Abstract
Two decades ago, it was discovered that the well-known plant vector Agrobacterium tumefaciens can also transform yeasts and fungi when these microorganisms are co-cultivated on a solid substrate in the presence of a phenolic inducer such as acetosyringone. It is important that the medium has a low pH (5–6) and that the temperature is kept at room temperature (20–25 °C) during co-cultivation. Nowadays, Agrobacterium-mediated transformation (AMT) is the method of choice for the transformation of many fungal species; as the method is simple, the transformation efficiencies are much higher than with other methods, and AMT leads to single-copy integration much more frequently than do other methods. Integration of T-DNA in fungi occurs by non-homologous end-joining (NHEJ), but also targeted integration of the T-DNA by homologous recombination (HR) is possible. In contrast to AMT of plants, which relies on the assistance of a number of translocated virulence (effector) proteins, none of these (VirE2, VirE3, VirD5, VirF) are necessary for AMT of yeast or fungi. This is in line with the idea that some of these proteins help to overcome plant defense. Importantly, it also showed that VirE2 is not necessary for the transport of the T-strand into the nucleus. The yeast Saccharomyces cerevisiae is a fast-growing organism with a relatively simple genome with reduced genetic redundancy. This yeast species has therefore been used to unravel basic molecular processes in eukaryotic cells as well as to elucidate the function of virulence factors of pathogenic microorganisms acting in plants or animals. Translocation of Agrobacterium virulence proteins into yeast was recently visualized in real time by confocal microscopy. In addition, the yeast 2-hybrid system, one of many tools that have been developed for use in this yeast, was used to identify plant and yeast proteins interacting with the translocated Agrobacterium virulence proteins. Dedicated mutant libraries, containing for each gene a mutant with a precise deletion, have been used to unravel the mode of action of some of the Agrobacterium virulence proteins. Yeast deletion mutant collections were also helpful in identifying host factors promoting or inhibiting AMT, including factors involved in T-DNA integration. Thus, the homologous recombination (HR) factor Rad52 was found to be essential for targeted integration of T-DNA by HR in yeast. Proteins mediating double-strand break (DSB) repair by end-joining (Ku70, Ku80, Lig4) turned out to be essential for non-homologous integration. Inactivation of any one of the genes encoding these end-joining factors in other yeasts and fungi was employed to reduce or totally eliminate non-homologous integration and promote efficient targeted integration at the homologous locus by HR. In plants, however, their inactivation did not prevent non-homologous integration, indicating that T-DNA is captured by different DNA repair pathways in plants and fungi.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Almeida AJ, Carmona JAC, Cunha C et al (2007) Towards a molecular genetic system for the pathogenic fungus Paracoccidioides brasilensis. Fungal Genet Biol 44:1387–1398
Amey RC, Mills PR, Bailey A, Foster GD (2003) Investigating the role of a Verticillium fungicola beta-1, 6-glucanase during infection of Agaricus bisporus using targeted gene disruption. Fungal Genet Biol 39:264–275
Anand A, Krichevsky A, Schornack S et al (2007) Arabidopsis VIRE2 INTERACTING PROTEIN2 is required for Agrobacterium T-DNA integration in plants. Plant Cell 19:1695–1708
