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The mechanism of gall induction makes galls red

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Abstract

We propose that the commonly observed red coloration of insect-induced plant galls is due to the production of exogenous cytokinins by gall-inducing insects. A growing body of evidence indicates that gall-inducing insects, bacteria, and fungi produce cytokinins. We hypothesize that gall induction generally requires an exogenous source of cytokinin and auxin. Plant galls are mobilizing sinks induced by cytokinin and reinforced by transport and accumulation of sugar. Exogenous cytokinins lead to a cascade of effects including the up-regulation of anthocyanin synthesis, the source of red coloration. Experiments demonstrate that exogenous cytokinins and sugars up-regulate the phenylpropanoid and flavonoid pathways, leading to localized anthocyanin accumulation. We suggest that red coloration in plant galls is merely a consequence of the mechanism of gall induction, and therefore an example of fabricational noise rather than aposematic coloration. Only color manipulation experiments can determine whether gall color is also secondarily aposematic.

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References

  • Abrahamson WG, Weis AE (1997) Evolutionary ecology across three trophic levels. Monographs in population biology, vol 29. Princeton University Press, Princeton

    Google Scholar 

  • Abrahamson WG, Sattler JF, McCrea KD, Weis AE (1989) Variation in selection pressures on the goldenrod gall fly and the competitive interactions of its natural enemies. Oecologia 79:15–22

    Article  Google Scholar 

  • Allan AC, Hellens RP, Liang WA (2008) MYB transcription factors that colour our fruit. Trends Plant Sci 13:99–102

    Article  PubMed  CAS  Google Scholar 

  • Arditti M, Doring TF, Hagen SB, Hughes NM, Leather SR, Lee DW, Lev-Yadun S, Manetas Y, Ougham HJ, Schaberg PG, Thomas H (2009) Unravelling the evolution of autumn colours: an interdisciplinary approach. Trends Ecol Evol 24:166–173

    Article  Google Scholar 

  • Bailey JK, Wooley SC, Lindroth RL, Whitham TG (2006) Importance of species interactions to community heritability: a genetic basis to trophic level interactions. Ecol Lett 9:78–85

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Briscoe AD, Chittka L (2001) The evolution of color vision in insects. Annu Rev Entomol 46:471–510

    Article  PubMed  CAS  Google Scholar 

  • Bruce SA, Saville BJ, Neil Emery RJ (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 

  • Cane JH, Kurczewski FE (1976) Mortality factors affecting Eurosta solidaginis (Diptera: Tephritidae). J NY Entomol Soc 84:275–282

    Google Scholar 

  • Carvalho RF, Quecini V, Pereira Peres LE (2010) Hormonal modulation of photomorphogenesis-controlled anthocyanin accumulation in tomato (Solanum lycopersicum L. cv. Micro-Tom) hypocotyls: physiological and genetic studies. Plant Sci 178:258–264

    Article  CAS  Google Scholar 

  • Chen DQ, Li ZY, Pan RC, Wang XJ (2006) Anthocyanin accumulation mediated by blue light and cytokinin in Arabidopsis seedlings. J Integr Plant Biol 48:420–425

    Article  CAS  Google Scholar 

  • Close DC, Beadle CL (2003) Ecophysiology of foliar anthocyanin. Bot Rev 69:149–161

    Article  Google Scholar 

  • Confer JL, Paicos P (1985) Downy woodpecker predation at goldenrod galls. J Field Ornithol 56:56–64

    Google Scholar 

  • Constabel F, Shyluk JP, Gamborg OL (1971) The effects of hormones on anthocyanin accumulation in cell cultures of Haplopappus gracilis. Planta 96:306–316

    Article  CAS  Google Scholar 

  • Cooper SJ, Ashby AM (1998) Comparison of cytokinin and cytokinin-O-glucoside cleaving β-glucosidase production in vitro by Venturia inaequalis and other phytopathogenic fungi with differing modes of nutrition in planta. Physiol Mol Plant Physiol 53:61–72

