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Plant tumors: a hundred years of study

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Abstract

Main conclusion

The review provides information on the mechanisms underlying the development of spontaneous and pathogen-induced tumors in higher plants. The activation of meristem-specific regulators in plant tumors of various origins suggests the meristem-like nature of abnormal plant hyperplasia.

Abstract

Plant tumor formation has more than a century of research history. The study of this phenomenon has led to a number of important discoveries, including the development of the Agrobacterium-mediated transformation technique and the discovery of horizontal gene transfer from bacteria to plants. There are two main groups of plant tumors: pathogen-induced tumors (e.g., tumors induced by bacteria, viruses, fungi, insects, etc.), and spontaneous ones, which are formed in the absence of any pathogen in plants with certain genotypes (e.g., interspecific hybrids, inbred lines, and mutants). The causes of the transition of plant cells to tumor growth are different from those in animals, and they include the disturbance of phytohormonal balance and the acquisition of meristematic characteristics by differentiated cells. The aim of this review is to discuss the mechanisms underlying the development of most known examples of plant tumors.

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References

  • Ahuja MR (1968) An hypothesis and evidence concerning the genetic components controlling tumor formation in Nicotiana. Mol Gen Genet 103:176–184

    CAS  PubMed  Google Scholar 

  • Ahuja MR (1971) Genetic control of phytohormones in tumor and non-tumor genotypes in Nicotiana. Indian J Exp Biol 9:60–68

    CAS  Google Scholar 

  • Ahuja MR (1998) Genetic tumors in Nicotiana and other plants. Q Rev Biol 73:439–459

    Google Scholar 

  • Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119:109–120. https://doi.org/10.1016/j.cell.2004.09.018

    Article  CAS  PubMed  Google Scholar 

  • Akiyoshi DE, Morris RO, Hinz R, Mischke BS, Kosuge T, Garfinkel DJ, Gordon MP, Nester EW (1983) Cytokinin/auxin balance in crown gall tumors is regulated by specific loci in the T-DNA. Proc Natl Acad Sci USA 80:407–411

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ali MA, Azeem F, Bohlmann H (2017) Smart parasitic nematodes use multifaceted strategies to parasitize plants. Front Plant Sci 8:1699. https://doi.org/10.3389/fpls.2017.01699

    Article  PubMed  PubMed Central  Google Scholar 

  • Ali MA, Anjam MS, Nawaz MA, Lam HM, Chung G (2018) Signal transduction in plant—nematode interactions. Int J Mol Sci. https://doi.org/10.3390/ijms19061648

    Article  PubMed  PubMed Central  Google Scholar 

  • de Almeida EJ, Gheysen G (2013) Nematode-induced endoreduplication in plant host cells: why and how? Mol Plant Microbe Interact 26:17–24. https://doi.org/10.1094/MPMI-05-12-0128-CR

    Article  CAS  Google Scholar 

  • Ames IH (1972) The influence of cytokinin on genetic tumor formation. Can J Bot 50:2235–2238

    CAS  Google Scholar 

  • Ames IH, Mistretta PW (1975) Auxin: its role in genetic tumor induction. Plant Physiol 56:744–746

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anzola JM, Sieberer T, Ortbauer M, Butt H, Korbei B, Weinhofer I, Müllner AE, Luschnig C (2010) Putative Arabidopsis transcriptional adaptor protein (PROPORZ1) is required to modulate histone acetylation in response to auxin. Proc Natl Acad Sci USA 107:10308–10313. https://doi.org/10.1073/pnas.0913918107

    Article  PubMed  PubMed Central  Google Scholar 

  • Aoki S, Syono K (1999) Synergistic function of rolB, rolC, ORF13 and ORF14 of TL-DNA of Agrobacterium rhizogenes in hairy root induction in Nicotiana tabacum. Plant Cell Physiol 40:252–256

    CAS  Google Scholar 

  • Aragón IM, Pérez-Martínez I, Moreno-Perez A, Cerezo M, Ramos C (2014) New insights into the role of indole-3-acetic acid in the virulence of Pseudomonas savastanoi pv. savastanoi. FEMS Microbiol Lett 356:184–192. https://doi.org/10.1111/1574-6968.12413

    Article  CAS  PubMed  Google Scholar 

  • Arguello-Astorga G, Lopez-Ochoa L, Kong LJ, Orozco BM, Settlage SB, Hanley-Bowdoin L (2004) A novel motif in geminivirus replication proteins interacts with the plant retinoblastoma-related protein. J Virol 78:4817–4826

    CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong WP (1995) To be or not to be a gall. Pac Hortic 56:39–45

    Google Scholar 

  • Ascencio-Ibáñez JT, Sozzani R, Lee TJ, Chu TM, Wolfinger RD, Cella R, Hanley-Bowdoin L (2008) Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol 148:436–454. https://doi.org/10.1104/pp.108.121038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bailey S, Percy DM, Hefer CA, Cronk QC (2015) The transcriptional landscape of insect galls: psyllid (Hemiptera) gall formation in Hawaiian Metrosideros polymorpha (Myrtaceae). BMC Genomics 16:943. https://doi.org/10.1186/s12864-015-2109-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Balkunde R, Kitagawa M, Xu XM, Wang J, Jackson D (2017) SHOOT MERISTEMLESS trafficking controls axillary meristem formation, meristem size and organ boundaries in Arabidopsis. Plant J 90:435–446. https://doi.org/10.1111/tpj.13504

    Article  CAS  PubMed  Google Scholar 

  • Bardaji L, Pérez-Martínez I, Rodríguez-Moreno L, Rodríguez-Palenzuela P, Sundin GW, Ramos C, Murillo J (2011) Sequence and role in virulence of the three plasmid complement of the model tumor-inducing bacterium Pseudomonas savastanoi pv. savastanoi NCPPB 3335. PLoS One 6:e25705. https://doi.org/10.1371/journal.pone.0025705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barry GF, Rogers SG, Fraley RT (1984) Identification of a cloned cytokinin biosynthesis gene. Proc Natl Acad Sci USA 81:4776–4780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Beeckman T, De Smet I (2014) Pericycle. Curr Biol 24:R378–R379. https://doi.org/10.1016/j.cub.2014.03.031

    Article  CAS  PubMed  Google Scholar 

  • Bellec Y, Harrar Y, Butaeye C, Darnet C, Bellini C, Faure J-D (2002) Pasticcino 2 is a protein tyrosine phosphatase-like involved in cell proliferation and differentiation in Arabidopsis. Plant J 32:713–722

    CAS  PubMed  Google Scholar 

  • Berger AH, Knudson AG, Pandolfi PP (2011) A continuum model for tumour suppression. Nature 476:163–169. https://doi.org/10.1038/nature10275

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Betsuyaku S, Sawa S (2011) Yamada M (2011) The function of the CLE peptides in plant development and plant-microbe interactions. Arabidopsis Book 9:e0149. https://doi.org/10.1199/tab.0149

    Article  PubMed  PubMed Central  Google Scholar 

  • Bird MD, Koltai H (2000) Plant parasitic nematodes: habitats, hormones and horizontally-acquired genes. J Plant Growth Regul 19:183–194

    CAS  PubMed  Google Scholar 

  • Bird MD, Loveys BR (1980) The involvement of cytokinins in a host-parasite relationship between tomato (Lycopersicon esculentum) and nematode (Meloidogyne javanica). Parasitology 80:497–505

    CAS  Google Scholar 

  • Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44

    CAS  PubMed  Google Scholar 

  • Bogani P, Lio P, Intrieri MC, Buiatti M (1997) A physiological and molecular analysis of the genus Nicotiana. Mol Phylogenet Evol 7:62–70

    CAS  PubMed  Google Scholar 

  • Boivin S, Fonouni-Farde C, Frugier F (2016) How auxin and cytokinin phytohormones modulate root microbe interactions. Front Plant Sci 7:1240. https://doi.org/10.3389/fpls.2016.01240

    Article  PubMed  PubMed Central  Google Scholar 

  • Boniotti MB, Gutierrez C (2001) A cell-cycle-regulated kinase activity phosphorylates plant retinoblastoma protein and contains, in Arabidopsis, a CDKA/cyclin D complex. Plant J 28:341–350

    CAS  PubMed  Google Scholar 

  • Borghi L, Gutzat R, Fütterer J, Laizet Y, Hennig L, Gruissem W (2010) Arabidopsis RETINOBLASTOMA-RELATED is required for stem cell maintenance, cell differentiation, and lateral organ production. Plant Cell 22:1792–1811. https://doi.org/10.1105/tpc.110.074591

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boucheron E, Healy JH, Bajon C, Sauvanet A, Rembur J, Noin M, Sekine M, Riou-Khamlichi C, Murray JA, Van Onckelen H, Chriqui D (2005) Ectopic expression of Arabidopsis CYCD2 and CYCD3 in tobacco has distinct effects on the structural organization of the shoot apical meristem. J Exp Bot 56:123–134

    CAS  PubMed  Google Scholar 

  • Boudolf V, Rombauts S, Naudts M, Inzé D, De Veylder L (2001) Identification of novel cyclin-dependent kinases interacting with the CKS1 protein of Arabidopsis. J Exp Bot 52:1381–1382

    CAS  PubMed  Google Scholar 

  • Bouton S, Leboeuf E, Mouille G, Leydecker MT, Talbotec J, Granier F, Lahaye M, Höfte H, Truong HN (2002) QUASIMODO1 encodes a putative membrane-bound glycosyltransferase required for normal pectin synthesis and cell adhesion in Arabidopsis. Plant Cell 14:2577–2590

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bulgakov VP, Shkryl YN, Veremeichik GN, Gorpenchenko TY, Vereshchagina YV (2013) Recent advances in the understanding of Agrobacterium rhizogenes-derived genes and their effects on stress resistance and plant metabolism. Adv Biochem Eng Biotechnol 134:1–22. https://doi.org/10.1007/10_2013_179

    Article  CAS  PubMed  Google Scholar 

  • Buzovkina IS, Lutova LA (2007) Genetic collection of inbred lines of radish: history and prospects. Rus J Genet 4:1411–1423

