Abstract
Recently, a renewed interest in cytokinins (CKs) has allowed the characterization of these phytohormones as key regulatory molecules in plant biotic interactions. They have been proved to be instrumental in microbe- and insect-mediated plant phenotypes that can be either beneficial or detrimental for the host-plant. In parallel, insect endosymbiotic bacteria have emerged as key players in plant-insect interactions mediating directly or indirectly fundamental aspects of insect nutrition, such as insect feeding efficiency or the ability to manipulate plant physiology to overcome food nutritional imbalances. However, mechanisms that regulate CK production and the role played by insects and their endosymbionts remain largely unknown. Against this backdrop, studies on plant-associated bacteria have revealed fascinating and complex molecular mechanisms that lead to the production of bacterial CKs and the modulation of plant-borne CKs which ultimately result in profound metabolic and morphological plant modifications. This review highlights major strategies used by plant-associated bacteria that impact the CK homeostasis of their host-plant, to raise parallels with strategies used by phytophagous insects and to discuss the possible role played by endosymbiotic bacteria in these CK-mediated plant phenotypes. We hypothesize that insects employ a CK-mix production strategy that manipulates the phytohormonal balance of their host-plant and overtakes plant gene expression causing a metabolic and morphological habitat modification. In addition, insect endosymbiotic bacteria may prove to be instrumental in these manipulations through the production of bacterial CKs, including specific forms that challenge the CK-degrading capacity of the plant (thus ensuring persistent effects) and the CK-mediated plant defenses.
Similar content being viewed by others
References
Absmanner B, Stadler R, Hammes UZ (2013) Phloem development in nematode-induced feeding sites: the implications of auxin and cytokinin. Front Plant Sci 4:241–255
Akiyoshi DE, Regier DA, Gordon MP (1987) Cytokinin production by Agrobacterium and Pseudomonas spp. J Bacteriol 169:4242–4248
Akiyoshi DE, Regier DA, Gordon MP (1989) Nucleotide sequence of the tzs gene from Pseudomonas solanacearum strain K60. Nucleic Acids Res 17:8886
Baldwin IT (1998) Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci U S A 95:8113–8118
Baldwin IT (2001) An ecologically motivated analysis of plant-herbivore interactions in native tobacco. Plant Physiol 127:1449–1458
Barr KL, Hearne LB, Briesacher S, Clark TL, Davis GE (2010) Microbial symbionts in insects influence down-regulation of defense genes in maize. PLoS One 5:e11339
Behr M, Motyka V, Weihmann F, Malbeck J, Deising HB, Wirsel SG (2012) Remodeling of cytokinin metabolism at infection sites of Colletotrichum graminicola on maize leaves. Mol Plant Microbe Interact 25:1073–1082
Biere A, Bennett AE (2013) Three-way interactions between plants, microbes and insects. Funct Ecol 27:567–573
Body M, Kaiser W, Dubreuil G, Casas J, Giron D (2013) Leaf-miners co-opt microorganisms to enhance their nutritional environment. J Chem Ecol 39:969–977
Chen X, Li S, Aksoy S (1999) Concordant evolution of a symbiont with its host insect species: molecular phylogeny of genus Glossina and its bacteriome-associated endosymbiont, Wigglesworthia glossinidia. J Mol Evol 48:49–58
Choi J, Choi D, Lee S, Ryu CM, Hwang I (2011) Cytokinins and plant immunity: old foes or new friends? Trends Plant Sci 16:388–394
Depuydt S, Trenkamp S, Fernie AR, Elftieh S, Renou JP, Vuylsteke M, Holsters M, Vereecke D (2009) An integrated genomics approach to define niche establishment by Rhodococcus fascians. Plant Physiol 149:1366–1386
Dervinis C, Frost CJ, Lawrence SD, Novak NG, Davis JM (2010) Cytokinin primes plant responses to wounding and reduces insect performance. J Plant Growth Regul 29:289–296
Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175
Douglas AE (1989) Mycetocyte symbiosis in insects. Biol Rev Camb Philos Soc 64:409–434
Douglas AE (2008) Conflict, cheats and persistence of symbioses. New Phytol 177:849–858
Douglas AE (2009) The microbial dimension in insect nutritional ecology. Funct Ecol 23:38–47
Douglas AE (2013) Microbial brokers of insect-plant interactions revisited. J Chem Ecol 39:952–961
Elzen GW (1983) Cytokinins and insect galls. Comput Biochem Physiol A 76:17–19
