Abstract
Main conclusion
The study challenges the general belief that plants are highly sensitive to oral cues of herbivores and reveals the role of the damage level on the magnitude of defense induction.
Abstract
Many leaf-feeding caterpillars share similar feeding behaviors involving repeated removal of previously wounded leaf tissue (semicircle feeding pattern). We hypothesized that this behavior is a strategy to attenuate plant-induced defenses by removing both the oral cues and tissues that detect it. Using tobacco (Nicotiana tabacum) and the tobacco hornworm (Manduca sexta), we found that tobacco increased defensive responses during herbivory compared to mechanical wounding at moderate damage levels (30%). However, tobacco did not differentiate between mechanical wounding and herbivory when the level of leaf tissue loss was either small (4%) or severe (100%, whole leaf removal). Higher amounts of oral cues did not induce higher defenses when damage was small. Severe damage led to the highest level of systemic defense proteins compared to other levels of leaf tissue loss with or without oral cues. In conclusion, we did not find clear evidence that semicircle feeding behavior compromises plant defense induction. In addition, the level of leaf tissue loss and oral cues interact to determine the level of induced defensive responses in tobacco. Although oral cues play an important role in inducing defensive proteins, the level of induction depends more on the level of leaf tissue loss in tobacco.
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References
Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW (2015) Cues from chewing insects—the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr Opin Plant Biol 26:80–86. https://doi.org/10.1016/j.pbi.2015.05.029
Acevedo FE, Peiffer M, Tan CW, Stanley BA, Stanley A, Wang J, Jones AG, Hoover K, Rosa C, Luthe D, Felton G (2017) Fall armyworm-associated gut bacteria modulate plant defense responses. Mol Plant Microbe Interact 30(2):127–137. https://doi.org/10.1094/MPMI-11-16-0240-R
Acevedo FE, Peiffer M, Ray S, Meagher R, Luthe DS, Felton GW (2018) Intraspecific differences in plant defense induction by fall armyworm strains. New Phytol 218(1):310–321. https://doi.org/10.1111/nph.14981
Agrawal AA (2007) Macroevolution of plant defense strategies. Trends Ecol Evol 22(2):103–109. https://doi.org/10.1016/j.tree.2006.10.012
Agrawal AA, Hastings AP (2019) Plant defense by latex: ecological genetics of inducibility in the milkweeds and a general review of mechanisms, evolution, and implications for agriculture. J Chem Ecol 45(11–12):1004–1018. https://doi.org/10.1007/s10886-019-01119-8
Agrawal AA, Konno K (2009) Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40(1):311–331. https://doi.org/10.1146/annurev.ecolsys.110308.120307
Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276(5314):945–949. https://doi.org/10.1126/science.276.5314.945
Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH, Schmelz EA, Teal PE (2007) Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. Proc Natl Acad Sci USA 104(32):12976–12981. https://doi.org/10.1073/pnas.0705947104
Appel HM, Cocroft RB (2014) Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175(4):1257–1266. https://doi.org/10.1007/s00442-014-2995-6
Arimura G, Kopke S, Kunert M, Volpe V, David A, Brand P, Dabrowska P, Maffei ME, Boland W (2008) Effects of feeding Spodoptera littoralis on lima bean leaves: IV. Diurnal and nocturnal damage differentially initiate plant volatile emission. Plant Physiol 146(3):965–973. https://doi.org/10.1104/pp.107.111088
Asai S, Shirasu K (2015) Plant cells under siege: plant immune system versus pathogen effectors. Curr Opin Plant Biol 28:1–8. https://doi.org/10.1016/j.pbi.2015.08.008
Baldwin IT (1988) The alkaloidal responses of wild tobacco to real and simulated herbivory. Oecologia 77(3):378–381. https://doi.org/10.1007/BF00378046
Bede JC, Musser RO, Felton GW, Korth KL (2006) Caterpillar herbivory and salivary enzymes decrease transcript levels of Medicago truncatula genes encoding early enzymes in terpenoid biosynthesis. Plant Mol Biol 60(4):519–531. https://doi.org/10.1007/s11103-005-4923-y
