Skip to main content
Log in

Exogenous phytohormones and the induction of plant galls by insects

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

The mechanism of gall induction by insects has remained elusive. Previous studies have met with limited success in attempting to induce galls by injection or application of chemical compounds. To determine whether an exogenous source of phytohormones plays a role in gall induction, we injected cytokinin (CK), auxin (IAA), gibberellic acid (GA), and abscisic acid (ABA) in various concentrations, ratios, and combinations into leaf petioles of Capsicum annuum L. cv. California Wonder (Solanaceae). We found that CK + IAA injections lead to gall-like growth in C. annuum. GA enhanced and ABA inhibited gall growth except in the presence of GA. Isopentenyl adenine (IP) was the most effective type of CK at inducing growth. Our work is consistent with the hypothesis that exogenous CK + IAA produced and supplied by insects leads to gall induction. We hypothesize that insects have obtained the capability to induce galls via acquisition of the biosynthetic pathways to produce IAA and trans-zeatin family CKs through microbial symbiosis or lateral gene transfer.

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

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abrahamson WG, Weis AR (1997) Evolutionary ecology across three trophic levels: goldenrods, gallmakers, and natural enemies. Princeton University Press, Princeton

    Google Scholar 

  • Barash I, Manulis-Sasson S (2007) Virulence mechanisms and host-specificity of gall forming Pantoea agglomerans. Trends Microbiol 15:538–545

    Article  CAS  PubMed  Google Scholar 

  • Barash I, Manulis-Sasson S (2009) Recent evolution of bacterial pathogens: the gall-forming Pantoea agglomerans case. Annu Rev Phytopathol 47:133–152

    Article  CAS  PubMed  Google Scholar 

  • Barnewall EC, De Clerck-Floate RA (2012) A preliminary histological investigation of gall induction in an unconventional galling system. Arthropod Plant Interact 6:449–459

    Article  Google Scholar 

  • Binns AN, Thomashow MF (1988) Cell biology of Agrobacterium infection and transformation of plants. Annu Rev Microbiol 42:575–606

    Article  CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Bruce SA, Saville BJ, Emery RJN (2011) Ustilago maydis produces cytokinins and abscisic acid for potential regulation of tumor formation in maize. J Plant Growth Regul 30:51–63

    Article  CAS  Google Scholar 

  • Byers JA, Brewer JW, Denna DW (1976) Plant growth hormones in pinyon insect galls. Marcellia 39:125–134

    CAS  Google Scholar 

  • Chen ZY, Agnew JL, Cohen JD, He P, Shan LB, Sheen J, Kunkel BN (2007) Pseudomonas syringae type III effector AvrRpt2 alters Arabidopsis thaliana auxin physiology. Proc Natl Acad Sci USA 104:20131–20136

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cobbs C, Heath J, Stireman JO, Abbot P (2013) Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Mol Phylogenet Evol 68:221–228

    Article  CAS  PubMed  Google Scholar 

  • Connor EF, Bartlett L, O’Toole S, Byrd S, Biskar K, Orozco J (2012) The mechanism of gall induction makes galls red. Arthropod Plant Interact 6:489–495

    Article  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 cytokinin synthase gene. RMBO J 11:795–804

    CAS  Google Scholar 

  • De Bruyn L, Vandevyere I, Jaminé D, Prinsen E (1997) The effects of gall formation by Lipara lucens (Diptera, Chloropidae) on its host Phragmites australis (Poaceae). In Csoka G, Mattson WJ, Stone GN, Price PW (eds) The biology of gall-inducing arthropods. USDA For Serv Gen Technical Rep NC-199

  • Dorchin N, Hoffman JH, Stirk WA, Novak O, Strnad M, Van Staden J (2009) Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasps. Physiol Entomol 34:359–369

    Article  Google Scholar 

  • Dreger-Jauffret F, Shorthouse JD (1992) Diversity of gall-inducing insects and their galls. In: Rohfritsch O (ed) Biology of insect-induced galls. Oxford University Press, Oxford, pp 8–33

    Google Scholar 

  • Elzen GW (1983) Cytokinins and insect galls. Comp Biochem Physiol 76A:17–19

    Article  CAS  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452

    Article  PubMed  Google Scholar 

  • Gagné R (1989) The plant-feeding gall midges of North America. Cornell University Press, Ithaca

    Google Scholar 

  • Gajdošová S, Spíchal L, Kamínek K, Hoyerová K, Novák O, Dobrev P, Galuszka P, Klíma P, Gaudinová A, Žižková E, Hanuš J, Dančák M, Trávníček B, Pešek B, Krupička M, Vaňková R, Strnad M, Motyka V (2011) Distribution, biological activities, metabolism, and conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot 62:2287–2840