Engelbrecht L (1971) Cytokinins in buds and leaves during growth, maturity and aging (with a comparison of two bioassays). Biochem Physiol Pflanz 162:547–558
Engelbrecht L, Orban U, Heese W (1969) Leaf-miner caterpillars and cytokinins in the “green islands” of autumn leaves. Nature 223:319–321
Erb M, Ton J, Degenhardt J, Turlings TCJ (2008) Interactions between arthropod-induced aboveground and belowground defences in plants. Plant Physiol 146:867–874
Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259
Falco MC, Marbach PAS, Pompermayer P, Lopes FCC, Silva-Filho (2001) Mechanisms of sugarcane response to herbivory. Genet Mol Biol 24:113–122
Farnsworth E (2004) Hormones and shifting ecology throughout plant development. Ecology 85:5–15
Feldhaar H (2011) Bacterial symbionts as mediators of ecologically important traits of insect hosts. Ecol Entomol 36:533–543
Frago E, Dicke M, Godfray HC (2012) Insect symbionts as hidden players in insect-plant interactions. Trends Ecol Evol 27:705–711
Frébort I, Kowalska M, Hluska T, Frébortová J, Galuszka P (2011) Evolution of cytokinin biosynthesis and degradation. J Exp Bot 62:2431–2452
Frugier F, Murray KJ, Crespi M, Szczyglowszki K (2008) Cytokinin: secret agent of symbiosis. Trends Plant Sci 13:115–120
Giron D, Huguet E (2011) A genomically tractable and ecologically relevant model herbivore for a model plant: new insights into the mechanisms of insect–plant interactions and evolution. Mol Ecol 33:990–994
Giron D, Kaiser W, Imbault N, Casas J (2007) Cytokinin-mediated leaf manipulation by a leafminer caterpillar. Biol Lett 3:340–343
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
Goggin FL (2007) Plant-aphid interactions: molecular and ecological perspectives. Curr Opin Plant Biol 10:399–408
Gonzalez-Rizzo S, Crespi M, Frugier F (2006) The Medicago truncatula CRE1 cytokinin receptor regulates lateral root development and early symbiotic interaction with Sinorhizobium meliloti. Plant Cell 18:2680–2693
Großkinsky DK, Naseem M, Abdelmohsen UR, Plickert N, Engelke T, Zeier TG, Novák O, Strnad M, Pfeifhofer H, Van der Graaff E, Simon U, Roitsch T (2011) Cytokinins mediate resistance against Pseudomonas syringae in tobacco through increased antimicrobial phytoalexin synthesis independent of salicylic acid signaling. Plant Physiol 157:815–830
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
Harcombe W, Hoffmann AA (2004) Wolbachia effects in Drosophila melanogaster: in search of fitness benefits. J Invertebr Pathol 87:45–50
Harris HL, Brennan LJ, Keddie BA, Braig HR (2010a) Bacterial symbionts in insects: balancing life and death. Symbiosis 51:37–53
Harris MO, Freeman TP, Anderson KG, Moore JA, Payne SA, Anderson KM, Rohfritsch O (2010b) H gene-mediated resistance to Hessian fly exhibits features of penetration resistance to fungi. Phytopathol 100:279–289
Hermsmeier D, Schittko U, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata: I. Large-scale changes in the accumulation of growth- and defense-related plant mRNAs. Plant Physiol 125:683–700
Hosokawa T, Kikuchi Y, Fukatsu T (2007) How many symbionts are provided by mothers, acquired by offspring, and needed for successful vertical transmission in an obligate insect–bacterium mutualism? Mol Ecol 16:5316–5325
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
Inbar M, Gerling D (2008) Plant-mediated interactions between whiteflies, herbivores, and natural enemies. Annu Rev Entomol 53:431–448
Jameson P (2000) Cytokinins and auxins in plant-pathogen interactions—an overview. Plant Growth Regul 32:69–380
Janson EM, Stireman JO 3rd, Singer MS, Abbot P (2008) Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification. Evolution 62:997–1012
Jiang CJ, Shimono M, Sugano S, Kojima M, Liu X, Inoue H, Sakakibara H, Takatsuji H (2013) Cytokinins act synergistically with salicylic acid to activate defence gene expression in rice. Mol Plant Microbe Interact 26:287–296
Kaiser W, Huguet E, Casas J, Commin C, Giron D (2010) Plant green-island phenotype induced by leaf-miners is mediated by bacterial symbionts. Proc R Soc B 277:2311–2319
Kakimoto T (2003) Perception and signal transduction of cytokinins. Annu Rev Plant Biol 54:605–627
Kempema LA, Cui X, Holzer FM, Walling LL (2007) Arabidopsis transcriptome changes in response to phloem-feeding silverleaf whitefly nymphs. Similarities and distinctions in responses to aphids. Plant Physiol 143:849–865
