Abstract
Plants perceive insect herbivores via a sophisticated surveillance system that detects a range of alarm signals, including herbivore-associated molecular patterns (HAMPs). Fatty acid-amino acid conjugates (FACs) are HAMPs present in oral secretions (OS) of lepidopteran larvae that induce defense responses in many plant species. In contrast to eggplant (Solanum melongena), tomato (S. lycopersicum) does not respond to FACs present in OS from Manduca sexta (Lepidoptera). Since both plants are found in the same genus, we tested whether loss of sensitivity to FACs in tomato may be a domestication effect. Using highly sensitive MAP kinase (MAPK) phosphorylation assays, we demonstrate that four wild tomato species and the closely related potato (S. tuberosum) do not respond to the FACs N-linolenoyl-L-glutamine and N-linolenoyl-L-glutamic acid, excluding a domestication effect. Among other genera within the Solanaceae, we found that bell pepper (Capsicum annuum) is responsive to FACs, while there is a differential responsiveness to FACs among tobacco (Nicotiana) species, ranging from strong responsiveness in N. benthamiana to no responsiveness in N. knightiana. The Petunia lineage is one of the oldest lineages within the Solanaceae and P. hybrida was responsive to FACs. Collectively, we demonstrate that plant responsiveness to FACs does not follow simple phylogenetic relationships in the family Solanaceae. Instead, sensitivity to FACs is a dynamic ancestral trait present in monocots and eudicots that was repeatedly lost during the evolution of Solanaceae species. Although tomato is insensitive to FACs, we found that other unidentified factors in M. sexta OS induce defenses in tomato.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH, Tumlinson JH (1997) An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:945–949. https://doi.org/10.1126/science.276.5314.945
Alborn HT, Jones TH, Stenhagen GS, Tumlinson JH (2000) Identification and synthesis of volicitin and related components from beet armyworm oral secretions. J Chem Ecol 26:203–220. https://doi.org/10.1023/A:1005401814122
Asai T, Tena G, Plotnikova J, Willmann MR, Chiu W-L, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415:977–983
Bartels S, Lori M, Mbengue M, van Verk M, Klauser D, Hander T, Boni R, Robatzek S, Boller T (2013) The family of peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J Exp Botany 64:5309–5321. https://doi.org/10.1093/jxb/ert330
Beloshistov RE, Dreizler K, Galiullina RA, Tuzhikov AI, Serebryakova MV, Reichardt S, Shaw J, Taliansky ME, Pfannstiel J, Chichkova NV, Stintzi A, Schaller A, Vartapetian AB (2018) Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytol 218:1167–1178. https://doi.org/10.1111/nph.14568
Bequette CJ, Hind SR, Pulliam S, Higgins R, Stratmann JW (2018) MAP kinases associate with high molecular weight multiprotein complexes. J Exp Bot 69:643–654. https://doi.org/10.1093/jxb/erx424
Bergey DR, Howe G, Ryan CA (1996) Polypeptide signaling for plant defensive genes exhibits analogies to defense signaling in animals. Proc Natl Acad Sci U S A 93:12053–12058
Chen H, Wilkerson CG, Kuchar JA, Phinney BS, Howe GA (2005) Jasmonate-inducible plant enzymes degrade essential amino acids in the herbivore midgut. Proc Natl Acad Sci USA 102:19237–19242. https://doi.org/10.1073/pnas.0509026102
Chen C-Y, Liu Y-Q, Song W-M, Chen D-Y, Chen F-Y, Chen X-Y, Chen Z-W, Ge S-X, Wang C-Z, Zhan S, Chen XY, Mao YB (2019) An effector from cotton bollworm oral secretion impairs host plant defense signaling. Proc Natl Acad Sci U S A 116:14331–14338. https://doi.org/10.1073/pnas.1905471116
Constabel CP, Yip L, Ryan CA (1998) Prosystemin from potato, black nightshade, and bell pepper: primary structure and biological activity of predicted systemin polypeptides. Plant Mol Biol 36:55–62. https://doi.org/10.1023/A:1005986004615