Atmakuri K, Cascales E, Burton OT et al (2007) Agrobacterium ParA/MinD-like VirC1 spatially coordinates early conjugative DNA transfer reactions. EMBO J 26:2540–2551
Ballas N, Citovsky V (1997) Nuclear localization signal binding protein from Arabidopsis mediates nuclear import of Agrobacterium VirD2 protein. Proc Natl Acad Sci U S A 94:10723–10728
Baumgartner K, Fujiyoshi P, Foster GD, Bailey AM (2010) Agrobacterium tumefaciens-mediated transformation for investigation of somatic recombination in the fungal pathogen Armillaria mellea. Appl Environ Microbiol 76:7990–7996
Betts MF, Tucker SL, Galadima N et al (2007) Development of a high throughput transformation system for insertional mutagenesis in Magnaporthe oryzae. Fungal Genet Biol 44:1035–1049
Beijersbergen A, Dulk-Ras AD, Schilperoort RA, Hooykaas PJ (1992) Conjugative transfer by the virulence system of Agrobacterium tumefaciens. Nature 256:1324–1327
Bhattacharjee S, Lee LY, Oltmanns H, Cao H, Veena Cuperus J, Gelvin SB (2008) IMPa-4, an Arabidopsis importin α isoform, is preferentially involved in Agrobacterium-mediated plant transformation. Plant Cell 20:2661–2680
Biggins S, Severin FF, Bhalla N et al (1999) The conserved protein kinase Ipl1 regulates microtubule binding to kinetochores in budding yeast. Genes Devel 13:532–544
Blaise F, Rémy E, Meyer M et al (2007) A critical assessment of Agrobacterium tumefaciens-mediated transformation as a tool for pathogenicity gene discovery in the phytopathogenic fungus Leptosphaeria maculans. Fungal Genet Biol 44:123–138
Bourras S, Meyer M, Grandaubert J et al (2012) Incidence of genome structure, DNA asymmetry, and cell physiology on T-DNA integration in chromosomes of the phytopathogenic fungus Leptosphaeria maculans. G3 (Bethesda) 2:891–904
Bundock P, Dulk-Ras A, Beijersbergen A, Hooykaas PJ (1995) Trans-kingdom T-DNA transfer from Agrobacterium tumefaciens to Saccharomyces cerevisiae. EMBO J 14:3206–3214
Bundock P, Hooykaas PJ (1996) Integration of Agrobacterium tumefaciens T-DNA in the Saccharomyces cerevisiae genome by illegitimate recombination. Proc Natl Acad Sci U S A 93:15272–15275
Bundock P, Mroczek K, Winkler AA et al (1999) T-DNA from Agrobacterium tumefaciens as an efficient tool for gene targeting in Kluyveromyces lactis. Mol Gen Genet 261:115–121
Bundock P, van Attikum H, Dulk-Ras A, Hooykaas PJ (2002) Insertional mutagenesis in yeasts using T-DNA from Agrobacterium tumefaciens. Yeast 19:529–536
Campoy S, Perez F, Martin JF et al (2003) Stable transformants of the azaphilone pigment-producing Monascus purpureus obtained by protoplast transformation and Agrobacterium-mediated DNA transfer. Curr Genet 43:447–452
Chilton MD, Que Q (2003) Targeted integration of T-DNA into the tobacco genome at double-stranded breaks: new insights on the mechanism of T-DNA integration. Plant Physiol 133:956–965
Choi J, Park J, Jeon J et al (2007) Genome-wide analysis of T-DNA integration into the chromosomes of Magnaporthe oryzae. Mol Microbiol 66:371–382
Combier JP, Melayah D, Raffier C et al (2003) Agrobacterium tumefaciens-mediated transformation as a tool for insertional mutagenesis in the symbiotic ectomycorrhizal fungus Hebeloma cylindrosporum. FEMS Microbiol Lett 220:141–148
Crane YM, Gelvin SB (2007) RNAi-mediated gene silencing reveals involvement of Arabidopsis chromatin-related genes in Agrobacterium-mediated root transformation. Proc Natl Acad Sci U S A 104:15156–15161