    Google Scholar 

  • Galuszka P, Spíchal L, Kopečný D, Tarkowski P, Frébortová J, Šebela M, Frébort I (2008) Metabolism of plant hormones cytokinins and their function in signaling, cell differentiation and plant development. In: Rahman AU (ed) Studies in natural products chemistry, vol 34. Elsevier, Amsterdam, pp 203–264

    Google Scholar 

  • Giron D, Frago E, Glevarec G, Pieterse CMJ, Dicke M (2013) Cytokinins as key regulators in plant–microbe–insect interactions: connecting plant growth and defence. Funct Ecol 27:599–609

    Article  Google Scholar 

  • Gisbert C, Trujillo-Moya C, Sanchez-Torres P, Sifres A, Sanchez-Castro E, Nuez F (2013) Resistance of pepper germplasm to Meloidogyne incognita. Ann Appl Biol 162:110–118

    Article  CAS  Google Scholar 

  • Goodner B, Hinkle G, Gattung S, Miller N, Blanchard M, Qurollo B, Goldman BS, Cao Y, Askenazi M, Halling C, Mullin L, Houmiel K, Gordon J, Vaudin M, Iartchouk O, Epp A, Liu F, Wollam C, Allinger M, Doughty D, Scott C, Lappas C, Markelz B, Flanagan C, Crowell C, Gurson J, Lomo C, Sear C, Strub G, Cielo C, Slater S (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294:2323–2328

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez OA, Wubben MJ, Howard M, Roberts B, Hanlon E, Wilkerson JR (2009) The role of phytohormones ethylene and auxin in plant–nematode interactions. Russ J Plant Physiol 56:1–5

    Article  CAS  Google Scholar 

  • Harris KM (1975) The taxonomic status of the carob gall midge, Asphondylia gennadi (Marchal), comb. n. (Diptera, Cecidomyiidae), and of other Asphondylia species recorded from Cyprus. Bull Entomol Res 65:377–380

    Article  Google Scholar 

  • Hartley SE (1999) Are gall insects large rhizobia? Oikos 84:333–342

    Article  Google Scholar 

  • Heyl A, Riefler M, Romanov GA, Schmülling T (2012) Properties, functions, and evolution of cytokinin receptors. Eur J Cell Biol 91:246–256

    Article  CAS  PubMed  Google Scholar 

  • Hori K (1992) Insect secretions and their effect on plant growth, with special reference to hemipterans. In: Shorthouse JD, Rohfritsch O (eds) Biology of insect-induced galls. Oxford University Press, New York, pp 157–170

    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

    Article  Google Scholar 

  • Jacqmard A, Houssa C, Bernier G (1995) Abscisic acid antagonizes the effect of cytokinin on DNA-replication origins. J Exp Bot 46:663–666

    Article  CAS  Google Scholar 

  • Jameson P (2000) Cytokinins and auxins in plant pathogen interactions—an overview. Plant Growth Regul 32:369–380

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kaldewey H (1965) Wachstrumsregulatoren aus pflanzengallen und larven der gallenbewohner. Ber Dtsch Bot Gesell 78:73–84

    Google Scholar 

  • Kamada-Nobusada T, Sakakibara H (2009) Molecular basis for cytokinin biosynthesis. Phytochemistry 70:444–449

    Article  CAS  PubMed  Google Scholar 

  • Leatherdale D (1955) Plant hyperplasia induced with a cell-free insect extract. Nature 175:553–554

    Article  Google Scholar 

  • Leitch IJ (1994) Induction and development of the bean gall caused by Pontania proxima. In: Williams MAJ (ed) Plant galls: organisms, interactions, and populations. Clarendon Press, Oxford, pp 283–300

    Google Scholar 

  • Lichter A, Barash I, Valinsky L, Manulis-Sasson 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 Central  PubMed  Google Scholar 

  • Liu W, Parrott WA, Hildebrand DF, Collins GB, Williams EG (1990) Agrobacterium induced gall formation in bell pepper (Capsicum annuum L.) and formation of shoot-like structures expressing introduced genes. Plant Cell Rep 9:360–364

    CAS  PubMed  Google Scholar 

  • Loper JE, Kado CI (1979) Host range conferred by the virulence-specifying plasmid of Agrobacterium tumefaciens. J Bacteriol 139:591–596

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ludwig-Muller J, Prinsen E, Rolfe SA, Scholes JD (2009) Metabolism and plant hormone action during clubroot disease. J Plant Growth Regul 28:229–244