Büchi R, Bachmann M, Keller F (1998) Carbohydrate metabolism in source leaves of sweet basil (Ocimum basilicum L.), a starch-storing and stachyose-translocating labiate. J Plant Physiol 153(3–4):308–315. https://doi.org/10.1016/s0176-1617(98)80156-9
Chung SH, Felton GW (2011) Specificity of induced resistance in tomato against specialist lepidopteran and coleopteran species. J Chem Ecol 37(4):378–386. https://doi.org/10.1007/s10886-011-9937-0
Chung SH, Rosa C, Scully ED, Peiffer M, Tooker JF, Hoover K, Luthe DS, Felton GW (2013) Herbivore exploits orally secreted bacteria to suppress plant defenses. Proc Natl Acad Sci USA 110(39):15728–15733. https://doi.org/10.1073/pnas.1308867110
Consales F, Schweizer F, Erb M, Gouhier-Darimont C, Bodenhausen N, Bruessow F, Sobhy I, Reymond P (2012) Insect oral secretions suppress wound-induced responses in Arabidopsis. J Exp Bot 63(2):727–737. https://doi.org/10.1093/jxb/err308
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. Induced plant resistance to herbivory. Springer, Amsterdam, pp 253–270
Dussourd DE, Denno RF (1991) Deactivation of plant defense—correspondence between insect behavior and secretory canal architecture. Ecology 72(4):1383–1396. https://doi.org/10.2307/1941110
Dussourd DE, Eisner T (1987) Vein-cutting behavior: insect counterploy to the latex defense of plants. Science 237(4817):898–901. https://doi.org/10.1126/science.3616620
Erb M, Reymond P (2019) Molecular interactions between plants and insect herbivores. Annu Rev Plant Biol 70(1):527–557. https://doi.org/10.1146/annurev-arplant-050718-095910
Evans PS (2012) The effect of repeated defoliation to three different levels on root growth of five pasture species. N Z J Agric Res 16(1):31–34. https://doi.org/10.1080/00288233.1973.10421155
Halitschke R, Schittko U, Pohnert G, Boland W, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. III. Fatty acid–amino acid conjugates in herbivore oral secretions are necessary and sufficient for herbivore-specific plant responses. Plant Physiol 125(2):711–717. https://doi.org/10.1104/pp.125.2.711
Hanway JJ (1969) Defoliation effects on different corn (Zea mays, L.) Hybrids as influenced by plant population and stage of development1. Agron J 61(4):534–538. https://doi.org/10.2134/agronj1969.00021962006100040016x
Hofius D, Hajirezaei MR, Geiger M, Tschiersch H, Melzer M, Sonnewald U (2004) RNAi-mediated tocopherol deficiency impairs photoassimilate export in transgenic potato plants. Plant Physiol 135(3):1256–1268. https://doi.org/10.1104/pp.104.043927
Huang HJ, Cui JR, Xia X, Chen J, Ye YX, Zhang CX, Hong XY (2019) Salivary DNase II from Laodelphax striatellus acts as an effector that suppresses plant defence. New Phytol 224(2):860–874. https://doi.org/10.1111/nph.15792
Johnson R, Narvaez J, An G, Ryan C (1989) Expression of proteinase inhibitors I and II in transgenic tobacco plants: effects on natural defense against Manduca sexta larvae. Proc Natl Acad Sci USA 86(24):9871–9875. https://doi.org/10.1073/pnas.86.24.9871
Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117):323–329. https://doi.org/10.1038/nature05286
Jones AC, Seidl-Adams I, Engelberth J, Hunter CT, Alborn H, Tumlinson JH (2019) Herbivorous caterpillars can utilize three mechanisms to alter green leaf volatile emission. Environ Entomol 48(2):419–425. https://doi.org/10.1093/ee/nvy191
Jongsma MA, Bakker PL, Visser B, Stiekema WJ (1994) Trypsin-inhibitor activity in mature tobacco and tomato plants is mainly induced locally in response to insect attack, wounding and virus-infection. Planta 195(1):29–35. https://doi.org/10.1007/bf00206288
Jwa NS, Hwang BK (2017) Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Front Plant Sci 8:1687. https://doi.org/10.3389/fpls.2017.01687
Karban R, Myers JH (1989) Induced plant-responses to herbivory. Annu Rev Ecol Syst 20(1):331–348. https://doi.org/10.1146/annurev.es.20.110189.001555
Kazan K, Lyons R (2014) Intervention of phytohormone pathways by pathogen effectors. Plant Cell 26(6):2285–2309. https://doi.org/10.1105/tpc.114.125419