    Google Scholar 

  • Cabrera J, Fenoll C, Escobar C (2015) Genes co-regulated with LBD16 in nematode feeding sites inferred from in silico analysis show similarities to regulatory circuits mediated by the auxin/cytokinin balance in Arabidopsis. Plant Signal Behav 10:e990825. https://doi.org/10.4161/15592324.2014.990825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Campbell L, Turner S (2017) Regulation of vascular cell division. J Exp Bot 68:27–43. https://doi.org/10.1093/jxb/erw448

    Article  CAS  PubMed  Google Scholar 

  • Campell BR, Town CD (1991) Physiology of hormone autonomous tissue lines derived form radiation-induced tumors of Arabidopsis thaliana. Plant Physiol 97:1166–1173

    CAS  PubMed  PubMed Central  Google Scholar 

  • Caponero A, Contesini AM, Iacobellis NS (1995) Population diversity of Pseudomonas syringae subsp. savastanoi on olive and oleander. Plant Pathol 44:848–855

    Google Scholar 

  • Chalupowicz L, Barash I, Schwartz M, Aloni R, Manulis S (2006) Comparative anatomy of gall development on Gypsophila paniculata induced by bacteria with different mechanisms of pathogenicity. Planta 224:429–437

    CAS  PubMed  Google Scholar 

  • Chalupowicz L, Weinthal D, Gaba V, Sessa V, Barash I, Manulis-Sasson S (2013) Polar auxin transport is essential for gall formation by Pantoea agglomerans on gypsophila. Mol Plant Pathol 14:185–190. https://doi.org/10.1111/j.1364-3703.2012.00839.x

    Article  CAS  PubMed  Google Scholar 

  • Chanclud E, Morel JB (2016) Plant hormones: a fungal point of view. Mol Plant Pathol 17:1289–1297. https://doi.org/10.1111/mpp.12393

    Article  PubMed  PubMed Central  Google Scholar 

  • Chaubet-Gigot N (2000) Plant A-type cyclins. Plant Mol Biol 43:659–675

    CAS  PubMed  Google Scholar 

  • Chen K, Dorlhac de Borne F, Szegedi E, Otten L (2014) Deep sequencing of the ancestral tobacco species Nicotiana tomentosiformis reveals multiple T-DNA inserts and a complex evolutionary history of natural transformation in the genus Nicotiana. Plant J 80:669–682. https://doi.org/10.1111/tpj.12661

    Article  CAS  PubMed  Google Scholar 

  • Chetverikov PE, Vishnyakov AE, Dodueva IE, Osipova MA, Sukhareva SI, Shavarda AL (2015) Gallogenesis induced by eryophyoid mites (Acariformes: Eriophyoidea). Entomol Rev 95:1137–1143

    Google Scholar 

  • Chilton MD, Drummond MH, Merio DJ, Sciaky D, Montoya AL, Gordon MP, Nester EW (1977) Stable incorporation of plasmid DNA into higher plant cells: the molecular basis of crown gall tumorigenesis. Cell 11:263–271

    CAS  PubMed  Google Scholar 

  • Chuck C, Lincoln C, Hake S (1996) KNAT1 induces lobed leaves with ectopic meristems when overexpressed in Arabidopsis. Plant Cell 8:1277–1289

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chung KR, Zheng DD (2004) Biosynthesis of indole-3-acetic acid by the gall-inducing fungus Ustillago esculenta. J Biol Sci 4:744–750

    CAS  Google Scholar 

  • Cissé OH, Almeida JM, Fonseca A, Kumar AA, Salojärvi J, Overmyer K, Hauser PM, Pagni M (2013) Genome sequencing of the plant pathogen Taphrina deformans, the causal agent of peach leaf curl. MBio 4:e00055–e113. https://doi.org/10.1128/mBio.00055-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark E, Vigodsky-Haas H, Gafni Y (1989) Characteristics in tissue culture of hyperplasias induced by Erwinia herbicola pathovar gypsophilae. Physiol Mol Plant Pathol 35:383–390

    CAS  Google Scholar 

  • Clark E, Manulis S, Ophir Y, Barash I, Gafni Y (1993) Cloning and characterization of iaaM and iaaH from Erwinia herbicola pathovar gypsophilae. Phytopathology 83:234–240

    CAS  Google Scholar 

  • Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122:1567–1575

    CAS  PubMed  Google Scholar 

  • Cockcroft CE, den Boer BG, Healy JM, Murray JA (2000) Cyclin D control of growth rate in plants. Nature 405:575–579

    CAS  PubMed  Google Scholar 

  • Coelho RR, Vieira P, de Souza A, Júnior JD, Martin-Jimenez C, De Veylder L, Cazareth J, Engler G, Grossi-de-Sa MF, de Almeida EJ (2017) Exploiting cell cycle inhibitor genes of the KRP family to control root-knot nematode induced feeding sites in plants. Plant Cell Environ 40:1174–1188. https://doi.org/10.1111/pce.12912

    Article  CAS  PubMed  Google Scholar 

  • Da Costa M, Bach L, Landrieu I, Bellec Y, Catrice O, Brown S, De Veylder L, Lippens G, Inze D, Faure JD (2006) Arabidopsis PASTICCINO2 is an antiphosphatase involved in regulation of cyclin-dependent kinase A. Plant Cell 18:1426–1437

    PubMed  PubMed Central  Google Scholar 

  • Crespi M, Messens E, Caplan AB, Van Montagu M, Desomer J (1992) Fasciation induction by the phytopathogen Rhodococcus fascians depends upon a linear plasmid encoding a cytokinin synthase gene. EMBO J 11:795–804

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cruz-Ramírez A, Díaz-Triviño S, Wachsman G, Du Y, Arteága-Vázquez M, Zhang H, Benjamins R, Blilou I, Neef AB, Chandler V, Scheres B (2013) A SCARECROW-RETINOBLASTOMA protein network controls protective quiescence in the Arabidopsis root stem cell organizer. PLoS Biol 11(11):e1001724. https://doi.org/10.1371/journal.pbio.1001724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davies JW (1987) Geminivirus genomes. Microbiol Sci 4:18–23

    CAS  PubMed  Google Scholar 

  • Dekhuijzen HM, Overeem JC (1971) The role of cytokinins in clubroot formation. Physiol Plant Pathol 1:151–161

    CAS  Google Scholar 

  • Deom CM, Mills-Lujan K (2015) Toward understanding the molecular mechanism of a geminivirus C4 protein. Plant Signal Behav 10:e1109758. https://doi.org/10.1080/15592324.2015.1109758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Depuydt S, Doležal K, Van Lijsebettens M, Moritz T, Holsters M, Vereecke D (2008) Modulation of the hormone setting by Rhodococcus fascians results in ectopic KNOX activation in Arabidopsis. Plant Physiol 146:1267–1281. https://doi.org/10.1104/pp.107.113969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Depuydt S, De Veylder L, Holsters M, Vereecke D (2009) Eternal youth, the fate of developing Arabidopsis leaves upon Rhodococcus fascians infection. Plant Physiol 149:1387–1398. https://doi.org/10.1104/pp.108.131797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Devos S, Vissenberg K, Verbelen J-P, Prinsen E (2005) Infection of Chinese cabbage by Plasmodiophora brassicae leads to a stimulation of plant growth: impacts on cell wall metabolism and hormone balance. New Phytol 166:241–250

    CAS  PubMed  Google Scholar 

  • Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jaqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia and inhibited differentiation in Arabidopsis caused by the D-type cyclin CycD3. Plant Cell 15:79–92

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, Braun N, Collins C, Nieuwland J, Prinsen E, Sundaresan V, Murray JA (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA 104:14537–14542

    CAS  PubMed  PubMed Central  Google Scholar 

  • Doehlemann G, Wahl R, Horst RJ, Voll L, Usadel B, Poree F, Stitt M, Pons-Kuehnemann J, Sonnewald U, Kahmann R (2008) Reprogramming a maize plant: transcriptional and metabolic changes induced by the fungal biotroph Ustilago maydis. Plant J 56:181–195. https://doi.org/10.1111/j.1365-313X.2008.03590.x

    Article  CAS  PubMed  Google Scholar 

  • Dolzblasz A, Nardmann J, Clerici E, Causier B, van der Graaff E, Chen J, Davies B, Werr W, Laux T (2016) Stem cell regulation by Arabidopsis WOX genes. Mol Plant 9:1028–1039. https://doi.org/10.1016/j.molp.2016.04.007

    Article  CAS  PubMed  Google Scholar 

  • Dolzblasz A, Banasiak A, Vereecke D (2018) Neovascularization during leafy gall formation on Arabidopsis thaliana upon Rhodococcus fascians infection. Planta 247:215–228. https://doi.org/10.1007/s00425-017-2778-5

    Article  CAS  PubMed  Google Scholar 

  • Doonan JH, Sablowski R (2010) Walls around tumours—why plants do not develop cancer. Nat Rev Cancer 10:794–802. https://doi.org/10.1038/nrc2942

    Article  CAS  PubMed  Google Scholar 

  • Dorchin N, Hoffmann JH, Stirk WA, Novak O, Strnad M, van Staden J (2009) Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae. Physiol Entomol 34:359–369. https://doi.org/10.1111/j.1365-3032.2009.00702.x

    Article  Google Scholar 

  • Dowd CD, Chronis D, Radakovic ZS, Siddique S, Schmülling T, Werner T, Kakimoto T, Grundler FMW, Mitchum MG (2017) Divergent expression of cytokinin biosynthesis, signaling and catabolism genes underlying differences in feeding sites induced by cyst and root-knot nematodes. Plant J 92:211–228. https://doi.org/10.1111/tpj.13647

    Article  CAS  PubMed  Google Scholar 

  • Eason JR, Morris RO, Jameson PE (1996) The relationship between virulence and cytokinin production by Rhodococcus fascians. Plant Pathol 45:323–331

    CAS  Google Scholar 

  • Eloy NB, Coppens F, Beemster GT, Hemerly AS, Ferreira PC (2004) The Arabidopsis anaphase promoting complex (APC): regulation through subunit availability in plant tissues. Cell Cycle 5:1957–1965

    Google Scholar 

  • Espírito-Santo MM, Fernandes GW (2007) How many species of galling insects are there on earth and where they are? Ann Entomol Soc Am 100:95–99

