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Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses

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Abstract

Induction of plant resistance by herbivory is a complex process, which follows a temporal dynamic and varies spatially at the within-plant scale. This study aimed at improving the understanding of the induction process in terms of time scale and within-plant allocation, using apple tree seedlings (Malus × domestica) as plant model. Feeding preferences of a leaf-chewing insect (Spodoptera littoralis) for previously damaged and undamaged plants were assessed for six different time intervals with respect to the herbivore damage treatment and for three leaf positions. In addition, main secondary defense compounds were quantified and linked to herbivore feeding preferences. Significant herbivore preference for undamaged plants (induced resistance) was first observed 3 days after herbivore damage in the most apical leaf. Responses were delayed in the other leaf positions, and induced resistance decreased within 10 days after herbivore damage simultaneously in all tested leaf positions. Chemical analysis revealed higher concentrations of the flavonoid phloridzin in damaged plants as compared to undamaged plants. This indicates that herbivore preference for undamaged apple plants may be linked to phloridzin, which is the main secondary metabolite of apple leaves. The observed time course and distribution of resistance responses within plants contribute to the understanding of induction processes and patterns, and support the optimal defense theory stating young tissue to be prioritized. Moreover, induced resistance responses occurred also basipetally in leaves below the damage site, which suggests that signaling pathways involved in resistance responses are not unidirectional.

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Abbreviations

RH:

Relative humidity

L:

Larval instar

CM:

Consumed dry mass

CA:

Consumed area

RA:

Remaining leaf disc area

RM:

Remaining leaf disc dry mass

CMu:

Consumed dry mass undamaged plant

CMd:

Consumed dry mass damaged plant

PI:

Preference index

SE:

Standard error

References

  • Agrawal AA (2000) Specificity of induced resistance in wild radish: causes and consequences for two specialist and two generalist caterpillars. Oikos 89:493–500

    Article  Google Scholar 

  • Agrell J, Oleszek W, Stochmal A, Olsen M, Anderson P (2003) Herbivore-induced responses in alfalfa (Medicago sativa). J Chem Ecol 29:303–320

    Article  CAS  Google Scholar 

  • Anderson P, Agrell J (2005) Within-plant variation in induced defence in developing leaves of cotton plants. Oecologia 144:427–434

    Article  PubMed  CAS  Google Scholar 

  • Anderson P, Jonsson M, Morte U (2001) Variation in damage to cotton affecting larval feeding preference of Spodoptera littoralis. Entomol Exp Appl 101:191–198

    Article  Google Scholar 

  • Arnold T, Appel H, Patel V, Stocum E, Kavalier A, Schultz J (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink-source model of plant defense. New Phytol 164:157–164

    Article  CAS  Google Scholar 

  • Babst BA, Ferrieri RA, Gray DW, Lerdau M, Schlyer DJ, Schueller M, Thorpe MR, Orians CM (2005) Jasmonic acid induces rapid changes in carbon transport and partitioning in Populus. New Phytol 167:63–72

    Article  PubMed  CAS  Google Scholar 

  • Baldwin IT, Preston CA (1999) The eco-physiological complexity of plant responses to insect herbivores. Planta 208:137–145

    Article  CAS  Google Scholar 

  • Ballhorn DJ, Schiwy S, Jensen M, Heil M (2008) Quantitative variability of direct chemical defense in primary and secondary leaves of lima bean (Phaseolus lunatus) and consequences for a natural herbivore. J Chem Ecol 34:1298–1301

    Article  PubMed  CAS  Google Scholar 

  • Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493

    Article  PubMed  Google Scholar 

  • Bingham RA, Agrawal AA (2010) Specificity and trade-offs in the induced plant defence of common milkweed Asclepias syriaca to two lepidopteran herbivores. J Ecol 98:1014–1022

    Article  Google Scholar 

  • Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448

    Article  PubMed  Google Scholar 

  • Boege K, Dirzo R, Siemens D, Brown P (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10:177–187

    Article  PubMed  Google Scholar 

  • Eichhorn MP, Nilus R, Compton SG, Hartley SE, Burslem D (2010) Herbivory of tropical rain forest tree seedlings correlates with future mortality. Ecology 91:1092–1101