Critchlow SE, Jackson SP (1998) DNA end-joining: from yeast to man. Trends Biochem Sci 23:394–398
Crotti LB, Basrai MA (2004) Functional roles for evolutionarily conserved Spt4p at centromeres and heterochromatin in Saccharomyces cerevisiae. EMBO J 23:1804–1814
De Cleene M, De Ley J (1976) The host range of crown gall. Botan Rev 42:389–466
Degefu Y, Hanif M (2003) Agrobacterium tumefaciens-mediated transformation of Helminthosporium turcicum, the maize leaf-blight fungus. Arch Microbiol 180:279–284
de Groot MJ, Bundock P, Hooykaas PJ, Beijersbergen AG (1998) Agrobacterium tumefaciens-mediated transformation of filamentous fungi. Nat Biotechnol 16:839–842
Deng W, Chen L, Wood DW et al (1998) Agrobacterium VirD2 protein interacts with plant host cyclophilins. Proc Natl Acad Sci U S A 95:7040–7045
Escudero J, den Dulk-Ras H, Regensburg-Tuïnk TJG, Hooykaas PJJ (2003) VirD4-independent transformation by CloDF13 evidences an unknown factor required for the genetic colonization of plants via Agrobacterium. Mol Microbiol 47:891–901
Flowers JL, Vaillancourt LJ (2005) Parameters affecting the efficiency of Agrobacterium tumefaciens-mediated transformation of Colletotrichum graminicola. Curr Genet 15:1–9
Frandsen RJ (2011) A guide to binary vectors and strategies for targeted genome modification in fungi using Agrobacterium tumefaciens-mediated transformation. J Microbiol Methods 87:247–262
Fullner KJ, Nester EW (1996) Temperature affects the T-DNA transfer machinery of Agrobacterium tumefaciens. J Bacteriol 178:1498–1504
García-Cano E, Magori S, Sun Q et al (2015) Interaction of Arabidopsis trihelix-domain transcription factors VFP3 and VFP5 with Agrobacterium virulence protein VirF. PLoS ONE 10:e0142128
García-Cano E, Hak H, Magori S et al (2018) The Agrobacterium F-box protein effector VirF destabilizes the Arabidopsis GLABROUS1 enhancer/binding protein-like transcription factor VFP4, a transcriptional activator of defense response genes. Mol Plant Microbe Interact 31:576–586
Garcia-Rodriguez FM, Schrammeijer B, Hooykaas PJJ (2006) The Agrobacterium VirE3 effector protein: a potential plant transcriptional activator. Nucleic Acids Res 34:6496–6504
Gardiner DM, Howlett BJ (2004) Negative selection using thymidine kinase increases the efficiency of recovery of transformants with targeted genes in the filamentous fungus Leptosphaeria maculans. Curr Genet 45:249–255
Gelvin SB (2003) Agrobacterium-mediated plant transformation: the biology behind the “gene-jockeying” tool. Microbiol Mol Biol Rev 67:16–37
Gelvin SB (2010) Plant proteins involved in Agrobacterium-mediated genetic transformation. Annu Rev Phytopathol 48:45–68
Grimaldi B, de Raaf MA, Filetici P et al (2005) Agrobacterium-mediated gene transfer and enhanced green fluorescent protein visualization in the mycorrhizal ascomycete Tuber borchii: a first step towards truffle genetics. Curr Genet 48:69–74
Hatoh K, Izumitsu K, Morita A et al (2013) Transformation of the mushroom species Hypsizigus marmoreus, Flammulina velutipes, and Grifola frondosa by an Agrobacterium-mediated method using a universal transformation plasmid. Mycoscience 54:8–12
Hauer MH, Gasser SM (2018) Chromatin and nucleosome dynamics in DNA damage and repair. Genes Devel 31:2204–2221
Hooykaas PJJ, van Attikum H, Bundock P (2000) Nucleic acid integration in eukaryotes. EP00204693.6
Hooykaas PJ, Hofker M, den Dulk-Ras H, Schilperoort RA (1984) A comparison of virulence determinants in an octopine Ti plasmid, a nopaline Ti plasmid, and an Ri plasmid by complementation analysis of Agrobacterium tumefaciens mutants. Plasmid 11:195–205
