesh Joung-Ho Lee Jinhee Kim Hye-Eun Lee Do-Sun Kim Byoung-Cheorl Kang |
| author_sort | Yoo-Joung Yoon |
| collection | DOAJ |
| description | Many of the recessive virus-resistance genes in plants encode eukaryotic translation initiation factors (eIFs), including eIF4E, eIF4G, and related proteins. Notably, eIF4E and its isoform eIF(iso)4E are pivotal for viral infection and act as recessive resistance genes against various potyviruses in a wide range of plants. In this study, we used Clustered Regularly Interspaced Palindromic Repeats/CRISPR-associated protein 9 (CRISPR/Cas9)-mediated targeted mutagenesis to test whether novel sequence-specific mutations at eIF4E1 in Solanum lycopersicum (tomato) cv. Micro-Tom could confer enhanced resistance to potyviruses. This approach produced heritable homozygous mutations in the transgene-free E1 generation. Sequence analysis of eIF4E1 from E0 transgenic plants expressing Cas9 and eIF4E-sgRNA transcripts identified chimeric deletions ranging from 11 to 43 bp. Genotype analysis of the eIF4E1-edited lines in E0, E1, and E2 transgenic tomato plants showed that the mutations were transmitted to subsequent generations. When homozygous mutant lines were tested for resistance to potyviruses, they exhibited no resistance to tobacco etch virus (TEV). Notably, however, several mutant lines showed no accumulation of viral particles upon infection with pepper mottle virus (PepMoV). These results indicate that site-specific mutation of tomato eIF4E1 successfully conferred enhanced resistance to PepMoV. Thus, this study demonstrates the feasibility of the use of CRISPR/Cas9 approach to accelerate breeding for trait improvement in tomato plants. |
| first_indexed | 2024-12-14T19:38:34Z |
| format | Article |
| id | doaj.art-65f458e480b74f928a38ad4735c2317c |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-14T19:38:34Z |
| publishDate | 2020-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-65f458e480b74f928a38ad4735c2317c2022-12-21T22:49:46ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2020-07-011110.3389/fpls.2020.01098564004Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle VirusYoo-Joung Yoon0Jelli Venkatesh1Joung-Ho Lee2Jinhee Kim3Hye-Eun Lee4Do-Sun Kim5Byoung-Cheorl Kang6Department of Plant Science and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, South KoreaDepartment of Plant Science and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, South KoreaDepartment of Plant Science and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, South KoreaVegetable Research Division, National Institute of Horticultural and Herbal Science, RDA, Jeonju-si, South KoreaVegetable Research Division, National Institute of Horticultural and Herbal Science, RDA, Jeonju-si, South KoreaVegetable Research Division, National Institute of Horticultural and Herbal Science, RDA, Jeonju-si, South KoreaDepartment of Plant Science and Plant Genomics and Breeding Institute, College of Agriculture and Life Sciences, Seoul National University, Seoul, South KoreaMany of the recessive virus-resistance genes in plants encode eukaryotic translation initiation factors (eIFs), including eIF4E, eIF4G, and related proteins. Notably, eIF4E and its isoform eIF(iso)4E are pivotal for viral infection and act as recessive resistance genes against various potyviruses in a wide range of plants. In this study, we used Clustered Regularly Interspaced Palindromic Repeats/CRISPR-associated protein 9 (CRISPR/Cas9)-mediated targeted mutagenesis to test whether novel sequence-specific mutations at eIF4E1 in Solanum lycopersicum (tomato) cv. Micro-Tom could confer enhanced resistance to potyviruses. This approach produced heritable homozygous mutations in the transgene-free E1 generation. Sequence analysis of eIF4E1 from E0 transgenic plants expressing Cas9 and eIF4E-sgRNA transcripts identified chimeric deletions ranging from 11 to 43 bp. Genotype analysis of the eIF4E1-edited lines in E0, E1, and E2 transgenic tomato plants showed that the mutations were transmitted to subsequent generations. When homozygous mutant lines were tested for resistance to potyviruses, they exhibited no resistance to tobacco etch virus (TEV). Notably, however, several mutant lines showed no accumulation of viral particles upon infection with pepper mottle virus (PepMoV). These results indicate that site-specific mutation of tomato eIF4E1 successfully conferred enhanced resistance to PepMoV. Thus, this study demonstrates the feasibility of the use of CRISPR/Cas9 approach to accelerate breeding for trait improvement in tomato plants.https://www.frontiersin.org/article/10.3389/fpls.2020.01098/fullCRISPR/Cas9eukaryotic translation initiation factor 4E (eIF4E)genome editingpotyvirusphytoene desaturase (PDS)Solanum lycopersicum cv. Micro-Tom |
| spellingShingle | Yoo-Joung Yoon Jelli Venkatesh Joung-Ho Lee Jinhee Kim Hye-Eun Lee Do-Sun Kim Byoung-Cheorl Kang Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus Frontiers in Plant Science CRISPR/Cas9 eukaryotic translation initiation factor 4E (eIF4E) genome editing potyvirus phytoene desaturase (PDS) Solanum lycopersicum cv. Micro-Tom |
| title | Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus |
| title_full | Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus |
| title_fullStr | Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus |
| title_full_unstemmed | Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus |
| title_short | Genome Editing of eIF4E1 in Tomato Confers Resistance to Pepper Mottle Virus |
| title_sort | genome editing of eif4e1 in tomato confers resistance to pepper mottle virus |
| topic | CRISPR/Cas9 eukaryotic translation initiation factor 4E (eIF4E) genome editing potyvirus phytoene desaturase (PDS) Solanum lycopersicum cv. Micro-Tom |
| url | https://www.frontiersin.org/article/10.3389/fpls.2020.01098/full |
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