    Article  PubMed  Google Scholar 

  • Erb M, Lenk C, Degenhardt J, Turlings TCJ (2009) The underestimated role of roots in defense against leaf attackers. Trends Plant Sci 14:653–659

    Article  PubMed  CAS  Google Scholar 

  • Escarpa A, Gonzalez MC (1998) High-performance liquid chromatography with diode-array detection for the determination of phenolic compounds in peel and pulp from different apple varieties. J Chromatogr A 823:331–337

    Article  PubMed  CAS  Google Scholar 

  • Eyles A, Bonello P, Ganley R, Mohammed C (2010) Induced resistance to pests and pathogens in trees. New Phytol 185:893–908

    Article  PubMed  Google Scholar 

  • Frost CJ, Hunter MD (2008) Herbivore-induced shifts in carbon and nitrogen allocation in red oak seedlings. New Phytol 178:835–845

    Article  PubMed  CAS  Google Scholar 

  • Fulcher AF, Ranney TG, Burton JD, Walgenbach JF, Danehower DA (1998) Role of foliar phenolics in host plant resistance of Malus taxa to adult Japanese beetles. Hortscience 33:862–865

    CAS  Google Scholar 

  • Gomez S, van Dijk W, Stuefer JF (2010) Timing of induced resistance in a clonal plant network. Plant Biol 12:512–517

    Article  PubMed  Google Scholar 

  • Gosch C, Halbwirth H, Kuhn J, Miosic S, Stich K (2009) Biosynthesis of phloridzin in apple (Malus domestica Borkh.). Plant Sci 176:223–231

    Article  CAS  Google Scholar 

  • Heil M, Ton J (2008) Long-distance signalling in plant defence. Trends Plant Sci 13:264–272

    Article  PubMed  CAS  Google Scholar 

  • Hern A, Dorn S (2001) Induced emissions of apple fruit volatiles by the codling moth: changing patterns with different time periods after infestation and different larval instars. Phytochemistry 57:409–416

    Article  PubMed  CAS  Google Scholar 

  • Hern A, Dorn S (2002) Induction of volatile emissions from ripening apple fruits infested with Cydia pomonella and the attraction of adult females. Entomol Exp Appl 102:145–151

    Article  CAS  Google Scholar 

  • Howe GA (2004) Jasmonates as signals in the wound response. J Plant Growth Regul 23:223–237

    CAS  Google Scholar 

  • Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66

    Article  PubMed  CAS  Google Scholar 

  • Hudgins JW, Ralph SG, Franceschi VR, Bohlmann J (2006) Ethylene in induced conifer defense: cDNA cloning, protein expression, and cellular and subcellular localization of 1-aminocyclopropane-1-carboxylate oxidase in resin duct and phenolic parenchyma cells. Planta 224:865–877

    Article  PubMed  CAS  Google Scholar 

  • Hui X, Jin C (2004) Interspecific variation of plant traits associated with resistance to herbivory among four species of Ficus (Moraceae). Ann Bot 94:377–384

    Article  Google Scholar 

  • Jones CG, Coleman JS (1988) Leaf disk size and insect feeding preference: implications for assays and studies on induction of plant defense. Entomol Exp Appl 47:167–172

    Article  Google Scholar 

  • Jones CG, Hopper RF, Coleman JS, Krischik VA (1993) Control of systemically induced herbivore resistance by plant vascular architecture. Oecologia 93:452–456

    Article  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008a) Constitutive and induced defenses to herbivory in above- and belowground plant tissues. Ecology 89:392–406

    Article  PubMed  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Sardanelli S, Denno RF (2008b) Effects of plant vascular architecture on aboveground-belowground-induced responses to foliar and root herbivores on Nicotiana tabacum. J Chem Ecol 34:1349–1359

    Article  PubMed  CAS  Google Scholar 

  • Karban R, Baldwin IT (1997) Induced responses to herbivory. The University of Chicago Press, Chicago

    Google Scholar 

  • Kindt M, Orsini MC, Costantini B (2007) Improved high-performance liquid chromatography-diode array detection method for the determination of phenolic compounds in leaves and peels from different apple varieties. J Chromatogr Sci 45:507–514