Hooykaas-van Slogteren GMS, Hooykaas PJJ, Schilperoort RA (1984) Expression of Ti plasmid genes in monocotyledonous plants infected with Agrobacterium tumefaciens. Nature 311:763–764
Idnurm A, Reedy JL, Nussbau JC, Heitman J (2004) Cryptococcus neoformans virulence gene discovery through insertional mutagenesis. Eukaryot Cell 3:420–429
Ishida Y, Saito H, Ohta S et al (1996) High efficiency transformation of maize (Zea mays L.) mediated by Agrobacterium tumefaciens. Nat Biotech 14:745–750
Jeon J, Park SY, Chi MH et al (2007) Genome-wide functional analysis of pathogenicity genes in the rice blast fungus. Nature Genet 39:561–565
Kilaru S, Collins CM, Hartley AJ et al (2009) Establishing molecular tools for genetic manipulation of the pleuromutilin-producing fungus Clitopilus passeckerianus. Appl Environ Microbiol 75:7196–7204
Knight CJ, Bailey AM, Foster GD (2010) Investigating Agrobacterium-mediated transformation of Verticillium albo-atrum on plant surfaces. PLoS ONE 5:e13684
Kooistra R, Hooykaas PJ, Steensma HY (2004) Efficient gene targeting in Kluyveromyces lactis. Yeast 21:781–792
Krysan PJ, Young JC, Sussman MR (1999) T-DNA as an insertional mutagen in Arabidopsis. Plant Cell 11:2283–2290
Kyndt T, Quispe D, Zhai H et al (2015) The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: An example of a naturally transgenic food crop. Proc Natl Acad Sci U S A 112:5844–5849
Lacroix B, Citovsky V (2013) Characterization of VIP1 activity as a transcriptional regulator in vitro and in planta. Sci Rep 3:2440
Leclerque A, Wan H, Abschütz A et al (2004) Agrobacterium-mediated insertional mutagenesis (AIM) of the entomopathogenic fungus Beauveria bassiana. Curr Genet 45:111–119
Lee MH, Bostock RM (2006) Agrobacterium T-DNA-mediated integration and gene replacement in the brown rot pathogen Monilinia fructicola. Curr Genet 49:309–322
Lewis LK, Resnick MA (2000) Tying up loose ends: nonhomologous end-joining in Saccharomyces cerevisiae. Mutat Res 451:71–89
Li G, Zhou Z, Liu G et al (2007) Characterization of T-DNA insertion patterns in the genome of rice blast fungus Magnaporthe oryzae. Curr Genet 51:233–243
Li X, Yang Q, Tu H et al (2014) Direct visualization of Agrobacterium-delivered VirE2 in recipient cells. Plant J 77:487–495
Loppnau P, Tanguay P, Breuil C (2004) Isolation and disruption of the melanin pathway polyketide synthase gene of the softwood deep stain fungus Ceratocystis resinifera. Fungal Genet Biol 41:33–41
Luo Y, Chen Z, Zhu D et al (2015) Yeast actin-related protein ARP6 negatively regulates Agrobacterium-mediated transformation of yeast cell. BioMed Res Int article ID 275092. http://dx.doi.org/10.1155/2015/275092
Magori S, Citovsky V (2011) Agrobacterium counteracts host-induced degradation of its effector F-box protein. Sci Signal 4(195):ra69
Malonek S, Meinhardt F (2001) Agrobacterium tumefaciens-mediated genetic transformation of the phytopathogenic ascomycete Calonectria morganii. Curr Genet 40:152–155
McClelland CM, Chang YC, Kwon-Chung KJ (2005) High frequency transformation of Cryptococcus neoformans and Cryptococcus gattii by Agrobacterium tumefaciens. Fungal Genet Biol 42:904–913
Meng Y, Patel G, Heist M et al (2007) A systematic analysis of T-DNA insertion events in Magnaporthe oryzae. Fungal Genet Biol 44:1050–1064
Meyer V, Mueller D, Strowig T, Stahl U (2003) Comparison of different transformation methods for Aspergillus giganteus. Curr Genet 43:371–377
