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Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells
Virulent Agrobacterium tumefaciens strains integrate their T-DNA into the plant genome where the encoded agrobacterial oncogenes are expressed and cause crown gall disease. Essential for crown gall development are IaaH (indole-3-acetamide hydrolase), IaaM (tryptophan monooxygenase) and Ipt (isopente...
Autores principales: | , , , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4304707/ https://www.ncbi.nlm.nih.gov/pubmed/25615824 http://dx.doi.org/10.1371/journal.ppat.1004620 |
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author | Zhang, Yi Lee, Chil-Woo Wehner, Nora Imdahl, Fabian Svetlana, Veselova Weiste, Christoph Dröge-Laser, Wolfgang Deeken, Rosalia |
author_facet | Zhang, Yi Lee, Chil-Woo Wehner, Nora Imdahl, Fabian Svetlana, Veselova Weiste, Christoph Dröge-Laser, Wolfgang Deeken, Rosalia |
author_sort | Zhang, Yi |
collection | PubMed |
description | Virulent Agrobacterium tumefaciens strains integrate their T-DNA into the plant genome where the encoded agrobacterial oncogenes are expressed and cause crown gall disease. Essential for crown gall development are IaaH (indole-3-acetamide hydrolase), IaaM (tryptophan monooxygenase) and Ipt (isopentenyl transferase), which encode enzymes for the biosynthesis of auxin (IaaH, IaaM) and cytokinin (Ipt). Although these oncogenes are well studied as the tumor-inducing principle, nothing is known about the regulation of oncogene expression in plant cells. Our studies show that the intergenic regions (IGRs) between the coding sequences (CDS) of the three oncogenes function as promoters in plant cells. These promoters possess a eukaryotic sequence organization and cis-regulatory elements for the binding of plant transcription factors. WRKY18, WRKY40, WRKY60 and ARF5 were identified as activators of the Ipt promoter whereas IaaH and IaaM is constitutively expressed and no transcription factor further activates their promoters. Consistent with these results, the wrky triple mutant plants in particular, develops smaller crown galls than wild-type and exhibits a reduced Ipt transcription, despite the presence of an intact ARF5 gene. WRKY40 and WRKY60 gene expression is induced by A. tumefaciens within a few hours whereas the ARF5 gene is transcribed later during crown gall development. The WRKY proteins interact with ARF5 in the plant nucleus, but only WRKY40 together with ARF5 synergistically boosts the activation of the Ipt promoter in an auxin-dependent manner. From our data, we propose that A. tumefaciens initially induces WRKY40 gene expression as a pathogen defense response of the host cell. The WRKY protein is recruited to induce Ipt expression, which initiates cytokinin-dependent host cell division. With increasing auxin levels triggered by ubiquitous expression of IaaH and IaaM, ARF5 is activated and interacts with WRKY40 to potentiate Ipt expression and balance cytokinin and auxin levels for further cell proliferation. |
format | Online Article Text |
id | pubmed-4304707 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-43047072015-01-30 Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells Zhang, Yi Lee, Chil-Woo Wehner, Nora Imdahl, Fabian Svetlana, Veselova Weiste, Christoph Dröge-Laser, Wolfgang Deeken, Rosalia PLoS Pathog Research Article Virulent Agrobacterium tumefaciens strains integrate their T-DNA into the plant genome where the encoded agrobacterial oncogenes are expressed and cause crown gall disease. Essential for crown gall development are IaaH (indole-3-acetamide hydrolase), IaaM (tryptophan monooxygenase) and Ipt (isopentenyl transferase), which encode enzymes for the biosynthesis of auxin (IaaH, IaaM) and cytokinin (Ipt). Although these oncogenes are well studied as the tumor-inducing principle, nothing is known about the regulation of oncogene expression in plant cells. Our studies show that the intergenic regions (IGRs) between the coding sequences (CDS) of the three oncogenes function as promoters in plant cells. These promoters possess a eukaryotic sequence organization and cis-regulatory elements for the binding of plant transcription factors. WRKY18, WRKY40, WRKY60 and ARF5 were identified as activators of the Ipt promoter whereas IaaH and IaaM is constitutively expressed and no transcription factor further activates their promoters. Consistent with these results, the wrky triple mutant plants in particular, develops smaller crown galls than wild-type and exhibits a reduced Ipt transcription, despite the presence of an intact ARF5 gene. WRKY40 and WRKY60 gene expression is induced by A. tumefaciens within a few hours whereas the ARF5 gene is transcribed later during crown gall development. The WRKY proteins interact with ARF5 in the plant nucleus, but only WRKY40 together with ARF5 synergistically boosts the activation of the Ipt promoter in an auxin-dependent manner. From our data, we propose that A. tumefaciens initially induces WRKY40 gene expression as a pathogen defense response of the host cell. The WRKY protein is recruited to induce Ipt expression, which initiates cytokinin-dependent host cell division. With increasing auxin levels triggered by ubiquitous expression of IaaH and IaaM, ARF5 is activated and interacts with WRKY40 to potentiate Ipt expression and balance cytokinin and auxin levels for further cell proliferation. Public Library of Science 2015-01-23 /pmc/articles/PMC4304707/ /pubmed/25615824 http://dx.doi.org/10.1371/journal.ppat.1004620 Text en © 2015 Zhang et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited. |
spellingShingle | Research Article Zhang, Yi Lee, Chil-Woo Wehner, Nora Imdahl, Fabian Svetlana, Veselova Weiste, Christoph Dröge-Laser, Wolfgang Deeken, Rosalia Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title | Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title_full | Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title_fullStr | Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title_full_unstemmed | Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title_short | Regulation of Oncogene Expression in T-DNA-Transformed Host Plant Cells |
title_sort | regulation of oncogene expression in t-dna-transformed host plant cells |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4304707/ https://www.ncbi.nlm.nih.gov/pubmed/25615824 http://dx.doi.org/10.1371/journal.ppat.1004620 |
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