    Google Scholar 

  • Etchells JP, Provost CM, Mishra L, Turner SR (2013) WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development 140:2224–2234. https://doi.org/10.1242/dev.091314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Etchells JP, Smit ME, Gaudinier A, Williams CJ, Brady SM (2016) A brief history of the TDIF-PXY signalling module: balancing meristem identity and differentiation during vascular development. New Phytol 209:474–484. https://doi.org/10.1111/nph.13642

    Article  CAS  PubMed  Google Scholar 

  • Eves-Van Den Akker S, Lilley CJ, Yusup HB, Jones JT, Urwin PE (2016) Functional C-TERMINALLY ENCODED PEPTIDE (CEP) plant hormone domains evolved de novo in the plant parasite Rotylenchulus reniformis. Mol Plant Pathol 17:1265–1275. https://doi.org/10.1111/mpp.12402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Faure JD, Vittorioso P, Santoni V, Fraisier V, Prinsen E, Barlier I, Van Onckelen H, Caboche M, Bellini C (1998) The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development 125:909–918

    CAS  PubMed  Google Scholar 

  • Frank M, Rupp HM, Prinsen E, Motyka V, Van Onckelen H, Schmulling T (2000) Hormone autotrophic growth and differentiation identifies mutant lines of Arabidopsis with altered cytokinin and auxin content or signaling. Plant Physiol 122:721–729

    CAS  PubMed  PubMed Central  Google Scholar 

  • Frank M, Guivarch A, Krupkova E, Lorenz-Meyer I, Chriqui D, Schmulling T (2002) Tumorous shoot development (TSD) genes are required for coordinated plant shoot development. Plant J 29:73–85

    CAS  PubMed  Google Scholar 

  • Frémont N, Riefler M, Stolz A, Schmülling T (2013) The ArabidopsisTUMOR PRONE5 gene encodes an acetylornithine aminotransferase required for arginine biosynthesis and root meristem maintenance in blue light. Plant Physiol. 161:1127–1140. https://doi.org/10.1104/pp.112.210583

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furner IJ, Huffman GA, Amasino RM, Garfinkel DJ, Gordon MP, Nester EW (1986) An Agrobacterium transformation in the evolution of the genus Nicotiana. Nature 319:422–427

    CAS  Google Scholar 

  • Gaffney TD, da Costa-e-Silva O, Yamada T, Kosuge T (1990) Indoleacetic acid operon of Pseudomonas syringae subsp. savastanoi: transcription analysis and promoter identification. J Bacteriol 172:5593–5601

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gao BL, Allen R, Maier T, Davis EL, Baum TJ, Hussey RS (2003) The parasitome of the phytonematode Heterodera glycines. Mol Plant Microbe Interact 16:720–726

    CAS  PubMed  Google Scholar 

  • Garfinkel DJ, Simpson RB, Ream LW, White FF, Gordon MP, Nester EW (1981) Genetic analysis of crown gall: fine structure map of the T-DNA by site-directed mutagenesis. Cell 27:143–153

    CAS  PubMed  Google Scholar 

  • Gelvin SB (2017) Integration of Agrobacterium T-DNA into the plant genome. Annu Rev Genet 51:195–217. https://doi.org/10.1146/annurev-genet-120215-035320

    Article  CAS  PubMed  Google Scholar 

  • Giron D, Huguet E, Stone GN, Body M (2016) Insect-induced effects on plants and possible effectors used by galling and leaf-mining insects to manipulate their host-plant. J Insect Physiol 84:70–89. https://doi.org/10.1016/j.jinsphys.2015.12.009

    Article  CAS  PubMed  Google Scholar 

  • Glass NL, Kosuge S (1988) Role of indoleacetic acid-lysine synthetase in regulation of indoleacetic acid pool size and virulence of Pseudomonas syringae subsp. savastanoi. J Bacteriol 170:2367–2373

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gohlke J, Deeken R (2014) Plant responses to Agrobacterium tumefaciens and crown gall development. Front Plant Sci 5:155. https://doi.org/10.3389/fpls.2014.00155

    Article  PubMed  PubMed Central  Google Scholar 

  • González-Lamothe R, El Oirdi M, Brisson N, Bouarab K (2012) The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development. Plant Cell 24:762–777. https://doi.org/10.1105/tpc.111.095190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goto M, Kuwata H (1988) Rhizobacter daucus, the causal agent of carrot bacterial gall. Int J Syst Bacteriol 38:233–239

    Google Scholar 

  • Goverse A, Overmars H, Engelbertink J, Schots A, Bakker J, Helder J (2000) Both induction and morphogenesis of cyst nematode feeding cells are mediated by auxin. Mol Plant Microbe Interact 13:1121–1129

    CAS  PubMed  Google Scholar 

  • van der Graaff E, Laux T, Rensing SA (2009) The WUS homeobox-containing (WOX) protein family. Genome Biol 10:238–248. https://doi.org/10.1186/gb-2009-10-12-248

    Article  CAS  Google Scholar 

  • Grsic-Rausch S, Kobelt P, Siemens JM, Bischoff M, Ludwig-Müller J (2000) Expression and localization of nitrilase during symptom development of the clubroot disease in Arabidopsis. Plant Physiol 122:369–378

    CAS  PubMed  PubMed Central  Google Scholar 

  • Grunewald W, Cannoot B, Friml J, Gheysen G (2009) Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection. PLoS Pathog 5:e1000266. https://doi.org/10.1371/journal.ppat.1000266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63:889–900. https://doi.org/10.1111/j.1365-313X.2010.04295.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X, Chronis D, De La Torre CM, Smeda J, Wang X, Mitchum MG (2015) Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors. Plant Biotechnol J 13:801–810. https://doi.org/10.1111/pbi.12313

    Article  CAS  PubMed  Google Scholar 

  • Guo X, Wang J, Gardner M, Fukuda H, Kondo Y, Etchells JP, Wang X, Mitchum MG (2017) Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation. PLoS Pathol 13:e1006142. https://doi.org/10.1371/journal.ppat.1006142

    Article  CAS  Google Scholar 

  • Hagen GL (1962) Morphogenesis in a tobacco hybrid tumor. Dev Biol 4:569–579

    CAS  PubMed  Google Scholar 

  • Hanley-Bowdoin L, Settlage SB, Robertson D (2004) Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Mol Plant Pathol 15:149–156

    Google Scholar 

  • Hann DR, Domínguez-Ferreras A, Motyka V, Dobrev PI, Schornack S, Jehle A, Felix G, Chinchilla D, Rathjen JP, Boller T (2014) The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol 201:585–598. https://doi.org/10.1111/nph.12544

    Article  CAS  PubMed  Google Scholar 

  • Hazak O, Hardtke CS (2016) CLAVATA 1-type receptors in plant development. J Exp Bot 67:4827–4833. https://doi.org/10.1093/jxb/erw247

    Article  CAS  PubMed  Google Scholar 

  • Heidstra R, Sabatini S (2014) Plant and animal stem cells: similar yet different. Nat Rev Mol Cell Biol 15:301–312. https://doi.org/10.1038/nrm3790

    Article  CAS  PubMed  Google Scholar 

  • Helfer A, Pien S, Otten L (2002) Functional diversity and mutational analysis of Agrobacterium 6B oncoproteins. Mol Genet Genomics 267:577–586

    CAS  PubMed  Google Scholar 

  • Helfer A, Clement B, Michler P, Otten L (2003) The Agrobacterium oncogene AB-6b causes a graft-transmissible enation syndrome in tobacco. Plant Mol Biol 52:483–493

    CAS  PubMed  Google Scholar 

  • Hibino H (1996) Biology and epidemiology of rice viruses. Ann Rev Phytopathol 34:249–274

    CAS  Google Scholar 

  • Hilbert M, Voll LM, Ding Y, Hofmann J, Sharma M, Zuccaro A (2012) Indole derivative production by the root endophyte Piriformospora indica is not required for growth promotion but for biotrophic colonization of barley roots. New Phytol 196:520–534. https://doi.org/10.1111/j.1469-8137.2012.04275.x

    Article  CAS  PubMed  Google Scholar 

  • Hinsch J, Vrabka J, Oeser B, Novák O, Galuszka P, Tudzynski P (2015) De novo biosynthesis of cytokinins in the biotrophic fungus Claviceps purpurea. Environ Microbiol 17:2935–2951. https://doi.org/10.1111/1462-2920.12838

    Article  CAS  PubMed  Google Scholar 

  • Hinsch J, Galuszka P, Tudzynski P (2016) Functional characterization of the first filamentous fungal tRNA-isopentenyl transferase and its role in the virulence of Claviceps purpurea. New Phytol 211:980–992. https://doi.org/10.1111/nph.13960

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa Y, Kondo Y, Fukuda H (2010) TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 22:2618–2629. https://doi.org/10.1105/tpc.110.076083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hough JS (1953) Studies on the common spangle gall of oak. III. The importance of the stage in laminar extension of the host leaf. New Phytol 52:218–228

    Google Scholar 

  • Huang GZ, Dong RH, Allen R, Davis EL, Baum TJ, Hussey RS (2006) A root-knot nematode secretory peptide functions as a ligand for a plant transcription factor. Mol Plant Microbe Interact 19:463–470

    CAS  PubMed  Google Scholar 

  • Hwang HH, Yang FJ, Cheng TF, Chen YC, Lee YL, Tsai YL, Lai EM (2013) The Tzs protein and exogenous cytokinin affect virulence gene expression and bacterial growth of Agrobacterium tumefaciens. Phytopathology 103:888–899. https://doi.org/10.1094/PHYTO-01-13-0020-R

    Article  CAS  PubMed  Google Scholar 

  • Iacobellis NS, Sisto A, Surico G, Evidente A, DiMaio E (1994) Pathogenicity of Pseudomonas syringae subsp. savastanoi mutants defective in phytohormone production. J Phytopathol 140:238–248

    Google Scholar 

  • Ikeuchi M, Sugimoto K, Iwase A (2013) Plant callus: mechanisms of induction and repression. Plant Cell 25:3159–3173. https://doi.org/10.1105/tpc.113.116053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ilina EL, Dodueva IE, Ivanova NM, Lutova LA (2006) Effect of cytokinins on in vitro cultivated inbred radish lines of Raphanus sativus var. radicula Pers. with genetically determined tumorigenesis. Rus J Plant Physiol 53:575–584