    Article  CAS  Google Scholar 

  • Cornell HV (1983) The secondary chemistry and complex morphology of galls formed by the Cynipinae (Hymenoptera): why and how? Am Midl Nat 110:225–234

    Article  Google Scholar 

  • Craig TP, Itami JK, Horner JD (2006) Geographic variation in the evolution and coevolution of a tritrophic interaction. Evolution 61:1137–1152

    Article  Google Scholar 

  • Diekman J, Hammer PE (1995) Induction of anthocyanin accumulation by cytokinins in Arabidopsis thaliana. Plant Physiol 108:47–57

    Google Scholar 

  • 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 

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

    Article  CAS  Google Scholar 

  • Engelbrecht L, Orban U, Heese W (1969) Leaf-miner caterpillars and cytokinins in the “green islands” of autumn leaves. Nature 233:319–321

    Article  Google Scholar 

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

    Article  PubMed  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 

  • Gan S, Amasino RM (1995) Inhibition of leaf senescence by auto regulated production of cytokinins. Science 270:1986–1988

    Article  PubMed  CAS  Google Scholar 

  • Gan S, Amasino RM (1996) Cytokinins in plant senescence: from spray and pray to clone and play. BioEssays 18:557–565

    Article  CAS  Google Scholar 

  • Giron D, Kaiser W, Imbault N, Casas J (2007) Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biol Lett 3:340–343

    Article  PubMed  CAS  Google Scholar 

  • Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol 15:273–282

    Article  Google Scholar 

  • Guo J, Hu X, Duan R (2005) Interactive effects of cytokinins, light, and sucrose on the phenotypes and the syntheses of anthocyanins and lignins in cytokinin overproducing transgenic Arabidopsis. J Plant Growth Regul 24:93–101

    Article  CAS  Google Scholar 

  • Guo J, Han W, Wang MH (2008) Ultraviolet and environmental stresses involved in the induction and regulation of anthocyanin biosynthesis: a review. Afr J Biotechnol 7:4966–4972

    CAS  Google Scholar 

  • Hartley SE (1998) The chemical composition of plant galls: are levels of nutrients and secondary compounds controlled by the gall-former? Oecologia 113:492–501

    Article  Google Scholar 

  • Hawkins BA (1994) Pattern and process in host-parasitoid interactions. Cambridge University Press, Cambridge

  • Ikai N, Hijii N (2007) Manipulation of tannins in oaks by galling cynipids. J For Res 12:316–319

    Article  CAS  Google Scholar 

  • Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediation by induced host-plant sinks. Ecology 76:1505–1515

    Article  Google Scholar 

  • Inbar M, Izhaki I, Koplovich A, Lupo I, Silanikove N, Glasser T, Gerchman Y, Perevolotsky A, Lev-Yadun S (2010) Why do many galls have conspicuous colors? A new hypothesis. Arthropod Plant Interact 4:1–6

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kaiser W, Hyguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc Ser B 277:2311–2319

    Article  CAS  Google Scholar 

  • Lara MEB, Gonzalez Garcia MC, Fatima T, Ehneß R, Lee TK, Proels R, Tanner W, Roitsch T (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16:1276–1287

    Article  Google Scholar 

  • Larson KC, Whitham TG (1991) Manipulation of food resources by a gall-forming aphid. The physiology of sink-source interactions. Oecologia 88:15–21

    Article  Google Scholar 

  • Lewis DR, Ramirez MV, Miller ND, Vallabhaneni P, Ray WK, Helm RF, Winkel BSJ, Muday GK (2011) Auxin and ethylene induce flavonol accumulation through distinct transcriptional networks. Plant Physiol 156:144–164

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P (2008) Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytol 179:1004–1016

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Mapes CC (2008) Gall formation. In: Capinera JL (ed) Encyclopedia of entomology, vol 2, 2nd edn. Springer, New York, pp 1572–1576

