Skip to main content
SpringerLink
Log in
Book cover

Agrobacterium Biology pp 319–348Cite as

Transcriptome Profiling of Plant Genes in Response to Agrobacterium tumefaciens-Mediated Transformation

  • Chapter
  • First Online:

Part of the book series: Current Topics in Microbiology and Immunology ((CT MICROBIOLOGY,volume 418))

Abstract

Agrobacterium tumefaciens is a plant pathogen that causes crown gall disease. During infection of the host plant, Agrobacterium transfers T-DNA from its Ti plasmid into the host cell, which can then be integrated into the host genome. This unique genetic transformation capability has been employed as the dominant technology for producing genetically modified plants for both basic research and biotechnological applications. Agrobacterium has been well studied as a disease-causing agent. The Agrobacterium-mediated transformation process involves early attachment of the bacterium to the host’s surface, followed by transfer of T-DNA and virulence proteins into the plant cell. Throughout this process, the host plants exhibit dynamic gene expression patterns at each infection stage or in response to Agrobacterium strains with varying pathogenic capabilities. Shifting host gene expression patterns throughout the transformation process have effects on transformation frequency, host morphology, and metabolism. Thus, gene expression profiling during the Agrobacterium infection process can be an important approach to help elucidate the interaction between Agrobacterium and plants. This review highlights recent findings on host plant differential gene expression patterns in response to A. tumefaciens or related elicitor molecules.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD   219.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Altpeter F, Springer NM, Bartley LE et al (2016) Advancing crop transformation in the era of genome editing. Plant Cell 28:1510–1520

    CAS  PubMed  PubMed Central  Google Scholar 

  • Azpiroz-Leehan R, Feldmann KA (1997) T-DNA insertion mutagenesis in Arabidopsis: going back and forth. Trends Genet 13:152–156

    Article  CAS  PubMed  Google Scholar 

  • Barton KA, Brill WJ (1983) Prospects in plant genetic engineering. Science 219:671–682

    Article  CAS  PubMed  Google Scholar 

  • Beijersbergen A, Smith SJ, Hooykaas PJ (1994) Localization and topology of VirB proteins of Agrobacterium tumefaciens. Plasmid 32:212–218

    Article  CAS  PubMed  Google Scholar 

  • Bhattacharya A, Priyanka S, Citovsky V (2010) The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol Plant Pathol 11:705–719

    CAS  PubMed  PubMed Central  Google Scholar 

  • Binns AN, Costantino P (1998) The Agrobacterium oncogenes. In: Spaink HP, Kondorosi A, Hooykaas PJJ (eds) The Rhizobiaceae. Springer, Netherlands, pp 251–266

    Chapter  Google Scholar 

  • Casassola A, Brammer SP, Chaves MS et al (2013) Gene expression: a review on methods for the study of defense-related gene differential expression in plants. Am J Plant Sci 4:64–73

    Article  Google Scholar 

  • Chilton MD, Drummond MH, Merio DJ et al (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271

    Article  CAS  PubMed  Google Scholar 

  • Chinchilla D, Bauer Z, Regenass M et al (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christie PJ, Vogel JP (2000) Bacterial type IV secretion: conjugation systems adapted to deliver effector molecules to host cells. Trends Microbiol 8:354–360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui H, Xiang T, Zhou JM (2009) Plant immunity: a lesson from pathogenic bacterial effector proteins. Cell Microbiol 11:1453–1461

    Article  CAS  PubMed  Google Scholar 

  • DeCleene M, DeLay J (1976) The host range of crown gall. Bot Rev 42:389–466

    Article  Google Scholar 

  • Ditt RF, Nester EW, Comai L (2001) Plant gene expression response to Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 98:10954–10959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ditt RF, Nester E, Comai L (2005) The plant cell defense and Agrobacterium tumefaciens. FEMS Microbiol Lett 247:207–213

    Article  CAS  PubMed  Google Scholar 

  • Ditt F, Kerr KF, de Figueiredo P et al (2006) The Arabidopsis thaliana transcriptome in response to Agrobacterium tumefaciens. Mol Plant Microbe Interact 19:665–681

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Duan K, Willig C, de Tar JR et al (2018) Transcriptomic analysis of Arabidopsis seedlings in response to Agrobacterium-mediated transformation process. Mol Plant Microbe Interact 31:445–459

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • García-Rodríguez FM, Schrammeijer B, Hooykaas PJ (2006) The Agrobacterium VirE3 effector protein: a potential plant transcriptional activator. Nucl Acids Res 34:6496–6504