    Google Scholar 

  • Imai KK, Ohashi Y, Tsuge T, Yoshizumi T, Matsui M, Oka A, Aoyama T (2006) The A-type cyclin CYCA2;3 is a key regulator of ploidy levels in Arabidopsis endoreduplication. Plant Cell 18:382–396

    CAS  PubMed  PubMed Central  Google Scholar 

  • Intrieri MC, Buiatti M (2001) The horizontal transfer of Agrobacterium rhizogenes genes and the evolution of the genus Nicotiana. Mol Phylogenet Evol 20:100–110

    CAS  PubMed  Google Scholar 

  • Inze D, Follin A, Velten J, Velten L, Prinsen E, Rudelsheim P, Van Onckelen H, Schell J, Van Montagu M (1987) The Pseudomonas savastanoi tryptophan-2-mono-oxygenase is biologically active in Nicotiana tabacum. Planta 172:555–562

    CAS  PubMed  Google Scholar 

  • Irani S, Trost B, Waldner M, Nayidu N, Tu J, Kusalik AJ, Todd CD, Wei Y, Bonham-Smith PC (2018) Transcriptome analysis of response to Plasmodiophora brassicae infection in the Arabidopsis shoot and root. BMC Genomics 19:23. https://doi.org/10.1186/s12864-017-4426-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito M, Machida Y (2015) Reprogramming of plant cells induced by 6b oncoproteins from the plant pathogen Agrobacterium. J Plant Res 128:423–435. https://doi.org/10.1007/s10265-014-0694-3

    Article  CAS  PubMed  Google Scholar 

  • Ivanov VB (2003) The problem of stem cells in plants. Russ J Dev Biol 34:205–212

    Google Scholar 

  • Iwai H, Masaoka N, Ishii T, Satoh S (2002) A pectin glucuronyl transferase gene is essential for intercellular attachment in the plant meristem. Proc Natl Acad Sci USA 10:16319–16324

    Google Scholar 

  • Jahn L, Mucha S, Bergmann S, Horn C, Staswick P, Steffens B, Siemens J, Ludwig-Müller J (2013) The clubroot pathogen (Plasmodiophora brassicae) influences auxin signaling to regulate auxin homeostasis in Arabidopsis. Plants (Basel) 2:726–749. https://doi.org/10.3390/plants2040726

    Article  CAS  Google Scholar 

  • Jameson PE, Dhandapani P, Song J, Zatloukal M, Strnad M, Remus-Emsermann MNP, Schlechter RO, Novák O (2019) The cytokinin complex associated with Rhodococcus fascians: which compounds are critical for virulence? Front Plant Sci 10:674. https://doi.org/10.3389/fpls.2019.00674

    Article  PubMed  PubMed Central  Google Scholar 

  • Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr Biol 6:1560–1565

    Google Scholar 

  • Ji J, Strable J, Shimizu R, Koenig D, Sinha N, Scanlon MJ (2010) WOX4 promotes procambial development. Plant Physiol 152:1346–1356. https://doi.org/10.1104/pp.109.149641

    Article  PubMed  Google Scholar 

  • Jin YS, Seong ES, Qu GZ, Han W, Yoon BS, Wang MH (2008) Cloning and morphological properties of Nicgl;CYCD3;1 gene in genetic tumors from interspecific hybrid of N. langsdorffii and N. glauca. Plant Physiol 165:317–323

    CAS  Google Scholar 

  • Johnston JC, Trione EJ (1974) Cytokinin production by the fungi Taphrina cerasi and T. deformans. Can J Bot 52:1583–1589

    CAS  Google Scholar 

  • Joshi MV, Loria R (2007) Streptomyces turgidiscabies possesses a functional cytokinin biosynthetic pathway and produces leafy galls. Mol Plant Microbe Interact 20:751–758

    CAS  PubMed  Google Scholar 

  • Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000) CDK-related protein kinases in plants. Plant Mol Biol 43:607–620

    PubMed  Google Scholar 

  • Kageyama K, Asano T (2009) Life cycle of Plasmodiophora brassicae. J Plant Growth Regul 28:203–211. https://doi.org/10.1007/s00344-009-9101-z

    Article  CAS  Google Scholar 

  • Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. P Roy Soc B-Biol Sci B 277:2311–2319. https://doi.org/10.1098/rspb.2010.0214

    Article  CAS  Google Scholar 

  • Kane NA, Jones CS, Vuorisalo T (1997) Development of galls of Alnus glutinosa and Alnus incana (Betulaceae) caused by the eriophyid mite Eriophyes laevis (Nalepa). Int J Plant Sci 158:13–23

    Google Scholar 

  • Kawarazaki H, Goto M, Kato K, Kijima T, Kawada H, Yamamoto K, Takikawa Y (2009) Identification of a bacterium isolated from galls on carrot and weeds. J Gen Plant Pathol 75:235–240. https://doi.org/10.1007/s10327-009-0160-6

    Article  CAS  Google Scholar 

  • Kemper E, Waffenschmidt S, Weiler EW, Raush T, Schroeder J (1985) T-DNA-encoded auxin formation in crown gall cells. Planta 163:257–262

    CAS  PubMed  Google Scholar 

  • Kers JA, Cameron KD, Joshi MV, Bukhalid RA, Morello JE, Wach MJ, Gibson DM, Loria R (2005) A large, mobile pathogenicity island confers plant pathogenicity on Streptomyces species. Mol Microbiol 55:1025–1033

    CAS  PubMed  Google Scholar 

  • Kind S, Hinsch J, Vrabka J, Hradilová M, Majeská-Čudejková M, Tudzynski P, Galuszka P (2018) Manipulation of cytokinin level in the ergot fungus Claviceps purpurea emphasizes its contribution to virulence. Curr Genet 64:1303–1319. https://doi.org/10.1007/s00294-018-0847-3

    Article  CAS  PubMed  Google Scholar 

  • Kitakura S, Terakura S, Yoshioka Y, Machida C, Machida Y (2008) Interaction between Agrobacterium tumefaciens oncoprotein 6b and a tobacco nucleolar protein that is homologous to TNP1 encoded by a transposable element of Antirrhinum majus. J Plant Res 121:425–433. https://doi.org/10.1007/s10265-008-0160-1

    Article  CAS  PubMed  Google Scholar 

  • Kobelt P, Siemens J, Sacristan MD (2000) Histological characterization of the incompatible interaction between Arabidopsis thaliana and the obligate biotrophic pathogen Plasmodiophora brassicae. Mycol Res 2:220–225

    Google Scholar 

  • Kong LJ, Orozco BM, Roe JL, Nagar S, Ou S, Feiler HS, Durfee T, Miller AB, Gruissem W, Robertson D, Hanley-Bowdoin L (2000) A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J 19:3485–3495

    CAS  PubMed  PubMed Central  Google Scholar 

  • Korenjak M, Brehm A (2005) E2F-Rb complexes regulating transcription of genes important for differentiation and development. Curr Opin Gen Dev 15:520–527

    CAS  Google Scholar 

  • Kornet N, Scheres B (2009) Members of the GCN5 histone acetyltransferase complex regulate PLETHORA-mediated root stem cell niche maintenance and transit amplifying cell proliferation in Arabidopsis. Plant Cell 21:1070–1079. https://doi.org/10.1105/tpc.108.065300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kostoff D (1930) Tumors and other malformations on certain Nicotiana hybrids. Zentralbl Barkt 81:244–280

    CAS  Google Scholar 

  • Krupková E, Schmülling T (2009) Developmental consequences of the tumorous shoot development1 mutation, a novel allele of the cellulose-synthesizing KORRIGAN1 gene. Plant Mol Biol 71:641–655. https://doi.org/10.1007/s11103-009-9546-2

    Article  CAS  PubMed  Google Scholar 

  • Krupková E, Immerzeel P, Pauly M, Schmülling T (2007) The TUMOROUS SHOOT DEVELOPMENT2 gene of Arabidopsis encoding a putative methyltransferase is required for cell adhesion and coordinated plant development. Plant J 50:735–750

    PubMed  Google Scholar 

  • Kyndt T, Quispe D, Zhai H, Jarret R, Ghislain M, Liu Q, Gheysen G (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 USA 112:5844–5849. https://doi.org/10.1073/pnas.1419685112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kyndt T, Goverse A, Haegeman A, Warmerdam S, Wanjau C, Jahani M, Engler G, de Almeida EJ, Gheysen G (2016) Redirection of auxin flow in Arabidopsis thaliana roots after infection by root-knot nematodes. J Exp Bot 67:4559–4570. https://doi.org/10.1093/jxb/erw230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Latham JR, Saunders K, Pinner MS, Stanley J (1997) Induction of plant cell division by beet curly top virus gene C4. Plant J 11:1273–1283

    CAS  Google Scholar 

  • Lebedeva MA, Tvorogova VE, Vinogradova AP, Gancheva MA, Azarakhsh M, Ilina EL, Demchenko KN, Dodueva IE, Lutova LA (2015) Initiation of spontaneous tumors in radish (Raphanus sativus): cellular, molecular and physiological events. J Plant Physiol 173:97–104. https://doi.org/10.1016/j.jplph.2014.07.030

    Article  CAS  Google Scholar 

  • Lee JH, Kim D-M, Lim YP, Pai H-S (2004) The shooty callus induced by suppression of tobacco CHRK1 receptor-like kinase is a phenocopy of the tobacco genetic tumor. Plant Cell Rep 23:397–403

    CAS  PubMed  Google Scholar 

  • Lee C, Chronis D, Kenning C, Peret B, Hewezi T, Davis EL, Baum TJ, Hussey R, Bennett M, Mitchum MG (2011) The novel cyst nematode effector protein 19C07 interacts with the Arabidopsis auxin influx transporter LAX3 to control feeding site development. Plant Physiol 155:866–880. https://doi.org/10.1104/pp.110.167197