Michielse CB, Ram AFJ, Hooykaas PJ, van den Hondel CAMJJ (2004a) Agrobacterium-mediated transformation of Aspergillus awamori in the absence of full length VirD2, VirC2 or VirE2 leads to insertion of aberrant T-DNA structures. J Bacteriol 186:2038–2045
Michielse CB, Ram AFJ, Hooykaas PJ, van den Hondel CAMJJ (2004b) Role of bacterial virulence proteins in Agrobacterium-mediated transformation of Aspergillus awamori. Fungal Genet Biol 45:571–578
Michielse CB, Hooykaas PJ, van den Hondel CAMJJ, Ram AFJ (2005a) Agrobacterium-mediated transformation as a tool for functional genomics in fungi. Curr Genet 48:1–17
Michielse CB, Arentshorst M, Ram AF, van den Hondel CAMJJ (2005b) Agrobacterium-mediated transformation leads to improved gene replacement efficiency in Aspergillus awamori. Fungal Genet Biol 42:9–19
Michielse CB, Hooykaas PJ, van den Hondel CA, Ram AF (2008) Agrobacterium-mediated transformation of the filamentous fungus Aspergillus awamori. Nat Protocols 3:1671–1678
Michielse CB, van Wijk R, Reijnen L et al (2009) Insight into the molecular requirements for pathogenicity of Fusarium oxysporum f. sp. lycopersici through large-scale insertional mutagenesis. Genome Biol 10:R4
Mikosch TS, Lavrijssen B, Sonnenberg AS, van Griensven LJ (2001) Transformation of the cultivated mushroom Agaricus bisporus (Lange) using T-DNA from Agrobacterium tumefaciens. Curr Genet 39:35–39
Mullins ED, Chen X, Romaine P at al. (2001) Agrobacterium-mediated transformation of Fusarium oxysporum: an efficient tool for insertional mutagenesis and gene transfer. Phytopathol 91:173–180
Murata H, Sunagawa M, Igasaki T, Shishido K (2006) Agrobacterium-mediated transformation of the ectomycorrhizal basidiomycete Tricholoma matsutake that produces commercially valuable fruit bodies, matsutake. Mycoscience 47:228–231
Nemecek JC, Wüthrich M, Klein BS (2006) Global control of dimorphism and virulence in fungi. Science 312:583–588
Nester EW, Gordon MP, Amasino RM, Yanofsky MF (1984) Crown gall: a molecular and physiological analysis. Annu Rev Plant Physiol 35:387–413
Ninomiya Y, Suzuki K, Ishii C, Inoue H (2004) Highly efficient gene replacements in Neurospora strains deficient for nonhomologous end-joining. Proc Natl Acad Sci U S A 101:12248–12253
Niu X (2013) Functional analysis of Agrobacterium virulence genes. Ph.D. thesis. Leiden University, Leiden, The Netherlands
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
Noack-Schonmann S, Bus T, Banasiak R et al. (2014) Genetic transformation of Knufia petricola A95—a model organism for biofilm-material interactions AMB Express 4:80
Offringa R, de Groot MJA, Haagsman HJ et al (1990) Extrachromosomal homologous recombination and gene targeting in plant cells after Agrobacterium mediated transformation. EMBO J 9:3077–3084
Ohmine Y, Satoh Y, Kiyokawa K et al (2016) DNA repair genes RAD52 and SRS2, a cell wall synthesis regulator gene SMI1, and the membrane sterol synthesis scaffold gene ERG28 are important in efficient Agrobacterium-mediated yeast transformation with chromosomal T-DNA. BMC Microbiol 16:58
Pansegrau W, Schoumacher F, Hohn B, Lanka E (1993) Site-specific cleavage and joining of single-stranded DNA by VirD2 protein of Agrobacterium tumefaciens Ti plasmids: analogy to bacterial conjugation. Proc Natl Acad Sci U S A 90:11538–11542
Pardo AG, Hanif M, Raudaskoski M, Gorfer M (2002) Genetic transformation of ectomycorrhizal fungi mediated by Agrobacterium tumefaciens. Mycol Res 106:132–137
Park SM, Kim DK (2004) Transformation of a filamentous fungus Cryphonectria parasitica using Agrobacterium tumefaciens. Biotechnol Bioprocess Eng 9:217–222
