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VIP1: linking Agrobacterium-mediated transformation to plant immunity?

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Abstract

Agrobacterium tumefaciens is the most efficient vehicle used today for the production of transgenic plants and plays an essential role in basic scientific research and in agricultural biotechnology. Previously, plant VirE2-interacting protein 1 (VIP1) was shown to play a role in Agrobacterium-mediated transformation. Recent reports demonstrate that VIP1, as one of the bZIP transcription factors, is also involved in plant immunity responses. Agrobacterium is able to activate and abuse VIP1 for transformation. These findings highlight Agrobacterium-host interaction and unveil how Agrobacterium hijacks host cellular mechanism for its own benefit. This review focuses on the roles played by VIP1 in Agrobacterium-mediated transformation and plant immunity.

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References

  • Anand A, Krichevsky A, Schornack S, Lahaye T, Tzfira T, Tang Y, Citovsky V, Mysore KS (2007) Arabidopsis VIRE2 INTERACTING PROTEIN2 is required for Agrobacterium T-DNA integration in plants. Plant Cell 19:1695–1708

    Article  PubMed  CAS  Google Scholar 

  • Andreasson E, Ellis B (2010) Convergence and specificity in the Arabidopsis MAPK nexus. Trends Plant Sci 15:106–113

    Article  PubMed  CAS  Google Scholar 

  • Aslam SN, Erbs G, Morrissey KL, Newman MA, Chinchilla D, Boller T, Molinaro A, Jackson RW, Cooper RM (2009) Microbe-associated molecular pattern (MAMP) signatures, synergy, size and charge: influences on perception or mobility and host defence responses. Mol Plant Pathol 10:375–387

    Article  PubMed  CAS  Google Scholar 

  • Avivi Y, Morad V, Ben-Meir H, Zhao J, Kashkush K, Tzfira T, Citovsky V, Grafi G (2004) Reorganization of specific chromosomal domains and activation of silent genes in plant cells acquiring pluripotentiality. Dev Dyn 230:12–22

    Article  PubMed  CAS  Google Scholar 

  • Bartels S, Anderson JC, Besteiro MA, Carreri A, Hirt H, Buchala A, Metraux JP, Peck SC, Ulm R (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21:2884–2897

    Article  PubMed  CAS  Google Scholar 

  • Baxevanis AD, Vinson CR (1993) Interactions of coiled coils in transcription factors: where is the specificity? Curr Opin Genet Dev 3:278–285

    Article  PubMed  CAS  Google Scholar 

  • Bethke G, Unthan T, Uhrig JF, Poschl Y, Gust AA, Scheel D, Lee J (2009) Flg22 regulates the release of an ethylene response factor substrate from MAP kinase 6 in Arabidopsis thaliana via ethylene signaling. Proc Natl Acad Sci USA 106:8067–8072

    Article  PubMed  Google Scholar 

  • Bhattacharjee S, Lee LY, Oltmanns H, Cao H, Veena, Cuperus J, Gelvin SB (2008) IMPa-4, an Arabidopsis importin alpha isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20:2661–2680

  • Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu Rev Plant Biol 60:379–406

    Article  PubMed  CAS  Google Scholar 

  • Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G (2009) Structure of the outer membrane complex of a type IV secretion system. Nature 462:1011–1015

    Article  PubMed  CAS  Google Scholar 

  • Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500

    Article  PubMed  CAS  Google Scholar 

  • Chinchilla D, Shan L, He P, de Vries S, Kemmerling B (2009) One for all: the receptor-associated kinase BAK1. Trends Plant Sci 14:535–541

    Article  PubMed  CAS  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  PubMed  CAS  Google Scholar 

  • Citovsky V, Warnick D, Zambryski P (1994) Nuclear import of Agrobacterium VirD2 and VirE2 proteins in maize and tobacco. Proc Natl Acad Sci USA 91:3210–3214

    Article  PubMed  CAS  Google Scholar 

  • Citovsky V, Kapelnikov A, Oliel S, Zakai N, Rojas MR, Gilbertson RL, Tzfira T, Loyter A (2004) Protein interactions involved in nuclear import of the Agrobacterium VirE2 protein in vivo and in vitro. J Biol Chem 279:29528–29533

    Article  PubMed  CAS  Google Scholar 

  • Dafny-Yelin M, Levy A, Tzfira T (2008) The ongoing saga of Agrobacterium-host interactions. Trends Plant Sci 13:102–105