    Article  CAS  PubMed  Google Scholar 

  • Lee ZH, Hirakawa T, Yamaguchi N, Ito T (2019) The roles of plant hormones and their interactions with regulatory genes in determining meristem activity. Int J Mol Sci. https://doi.org/10.3390/ijms20164065

    Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Zeng R, Chen Z, Liu X, Cao Z, Xie Q, Yang C, Lai J (2018) S-acylation of a geminivirus C4 protein is essential for regulating the CLAVATA pathway in symptom determination. J Exp Bot 69:4459–4468. https://doi.org/10.1093/jxb/ery228

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lichter A, Barash I, Valinsky L, Manulis S (1995) The genes involved in cytokinin biosynthesis in Erwinia herbicola pv. gypsophilae: characterization and role in gall formation. J Bacteriol 177:4457–4465

    CAS  PubMed  PubMed Central  Google Scholar 

  • De Ropp RS (1948) The interaction of normal and crown gall tumor tissue in vitro grafts. Am J Bot 35:372–377

    Google Scholar 

  • De Lillo E, Monfreda R (2004) Salivary secretions of eriophyoids (Acari: Eriophyoidea): first results of an experimental model. Exp App Acarol 34:291–306

    Google Scholar 

  • De Meutter J, Tytgat T, Witters E, Gheysen G, Van Onckelen H, Gheysen G (2003) Identification of cytokinin produced by the plant parasitic nematodes Heterodera schachtii and Meloidogyne incognita. Mol Plant Pathol 4:271–277

    PubMed  Google Scholar 

  • De O-Manes CL, Van Montagu M, Prinsen E, Goethals K, Holsters M (2001) De novo cortical cell division triggered by the phytopathogen Rhodococcus fascians in tobacco. Mol Plant Microbe Interact 14:189–195

    Google Scholar 

  • De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jürgens G, Ingram GC, Inzé D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597. https://doi.org/10.1126/science.1160158

    Article  CAS  PubMed  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GT, Krols L, Terras F, Landrieu I, van der Schueren E, Maes S, Naudts M, Inzé D (2001) Functional analysis of cyclin-dependent kinase inhibitors of Arabidopsis. Plant Cell 13:1653–1668

    PubMed  PubMed Central  Google Scholar 

  • De Veylder L, Beeckman T, Beemster GT, de Almeida EJ, Ormenese S, Maes S, Naudts M, Van Der Schueren E, Jacqmard A, Engler G, Inzé D (2002) Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa-DPa transcription factor. EMBO J 21:1360–1368

    PubMed  PubMed Central  Google Scholar 

  • Littau VC, Black LM (1952) Spontaneous tumors in sweet clover. Am J Bot 39:191–194

    Google Scholar 

  • Lohar DP, Schaff JE, Laskey JG, Kieber JJ, Bilyeu KD, Bird DM (2004) Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. Plant J 38:203–214

    CAS  PubMed  Google Scholar 

  • Long JA, Moan EI, Medford JJ, Barton MK (1996) A member of the KNOTTED class of homeodomain proteins encoded by the SHOOT-MERISTEMLESS gene of Arabidopsis. Nature 379:66–69

    CAS  PubMed  Google Scholar 

  • Lopez-Bucio J, Millán-Godínez M, Méndez-Bravo A, Morquecho-Contreras A, Ramírez-Chávez E, Molina-Torres J, Pérez-Torres A, Higuchi M, Kakimoto T, Herrera-Estrella L (2007) Cytokinin receptors are involved in alkamide regulation of root and shoot development in Arabidopsis. Plant Physiol 145:1703–1713

    CAS  PubMed  PubMed Central  Google Scholar 

  • Lv MF, Xie L, Song XJ, Hong J, Mao QZ, Wei TY, Chen JP, Zhang HM (2017) Phloem-limited reoviruses universally induce sieve element hyperplasia and more flexible gateways, providing more channels for their movement in plants. Sci Rep 7:16467. https://doi.org/10.1038/s41598-017-15686-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma LJ, Geiser DM, Proctor RH, Rooney AP, O'Donnell K, Trail F, Gardiner DM, Manners JM, Kazan K (2013) Fusarium pathogenomics. Annu Rev Microbiol 67:399–416. https://doi.org/10.1146/annurev-micro-092412-155650

    Article  CAS  PubMed  Google Scholar 

  • MacDermott J, Meilan R, Thornburg R (1996) Plant-insect interactions: the hackberry nipple gall. World Wide Web J Biol 2. https://epress.com/w3jbio/vol2/mcdermott/mcdermott.html

  • MacDonald EMS, Powell GK, Regier DA, Glass LN, Roberto F, Kosuge T, Morris RO (1986) Secretion of zeatin, ribosylzeatin and ribosyl-1ʺ-methylzeatin by Pseudomonas savastanoi. Plant Physiol 82:742–747

    CAS  PubMed  PubMed Central  Google Scholar 

  • Magyar Z, Atanassova A, De Veylder L, Rombauts S, Inzé D (2000) Characterization of two distinct DP-related genes from Arabidopsis thaliana. FEBS Lett 486:79–87

    CAS  PubMed  Google Scholar 

  • Malinowski R, Smith JA, Fleming AJ, Scholes JD, Rolfe SA (2012) Gall formation in clubroot-infected Arabidopsis results from an increase in existing meristematic activities of the host but is not essential for the completion of the pathogen life cycle. Plant J 71:226–238. https://doi.org/10.1111/j.1365-313X.2012.04983.x

    Article  CAS  PubMed  Google Scholar 

  • Manulis S, Barash I (2003) Pantoea agglomerans pvs. gypsophilae and betae, recently evolved pathogens? Mol Plant Pathol 4:307–314

    CAS  PubMed  Google Scholar 

  • Manulis S, Haviv-Chesner A, Brandl MT, Lindow SE, Barash I (1998) Differential involvement of indole-3-acetic acid biosynthetic pathways in pathogenicity and epiphytic fitness of Erwinia herbicola pv. gypsophilae. Mol Plant Microbe Interact 11:634–642

    CAS  PubMed  Google Scholar 

  • Mao Y, Pavangadkar KA, Thomashow MF, Triezenberg SJ (2006) Physical and functional interactions of Arabidopsis ADA2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim Biophys Acta 1759:69–79

    CAS  PubMed  Google Scholar 

  • Mapes CC, Davies PJ (2001) Indole-3-acetic acid and ball gall development on Solidago altissima. New Phytol 151:195–202

    CAS  PubMed  Google Scholar 

  • Marchi G, Sisto A, Cimmino A, Andolfi A, Cipriani MG, Evidente A, Surico G (2006) Interaction between Pseudomonas savastanoi pv. savastanoi and Pantoea agglomerans in olive knots. Plant Pathol 55:614–624

    Google Scholar 

  • Mariconti L, Pellegrini B, Cantoni R, Stevens R, Bergounioux C, Cella R, Albani D (2002) The E2F family of transcription factors from Arabidopsis thaliana. Novel and conserved components of the retinoblastoma/E2F pathway in plants. J Biol Chem 277:9911–9919

    CAS  PubMed  Google Scholar 

  • Matas IM, Perez-Martinez I, Quesada JM, Rodrıguez-Herva JJ, Penyalver R, Ramos C (2009) Pseudomonas savastanoi pv. savastanoi contains two iaaL paralogs, one of which exhibits a variable number of a trinucleotide (TAC) tandem repeat. Appl Environ Microbiol 75:1030–1035. https://doi.org/10.1128/AEM.01572-08

    Article  CAS  PubMed  Google Scholar 

  • Matveeva TV, Frolova NV, Smets R, Dodueva IE, Buzovkina IS, Van Onckelen H, Lutova LA (2004) Hormonal control of tumor formation in radish. J Plant Growth Regul 23:37–43

    CAS  Google Scholar 

  • Matveeva TV, Bogomaz DI, Pavlova OA, Nester EW, Lutova LA (2012) Horizontal gene transfer from genus Agrobacterium to the plant Linaria in nature. Mol Plant Microbe Interact 25:1542–1551. https://doi.org/10.1094/MPMI-07-12-0169-R

    Article  CAS  PubMed  Google Scholar 

  • Mayer KF, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998) Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95:805–815

    CAS  PubMed  Google Scholar 

  • Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ (2003) Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol 53:513–530

    CAS  PubMed  Google Scholar 

  • Mei Y, Yang X, Huang C, Zhang X, Zhou X (2018) Tomato leaf curl Yunnan virus-encoded C4 induces cell division through enhancing stability of Cyclin D 11 via impairing NbSKη -mediated phosphorylation in Nicotiana benthamiana. PLoS Pathog. 14:e1006789. https://doi.org/10.1371/journal.ppat.1006789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meyerowitz EM (2002) Plants compared to animals: the broadest comparative study of development. Science 295:1482–1485

    CAS  PubMed  Google Scholar 

  • Mills-Lujan K, Deom CM (2010) Geminivirus C4 protein alters Arabidopsis development. Protoplasma 239:95–110. https://doi.org/10.1007/s00709-009-0086-z

    Article  CAS  PubMed  Google Scholar 

  • Mills-Lujan K, Andrews DL, Chou CW, Deom CM (2015) The roles of phosphorylation and SHAGGY-like protein kinases in geminivirus C4 protein induced hyperplasia. PLoS One 10:e0122356. https://doi.org/10.1371/journal.pone.0122356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Miransari M, Abrishamchi A, Khoshbakht K, Niknam V (2014) Plant hormones as signals in arbuscular mycorrhizal symbiosis. Crit Rev Biotechnol 34:123–133. https://doi.org/10.3109/07388551.2012

    Article  CAS  PubMed  Google Scholar 

  • Mitchum MG, Wang X, Wang J, Davis EL (2012) Role of nematode peptides and other small molecules in plant parasitism. Annu Rev Phytopathol 50:175–195. https://doi.org/10.1146/annurev-phyto-081211-173008

    Article  CAS  PubMed  Google Scholar 

  • Miyazaki N, Hagiwara K, Naitow H, Higashi T, Cheng RH, Tsukihara T, Nakagawa A, Omura T (2005) Transcapsidation and the conserved interactions of two major structural proteins of a pair of phytoreoviruses confirm the mechanism of assembly of the outer capsid layer. J Mol Biol 345:229–237