Konno K (2011) Plant latex and other exudates as plant defense systems: roles of various defense chemicals and proteins contained therein. Phytochemistry 72(13):1510–1530. https://doi.org/10.1016/j.phytochem.2011.02.016
Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Softw 69(1):1–33. https://doi.org/10.18637/jss.v069.i01
Leon J, Rojo E, Sanchez-Serrano JJ (2001) Wound signalling in plants. J Exp Bot 52(354):1–9. https://doi.org/10.1093/jexbot/52.354.1
Li C, Schilmiller AL, Liu G, Lee GI, Jayanty S, Sageman C, Vrebalov J, Giovannoni JJ, Yagi K, Kobayashi Y, Howe GA (2005) Role of beta-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17(3):971–986. https://doi.org/10.1105/tpc.104.029108
Li G, Bartram S, Guo H, Mithöfer A, Kunert M, Boland W (2019) SpitWorm, an herbivorous robot: mechanical leaf wounding with simultaneous application of salivary components. Plants 8(9):318. https://doi.org/10.1101/468702
Mangiafico S (2018) rcompanion: Functions to support extension education program evaluation. R package version 2.0
McCall AC, Fordyce JA (2010) Can optimal defence theory be used to predict the distribution of plant chemical defences? J Ecol 98(5):985–992. https://doi.org/10.1111/j.1365-2745.2010.01693.x
Mckey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108(961):305–320. https://doi.org/10.1086/282909
Musser RO, Hum-Musser SM, Eichenseer H, Peiffer M, Ervin G, Murphy JB, Felton GW (2002) Herbivory: caterpillar saliva beats plant defences. Nature 416(6881):599–600. https://doi.org/10.1038/416599a
Ohyama A, Nishimura S, Hirai M (1998) Cloning of cDNA for a cell wall-bound acid invertase from tomato (Lycopersicon esculentum) and expression of soluble and cell wall-bound invertases in plants and wounded leaves of L. esculentum and L. peruvianum. Genes Genet Syst 73(3):149–157. https://doi.org/10.1266/ggs.73.149
Peiffer M, Felton GW (2009) Do caterpillars secrete "oral secretions"? J Chem Ecol 35(3):326–335. https://doi.org/10.1007/s10886-009-9604-x
Peterson R (2017) Estimating normalization transformations with bestNormalize. https://github.com/petersonR/bestNormalize
Pinto CF, Torrico-Bazoberry D, Penna M, Cossio-Rodriguez R, Cocroft R, Appel H, Niemeyer HM (2019) Chemical responses of Nicotiana tabacum (Solanaceae) induced by vibrational signals of a generalist herbivore. J Chem Ecol 45(8):708–714. https://doi.org/10.1007/s10886-019-01089-x
R Core Team (2017) R: a language and environment for statistical computing. https://www.R-project.org/. Accessed 20 Feb 2018
Roitsch T (1999) Source–sink regulation by sugar and stress. Curr Opin Plant Biol 2(3):198–206. https://doi.org/10.1016/S1369-5266(99)80036-3
Ryan CA (1990) Protease inhibitors in plants—genes for improving defenses against insects and pathogens. Annu Rev Phytopathol 28(1):425–449. https://doi.org/10.1146/annurev.py.28.090190.002233
Ryan CA, Moura DS (2002) Systemic wound signaling in plants: a new perception. Proc Natl Acad Sci USA 99(10):6519–6520. https://doi.org/10.1073/pnas.112196499
Schilmiller AL, Howe GA (2005) Systemic signaling in the wound response. Curr Opin Plant Biol 8(4):369–377. https://doi.org/10.1016/j.pbi.2005.05.008
Schittko U, Preston CA, Baldwin IT (2000) Eating the evidence? Manduca sexta larvae cannot disrupt specific jasmonate induction in Nicotiana attenuata by rapid consumption. Planta 210(2):343–346. https://doi.org/10.1007/PL00008143
Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PE (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci USA 103(23):8894–8899. https://doi.org/10.1073/pnas.0602328103
Schwachtje J, Baldwin IT (2008) Why does herbivore attack reconfigure primary metabolism? Plant Physiol 146(3):845–851. https://doi.org/10.1104/pp.107.112490
Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annu Rev Plant Biol 63(1):451–482. https://doi.org/10.1146/annurev-arplant-042811-105518
Singh DK, Sale PWG (1997) Defoliation frequency and the response by white clover to increasing phosphorus supply 2. Non-structural carbohydrate concentrations in plant parts. Aust J Agric Res 48(1):119–124. https://doi.org/10.1071/a96052
Smith AM, Stitt M (2007) Coordination of carbon supply and plant growth. Plant Cell Environ 30(9):1126–1149. https://doi.org/10.1111/j.1365-3040.2007.01708.x
Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17(6):278–285. https://doi.org/10.1016/S0169-5347(02)02483-7
Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121(1):1–8. https://doi.org/10.1104/pp.121.1.1
Su Q, Peng Z, Tong H, Xie W, Wang S, Wu Q, Zhang J, Li C, Zhang Y (2019) A salivary ferritin in the whitefly suppresses plant defenses and facilitates host exploitation. J Exp Bot 70(12):3343–3355. https://doi.org/10.1093/jxb/erz152
Susko DJ, Superfisky B (2009) A comparison of artificial defoliation techniques using canola (Brassica napus). Plant Ecol 202(1):169–175. https://doi.org/10.1007/s11258-008-9462-6
Tallamy DW (1985) Squash beetle feeding-behavior—an adaptation against induced cucurbit defenses. Ecology 66(5):1574–1579. https://doi.org/10.2307/1938019
Tamayo MC, Rufat M, Bravo JM, San Segundo B (2000) Accumulation of a maize proteinase inhibitor in response to wounding and insect feeding, and characterization of its activity toward digestive proteinases of Spodoptera littoralis larvae. Planta 211(1):62–71. https://doi.org/10.1007/s004250000258
Thomas MA, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of populus. Oecologia 130(4):585–593
Tian D, Peiffer M, De Moraes CM, Felton GW (2014) Roles of ethylene and jasmonic acid in systemic induced defense in tomato (Solanum lycopersicum) against Helicoverpa zea. Planta 239(3):577–589. https://doi.org/10.1007/s00425-013-1997-7
Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T, Koo AJ, Howe GA, Gilroy S (2018) Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361(6407):1112–1115. https://doi.org/10.1126/science.aat7744
Vincent R, Nadeau D (1983) A micromethod for the quantitation of cellular proteins in Percoll with the Coomassie brilliant blue dye-binding assay. Anal Biochem 135(2):355–362. https://doi.org/10.1016/0003-2697(83)90696-6
Von Dahl CC, Baldwin IT (2004) Methyl jasmonate and cis-jasmone do not dispose of the herbivore-induced jasmonate burst in Nicotiana attenuata. Physiol Plant 120(3):474–481. https://doi.org/10.1111/j.0031-9317.2004.00269.x
Wagner MR, Evans PD (1985) Defoliation increases nutritional quality and allelochemics of pine seedlings. Oecologia 67(2):235–237. https://doi.org/10.1007/BF00384291
Weisberg S, Fox J (2011) An R companion to applied regression. Sage, Thousand Oaks
Wickham H, Francise R, Henry L, Müller K (2017) dplyr: A grammar of data manipulation. R package version 0.74
Winz RA, Baldwin IT (2001) Molecular interactions between the specialist herbivore Manduca sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. IV. Insect-induced ethylene reduces jasmonate-induced nicotine accumulation by regulating putrescine N-methyltransferase transcripts. Plant Physiol 125(4):2189–2202
Zavala JA, Patankar AG, Gase K, Hui D, Baldwin IT (2004) Manipulation of endogenous trypsin proteinase inhibitor production in Nicotiana attenuata demonstrates their function as antiherbivore defenses. Plant Physiol 134(3):1181–1190. https://doi.org/10.1104/pp.103.035634
Zhang L, Cohn NS, Mitchell JP (1996) Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol 112(3):1111–1117. https://doi.org/10.1104/pp.112.3.1111
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1(1):3–14. https://doi.org/10.1111/j.2041-210X.2009.00001.x
Acknowledgements
We thank Dr. Yinong Yang for providing plant material, and Brandon Gominho and Bipana Paudel Timilsena for providing insect material, and Michelle Peiffer for technical assistance. This project was funded by the Sigma-Xi Grants-in-Aid of Research (GIAR) program [https://www.sigmaxi.org/programs/grants-in-aid], the Agricultural and Food Research Initiative Program of the United States Department of Agriculture (Grant no. 2017-67013-26596) and the Hatch Project Grant PEN04576.
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Lin, PA., Felton, G.W. Oral cues are not enough: induction of defensive proteins in Nicotiana tabacum upon feeding by caterpillars. Planta 251, 89 (2020). https://doi.org/10.1007/s00425-020-03385-3
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DOI: https://doi.org/10.1007/s00425-020-03385-3