    Article  PubMed  CAS  Google Scholar 

  • Ditt RF, Kerr KF, de Figueiredo P, Delrow J, Comai L, Nester EW (2006) The Arabidopsis thaliana transcriptome in response to Agrobacterium tumefaciens. Mol Plant Microbe Interact 19:665–681

    Article  PubMed  CAS  Google Scholar 

  • Djamei A, Pitzschke A, Nakagami H, Rajh I, Hirt H (2007) Trojan horse strategy in Agrobacterium transformation: abusing MAPK defense signaling. Science 318:453–456

    Article  PubMed  CAS  Google Scholar 

  • Durrenberger F, Crameri A, Hohn B, Koukolikova-Nicola Z (1989) Covalently bound VirD2 protein of Agrobacterium tumefaciens protects the T-DNA from exonucleolytic degradation. Proc Natl Acad Sci USA 86:9154–9158

    Article  PubMed  CAS  Google Scholar 

  • Erbs G, Silipo A, Aslam S, De Castro C, Liparoti V, Flagiello A, Pucci P, Lanzetta R, Parrilli M, Molinaro A, Newman MA, Cooper RM (2008) Peptidoglycan and muropeptides from pathogens Agrobacterium and Xanthomonas elicit plant innate immunity: structure and activity. Chem Biol 15:438–448

    Article  PubMed  CAS  Google Scholar 

  • Escobar MA, Dandekar AM (2003) Agrobacterium tumefaciens as an agent of disease. Trends Plant Sci 8:380–386

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Boller T (2003) Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J Biol Chem 278:6201–6208

    Article  PubMed  CAS  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

    Article  PubMed  CAS  Google Scholar 

  • Foster R, Izawa T, Chua NH (1994) Plant bZIP proteins gather at ACGT elements. FASEB J 8:192–200

    PubMed  CAS  Google Scholar 

  • Fronzes R, Christie PJ, Waksman G (2009a) The structural biology of type IV secretion systems. Nat Rev Microbiol 7:703–714

    Article  PubMed  CAS  Google Scholar 

  • Fronzes R, Schafer E, Wang L, Saibil HR, Orlova EV, Waksman G (2009b) Structure of a type IV secretion system core complex. Science 323:266–268

    Article  PubMed  CAS  Google Scholar 

  • Garcia AV, Parker JE (2009) Heaven’s Gate: nuclear accessibility and activities of plant immune regulators. Trends Plant Sci 14:479–487

    Article  PubMed  CAS  Google Scholar 

  • Gelvin SB (1998) Agrobacterium VirE2 proteins can form a complex with T strands in the plant cytoplasm. J Bacteriol 180:4300–4302

    PubMed  CAS  Google Scholar 

  • Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37

    Article  PubMed  CAS  Google Scholar 

  • Gelvin SB (2010a) Finding a way to the nucleus. Curr Opin Microbiol 13:53–58

    Article  PubMed  CAS  Google Scholar 

  • Gelvin SB (2010b) Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu Rev Phytopathol 48:3.1–3.24. doi:10.1146/annurev-phyto-080508-081852

    Article  Google Scholar 

  • Gomez-Gomez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011

    Article  PubMed  CAS  Google Scholar 

  • Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222

    Article  PubMed  CAS  Google Scholar 

  • Hirooka T, Rogowsky PM, Kado CI (1987) Characterization of the virE locus of Agrobacterium tumefaciens plasmid pTiC58. J Bacteriol 169:1529–1536

    PubMed  CAS  Google Scholar 

  • Ho MS, Ou C, Chan YR, Chien CT, Pi H (2008) The utility F-box for protein destruction. Cell Mol Life Sci 65:1977–2000

    Article  PubMed  CAS  Google Scholar 

  • Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111

    Article  PubMed  CAS  Google Scholar 

  • Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  CAS  Google Scholar 

  • Kunze G, Zipfel C, Robatzek S, Niehaus K, Boller T, Felix G (2004) The N terminus of bacterial elongation factor Tu elicits innate immunity in Arabidopsis plants. Plant Cell 16:3496–3507

    Article  PubMed  CAS  Google Scholar 

  • Lacroix B, Vaidya M, Tzfira T, Citovsky V (2005) The VirE3 protein of Agrobacterium mimics a host cell function required for plant genetic transformation. EMBO J 24:428–437

    Article  PubMed  CAS  Google Scholar 

  • Lacroix B, Tzfira T, Vainstein A, Citovsky V (2006) A case of promiscuity: Agrobacterium’s endless hunt for new partners. Trends Genet 22:29–37