Park SY, Jeong MH, Wang HY et al (2013) Agrobacterium tumefaciens-mediated transformation of the lichen fungus, Umbilicaria muehlenbergii. PLoS ONE 8:e83896
Park SY, Vaghchhipawala Z, Vasudevan B et al (2015) Agrobacterium T-DNA integration into the plant genome can occur without the activity of key non-homologous end-joining proteins. Plant J 81:934–946
Piers KL, Heath JD, Liang X et al (1996) Agrobacterium tumefaciens-mediated transformation of yeast. Proc Natl Acad Sci U S A 93:1613–1618
Rho HS, Kang S, Lee YH (2001) Agrobacterium tumefaciens-mediated transformation of the plant pathogenic fungus, Magnaporthe grisea. Mol Cells 12:407–411
Risseeuw E, Franke-van Dijk ME, Hooykaas PJ (1996) Integration of an insertion-type transferred DNA vector from Agrobacterium tumefaciens into the Saccharomyces cerevisiae genome by gap repair. Mol Cell Biol 16:5924–5932
Roberts RL, Metz M, Monks DE et al (2003) Purine synthesis and increased Agrobacterium tumefaciens transformation of yeast and plants. Proc Natl Acad Sci U S A 100:6634–6639
Rogers CW, Challen MP, Green JR, Whipps JM (2004) Use of REMI and Agrobacterium-mediated transformation to identify pathogenicity mutants of the biocontrol fungus, Coniothyrium minitans. FEMS Microbiol Lett 241:207–214
Rolland S, Jobic C, Fevre M, Bruel C (2003) Agrobacterium-mediated transformation of Botrytis cinerea, simple purification of monokaryotic transformants and rapid conidia-based identification of the transfer-DNA host genomic DNA flanking sequences. Curr Genet 44:164–171
Rolloos M, Dohmen MHC, Hooykaas PJJ, van der Zaal BJ (2014) Involvement of Rad52 in T-circle formation during Agrobacterium tumefaciens-mediated transformation of Saccharomyces cerevisiae. Mol Microbiol 91:1240–1251
Rolloos M, Hooykaas PJJ, van der Zaal BJ (2015) Enhanced targeted integration mediated by translocated I-SceI during the Agrobacterium mediated transformation of yeast. Sci Rep 5:8345
Rossi L, Hohn B, Tinland B (1996) Integration of complete transferred DNA units is dependent on the activity of virulence E2 protein of Agrobacterium tumefaciens. Proc Natl Acad Sci U S A 93:126–130
Sakalis PA, van Heusden GPH, Hooykaas PJJ (2014) Visualization of VirE2 protein translocation by the Agrobacterium type IV secretion system into host cells. Microbiol Open 3:104–117
Salomon S, Puchta H (1998) Capture of genomic and T-DNA sequences during double-strand break repair in somatic plant cells. EMBO J 17:6086–6095
Schrammeijer B, Risseeuw E, Pansegrau W et al (2001) Interaction of the virulence protein VirF of Agrobacterium tumefaciens with plant homologs of the yeast Skp1 protein. Curr Biol 11:258–262
Schrammeijer B, 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. Nucleic Acids Res 31:860–868
Shi Y, Lee LY, Gelvin SB (2014) Is VIP1 important for Agrobacterium-mediated transformation? Plant J 79:848–860
Singer K, Shiboleth YM, Li J, Tzfira T (2012) Formation of complex extrachromosomal T-DNA structures in Agrobacterium tumefaciens-infected plants. Plant Physiol 160:511–522
Skowyra D, Craig KL, Tyers M et al (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91:209–219
Smeenk G, van Attikum H (2013) The chromatin response to DNA breaks: leaving a mark on genome integrity. Annu Rev Biochem 82:55–80
Soltani J (2009) Host genes involved in Agrobacterium-mediated transformation. Ph.D. thesis. Leiden University, Leiden, The Netherlands
