Reports

Trojan Horse Strategy in Agrobacterium Transformation: Abusing MAPK Defense Signaling

Armin Djamei,^1* Andrea Pitzschke,¹ Hirofumi Nakagami,¹ Iva Rajh,¹ Heribert Hirt^1,2

Nuclear import of transfer DNA (T-DNA) is a central event in Agrobacterium transformation of plant cells and is thought to occur by the hijacking of certain host cell proteins. The T-DNA–associated virulence protein VirE2 mediates this process by binding to the nuclear import machinery via the host cell factor VIP1, whose role in plants has been so far unknown. Here we show that VIP1 is a transcription factor that is a direct target of the Agrobacterium-induced mitogen-activated protein kinase (MAPK) MPK3. Upon phosphorylation by MPK3, VIP1 relocalizes from the cytoplasm to the nucleus and regulates the expression of the PR1 pathogenesis-related gene. MAPK-dependent phosphorylation of VIP1 is necessary for VIP1-mediated Agrobacterium T-DNA transfer, indicating that Agrobacterium abuses the MAPK-targeted VIP1 defense signaling pathway for nuclear delivery of the T-DNA complex as a Trojan horse.

¹ Department of Plant Molecular Biology, Max F. Perutz Laboratories, University of Vienna, Dr.-Bohr-Gasse 9, 1030 Vienna, Austria.
² URGV Plant Genomics Laboratory, 2 Rue Gaston Crémieux, 91057 Evry, France.

^* Present address: Department of Organismic Interactions, Max-Planck-Institut für terrestrische Mikrobiologie, Karlvon-Frisch-Strasse, 35043 Marburg, Germany.

These authors contributed equally to this work.

Present address: Plant Immunity Research Team, RIKEN Plant Science Center, 1-7-22 Suehiro-cho, Tsurumi, Yokohama 230-0045, Japan.

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VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression.

A. Pitzschke, A. Djamei, M. Teige, and H. Hirt (2009)
PNAS 106, 18414-18419
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Proline antagonizes GABA-induced quenching of quorum-sensing in Agrobacterium tumefaciens.

E. Haudecoeur, S. Planamente, A. Cirou, M. Tannieres, B. J. Shelp, S. Morera, and D. Faure (2009)
PNAS 106, 14587-14592
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Mitogen-Activated Protein Kinases 3 and 6 Are Required for Full Priming of Stress Responses in Arabidopsis thaliana.

G. J.M. Beckers, M. Jaskiewicz, Y. Liu, W. R. Underwood, S. Y. He, S. Zhang, and U. Conrath (2009)
PLANT CELL 21, 944-953
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Disentangling the Complexity of Mitogen-Activated Protein Kinases and Reactive Oxygen Species Signaling.

A. Pitzschke and H. Hirt (2009)
Plant Physiology 149, 606-615
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MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays.

S. C. Popescu, G. V. Popescu, S. Bachan, Z. Zhang, M. Gerstein, M. Snyder, and S. P. Dinesh-Kumar (2009)
Genes & Dev. 23, 80-92
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Association of the Agrobacterium T-DNA-protein complex with plant nucleosomes.

B. Lacroix, A. Loyter, and V. Citovsky (2008)
PNAS 105, 15429-15434
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Crystal structure of the Agrobacterium virulence complex VirE1-VirE2 reveals a flexible protein that can accommodate different partners.

O. Dym, S. Albeck, T. Unger, J. Jacobovitch, A. Branzburg, Y. Michael, D. Frenkiel-Krispin, S. G. Wolf, and M. Elbaum (2008)
PNAS 105, 11170-11175
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A Novel WRKY Transcription Factor Is Required for Induction of PR-1a Gene Expression by Salicylic Acid and Bacterial Elicitors.

M. C. van Verk, D. Pappaioannou, L. Neeleman, J. F. Bol, and H. J.M. Linthorst (2008)
Plant Physiology 146, 1983-1995
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