    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 

  • Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603

    Article  PubMed  Google Scholar 

  • McDermott J, Melian R, Thornburg R (1996) Plant-insect interactions: the hackberry nipple gall. J Biol 2:7. http://www.epress.com/w3jbio/vol2/mcdermott/mcdermott.html. Accessed 10 Apr 2012

  • Mills LJ, van Staden J (1978) Extraction of cytokinins from maize, smut tumors of maize and Ustilago maydis cultures. Physiol Plant Pathol 13:73–80

    Article  CAS  Google Scholar 

  • Mortain-Bertrand A, Stammitti L, Telef N, Colardella P, Brouquisse R, Rolin D, Gallusci P (2008) Effects of exogenous glucose on carotenoid accumulation in tomato leaves. Physiol Plant 134:246–256

    Article  PubMed  CAS  Google Scholar 

  • Motta LB, Kraus JE, Salatino A, Salatino MLF (2005) Distribution of metabolites in galled and non-galled foliar tissues of Tibouchina pulchra. Biochem Syst Ecol 33:971–981

    Article  CAS  Google Scholar 

  • Noodén LD, Kahanak GM, Okatan Y (1979) Prevention of monocarpic senescence in soybeans with auxin and cytokinin: an antidote for self-destruction. Science 206:841–843

    Article  PubMed  Google Scholar 

  • Nyman T, Julkunen-Tiitto R (2000) Manipulation of the phenolic chemistry of willows by gall-inducing sawflies. Proc Natl Acad Sci USA 97:13184–13187

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Ougham HJ, Morris P, Thomas H (2005) The colors of autumn leaves as symptoms of cellular recycling and defenses against environmental stresses. Curr Top Dev Biol 66:135–160

    Article  PubMed  CAS  Google Scholar 

  • Ozreki Y, Komamine A (1981) Induction of anthocyanin synthesis in relation to embryogenesis in a carrot suspension cell culture: correlation of metabolic differentiation with morphological differentiation. Physiol Plant 53:570–577

    Article  Google Scholar 

  • Pehkonen T, Koskimäki J, Riihinen K, Pirttilä AM, Hohtola A, Jaakola L, Tolvanen A (2008) Artificial infection of Vaccinium vitis-idaea L. and defence responses of Exobasidium species. Physiol Mol Plant Pathol 72:146–150

    Article  CAS  Google Scholar 

  • Piazza P, Procissi A, Jenkins GI, Tonelli C (2002) Members of the c1/pl1 regulatory gene family mediate the response of maize aleurone and mesocotyl to different light qualities and cytokinins. Plant Physiol 128:1077–1086

    Article  PubMed  CAS  Google Scholar 

  • Putnam M (2012) Images of symptoms caused by Rhodococcus fascians on different hosts. http://plant-clinic.bpp.oregonstate.edu/rhodococcus-hosts. Accessed 10 Apr 2012

  • Putnam M (2012) Images of crown gall caused by Agrobacterium tumefaciens. http://plant-clinic.bpp.oregonstate.edu/crown-gall. Accessed 10 Apr 2012

  • Rehill BJ, Schultz JC (2003) Enhanced invertase activities in the galls of Hormaphis hamamelidis. J Chem Ecol 29:2703–2720

    Article  PubMed  CAS  Google Scholar 

  • Reineke G, Heinze B, Schiraski 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 tumor formation. Mol Plant Pathol 9:339–355

    Article  PubMed  CAS  Google Scholar 

  • Roitsch T, Ehneß R (2000) Regulation of source/sink relations by cytokinins. Plant Growth Regul 32:359–367

    Article  CAS  Google Scholar 

  • Roitsch T, Lara MEB, Hoffman M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524

    Article  PubMed  CAS  Google Scholar 

  • Schaefer HM, Ruxton GD (2008) Fatal attraction: carnivorous plants roll out the red carpet to attract insects. Biol Lett 4:153–155