    Article  PubMed  CAS  Google Scholar 

  • Lacroix B, Loyter A, Citovsky V (2008) Association of the Agrobacterium T-DNA-protein complex with plant nucleosomes. Proc Natl Acad Sci USA 105:15429–15434

    Article  PubMed  Google Scholar 

  • Lee CW, Efetova M, Engelmann JC, Kramell R, Wasternack C, Ludwig-Muller J, Hedrich R, Deeken R (2009) Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. Plant Cell 21:2948–2962

    Article  PubMed  CAS  Google Scholar 

  • Li J, Krichevsky A, Vaidya M, Tzfira T, Citovsky V (2005) Uncoupling of the functions of the Arabidopsis VIP1 protein in transient and stable plant genetic transformation by Agrobacterium. Proc Natl Acad Sci USA 102:5733–5738

    Article  PubMed  CAS  Google Scholar 

  • Loyter A, Rosenbluh J, Zakai N, Li J, Kozlovsky SV, Tzfira T, Citovsky V (2005) The plant VirE2 interacting protein 1. A molecular link between the Agrobacterium T-complex and the host cell chromatin? Plant Physiol 138:1318–1321

    Article  PubMed  CAS  Google Scholar 

  • Lu D, Wu S, Gao X, Zhang Y, Shan L, He P (2010) A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity. Proc Natl Acad Sci USA 107:496–501

    Article  PubMed  Google Scholar 

  • MAPK Group (2002) Mitogen-activated protein kinase cascades in plants: a new nomenclature. Trends Plant Sci 7:301–308

    Article  Google Scholar 

  • Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, Lacombe S, Rougon A, Bittel P, Kiss-Papp M, Chinchilla D, van Esse HP, Jorda L, Schwessinger B, Nicaise V, Thomma BP, Molina A, Jones JD, Zipfel C (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J 28:3428–3438

    Article  PubMed  CAS  Google Scholar 

  • Nicaise V, Roux M, Zipfel C (2009) Recent advances in PAMP-triggered immunity against bacteria: pattern recognition receptors watch over and raise the alarm. Plant Physiol 150:1638–1647

    Article  PubMed  CAS  Google Scholar 

  • Panstruga R, Parker JE, Schulze-Lefert P (2009) SnapShot: plant immune response pathways. Cell 136:978

    Article  PubMed  CAS  Google Scholar 

  • Pelczar P, Kalck V, Gomez D, Hohn B (2004) Agrobacterium proteins VirD2 and VirE2 mediate precise integration of synthetic T-DNA complexes in mammalian cells. EMBO Rep 5:632–637

    Article  PubMed  CAS  Google Scholar 

  • Pemberton LF, Rosenblum JS, Blobel G (1999) Nuclear import of the TATA-binding protein: mediation by the karyopherin Kap114p and a possible mechanism for intranuclear targeting. J Cell Biol 145:1407–1417

    Article  PubMed  CAS  Google Scholar 

  • Phair RD, Misteli T (2000) High mobility of proteins in the mammalian cell nucleus. Nature 404:604–609

    Article  PubMed  CAS  Google Scholar 

  • Pitzschke A, Hirt H (2010) New insights into an old story: Agrobacterium-induced tumour formation in plants by plant transformation. EMBO J 29:1021–1032

    Article  PubMed  CAS  Google Scholar 

  • Pitzschke A, Djamei A, Teige M, Hirt H (2009a) VIP1 response elements mediate mitogen-activated protein kinase 3-induced stress gene expression. Proc Natl Acad Sci USA 106:18414–18419

    Article  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009b) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  PubMed  CAS  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S, Palma K, Suarez-Rodriguez MC, Sandbech-Clausen S, Lichota J, Brodersen P, Grasser KD, Mattsson O, Glazebrook J, Mundy J, Petersen M (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    Article  PubMed  CAS  Google Scholar 

  • Regensburg-Tuink AJ, Hooykaas PJ (1993) Transgenic N. glauca plants expressing bacterial virulence gene virF are converted into hosts for nopaline strains of A. tumefaciens. Nature 363:69–71

    Article  PubMed  CAS  Google Scholar 

  • Saijo Y, Tintor N, Lu X, Rauf P, Pajerowska-Mukhtar K, Haweker H, Dong X, Robatzek S, Schulze-Lefert P (2009) Receptor quality control in the endoplasmic reticulum for plant innate immunity. EMBO J 28:3439–3449