    Article  PubMed  PubMed Central  Google Scholar 

  • Gelvin SB (2000) Agrobacterium and plant genes involved in T-DNA transfer and integration. Annu Rev Plant Physiol Plant Mol Biol 51:223–256

    Article  CAS  PubMed  Google Scholar 

  • Gelvin SB (2010) Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu Rev Phytopathol 48:45–68

    Article  CAS  PubMed  Google Scholar 

  • Gelvin SB (2017) Integration of Agrobacterium T-DNA into the plant genome. Annu Rev Genet 51:195–217

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Gómez 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  Google Scholar 

  • Gust AA, Biswas R, Lenz HD et al (2007) Bacteria-derived peptidoglycans constitute pathogen-associated molecular patterns triggering innate immunity in Arabidopsis. J Biol Chem 282:32338–32348

    Article  CAS  PubMed  Google Scholar 

  • Kuldau GA, DeVos G, Owen J et al (1990) The virB operon of Agrobacterium tumefaciens pTiC58 encodes 11 open reading frames. Mol Gen Genet 221:256–266

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lacroix B, Citovsky V (2013) The roles of bacterial and host plant factors in Agrobacterium-mediated genetic transformation. Int J Dev Biol 57:467–481

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Lapham R, Lee LY, Tsugama D et al (2018) VIP1 and its homologs are not required for Agrobacterium-mediated transformation, but play a role in Botrytis and salt stress responses. Front Plant Sci 9:749

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee CW, Efetova M, Engelmann JC et al (2009) Agrobacterium tumefaciens promotes tumor induction by modulating pathogen defense in Arabidopsis thaliana. Plant Cell 21:2948–2962

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livaja M, Zeidler D, von Rad U et al (2008) Transcriptional responses of Arabidopsis thaliana to the bacteria-derived PAMPs harpin and lipopolysaccharide. Immunobiology 213:161–171

    Article  CAS  PubMed  Google Scholar 

  • Magori S, Citovsky V (2011) Agrobacterium counteracts host-induced degradation of its effector F-box protein. Sci Signal 4:ra69

    Google Scholar 

  • Morris RO (1986) Genes specifying auxin and cytokinin biosynthesis in phytopathogens. Annu Rev Plant Physiol 37:509–538

    Article  CAS  Google Scholar 

  • Mysore KS, Bassuner B, Deng XB et al (1998) Role of the Agrobacterium tumefaciens VirD2 protein in T-DNA transfer and integration. Mol Plant Microbe Interact 11:668–683

    Article  CAS  PubMed  Google Scholar 

  • Niu X, Zhou M, Henkel CV et al (2015) The Agrobacterium tumefaciens virulence protein VirE3 is a transcriptional activator of the F-box gene VBF. Plant J 84:914–924

    Article  CAS  PubMed  Google Scholar 

  • Pu XA, Goodman RN (1993) Attachment of agrobacteria to grape cells. Appl Environ Microbiol 59:2572–2577

    CAS  PubMed  PubMed Central  Google Scholar 

  • Schrammeijer B, den Dulk-Ras A, Vergunst AC et al (2003) Analysis of Vir protein translocation from Agrobacterium tumefaciens using Saccharomyces cerevisiae as a model: Evidence for transport of a novel effector protein VirE3. Nucl Acids Res 31:860–868

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi Y, Lee LY, Gelvin SB (2014) Is VIP1 important for Agrobacterium-mediated transformation? Plant J 79:848–860

    Article  CAS  PubMed  Google Scholar 

  • Shirasu K, Morel P, Kado CI (1990) Characterization of the virB operon of an Agrobacterium tumefaciens Ti plasmid: nucleotide sequence and protein analysis. Mol Microbiol 4:1153–1163

    Article  CAS  PubMed  Google Scholar 

  • Staskawicz BJ, Ausubel FM, Baker BJ et al (1995) Molecular genetics of plant disease resistance. Science 268:661–667

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Xie Z, Chen W et al (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson DV, Melchers LS, Idler KB et al (1988) Analysis of the complete nucleotide sequence of the Agrobacterium tumefaciens virB operon. Nucleic Acids Res 16:4621–4636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tie W, Zhou F, Wang L et al (2012) Reasons for lower transformation efficiency in indica rice using Agrobacterium tumefaciens-mediated transformation: lessons from transformation assays and genome-wide expression profiling. Plant Mol Biol 78:1–18

