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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...

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Autores principales: Zhang, Yi, Lee, Chil-Woo, Wehner, Nora, Imdahl, Fabian, Svetlana, Veselova, Weiste, Christoph, Dröge-Laser, Wolfgang, Deeken, Rosalia
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
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.
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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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