Couto D, Zipfel C (2016) Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol 16:537. https://doi.org/10.1038/nri.2016.77
Degenhardt DC, Refi-Hind S, Stratmann JW, Lincoln DE (2010) Systemin and jasmonic acid regulate constitutive and herbivore-induced systemic volatile emissions in tomato, Solanum lycopersicum. Phytochemistry 71:2024–2037. https://doi.org/10.1016/j.phytochem.2010.09.010
Doczi R, Bogre L (2018) The quest for MAP kinase substrates: gaining momentum. Trends Plant Sci 23:918–932. https://doi.org/10.1016/j.tplants.2018.08.002
Dombrowski JE, Hind SR, Martin RC, Stratmann JW (2011) Wounding systemically activates a mitogen-activated protein kinase in forage and turf grasses. Plant Sci 180:686–693. https://doi.org/10.1016/j.plantsci.2011.01.010
Dorokhov YL, Komarova TV, Petrunia IV, Frolova OY, Pozdyshev DV, Gleba YY (2012) Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog 8:e1002640. https://doi.org/10.1371/journal.ppat.1002640
Duran-Flores D, Heil M (2016) Sources of specificity in plant damaged-self recognition. Curr Opin Plant Biol 32:77–87. https://doi.org/10.1016/j.pbi.2016.06.019
Farmer EE, Gasperini D, Acosta IF (2014) The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 204:282–288. https://doi.org/10.1111/nph.12897
Felton GW, Tumlinson JH (2008) Plant-insect dialogs: complex interactions at the plant-insect interface. Curr Opin Plant Biol 11:457–463. https://doi.org/10.1016/j.pbi.2008.07.001
Gomez S, Steinbrenner AD, Osorio S, Schueller M, Ferrieri RA, Fernie AR, Orians CM (2012) From shoots to roots: transport and metabolic changes in tomato after simulated feeding by a specialist lepidopteran. Entomol Exp Appl 144:101–111. https://doi.org/10.1111/j.1570-7458.2012.01268.x
Green TR, Ryan CA (1972) Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–777. https://doi.org/10.1126/science.175.4023.776
Gust AA, Pruitt R, Nurnberger T (2017) Sensing danger: key to activating plant immunity. Trends Plant Sci 22:779–791. https://doi.org/10.1016/j.tplants.2017.07.005
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 125:711–717
Halitschke R, Gase K, Hui D, Schmidt DD, Baldwin IT (2003) Molecular interactions between the specialist herbivore Manduca Sexta (Lepidoptera, Sphingidae) and its natural host Nicotiana attenuata. VI. Microarray analysis reveals that Most herbivore-specific transcriptional changes are mediated by fatty acid-amino acid conjugates. Plant Physiol 131:1894–1902
Hann CT, Bequette CJ, Dombrowski JE, Stratmann JW (2014) Methanol and ethanol modulate responses to danger- and microbe-associated molecular patterns Frontiers in Plant Science 5. https://doi.org/10.3389/fpls.2014.00550
Heil M, Land WG (2014) Danger signals - damaged-self recognition across the tree of life. Front Plant Sci 5. https://doi.org/10.3389/fpls.2014.00578
Higgins R, Lockwood T, Holley S, Yalamanchili R, Stratmann J (2007) Changes in extracellular pH are neither required nor sufficient for activation of mitogen-activated protein kinases (MAPKs) in response to systemin and fusicoccin in tomato. Planta 225:1535–1546. https://doi.org/10.1007/s00425-006-0440-8
Hind SR, Strickler SR, Boyle PC, Dunham DM, Bao ZL, O'Doherty IM, Baccile JA, Hoki JS, Viox EG, Clarke CR et al. (2016) Tomato receptor FLAGELLIN-SENSING 3 binds flgII-28 and activates the plant immune system. Nature Plants 2. https://doi.org/10.1038/Nplants.2016.128
Holley SR, Yalamanchili RD, Moura SD, Ryan CA, Stratmann JW (2003) Convergence of signaling pathways induced by systemin, oligosaccharide elicitors, and ultraviolet-B radiation at the level of mitogen-activated protein kinases in Lycopersicon peruvianum suspension-cultured cells. Plant Physiol 132:1728–1738. https://doi.org/10.1104/pp.103.024414