    PubMed  CAS  Google Scholar 

  • Lempa K, Agrawal AA, Salminen JP, Turunen T, Ossipov V, Ossipova S, Haukioja E, Pihlaja K (2004) Rapid herbivore-induced changes in mountain birch phenolics and nutritive compounds and their effects on performance of the major defoliator, Epirrita autumnata. J Chem Ecol 30:303–321

    Article  PubMed  CAS  Google Scholar 

  • Leser C, Treutter D (2005) Effects of nitrogen supply on growth, contents of phenolic compounds and pathogen (scab) resistance of apple trees. Physiol Plant 123:49–56

    Article  CAS  Google Scholar 

  • Mattiacci L, Rudelli S, Rocca BA, Genini S, Dorn S (2001) Systemically-induced response of cabbage plants against a specialist herbivore, Pieris brassicae. Chemoecology 11:167–173

    Article  Google Scholar 

  • McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98:985–992

    Article  Google Scholar 

  • McGuire RJ, Johnson MTJ (2006) Plant genotype and induced responses affect resistance to herbivores on evening primrose (Oenothera biennis). Ecol Entomol 31:20–31

    Article  Google Scholar 

  • Metlen KL, Aschehoug ET, Callaway RM (2009) Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant Cell Environ 32:641–653

    Article  PubMed  CAS  Google Scholar 

  • Mitchell MJ, Keogh DP, Crooks JR, Smith SL (1993) Effects of plant flavonoids and other allelochemicals on insect cytochrome P-450 dependent steroid hydroxylase-activity. Insect Biochem Mol Biol 23:65–71

    Article  PubMed  CAS  Google Scholar 

  • Mody K, Eichenberger D, Dorn S (2009) Stress magnitude matters: different intensities of pulsed water stress produce non-monotonic resistance responses of host plants to insect herbivores. Ecol Entomol 34:133–143

    Article  Google Scholar 

  • Mumm R, Hilker M (2006) Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci 11:351–358

    Article  PubMed  CAS  Google Scholar 

  • Ohnmeiss TE, Baldwin IT (2000) Optimal defense theory predicts the ontogeny of an induced nicotine defense. Ecology 81:1765–1783

    Article  Google Scholar 

  • Olson DM, Cortesero AM, Rains GC, Potter T, Lewis WJ (2009) Nitrogen and water affect direct and indirect plant systemic induced defense in cotton. Biol Control 49:239–244

    Article  CAS  Google Scholar 

  • Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242

    Article  PubMed  CAS  Google Scholar 

  • Petkovsek MM, Stampar E, Veberic R (2008) Increased phenolic content in apple leaves infected with the apple scab pathogen. J Plant Pathol 90:49–55

    CAS  Google Scholar 

  • Philippe RN, Ralph SG, Mansfield SD, Bohlmann J (2010) Transcriptome profiles of hybrid poplar (Populus trichocarpa × deltoides) reveal rapid changes in undamaged, systemic sink leaves after simulated feeding by forest tent caterpillar (Malacosoma disstria). New Phytol 188:787–802

    Article  PubMed  CAS  Google Scholar 

  • Picinelli A, Dapena E, Mangas JJ (1995) Polyphenolic pattern in apple tree leaves in relation to scab resistance: a preliminary study. J Agric Food Chem 43:2273–2278

    Article  CAS  Google Scholar 

  • Radhika V, Kost C, Bartram S, Heil M, Boland W (2008) Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 228:449–457

    Article  PubMed  CAS  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54

    Google Scholar 

  • Roach WA (1939) Plant injection as a physiological method. Ann Bot 3:155–226

    CAS  Google Scholar 

  • Ruuhola T, Yang SY, Ossipov V, Haukioja E (2008) Foliar oxidases as mediators of the rapidly induced resistance of mountain birch against Epirrita autumnata. Oecologia 154:725–730

    Article  PubMed  Google Scholar 

  • Schaller A, Ryan CA (1996) Systemin: a polypeptide defense signal in plants. Bioessays 18:27–33

    Article  PubMed  CAS  Google Scholar 

  • Schieber A, Keller P, Carle R (2001) Determination of phenolic acids and flavonoids of apple and pear by high-performance liquid chromatography. J Chromatogr A 910:265–273

    Article  PubMed  CAS  Google Scholar 

  • Schittko U, Baldwin IT (2003) Constraints to herbivore-induced systemic responses: bidirectional signaling along orthostichies in Nicotiana attenuata. J Chem Ecol 29:763–770