    Article  CAS  PubMed  Google Scholar 

  • Tomlinson AD, Fuqua C (2009) Mechanisms and regulation of polar surface attachment in Agrobacterium tumefaciens. Curr Opin Microbiol 12:708–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsuda K, Qi Y, le Nguyen V et al (2012) An efficient Agrobacterium-mediated transient transformation of Arabidopsis. Plant J 69:713–719

    Article  CAS  PubMed  Google Scholar 

  • Tzfira T, 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  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Veena JH, 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

    Article  CAS  PubMed  Google Scholar 

  • Vences-Guzman MA, Guan Z, Bermudez-Barrientos JR et al (2013) Agrobacteria lacking ornithine lipids induce more rapid tumour formation. Environ Microbiol 15:895–906

    Article  CAS  PubMed  Google Scholar 

  • Vergunst AC, Schrammeijer B, den Dulk-Ras A et al (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979–982

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Peng W, Zhou X et al (2014) The putative Agrobacterium transcriptional activator-like virulence protein VirD5 may target T-complex to prevent the degradation of coat proteins in the plant cell nucleus. New Phytol 203:1266–1281

    Article  CAS  PubMed  Google Scholar 

  • Ward DV, Draper O, Zupan JR, Zambryski PC (2002) Peptide linkage mapping of the Agrobacterium tumefaciens vir-encoded type IV secretion system reveals protein subassemblies. Proc Natl Acad Sci USA 99:11493–11500

    Article  CAS  Google Scholar 

  • Ward JE, Akiyoshi DE, Regier D et al (1988) Characterization of the virB operon from an Agrobacterium tumefaciens Ti plasmid. J Biol Chem 263:5804–5814

    CAS  PubMed  Google Scholar 

  • Watson B, Currier TC, Gordon MP et al (1975) Plasmid required for virulence of Agrobacterium tumefaciens. J Bacteriol 123:255–264

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weigel RR, Pfitzner UM, Gatz C (2005) Interaction of NIMIN1 with NPR1 modulates PR gene expression in Arabidopsis. Plant Cell 17:1279–1291

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wood DW, Setubal JC, Kaul R et al (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–2323

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang WJ, Dewey RE, Boss W et al (2013) Enhanced Agrobacterium-mediated transformation efficiencies in monocot cells is associated with attenuated defense responses. Plant Mol Biol 81:273–286

    Article  CAS  PubMed  Google Scholar 

  • Zhang YM, Liu ZH, Yang RJ et al (2016) Improvement of soybean transformation via Agrobacterium tumefaciens methods involving α-aminooxyacetic acid and sonication treatments enlightened by gene expression profile analysis. Plant Cell Rep 35:1259–1271

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, van Heusden GPH, Hooykaas PJ (2017) Virulence protein VirD5 of Agrobacterium tumefaciens binds to kinetochores in host cells via an interaction with Spt4. Proc Natl Acad Sci 114:10238–10243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Wang K, Lv D et al (2013) Global analysis of differentially expressed genes and proteins in the wheat callus infected by Agrobacterium tumefaciens. PLoS ONE 8:e79390

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C, Robatzek S (2010) Pathogen-associated molecular pattern-triggered immunity: veni, vidi…? Plant Physiol 154:551–554

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zipfel C, Robatzek S, Navarro L et al (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428:764–767

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D et al (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749–760

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We want to thank members of the Zhanyuan Zhang’s laboratory for their technical assistance during the course of the RNA-Seq study. This review work was supported by a University of Missouri Research Board grant and the Life Science Fellowship.

Author information

Authors and Affiliations

  1. Division of Plant Sciences, University of Missouri, Columbia, MO, USA

    Christopher J. Willig, Kaixuan Duan & Zhanyuan J. Zhang

Authors
  1. Christopher J. Willig
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kaixuan Duan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhanyuan J. Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhanyuan J. Zhang .

Editor information

Editors and Affiliations

  1. Department of Biological Sciences, Purdue University, West Lafayette, IN, USA

    Stanton B. Gelvin

Rights and permissions

Reprints and permissions

Copyright information

© 2018 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Willig, C.J., Duan, K., Zhang, Z.J. (2018). Transcriptome Profiling of Plant Genes in Response to Agrobacterium tumefaciens-Mediated Transformation. In: Gelvin, S. (eds) Agrobacterium Biology. Current Topics in Microbiology and Immunology, vol 418. Springer, Cham. https://doi.org/10.1007/82_2018_115

Download citation

Publish with us

Policies and ethics

Search

Navigation