    CAS  PubMed  Google Scholar 

  • Morrison EN, Emery RJ, Saville BJ (2015) Phytohormone involvement in the Ustilago maydisZea mays pathosystem: relationships between abscisic acid and cytokinin levels and strain virulence in infected cob tissue. PLoS One 10:e0130945. https://doi.org/10.1371/journal.pone.0130945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mouille G, Ralet MC, Cavelier C, Eland C, Effroy D, Hématy K, McCartney L, Truong HN, Gaudon V, Thibault JF (2007) Homogalacturonan synthesis in Arabidopsis thaliana requires a golgi-localized protein with a putative methyltransferase domain. Plant J 50:605–614

    CAS  PubMed  Google Scholar 

  • Naf U (1958) Studies in tumor formation in Nicotiana hybrids. The classification of parents into two etiologically significant groups. Growth 22:167–180

    CAS  PubMed  Google Scholar 

  • Nagata N, Kosono S, Sekine M, Shinmyo A, Syono K (1996) Different expression patterns of the promoters of the NgrolB and NgrolC genes during the development of tobacco genetic tumors. Plant Cell Physiol 37:489–498

    CAS  Google Scholar 

  • Narbut SI (1967) Genetic tumor generated during inbreeding in radish. Vestnik Leningr Univ 15:144–149 (in Russian)

    Google Scholar 

  • Navarro L, Dunoyer P, Jay F, Arnold B, Dharmasiri N, Estelle M, Voinnet O, Jones JD (2006) A plant miRNA contributes to antibacterial resistance by repressing auxin signaling. Science 312:436–439

    CAS  PubMed  Google Scholar 

  • Nicol F, His I, Jauneau A, Vernhettes S, Canut H, Höfte H (1998) A plasma membrane–bound putative endo-1, 4-β-d-glucanase is required for normal wall assembly and cell elongation in Arabidopsis. EMBO J 17:5563–5576

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niehaus EM, Münsterkötter M, Proctor RH, Brown DW, Sharon A, Idan Y, Oren-Young L, Sieber CM, Novák O, Pěnčík A, Tarkowská D, Hromadová K, Freeman S, Maymon M, Elazar M, Youssef SA, El-Shabrawy ES, Shalaby AB, Houterman P, Brock NL, Burkhardt I, Tsavkelova EA, Dickschat JS, Galuszka P, Güldener U, Tudzynski B (2016) Comparative "omics" of the Fusarium fujikuroi species complex highlights differences in genetic potential and metabolite synthesis. Genome Biol Evol 8:3574–3599. https://doi.org/10.1093/gbe/evw259

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nowack MK, Harashima H, Dissmeyer N, Zhao X, Bouyer D, Weimer AK, De Winter F, Yang F, Schnittger A (2012) Genetic framework of cyclin-dependent kinase function in Arabidopsis. Dev Cell 22:1030–1040. https://doi.org/10.1016/j.devcel.2012.02.015

    Article  CAS  PubMed  Google Scholar 

  • Oakenfull EA, Riou-Khamlichi C, Murray JA (2002) Plant D-type cyclins and the control of G1 progression. Philos Trans R Soc Lond B Biol Sci 357:749–760

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294. https://doi.org/10.1126/science.1150083(hu Curr Top Microbiol Immunol 418:375–419)

    Article  CAS  PubMed  Google Scholar 

  • Oliveira DC, Isaias RMS, Fernandes GW, Ferreira BG, Carneiro RGS, Fuzaro L (2016) Manipulation of host plant cells and tissues by gall-inducing insects and adaptive strategies used by different feeding guilds. J Insect Physiol 84:103–113

    CAS  PubMed  Google Scholar 

  • Otten L (2018) The Agrobacterium phenotypic plasticity (Plast) genes. Curr Top Microbiol Immunol 418:375–419

    CAS  PubMed  Google Scholar 

  • Palomares-Rius JE, Escobar C, Cabrera J, Vovlas A, Castillo P (2017) Anatomical alterations in plant tissues induced by plant-parasitic nematodes. Front Plant Sci 8:1987. https://doi.org/10.3389/fpls.2017.01987

    Article  PubMed  PubMed Central  Google Scholar 

  • Paponova SS, Chetverikov PE, Pautov AA, Yakovleva OV, Zukoff SN, Vishnyakov AE, Sukhareva SI, Krylova EG, Dodueva IE, Lutova LA (2017) Gall mite Fragariocoptes setiger (Eriophyoidea) changes leaf developmental program and regulates gene expression in the leaf tissues of Fragaria viridis (Rosaceae). Ann App Biol 172:33–46. https://doi.org/10.1111/aab.12399

    Article  CAS  Google Scholar 

  • Paredez AR, Persson S, Ehrhardt DW, Somerville CR (2008) Genetic evidence that cellulose synthase activity influences microtubule cortical array organization. Plant Physiol 147:1723–1734. https://doi.org/10.1104/pp.108.120196

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patten CL, Blakney AJ, Coulson TJ (2013) Activity, distribution and function of indole-3-acetic acid biosynthetic pathways in bacteria. Crit Rev Microbiol 39:395–415. https://doi.org/10.3109/1040841X.2012.716819

    Article  CAS  PubMed  Google Scholar 

  • Pautot V, Dockx J, Hamant O, Kronenberger J, Grandjean O, Jublot D, Traas J (2001) KNAT2: evidence for a link between knotted-like genes and carpel development. Plant Cell 13:1719–1734

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pelagio-Flores R, Ortiz-Castro R, López-Bucio J (2013) dhm1, an Arabidopsis mutant with increased sensitivity to alkamides shows tumorous shoot development and enhanced lateral root formation. Plant Mol Biol 81:609–625. https://doi.org/10.1007/s11103-013-0023-6

    Article  CAS  PubMed  Google Scholar 

  • Perez-Martínez I, Zhao Y, Murillo J, Sundin GW, Ramos C (2008) Global genomic analysis of Pseudomonas savastanoi pv. savastanoi plasmids. J Bacteriol 190:625–635

    PubMed  Google Scholar 

  • Pertry I, Václavíková K, Gemrotová M, Spíchal L, Galuszka P, Depuydt S, Temmerman W, Stes E, De Keyser A, Riefler M, Biondi S, Novák O, Schmülling T, Strnad M, Tarkowski P, Holsters M, Vereecke D (2010) Rhodococcus fascians impacts plant development through the dynamic fas-mediated production of a cytokinin mix. Mol Plant Microbe Interact 23:1164–1174. https://doi.org/10.1094/MPMI-23-9-1164

    Article  CAS  PubMed  Google Scholar 

  • Piepenbring M, Stoll M, Oberwinkler F (2002) The generic position of Ustilago maydis, Ustilago scitaminea, and Ustilago esculenta (Ustilaginales). Mycol Prog 1:71–80

    Google Scholar 

  • Piroux N, Saunders K, Page A, Stanley J (2007) Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggy-related protein kinase AtSKn, a component of the brassinosteroid signalling pathway. Virology 362:428–440

    CAS  PubMed  Google Scholar 

  • Polyn S, Willems A, De Veylder L (2015) Cell cycle entry, maintenance, and exit during plant development. Curr Opin Plant Biol 23:1–7. https://doi.org/10.1016/j.pbi.2014.09.012

    Article  CAS  PubMed  Google Scholar 

  • del Pozo JC, Boniotti MB, Gutierrez C (2002) Arabidopsis E2Fc functions in cell division and is degraded by the ubiquitin-SCF(AtSKP2) pathway in response to light. Plant Cell 14:3057–3071

    PubMed  PubMed Central  Google Scholar 

  • Qu G, Heo S, Yoon B-S, Wang MH (2006) The effects of exogenous hormones on genetic tumor formation in Nicotiana hybrids. EXCLI J 5:33–41

    Google Scholar 

  • Raman A, Schaefer CW, Withers TM (2005) Galls and gall-inducing arthropods: an overview of their biology, ecology and evolution. In: Raman A, Schaefer CW, Withers TM (eds) Biology, ecology, and evolution of gall-inducing arthropods. Science Publishers, Enfield, NH, USA, pp 1–33

    Google Scholar 

  • Ramos C, Matas IM, Bardaji L, Aragón IM, Murillo J (2012) Pseudomonas savastanoi pv. savastanoi: some like it knot. Mol Plant Pathol 13:998–1009. https://doi.org/10.1111/j.1364-3703.2012.00816.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reineke G, Heinze B, Schirawski J, Buettner H, Kahmann R, Basse CW (2008) Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue and host tumour formation. Mol Plant Pathol 9:339–355. https://doi.org/10.1111/j.1364-3703.2008.00470.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reiser L, Sanchez-Baracaldo P, Hake S (2000) Knots in the family tree: evolutional relationship and functions of KNOX homeobox genes. Plant Mol Biol 42:151–166

    CAS  PubMed  Google Scholar 

  • Rojas MR, Hagen C, Lucas WJ, Gilbertson RL (2005) Exploiting chinks in the plant’s armor: evolution and emergence of geminiviruses. Annu Rev Phytopathol 43:361–394

    CAS  PubMed  Google Scholar 

  • Roumagnac P, Granier M, Bernardo P, Deshoux M, Ferdinand R, Galzi S, Fernandez E, Julian C, Abt I, Filloux D, Mesléard F, Varsani A, Blanc S, Martin DP, Peterschmitt M (2015) Alfalfa leaf curl virus: an aphid-transmitted geminivirus. J Virol 89:9683–9688. https://doi.org/10.1128/JVI.00453-15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rutter WB, Hewezi T, Maier TR, Mitchum MG, Davis EL, Hussey RS, Baum TJ (2014) Members of the Meloidogyne avirulence protein family contain multiple plant ligand-like motifs. Phytopathology 104:879–885. https://doi.org/10.1094/phyto-11-13-0326-R

    Article  CAS  PubMed  Google Scholar 

  • Sabatini S, Heidstra R, Wildwater M, Scheres B (2000) SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Gen Dev 17:354–358

    Google Scholar 

  • Samorodova AP, Tvorogova VE, Tkachenko AA, Potsenkovskaya EA, Lebedeva MA, Tikhonovich IA, Lutova LA (2018) Agrobacterial tumors interfere with nodulation and demonstrate the expression of nodulation-induced CLE genes in pea. J Plant Physiol 221:94–100. https://doi.org/10.1016/j.jplph.2017.12.005