    Article  Google Scholar 

  • Madden JL, Stone C (1984) Induction and formation of pouch and emergence galls in Eucalyptus pulcehlla leaves. Aust J Bot 32:33–42

    Article  Google Scholar 

  • Mapes CC, Davies PJ (2001a) Cytokinins in the ball gall of Solidago altissima and the gall forming larvae of Eurosta solidaginis. New Phytol 151:203–212

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • McCalla DR, Genthe MK, Hovanitz W (1962) Chemical nature of an insect gall growth-factor. Plant Physiol 37:98–103

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mills RR (1969) Effect of plant and insect hormones on the formation of the goldenrod gall. Natl Cancer Inst Monogr 31:487–491

    CAS  PubMed  Google Scholar 

  • Mockaitis K, Estelle M (2008) Auxin receptors and plant development: a new signaling paradigm. Annu Rev Cell Dev Biol 24:55–80

    Article  CAS  PubMed  Google Scholar 

  • Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci USA 104:8627–8633

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Narendran TC, Santhosh S, Sudheer K (2007) Biosystematics and biogeography of oriental Chalcidoidea (Hymenoptera) associated with plant galls. Oriental Insects 41:141–167

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ohkawa M (1974) Isolation of zeatin from larvae of Drycocosmus kuriplilus Yasamatsu. HortScience 9:458–459

    CAS  Google Scholar 

  • Ostojá-Starzewski JC (2009) Goji gall mite—Aceria kuko (Kishida). Food and Environment Research Agency. (http://www.fera.defra.gov.uk/plants/publications/documents/factsheets/gojiGallMite.pdf). Accessed 17 Feb 2014

  • Pascal-Avarado E, Cuevas-Reyes P, Quesada M, Oyama K (2008) Interactions between galling insects and leaf-feeding insects: the role of plant phenolic compounds and their possible interference with herbivores. J Tropical Ecol 24:329–336

    Google Scholar 

  • Pelet F, Hildebrandt AC, Riker AJ, Skoog F (1960) Growth in vitro of tissues isolated from normal stems and insect galls. Am J Bot 47:186–195

    Article  Google Scholar 

  • Pertry I, Václavikova K, Depuydt S, Galuszka P, Spíchal L, Temmerman W, Stes E, Schmülling T, Kakimoto T, Van Montagu MCE, Strnad M, Holsters M, Tarkowski P, Vereecke D (2009) Identification of Rhodococcus fascians cytokinins and their modus operandi to reshape the plant. Proc Natl Acad Sci USA 106:929–934

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Pertry I, Václavikova K, Gemrotová M, Spíchal L, Galuszka P, Depuydt S, Temmerman W, Stes E, 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-meditated production of a cytokinin mix. Mol Plant Microbe Interact 25:1164–1174

    Article  Google Scholar 

  • Plumb GH (1953) The formation and development of the Norway spruce gall caused by Adelges abietis L. Bull Conn Agric Exp Stn 566:1–77

    Google Scholar 

  • Raman A (2011) Morphogenesis of insect-induced plant galls: facts and questions. Flora Morphol Distrib Funct Ecol Plants 206:517–533

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Sakakibara H, Kashara H, Ueda N, Kojima M, Takei K, Hishlyama S, Asami T, Okada K, Kamlya Y, Yamaya T, Yamaguchi S (2005) Agrobacterium tumefaciens increases cytokinin production in plastids by modifying the biosynthetic pathway in the host plant. Proc Natl Acad Sci USA 102:9972–9977

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Spaepen S, Vanderleyden J (2011) Auxin and plant–microbe interactions. Cold Spring Harb Perspect Biol 2011(3):a001438

    Google Scholar 

  • Spíchal L (2012) Cytokinins—recent news and views of evolutionally old molecules. Funct Plant Biol 39:267–284

    Article  Google Scholar 

  • Stirk WA, van Staden J (2010) Flow of cytokinins through the environment. Plant Growth Regul 62:101–116

    Article  CAS  Google Scholar 

  • Straka JR, Hayward AR, Emery RJN (2010) Gall-inducing Pachypsylla celtidis (Psyllidae) infiltrate hackberry trees with high concentrations of phytohormones. J Plant Interact 5:197–203

    Article  CAS  Google Scholar 

  • Tabur S, Öney S (2012) Comparison of cytogenetic antagonism between abscisic acid and plant growth regulators. Pak J Bot 44:1581–1586