Soltani J, van Heusden GPH, Hooykaas PJJ (2008) Agrobacterium-mediated transformation of non-plant organisms. In: Tzfira T, Citovsky V (eds) Agrobacterium: from biology to biotechnology, pp 649–675. Springer Press, New York
Soltani J, van Heusden GPH, Hooykaas PJJ (2009) Deletion of host histone acetyltransferases and deacetylases strongly affects Agrobacterium-mediated transformation of Saccharomyces cerevisiae. FEMS Microbiol Lett 298:228–233
Sugui JA, Chang YC, Kwon-Chung KJ (2005) Agrobacterium tumefaciens-mediated transformation of Aspergillus fumigatus: an efficient tool for insertional mutagenesis and targeted gene disruption. Appl Environ Microbiol 71:1798–1802
Sullivan TD, Rooney PJ, Klein BS (2002) Agrobacterium tumefaciens integrates transfer DNA into single chromosomal sites of dimorphic fungi and yields homokaryotic progeny from multinucleate yeast. Eukaryot Cell 1:895–905
Tanguay P, Breuil C (2003) Transforming the sapstaining fungus Ophiostoma piceae with Agrobacterium tumefaciens. Can J Microbiol 49:301–304
Tsuji G, Fujii S, Fujihara N et al (2003) Agrobacterium tumefaciens-mediated transformation for random insertional mutagenesis in Colletotrichum lagenarium. J Gen Plant Pathol 69:230–239
Turk SC, Melchers LS, den Dulk-Ras H et al (1991) Environmental conditions differentially affect vir gene induction in different Agrobacterium strains. Role of the VirA sensor protein. Plant Mol Biol 16:1051–1059
Tzfira T, Rhee Y, Chen MH et al (2000) Nucleic acid transport in plant-microbe interactions: the molecules that walk through the walls. Annu Rev Microbiol 54:187–219
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
Tzfira T, Frankman LR, Vaidya M, Citovsky V (2003) Site-specific integration of Agrobacterium tumefaciens T-DNA via double-stranded intermediates. Plant Physiol 133:1011–1023
Tzfira T, Vaidya M, Citovsky V (2004) Involvement of targeted proteolysis in plant genetic transformation by Agrobacterium. Nature 431:87–92
van Attikum H, Bundock P, Hooykaas PJ (2001) Non-homologous end-joining proteins are required for Agrobacterium T-DNA integration. EMBO J 20:6550–6558
van Attikum H (2003) Genetic requirements for the integration of Agrobacterium T-DNA in the eukaryotic genome. PhD thesis. Leiden University, Leiden, The Netherlands
van Attikum H, Hooykaas PJ (2003) Genetic requirements for the targeted integration of Agrobacterium T-DNA in Saccharomyces cerevisiae. Nucleic Acids Res 31:826–832
van Kregten M, Lindhout BI, Hooykaas PJJ, van der Zaal BJ (2009) Agrobacterium-mediated T-DNA transfer and integration by minimal VirD2 consisting of the relaxase domain and a type IV secretion system translocation signal. Mol Plant-Micr Int 22:1356–1365
van Kregten M, de Pater S, Romeijn R, van Schendel R, Hooykaas PJJ, Tijsterman M (2016) T-DNA integration in plants results from polymerase-θ-mediated DNA repair. Nature Plants 2:16164
Vergunst AC, Schrammeijer B, Den Dulk A et al (2000) VirB/D4-dependent protein translocation from Agrobacterium into plant cells. Science 290:979–982
Vergunst AC, van Lier MCM, den Dulk-Ras A et al (2005) Positive charge is an important feature of the C-terminal teransport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc Natl Acad Sci U S A 102:832–837
Walton FJ, Idnurm A, Heitman J (2005) Novel gene functions required for melanization of the human pathogen Cryptococcus neoformans. Mol Microbiol 57:1381–1396
Wang Y, Peng W, Zhou X, Huang F, Shao L, Luo M (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
Wang Y, Wang R, Mao WJ et al (2016) A simple and efficient transformation system for the edible mushroom Pleurotus eryngii. Mycoscience 57:356–360