    Article  CAS  PubMed  Google Scholar 

  • Sardesai N, Lee LY, Chen HB, Yi HC, Olbricht GR, Stirnberg A, Jeffries J, Xiong K, Doerge RW, Gelvin SB (2013) Cytokinins secreted by Agrobacterium promote transformation by repressing a plant Myb transcription factor. Sci Signal 6:ra100. https://doi.org/10.1126/scisignal.2004518

    Article  CAS  PubMed  Google Scholar 

  • Sarkar AK, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007) Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature 446:811–814

    CAS  PubMed  Google Scholar 

  • Schaller GE, Bishopp A, Kieber JJ (2015) The yin-yang of hormones: cytokinin and auxin interactions in plant development. Plant Cell 27:44–63. https://doi.org/10.1105/tpc.114.133595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scheidt HA, Vogel A, Eckhoff A, Koenig BW, Huster D (2007) Solid-state NMR characterization of the putative membrane anchor of TWD1 from Arabidopsis thaliana. Eur Biophys J 36:393–404

    CAS  PubMed  Google Scholar 

  • Schultz JC, Edger PP, Body MJA, Appel HM (2019) A galling insect activates plant reproductive programs during gall development. Sci Rep 9:1833. https://doi.org/10.1038/s41598-018-38475-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schwelm A, Fogelqvist J, Knaust A, Jülke S, Lilja T, Bonilla-Rosso G, Karlsson M, Shevchenko A, Dhandapani V, Choi SR, Kim HG, Park JY, Lim YP, Ludwig-Müller J, Dixelius C (2015) The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep 5:11153. https://doi.org/10.1038/srep11153

    Article  PubMed  PubMed Central  Google Scholar 

  • Shanks CM, Rice JH, Zubo Y, Schaller GE, Hewezi T, Kieber JJ (2016) The role of cytokinin during infection of Arabidopsis thaliana by the cyst nematode Heterodera schachtii. Mol Plant Microbe Interact 29:57–68. https://doi.org/10.1094/mpmi-07-15-0156-R

    Article  CAS  PubMed  Google Scholar 

  • Shen Q, Liu Y, Naqvi NI (2018) Fungal effectors at the crossroads of phytohormone signaling. Curr Opin Microbiol 46:1–6. https://doi.org/10.1016/j.mib.2018.01.006

    Article  CAS  PubMed  Google Scholar 

  • Shih TH, Lin SH, Huang MY, Sun CW, Yang CM (2018) Transcriptome profile of cup-shaped galls in Litsea acuminata leaves. PLoS One 13(10):e0205265. https://doi.org/10.1371/journal.pone.0205265

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shorthouse JD, Wool D, Raman A (2005) Gall-inducing insects—nature’s most sophisticated herbivores. Basic Appl Ecol 6:407–411

    Google Scholar 

  • Siddique S, Radakovic ZS, De La Torre CM, Chronis D, Novák O, Ramireddy E, Holbein J, Matera C, Hütten M, Gutbrod P, Anjam MS, Rozanska E, Habash S, Elashry A, Sobczak M, Kakimoto T, Strnad M, Schmülling T, Mitchum MG, Grundler FM (2015) A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci USA 112:12669–12674. https://doi.org/10.1073/pnas.1503657112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sieberer T, Hauser MT, Seifert GJ, Luschnig C (2003) PROPORZ1, a putative Arabidopsis transcriptional adaptor protein, mediates auxin and cytokinin signals in the control of cell proliferation. Curr Biol 13:837–842

    CAS  PubMed  Google Scholar 

  • Silverstone SE, Gilchrist DG, Bostock RM, Kosuge T (1993) The 73-kb pIAA plasmid increases competitive fitness of Pseudoimonas syringae subspecies savastanoi in oleander. Can J Microbiol 39:659–664

    CAS  PubMed  Google Scholar 

  • Smith HH (1988) The inheritance of genetic tumors in Nicotiana hybrids. J Hered 79:277–283

    Google Scholar 

  • Smith EF, Townsend CO (1907) A plant tumor of bacterial origin. Science 25:671–673

    CAS  PubMed  Google Scholar 

  • Smyczynski C, Roudier F, Gissot L, Vaillant E, Grandjean O, Morin H, Masson T, Bellec Y, Geelen D, Faure JD (2006) The C terminus of the immunophilin PASTICCINO1 is required for plant development and for interaction with a NAC-like transcription factor. J Biol Chem 281:25475–25484

    CAS  PubMed  Google Scholar 

  • Sørensen JL, Benfield AH, Wollenberg RD, Westphal K, Wimmer R, Nielsen MR, Nielsen KF, Carere J, Covarell L, Beccari G, Powell J, Yamashino T, Kogler H, Sondergaard TE, Gardiner DM (2018) The cereal pathogen Fusarium pseudograminearum produces a new class of active cytokinins during infection. Mol Plant Pathol 19:1140–1154. https://doi.org/10.1111/mpp.12593

    Article  CAS  PubMed  Google Scholar 

  • Spallek T, Gan P, Kadota Y, Shirasu K (2018) Same tune, different song-cytokinins as virulence factors in plant-pathogen interactions? Curr Opin Plant Biol 44:82–87. https://doi.org/10.1016/j.pbi.2018.03.002

    Article  CAS  PubMed  Google Scholar 

  • Stahl Y, Simon R (2010) Plant primary meristems: shared functions and regulatory mechanisms. Curr Opin Plant Biol 13:53–58. https://doi.org/10.1016/j.pbi.2009.09.008

    Article  CAS  PubMed  Google Scholar 

  • Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914. https://doi.org/10.1016/j.cub.2009.03.060

    Article  CAS  PubMed  Google Scholar 

  • Stes E, Biondi S, Holsters M, Vereecke D (2011) Bacterial and plant signal integration via D3-type cyclins enhances symptom development in the Arabidopsis—Rhodococcus fascians interaction. Plant Physiol 156:712–725. https://doi.org/10.1104/pp.110.171561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stes E, Prinsen E, Holsters M, Vereecke D (2012) Plant-derived auxin plays an accessory role in symptom development upon Rhodococcus fascians infection. Plant J 70:513–527. https://doi.org/10.1111/j.1365-313X.2011.04890.x

    Article  CAS  PubMed  Google Scholar 

  • Sugimoto K, Jiao Y, Meyerowitz EM (2010) Arabidopsis regeneration from multiple tissues occurs via a root development pathway. Dev Cell 18:463–471. https://doi.org/10.1016/j.devcel.2010.02.004

    Article  CAS  PubMed  Google Scholar 

  • Takei K, Sakakibara H, Sugiyama T (2001) Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J Biol Chem 276:26405–26410

    CAS  PubMed  Google Scholar 

  • Tanaka E, Koga H, Mori M, Mori M (2011) Auxin production by the rice blast fungus and its localization in host tissue. J Phytopathol 159:522–530. https://doi.org/10.1111/j.1439-0434.2011.01799.x

    Article  CAS  Google Scholar 

  • Tanaka Y, Okada K, Asami T, Suzuki Y (2013) Phytohormones in Japanese mugwort gall induction by a gall-inducing gall midge. Biosci Biotechnol Biochem 77:1942–1948. https://doi.org/10.1271/bbb.130406

    Article  CAS  PubMed  Google Scholar 

  • Taya Y, Tanaka Y, Nishimura S (1978) 5'-AMP is a direct precursor of cytokinin in Dictyostelium discoideum. Nature 271:545–547

    CAS  PubMed  Google Scholar 

  • Temmerman W, Rietsma T, Simon-Mateo C, Van Montagu M, Mironov V, Inze D, Goenthals K, Holsters M (2001) The fas locus of the phytopathogen Rhodococcus fascians affects mithosis of tobacco BY-2 cells. FEBS Lett 492:127–132

    CAS  PubMed  Google Scholar 

  • Terakura S, Kitakura S, Ishikawa M, Ueno Y, Fujita T, Machida C, Wabiko H, Machida Y (2006) Oncogene 6b from Agrobacterium tumefaciens induces abaxial cell division at late stages of leaf development and modifies vascular development in petioles. Plant Cell Physiol 47:664–672

    CAS  PubMed  Google Scholar 

  • Terakura S, Ueno Y, Tagami H, Kitakura S, Machida C, Wabiko H, Aiba H, Otten L, Tsukagoshi H, Nakamura K, Machida Y (2007) An oncoprotein from the plant pathogen agrobacterium has histone chaperone-like activity. Plant Cell 19:2855–2865

    CAS  PubMed  PubMed Central  Google Scholar 

  • Testone G, Bruno L, Condello E, Chiappetta A, Bruno A, Mele G, Tartarini A, Spanò L, Innocenti AM, Mariotti D, Bitonti MB, Giannino D (2008) Peach [Prunus persica (L.) Batsch] KNOPE1, a class 1 KNOX orthologue to Arabidopsis BREVIPEDICELLUS/KNAT1, is misexpressed during hyperplasia of leaf curl disease. J Exp Bot 59:389–402. https://doi.org/10.1093/jxb/erm317

    Article  CAS  PubMed  Google Scholar 

  • Todd R, Wong DT (1999) Oncogenes. Anticancer Res 19:729–4746

    Google Scholar 

  • Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species increases levels of indole-3-acetic and decreases abscisic acid in Solidago altissimastems. Arthropod Plant Interact 5:115–124. https://doi.org/10.1007/s11829-010-9120-5

    Article  Google Scholar 

  • Torres Acosta JA, Fowke LC, Wang H (2011) Analyses of phylogeny, evolution, conserved sequences and genome-wide expression of the ICK/KRP family of plant CDK inhibitors. Ann Bot 107:1141–1157. https://doi.org/10.1093/aob/mcr034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trdá L, Barešová M, Šašek V, Nováková M, Zahajská L, Dobrev PI, Motyka V, Burketová L (2017) Cytokinin metabolism of pathogenic fungus Leptosphaeria maculans involves isopentenyltransferase, adenosine kinase and cytokinin oxidase/dehydrogenase. Front Microbiol 8:1374. https://doi.org/10.3389/fmicb.2017.01374