Kessler A, Baldwin IT (2002) Plant responses to insect herbivory: the emerging molecular analysis. Annu Rev Plant Biol 53:299–328
Kessler AR, Halitschke R, Baldwin IT (2004) Silencing the jasmonate cascade: induced plant defenses and insect populations. Science 305:665–668
Kieber JJ, Schaller GE (2014) Cytokinins. Arabidopsis book 12:e0168
Kisiala A, Laffont C, Emery RJ, Frugier F (2013) Bioactive cytokinins are selectively secreted by Sinorhizobium meliloti nodulating and nonnodulating strains. Mol Plant Microbe Interact 26:1225–1231
Lai CY, Baumann L, Baumann P (1994) Amplification of trpEG: adaptation of Buchnera aphidicola to an endosymbiotic association with aphids. Proc Natl Acad Sci U S A 91:3819–3823
Leicht IJ (1994) Induction and development of the bean gall caused by Pontania proxima. In: Williams MAJ (ed) Plant galls: organisms, interactions, population. Oxford University Press, New-York, pp 283–300
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
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
Ludwig-Müller J, Schuller A (2008) What can we learn from clubroots: alterations in host roots and hormone homeostasis caused by Plasmodiophora brassicae. Eur J Plant Pathol 121:291–302
Mapes CC, Davies PJ (2001) Cytokinins in the ball gall of Solidago altissima and in the gall forming larvae of Eurosta solidaginis. New Phytol 151:203–212
McDermott J, Meilan R, Thornburg R (1996) Plant-insect interactions: The hackberry nipple gall.World Wide Web J Bio. http://epress.com/w3jbio/vol2/mcdermott/mcdermott.html
Meldau S, Erb M, Baldwin IT (2012) Defence on demand: mechanisms behind optimal defence patterns. Ann Bot 110:1503–1514
Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu. Rev Plant Physiol Plant Mol Biol 52:89–118
Moran NA (2007) Symbiosis as an adaptive process and source of phenotypic complexity. Proc Natl Acad Sci U S A 104(Suppl 1):8627–8633
Moran NA, Degnan PH (2006) Functional genomics of Buchnera and the ecology of aphid hosts. Mol Ecol 15:1251–1261
Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190
Murray JD, Karas BJ, Sato S, Tabata S, Amyot L, Szczyglowski K (2007) A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis. Science 315:101–104
Perlman SJ, Zchori-Fein E, Hunter MS (2006) The emerging diversity of Rickettsia. Proc R Soc B 273:2097–2106
Pertry I, Václavíková 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 U S A 106:929–934
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
Pieterse CM, Dicke M (2007) Plant interactions with microbes and insects: from molecular mechanisms to ecology. Trends Plant Sci 12:564–569
Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521
Plet J, Wasson A, Ariel F, Le Signor C, Baker D, Mathesius U, Crespi M, Frugier F (2011) MtCRE1-dependent cytokinin signaling integrates bacterial and plant cues to coordinate symbiotic nodule organogenesis in Medicago truncatula. Plant J 65:622–633
Podlešáková K, Fardoux J, Patrel D, Bonaldi K, Novák O, Strnad M, Giraud E, Spíchal L, Nouwen N (2013) Rhizobial synthesized cytokinins contribute to but are not essential for the symbiotic interaction between photosynthetic Bradyrhizobia and Aeschynomene légumes. Mol Plant Microbe Interact 26:1232–1238
Poelman EH, Broekgaarden C, Van Loon JJA, Dicke M (2008a) Early season herbivore differentially affects plant defence responses to subsequently colonizing herbivores and their abundance in the field. Mol Ecol 17:3352–3365
Poelman EH, Van Loon JJA, Dicke M (2008b) Consequences of variation in plant defence for biodiversity at higher trophic levels. Trends Plant Sci 13:534–541
Poelman EH, Zheng SJ, Zhang Z, Heemskerk NM, Cortesero AM, Dicke M (2011) Parasitoid-specific induction of plant responses to parasitized herbivores affects colonization by subsequent herbivores. Proc Natl Acad Sci U S A 108:19647–19652
Robert CAM, Frank DL, Leach KA, Turlings TCJ, Hibbard BE, Erb M (2013) Direct and indirect plant defences are not suppressed by endosymbionts of a specialist root herbivore. J Chem Ecol 39:507–515
Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379
Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49:317–343
Saharan BS, Nehra V (2011) Plant growth promoting rhizobacteria: a critical review. Life Sci Med Res p. LSMR-21
Sakakibara H (2006) Cytokinins: activity, biosynthesis, and translocation. Annu Rev Plant Biol 57:431–449