White D, Chen W (2006) Genetic transformation of Ascochyta rabiei using Agrobacterium-mediated transformation. Curr Genet 49:272–280
Winans SC (1991) An Agrobacterium two-component regulatory system for the detection of chemicals released from plant wounds. Mol Microbiol 5:2345–2350
Wolterink-van Loo S, Ayala AAE, Hooykaas PJJ, van Heusden GPH (2015) Interaction of the Agrobacterium tumefaciens virulence protein VirD2 with histones. Microbiology 161:401–410
Yousefi-Pour HM, Soltani J, Nazeri S (2013) A survey on optimization of Agrobacterium-mediated genetic transformation of the fungus Colletotrichum gloeosporioides. J Cell Mol Res 5:35–41
Yu X, Huo L, Liu H et al (2015) Melanin is required for the formation of the multi-cellular conidia in the endophytic fungus Pestalotiopsis microspora. Microbiol Res 179:1–11
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
Zhang A, Lu P, Dahl-Roshak AM et al (2003) Efficient disruption of a polyketide synthase gene (pks1) required for melanin synthesis through Agrobacterium-mediated transformation of Glarea lozoyensis. Mol Genet Genomics 268:645–655
Zhang J, Shi L, Chen H et al (2014) An efficient Agrobacterium-mediated transformation method for the edible mushroom Hypsizygus marmoreus. Microbiol Res 169:741–748
Zhang T, Ren P, Chaturvedi V et al (2015) Development of an Agrobacterium-mediated transformation system for the cold-adapted fungi Pseudogymnoascus destructans and P. pannorum. Fungal Genet Biol 81:73–81
Zhang X (2016) Functional analysis of Agrobacterium tumefaciens virulence protein VirD5. Ph.D. thesis. Leiden University, Leiden, The Netherlands
Zhang X, van Heusden GPH, Hooykaas PJJ (2017) Virulence protein VirD5 of Agrobacterium tumefaciens binds to kinetochores in host cells via an interaction with Spt4. Proc Natl Acad Sci U S A 114:10238–10243
Zhu J, Oger PM, Schrammeijer B et al (2000) The bases of crown gall tumorigenesis. J Bacteriol 182:3885–3895
Zhu Y, Nam J, Humara JM et al (2003) Identification of Arabidopsis rat mutants. Plant Physiol 132:494–505
Zwiers LH, de Waard MA (2001) Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Curr Genet 39:388–393
Acknowledgements
We acknowledge the contributions of Amke den Dulk-Ras, Alice Beijersbergen, Paul Bundock, Haico van Attikum, Jesus Escudero, Marcel de Groot, Carolien Michielse, Barbara Schrammeijer, Martijn Rolloos, and Suzanne Wolterink to our research regarding AMT of yeast and fungi. We had to restrict the numbers of references. Therefore, we apologize to those whose work related to the topic we did not refer to. The work in our laboratory was supported over the years by grants from the divisions Earth and Life Sciences (ALW) and Chemical Sciences (CW) of the Netherlands Organization of Scientific Research NWO, the organization for Applied Research (STW), and the Royal Netherlands Academy of Arts and Sciences (KNAW).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2018 Springer International Publishing AG, part of Springer Nature
About this chapter
Cite this chapter
Hooykaas, P.J.J. et al. (2018). Agrobacterium-Mediated Transformation of Yeast and Fungi. In: Gelvin, S. (eds) Agrobacterium Biology. Current Topics in Microbiology and Immunology, vol 418. Springer, Cham. https://doi.org/10.1007/82_2018_90
Download citation
DOI: https://doi.org/10.1007/82_2018_90
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-03256-2
Online ISBN: 978-3-030-03257-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)