    Article  PubMed  Google Scholar 

  • Schlichter L (1978) Winter predation by black-capped chickadees and downy woodpeckers on inhabitants of the goldenrod ball gall. Can Field Nat 92:71–74

    Google Scholar 

  • Seilacher A (1973) Fabricational noise in adaptive morphology. Syst Zool 22:451–465

    Article  Google Scholar 

  • Shealer DA, Snyder JP, Dresbach VC, Sunderlin DF, Novak JA (1999) Foraging patterns of eastern gray squirrels (Sciurus carolinensis) on goldenrod gall insects, a potentially important winter food resource. Am Midl Nat 142:102–109

    Article  Google Scholar 

  • Smith DS, Bailey JK, Shuster SM, Whitham TG (2011) A geographic mosaic of trophic interactions and selection: trees, aphids, and birds. J Evol Biol 24:422–429

    Article  PubMed  CAS  Google Scholar 

  • Stern RA, Korchinsky R, Ben-Arie R, Migal YC (2010) Early application of the synthetic auxin 2,4-DP enhances the red colouration of ‘Cripp’s Pink’ apple. J Horticult Sci Biotechnol 85:35–41

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Stone GN, Schrönrogge K (2003) The adaptive significance of insects gall morphology. Trends Ecol Evol 18:512–522

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Su W, Howell SH (1995) The effects of cytokinin and light on hypocotyls elongation in Arabidopsis seedling are independent and additive. Plant Physiol 108:1423–1430

    PubMed  CAS  Google Scholar 

  • Sunose T (1980) Predation by tree-sparrow (Passer montanus L.) on gall-making aphids. Kontyû, Tokyo 48:362–369

    Google Scholar 

  • Templeton CN (2011) Black-capped chickadees select spotted knapweed seedheads with high densities of gall fly larvae. Condor 113:395–399

    Article  Google Scholar 

  • Tscharntke T (1992) Cascade effects among four trophic levels: bird predation on galls affects density-dependent parasitism. Ecology 73:1689–1698

    Article  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 

  • Walters DR, McRoberts N, Fitt BDL (2008) Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biol Rev 83:79–102

    Article  PubMed  Google Scholar 

  • White TCR (2010) Why do many galls have conspicuous colours? An alternative hypothesis. Arthropod Plant Interact 4:149–150

    Article  Google Scholar 

  • Wingler A, Roitsch T (2008) Metabolic regulation of leaf senescence: interventions of sugar signaling with biotic and abiotic stress responses. Plant Biol 10:50–62

    Article  PubMed  CAS  Google Scholar 

  • Xiong LH, Wu X, Lu JJ (2010) Bird predation on concealed insects in a reed dominated estuarine tidal marsh. Wetlands 30:1203–1211

    Article  Google Scholar 

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Acknowledgments

We would like to thank C. Low, Z. H. He, T. P. Craig, D. Miller, E. Routman, G. Spicer, the editor, and two anonymous reviewers for valuable suggestions on an earlier draft of this manuscript. We would also like to thank T. P. Craig and D. G. Miller for their continuing assistance and stimulation in studying gall induction in Eurosta and Tamalia, M. Putnam for advice and information on coloration in bacterial and fungal galls, and M. McKone for permission to collect Eurosta galls in the Carleton College Arboretum. This work was supported by NSF grant DEB-0943263 to Edward F. Connor.

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  1. Department of Biology, San Francisco State University, 1600 Holloway Avenue, San Francisco, CA, 94132, USA

    Edward F. Connor, Linnea Bartlett, Sean O’Toole, Steven Byrd, Kevin Biskar & Jessica Orozco

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  1. Edward F. Connor
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  2. Linnea Bartlett
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Correspondence to Edward F. Connor.

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Connor, E.F., Bartlett, L., O’Toole, S. et al. The mechanism of gall induction makes galls red. Arthropod-Plant Interactions 6, 489–495 (2012). https://doi.org/10.1007/s11829-012-9210-7

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