    Article  PubMed  CAS  Google Scholar 

  • Schrammeijer B, Risseeuw E, Pansegrau W, Regensburg-Tuink TJ, Crosby WL, Hooykaas PJ (2001) Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homologs of the yeast Skp1 protein. Curr Biol 11:258–262

    Article  PubMed  CAS  Google Scholar 

  • Tzfira T, Citovsky V (2006) Agrobacterium-mediated genetic transformation of plants: biology and biotechnology. Curr Opin Biotechnol 17:147–154

    PubMed  CAS  Google Scholar 

  • Tzfira T, Vaidya M, Citovsky V (2001) VIP1, an Arabidopsis protein that interacts with Agrobacterium VirE2, is involved in VirE2 nuclear import and Agrobacterium infectivity. EMBO J 20:3596–3607

    Article  PubMed  CAS  Google Scholar 

  • Tzfira T, Vaidya M, Citovsky V (2002) Increasing plant susceptibility to Agrobacterium infection by overexpression of the Arabidopsis nuclear protein VIP1. Proc Natl Acad Sci USA 99:10435–10440

    Article  PubMed  CAS  Google Scholar 

  • Tzfira T, Li J, Lacroix B, Citovsky V (2004a) Agrobacterium T-DNA integration: molecules and models. Trends Genet 20:375–383

    Article  PubMed  CAS  Google Scholar 

  • Tzfira T, Vaidya M, Citovsky V (2004b) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431:87–92

    Article  PubMed  CAS  Google Scholar 

  • Veena, Jiang H, Doerge RW, Gelvin SB (2003) Transfer of T-DNA and Vir proteins to plant cells by Agrobacterium tumefaciens induces expression of host genes involved in mediating transformation and suppresses host defense gene expression. Plant J 35:219–236

  • Wiermer M, Palma K, Zhang Y, Li X (2007) Should I stay or should I go? Nucleocytoplasmic trafficking in plant innate immunity. Cell Microbiol 9:1880–1890

    Article  PubMed  CAS  Google Scholar 

  • Zaltsman A, Krichevsky A, Loyter A, Citovsky V (2010) Agrobacterium induces expression of a host F-box protein required for tumorigenicity. Cell Host Microbe 7:197–209

    Article  PubMed  CAS  Google Scholar 

  • Zhu Y, Nam J, Humara JM, Mysore KS, Lee LY, Cao H, Valentine L, Li J, Kaiser AD, Kopecky AL, Hwang HH, Bhattacharjee S, Rao PK, Tzfira T, Rajagopal J, Yi H, Veena, Yadav BS, Crane YM, Lin K, Larcher Y, Gelvin MJ, Knue M, Ramos C, Zhao X, Davis SJ, Kim SI, Ranjith-Kumar CT, Choi YJ, Hallan VK, Chattopadhyay S, Sui X, Ziemienowicz A, Matthysse AG, Citovsky V, Hohn B, Gelvin SB (2003) Identification of Arabidopsis rat mutants. Plant Physiol 132:494–505

  • Ziemienowicz A, Merkle T, Schoumacher F, Hohn B, Rossi L (2001) Import of Agrobacterium T-DNA into plant nuclei: two distinct functions of VirD2 and VirE2 proteins. Plant Cell 13:369–383

    Article  PubMed  CAS  Google Scholar 

  • Ziemienowicz A, Tzfira T, Hohn B (2008) Mechanisms of T-DNA integration. In: Tzfira T, Citovsky V (eds) Agrobacterium: from biology to biotechnology. Springer, Berlin, pp 395–440

    Chapter  Google Scholar 

  • Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Curr Opin Plant Biol 12:414–420

    Article  PubMed  CAS  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

We apologize to authors whose work was not cited because of space limitations. Researches in our laboratory are supported by the National Natural Science Foundation of China (Nos. 30471052, 30871457), the State Key Basic Research and Development Plan of China (No. 2009CB118500) and the Program for Changjiang Scholars and Innovative Research Team in University (No. IRT0635).

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The authors have no conflict of interest with the work cited in this paper.

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Correspondence to Dequan Li.

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Communicated by R. Reski.

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Liu, Y., Kong, X., Pan, J. et al. VIP1: linking Agrobacterium-mediated transformation to plant immunity?. Plant Cell Rep 29, 805–812 (2010). https://doi.org/10.1007/s00299-010-0870-4

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