    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 9:1942–1948

    Article  Google Scholar 

  • Tokuda M, Jikumaru Y, Matsukura K, Takebayashi Y, Kumashiro S, Matsumura M, Kamiya Y (2013) Phytohormones related to host plant manipulation by a gall-inducing leafhopper. PLoS ONE 8(4):e62350. doi:10.1371/journal.pone.0062350

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tomaszewska-Sowa M, Drodowska L, Szota M (2002) Effects of cytokinins on in vitro morphogenesis and ploidy of pepper Capsicum annuum L. Electron J Pol Agric Univ Agron 5(1):#4. http://www.ejpau.media.pl/volume5/issue1/agronomy/art-04.html

  • Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic acid and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod Plant Interact 5:115–124

    Article  Google Scholar 

  • Uechi N, Tokuda M, Yukawa J, Kawamura F, Teramoto KK, Karris KM (2003) Confirmation by DNA analysis that Contarinia maculipennis (Diptera: Cecidomyiidae) is a polyphagous pest of orchids and other unrelated cultivated plants. Bull Entomol Res 93:545–551

    Article  CAS  PubMed  Google Scholar 

  • van Staden J, Bennett PH (1991) Gall formation in crofton weed. Differences between normal stem tissue and gall tissue with respect to cytokinin levels and requirement for in vitro culture. S Afr J Bot 57:246–248

    Google Scholar 

  • van Staden J, Davey JE (1978) Endogenous cytokinins in the laminae and galls of Erythrina altissima leaves. Bot Gaz 139:36–41

    Article  Google Scholar 

  • Vovlas N, Nico LL, De Luca F, De Giorgi C, Castillo P (2007) Diagnosis and molecular variability of an Argentinean population of Nacobbus aberrans with some observations on histopathology in tomato. J Nematol 39:17–26

    CAS  PubMed Central  PubMed  Google Scholar 

  • Weis AE, Walton R, Crego CL (1988) Reactive plant tissue sites and the population biology of gall makers. Annu Rev Entomol 33:467–486

    Article  Google Scholar 

  • Wood BW, Payne JA (1988) Growth regulators in chestnut shoot galls infected with oriental chestnut gall wasp, Dyocosmus kuriphilus (Hymenoptera: Cynipidae). Environ Entomol 17:915–920

    CAS  Google Scholar 

  • Wood DW, Setubal JC, Kaul R, Monks DE, Kitajima JP, Okura VK, Zhou Y, Chen L, Wood GE, Almeida NF, Woo L, Chen Y, Paulsen IT, Eisen JA, Karp PD, Bovee D, Chapman P, Clendenning J, Deatherage G, Gillet W, Grant C, Kutyavin T, Levy R, Li M, McClelland E, Palmieri A, Raymond C, Rouse G, Saenphimmachak C, Wu Z, Romero P, Gordon D, Zhang S, Yoo H, Tao Y, Biddle P, Jung M, Krespan W, Perry M, Gordon-Kamm B, Liao L, Kim S, Hendrick C, Zhao Z, Dolan M, Chumley F, Tingey SV, Tomb J, Gordon MP, Olson MV, Nester EW (2001) The genome of the natural genetic engineer Agrobacterium tumefaciens C58. Science 294:2317–2323

    Article  CAS  PubMed  Google Scholar 

  • Xu X, van Lammeren A, Vermeer E, Vreugdenhil D (1998) The role of gibberellin, abscisic acid, and sucrose in regulation of potato tuber formation in vitro. Plant Physiol 117:575–584

    Article  CAS  PubMed Central  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Zhang H, Li C, MA S (2010) Physiological responses of gall tissues on Ivy tree leaves induced by thrip. Acta Bot Yunnanica 32:339–346

    CAS  Google Scholar 

  • Zhu J, Oger PM, Schrammeijer B, Hooykaas PJJ, Farrand SK, Winans SC (2000) The bases of crown gall tumorigenesis. J Bacteriol 182:3885–3895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank K. Biskar and S. Byrd for their assistance in injections and plant maintenance, and Z.H. He for assisting with the hormone solutions and providing laboratory facilities. We would also like to thank V.T. Parker, Z. Hajian-Forooshani, Z.H. He, and two anonymous reviewers for their comments on an earlier draft of this manuscript. This work was supported in part by a grant from the Office of the Vice Provost for Research at SFSU and by NSF Grant DEB 0943263.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Edward F. Connor.

Additional information

Handling Editor: John F. Tooker.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bartlett, L., Connor, E.F. Exogenous phytohormones and the induction of plant galls by insects. Arthropod-Plant Interactions 8, 339–348 (2014). https://doi.org/10.1007/s11829-014-9309-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-014-9309-0

Keywords

Navigation