    Article  PubMed  CAS  Google Scholar 

  • Schwachtje J, Minchin PEH, Jahnke S, van Dongen JT, Schittko U, Baldwin IT (2006) SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc Natl Acad Sci USA 103:12935–12940

    Article  PubMed  CAS  Google Scholar 

  • Stoeckli S, Mody K, Gessler C, Patocchi A, Jermini M, Dorn S (2008) QTL analysis for aphid resistance and growth traits in apple. Tree Genet Genomes 4:833–847

    Article  Google Scholar 

  • Stoeckli S, Mody K, Gessler C, Christen D, Dorn S (2009) Quantitative trait locus mapping of resistance in apple to Cydia pomonella and Lyonetia clerkella and of two selected fruit traits. Ann Appl Biol 154:377–387

    Article  Google Scholar 

  • Stout MJ, Riggio MR, Yang Y (2009) Direct induced resistance in Oryza sativa to Spodoptera frugiperda. Environ Entomol 38:1174–1181

    Article  PubMed  CAS  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Szankowski I, Flachowsky H, Li H, Halbwirth H, Treutter D, Regos I, Hanke MV, Stich K, Fischer TC (2009) Shift in polyphenol profile and sublethal phenotype caused by silencing of anthocyanidin synthase in apple (Malus sp.). Planta 229:681–692

    Article  PubMed  CAS  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  PubMed  CAS  Google Scholar 

  • Underwood NC (1998) The timing of induced resistance and induced susceptibility in the soybean Mexican bean beetle system. Oecologia 114:376–381

    Article  Google Scholar 

  • Viswanathan DV, Thaler JS (2004) Plant vascular architecture and within-plant spatial patterns in resource quality following herbivory. J Chem Ecol 30:531–543

    Article  PubMed  CAS  Google Scholar 

  • Wardlaw IF (1990) The control of carbon partitioning in plants. New Phytol 116:341–381

    Article  CAS  Google Scholar 

  • Zhao T, Krokene P, Bjorklund N, Langstrom B, Solheim H, Christiansen E, Borg-Karlson AK (2010) The influence of Ceratocystis polonica inoculation and methyl jasmonate application on terpene chemistry of Norway spruce, Picea abies. Phytochemistry 71:1332–1341

    Article  PubMed  CAS  Google Scholar 

  • Zong N, Wang CZ (2007) Larval feeding induced defensive responses in tobacco: comparison of two sibling species of Helicoverpa with different diet breadths. Planta 226:215–224

    Article  PubMed  CAS  Google Scholar 

  • Zvereva EL, Kozlov MV, Niemela P, Haukioja E (1997) Delayed induced resistance and increase in leaf fluctuating asymmetry as responses of Salix borealis to insect herbivory. Oecologia 109:368–373

    Article  Google Scholar 

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Acknowledgments

We thank Rafal Piskorski (ETHZ, Applied Entomology) for useful support in chemical analyses; Sybille Unsicker (MPI for Chemical Ecology, Jena, Germany) and Barbara Eder-Aebersold (ETHZ, Institute for Food Science) for their help in establishing and verifying the presented chemical method; Syngenta Switzerland for providing test insects; Lukas Rosinus (ETHZ, Seminar for Statistics) for statistical advice; Andreas Schaller (University Hohenheim, Germany) and Rafal Piskorski for fruitful discussions and constructive comments on the manuscript and two anonymous reviewers for helpful comments and suggestions.

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  1. ETH Zurich, Institute of Plant, Animal and Agroecosystem Sciences, Applied Entomology, Schmelzbergstrasse 9/LFO, 8092, Zurich, Switzerland

    Bettina Gutbrodt, Karsten Mody, Raphaël Wittwer & Silvia Dorn

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  1. Bettina Gutbrodt
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  2. Karsten Mody
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  3. Raphaël Wittwer
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Correspondence to Karsten Mody.

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Gutbrodt, B., Mody, K., Wittwer, R. et al. Within-plant distribution of induced resistance in apple seedlings: rapid acropetal and delayed basipetal responses. Planta 233, 1199–1207 (2011). https://doi.org/10.1007/s00425-011-1371-6

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