    Article  PubMed  PubMed Central  Google Scholar 

  • Tsai IJ, Tanaka E, Masuya H, Tanaka R, Hirooka Y, Endoh R, Sahashi N, Kikuchi T (2014) Comparative genomics of Taphrina fungi causing varying degrees of tumorous deformity in plants. Genome Biol Evol 6:861–872. https://doi.org/10.1093/gbe/evu067

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsavkelova E, Oeser B, Oren-Young L, Israeli M, Sasson Y, Tudzynski B, Sharon A (2012) Identification and functional characterization of indole-3-acetamide-mediated IAA biosynthesis in plant-associated Fusarium species. Fungal Genet Biol 49:48–57. https://doi.org/10.1016/j.fgb.2011.10.005

    Article  CAS  PubMed  Google Scholar 

  • Tsuda K, Hake S (2015) Diverse functions of KNOX transcription factors in the diploid body plan of plants. Curr Opin Plant Biol 27:91–96. https://doi.org/10.1016/j.pbi.2015.06.015

    Article  CAS  PubMed  Google Scholar 

  • Ullrich CI, Aloni R (2000) Vascularization is a general requirement for growth of plant and animal tumours. J Exp Bot 51:1951–1960

    CAS  PubMed  Google Scholar 

  • Ullrich CI, Aloni R, Saeed MEM, Ullrich W, Efferth T (2019) Comparison between tumors in plants and human beings: mechanisms of tumor development and therapy with secondary plant metabolites. Phytomedicine 64:153081. https://doi.org/10.1016/j.phymed.2019.153081

    Article  CAS  PubMed  Google Scholar 

  • Vandeputte O, Oden S, Mol A, Vereecke D, Goethals K, El Jaziri M, Prinsen E (2005) Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues. Appl Environ Microbiol 71:1169–1177

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vanstaden J, Nicholson RID (1989) Cytokinins and mango flower malformation II: the cytokinin complement produced by Fusarium moniliforme and the ability of the fungus to incorporate [8–14C] adenine into cytokinins. Physiol Mol Plant Pathol 35:423–431

    CAS  Google Scholar 

  • Veselov D, Langhans M, Hartung W, Aloni R, Feussner I, Gotz C, Veselova S, Schlomski S, Dicker C, Bachmann K, Ullrich C (2003) Development of Agrobacterium tumefaciens C58-induced plant tumors and impact on host shoots are controlled by a cascade of jasmonic acid, auxin, cytokinin, ethylene and abscisic acid. Planta 216:512–522

    CAS  PubMed  Google Scholar 

  • Vinogradova AP, Lebedeva MA, Lutova LA (2015) Meristematic characteristics of tumors initiated by Agrobacterium tumefaciens in pea plants. Rus J Genet 51:46–54. https://doi.org/10.1134/S1022795415010123

    Article  CAS  Google Scholar 

  • Walbot V, Skibbe DS (2010) Maize host requirements for Ustilago maydis tumor induction. Sex Plant Reprod 23:1–13. https://doi.org/10.1007/s00497-009-0109-0

    Article  PubMed  Google Scholar 

  • Wang MH, Doonan JH, Sastry GRK (1999) Cloning and characterization of the unusual cyclin gene from an amphidiploid of Nicotiana glauca—Nicotiana langsdorfii hybrid. Biochim Biophys Acta 1489:399–404

    CAS  PubMed  Google Scholar 

  • Wang XH, Allen R, Ding XF, Goellner M, Maier T, de Boer JM, Baum TJ, Hussey RS, Davis EL (2001) Signal peptide selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol Plant Microbe Interact 14:536–544

    CAS  PubMed  Google Scholar 

  • Wang G, Kong H, Sun Y, Zhang W, Altman N, Depamphilis CW, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135:1084–1099

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Mitchum MG, Gao B, Li C, Diab H, Baum TJ, Hussey RS, Davis EL (2005) A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana. Mol Plant Pathol 6:187–191

    PubMed  Google Scholar 

  • Wang J, Lee C, Replogle A, Joshi S, Korkin D, Hussey R, Baum TJ, Davis EL, Wang X, Mitchum MG (2010) Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins. New Phytol 187:1003–1017. https://doi.org/10.1111/j.1469-8137.2010.03300.x

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Replogle A, Hussey R, Baum T, Wang X, Davis EL, Mitchum MG (2011) Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii. Mol Plant Pathol 12:177–186. https://doi.org/10.1111/j.1364-3703.2010.00660.x

    Article  CAS  PubMed  Google Scholar 

  • Wang ZD, Yan N, Wang ZH, Zhang XH, Zhang JZ, Xue HM, Wang LX, Zhan Q, Xu YP, Guo DP (2017) RNA-seq analysis provides insight into reprogramming of culm development in Zizania latifolia induced by Ustilago esculenta. Plant Mol Biol 95:533–547. https://doi.org/10.1007/s11103-017-0658-9

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Li Y (2016) Rice reoviruses in insect vectors. Annu Rev Phytopathol 54:99–120. https://doi.org/10.1146/annurev-phyto-080615-095900

    Article  CAS  PubMed  Google Scholar 

  • Weingartner M, Pelayo HR, Binarova P, Zwerger K, Melikant B, De La Torre C, Heberle-Bors E, Bogre L (2003) A plant cyclin B2 is degraded early in mitosis and its ectopic expression shortens G2-phase and alleviates the DNA-damage checkpoint. J Cell Sci 116:487–498

    CAS  PubMed  Google Scholar 

  • White PR (1948) Transplantation of plant tumors of genetic origin. Cancer Res 4:791–794

    Google Scholar 

  • Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 123:1337–1349

    CAS  PubMed  Google Scholar 

  • Xin W, Wang Z, Liang Y, Wang Y, Hu Y (2017) Dynamic expression reveals a two-step patterning of WUS and CLV3 during axillary shoot meristem formation in Arabidopsis. J Plant Physiol 214:1–6. https://doi.org/10.1016/j.jplph.2017.03.017

    Article  CAS  PubMed  Google Scholar 

  • Yadav RK, Perales M, Gruel J, Girke T, Jonsson H, Reddy GV (2011) WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Gen Dev 25:2025–2030. https://doi.org/10.1101/gad.17258511

    Article  CAS  Google Scholar 

  • Yamada T, Tsukamoto H, Shiraishi T, Nomura T, Oku H (1990) Detection of indoleacetic acid biosynthesis in some species of Taphrina causing hyperplastic diseases in plants. Ann Phytopathol Soc Jpn 56:532–540

    CAS  Google Scholar 

  • Yamaguchi H, Tanaka H, Hasegawa M, Tokuda M, Asami T, Suzuki Y (2012) Phytohormones and willow gall induction by a gall-inducing sawfly. New Phytol 196:586–595. https://doi.org/10.1111/j.1469-8137.2012.04264.x

    Article  CAS  PubMed  Google Scholar 

  • Yan Z, Zhao J, Peng P, Chihara RK, Li J (2009) BIN2 functions redundantly with other Arabidopsis GSK3-like kinases to regulate brassinosteroid signaling. Plant Physiol 150:710–721. https://doi.org/10.1104/pp.109.138099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao C, Escalante LN, Chen H, Benatti TR, Qu J, Chellapilla S, Waterhouse RM, Wheeler D, Andersson MN, Bao R, Batterton M, Behura SK, Blankenburg KP, Caragea D, Carolan JC, Coyle M, El-Bouhssini M, Francisco L, Friedrich M, Gill N, Grace T, Grimmelikhuijzen CJP, Han Y, Hauser F, Herndon N, Holder M, Ioannidis P, Jackson LR, Javaid M, Jhangiani SN, Johnson AJ, Kalra D, Korchina V, Kovar CL, Lara F, Lee SL, Liu X, Löfstedt C, Mata R, Mathew T, Muzny DM, Nagar S, Nazareth LV, Okwuonu G, Ongeri F, Perales L, Peterson BF, Pu L-L, Robertson HM, Schemerhorn BJ, Scherer SE, Shreve JT, Simmons DN, Subramanyam S, Thornton RL, Xue K, Weissenberger GM, Williams CE, Worley KC, Zhu D, Zhu Y, Harris MO, Shukle RH, Werren JH, Zdobnov EM, Chen M-S, Brown SJ, Stuart JJ, Richards S (2015) A massive expansion of effector genes underlies gall-formation in the wheat pest Mayetiola destructor. Curr Biol 25:613–620. https://doi.org/10.1016/j.cub.2014.12.057

    Article  CAS  PubMed  Google Scholar 

  • Zhao C, Shukle R, Navarro Escalante L, Chen M, Richards S, Stuart JJ (2016) Avirulence gene mapping in the Hessian fly (Mayetiola destructor) reveals a protein phosphatase 2C effector gene family. J Insect Physiol 84:22–31. https://doi.org/10.1016/j.jinsphys.2015.10.001

    Article  CAS  PubMed  Google Scholar 

  • Zhou Y, Yan A, Han H, Li T, Geng Y, Liu X, Meyerowitz EM (2018) HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 361:502–506. https://doi.org/10.1126/science.aar8638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu S, Gao F, Cao X, Chen M, Ye G, Wei C, Li Y (2005) The rice dwarf virus P2 protein interacts with ent-kaurene oxidases in vivo, leading to reduced biosynthesis of gibberellins and rice dwarf symptoms. Plant Physiol 139:1935–1945

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Chen MS, Liu X (2011) Changes in phytohormones and fatty acids in wheat and rice seedlings in response to Hessian fly (Diptera: Cecidomyiidae) infestation. J Econ Entomol 104:1384–1392. https://doi.org/10.1603/029.102.0434

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The study of mechanisms of tumor growth in higher plants at Saint-Petersburg State University was supported by grant from Russian Scientific Foundation 16-16-10011, and Russian Foundation for Basic Research 18-04-01107.

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Correspondence to Irina E. Dodueva.

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Dodueva, I.E., Lebedeva, M.A., Kuznetsova, K.A. et al. Plant tumors: a hundred years of study. Planta 251, 82 (2020). https://doi.org/10.1007/s00425-020-03375-5

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