Sano H, Seo S, Orudgev E, Youssefian S, Ishizuka K, Ohashi Y (1994) Expression of the gene for a small GTP binding protein in transgenic tobacco elevates endogenous cytokinin levels, abnormally induces salicylic acid in response to wounding, and increases resistance to tobacco mosaic virus infection. Proc Natl Acad Sci U S A 91:10556–10560
Schäfer M, Gase K, Reichelt M, Baldwin I, Meldau S (2013) Real time’ genetic manipulation: a new tool for ecological field studies. Plant J 76:506–518
Schultz JC (2002) Signals shared by plants and insects and the potential for phylogenetic espionage. J Integr Comp Biol 42:454–462
Schultz JC, Appel HM (2004) Cross-kingdom cross-talk: hormones shared by plants and their insect herbivores. Ecology 85:70–77
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146:845–851
Siemens J, Keller I, Sarx J, Kunz S, Schuller A, Nagel W, Schmülling T, Parniske M, Ludwig-Müller J (2006) Transcriptome analysis of Arabidopsis clubroots indicate a key role for cytokinins in disease development. Mol Plant Microbe Interact 19:480–494
Soler R, Van der Putten WH, Harvey JA, Vet LEM, Dicke M, Bezemer M (2012) Root herbivore effects on aboveground multitrophic interactions: patterns, processes and mechanisms. J Chem Ecol 38:755–767
Spíchal L (2012) Cytokinins—recent news and views of evolutionally old molecules. Funct Plant Biol 39:267–284
Stes E, Vandeputte OM, El Jaziri M, Holsters M, Verecke D (2011) A successful bacterial coup d’état: how Rhodococcus fascians redirects plant development. Annu Rev Phytopathol 49:69–86
Stes E, Francis I, Pertry I, Dolzblasz A, Depuydt S, Vereecke D (2013) The leafy gall syndrome induced by Rhodococcus fascians. FEMS Microbiol Lett 342:187–194
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
Stuart JJ, Chen MS, Shukle R, Harris MO (2012) Gall midges (Hessian flies) as plant pathogens. Annu Rev Phytopathol 50:339–358
Tarkowski P, Václavíková K, Novák O, Pertry I, Hanuš J, Whenham R, Vereecke D, Šebela M, Strnad M (2010) Analysis of 2-methylthio-derivatives of isoprenoid cytokinins by liquid chromatography-tandem mass spectrometry. Anal Chim Acta 680:86–91
Thaler JS, Fidantsef AL, Duffey SS, Bostock RM (1999) Trade-offs in plant defense against pathogens and herbivores: a field demonstration of chemical elicitors of induced resistance. J Chem Ecol 25:1597–1609
Tirichine L, Sandal N, Madsen LH, Radutoiu S, Albrektsen AS, Sato S, Asamizu E, Tabata S, Stougaard J (2007) A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis. Science 315:104–107
Vadassery J, Ritter C, Venus Y, Camehl I, Varma A, Shahollari B, Novák O, Strnad M, Ludwig-Müller J, Oelmüller R (2008) The role of auxins and cytokinins in the mutualistic interaction between Arabidopsis and piriformospora indica. Mol Plant Microbe Interact 21:1371–1383
Vereecke D, Cornelis K, Temmerman W, Jaziri M, Van Montagu M, Holsters M, Goethals K (2002) Chromosomal locus that affects pathogenicity of Rhodococcus fascians. J Bacteriol 184:1112–1120
Voelckel C, Baldwin IT (2003) Detecting herbivore-specific transcriptional responses in plants with multiple DDRT-PCR and subtractive library procedures. Physiol Plant 118:240–252
Walters DR, McRoberts N (2006) Plants and biotrophs: a pivotal role for cytokinins? Trends Plant Sci 11:581–586
Walters DR, McRoberts N, Fitt BD (2008) Are green islands red herrings? Significance of green islands in plant interactions with pathogens and pests. Biol Rev Camb Philos Soc 83:79–102
Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12:527–538
Whiteman NK, Groen SC, Chevasco D, Beckwith N, Gregory TR, Denoux C, Mammarella N, Ausubel FM, Pierce NE (2011) Mining the plant-insect interface with a leafmining Drosophila of Arabidopsis. Mol Ecol 20:995–1014
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
Ackowledgements
This study was supported by the ANR project ECOREN ANR-JC05-46491 and the Région Centre project 201000047141 to D. GIRON. Further support was also provided by the National Centre of Scientific Research (CNRS) and the University François-Rabelais. We also thank D. Daudu, M. Body, J. Casas, E. Huguet, W. Kaiser, A. Lanoue, N. Imbault, J. Crèche, N. Guivarch’, J. Schultz, M. Dicke, and H. Appel for fruitful discussions.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Giron, D., Glevarec, G. Cytokinin-Induced Phenotypes in Plant-Insect Interactions: Learning from the Bacterial World. J Chem Ecol 40, 826–835 (2014). https://doi.org/10.1007/s10886-014-0466-5
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-014-0466-5