Howe GA, Lightner J, Browse J, Ryan CA (1996) An octadecanoid pathway mutant (JL5) of tomato is compromised in signaling for defense against insect attack. Plant Cell 8:2067–2077
Huffaker A (2015) Plant elicitor peptides in induced defense against insects. Curr Opin Insect Sci 9:44–50. https://doi.org/10.1016/j.cois.2015.06.003
Johnson R, Narvaez J, An GH, Ryan C (1989) Expression of proteinase inhibitor-I and inhibitor-II in transgenic tobacco plants - effects on natural defense against Manduca-sexta larvae. Proc Natl Acad Sci USA 86:9871–9875. https://doi.org/10.1073/pnas.86.24.9871
Kandoth PK, Ranf S, Pancholi SS, Jayanty S, Walla MD, Miller W, Howe GA, Lincoln DE, Stratmann JW (2007) Tomato MAPKs LeMPK1, LeMPK2, and LeMPK3 function in the systemin-mediated defense response against herbivorous insects. Proc Natl Acad Sci U S A 104:12205–12210. https://doi.org/10.1073/pnas.0700344104
Kawazu K, Mochizuki A, Sato Y, Sugeno W, Murata M, Seo S, Mitsuhara I (2012) Different expression profiles of jasmonic acid and salicylic acid inducible genes in the tomato plant against herbivores with various feeding modes. Arthropod-Plant Inter 6:221–230. https://doi.org/10.1007/s11829-011-9174-z
Lee GI, Howe GA (2003) The tomato mutant spr1 is defective in systemin perception and the production of a systemic wound signal for defense gene expression. Plant J 33:567–576
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 β-oxidation in jasmonate biosynthesis and systemic wound signaling in tomato. Plant Cell 17:971–986. https://doi.org/10.1105/tpc.104.029108
Li G, Bartram S, Guo H, Mithöfer A, Kunert M, Boland W (2018) SpitWorm, an herbivorous robot: mechanical leaf wounding with simultaneous application of salivary components. bioRxiv:468702. https://doi.org/10.1101/468702
Liu Y, Zhang S (2004) Phosphorylation of 1-Aminocyclopropane-1-carboxylic acid synthase by MPK6, a stress-responsive mitogen-activated protein kinase, induces ethylene biosynthesis in Arabidopsis. Plant Cell 16:3386–3399
Ma H, Chen J, Zhang Z, Ma L, Yang Z, Zhang Q, Li X, Xiao J, Wang S (2017) MAPK kinase 10.2 promotes disease resistance and drought tolerance by activating different MAPKs in rice. Plant J 92:557–570. https://doi.org/10.1111/tpj.13674
McGurl B, Pearce G, Orozco-Cardenas M, Ryan CA (1992) Structure, expression, and antisense inhibition of the systemin precursor gene. Science 255:1570–1573
McGurl B, Orozco-Cardenas ML, Pearce G, Ryan CA (1994) Overexpression of the prosystemin gene in transgenic tomato plants generates a systemic signal that constitutively induces proteinase inhibitor synthesis. Proc Natl Acad Sci U S A 91:9799–9802
Mithöfer A, Wanner G, Boland W (2005) Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160-1168. doi.org/10.1104/pp.104.054460
Miya A, Albert P, Shinya T, Desaki Y, Ichimura K, Shirasu K, Narusaka Y, Kawakami N, Kaku H, Shibuya N (2007) CERK1, a LysM receptor kinase, is essential for chitin elicitor signaling in Arabidopsis. Proc Natl Acad Sci U S A 104:19613–19618. https://doi.org/10.1073/pnas.0705147104
Mizoguchi T, Irie K, Hirayama TNH, Yamaguchi-Shinozaki K, Matsumoto K, Shinozaki K (1996) A gene encoding a mitogen-activated protein kinase kinase kinase is induced simultaneously with genes for a mitogen-activated protein kinase and an S6 ribosomal protein kinase by touch, cold and water stress in Arabidopsis thaliana. Proc Natl Acad Sci USA 93:765–769. https://doi.org/10.1073/pnas.93.2.765
Nguyen CT, Kurenda A, Stolz S, Chételat A, Farmer EE (2018) Identification of cell populations necessary for leaf-to-leaf electrical signaling in a wounded plant. Proc Natl Acad Sci U S A 115:10178–10183. https://doi.org/10.1073/pnas.1807049115
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181. https://doi.org/10.1002/tax.574010
Orozco-Cardenas ML, McGurl B, Ryan CA (1993) Expression of an antisense prosystemin gene in tomato plants reduces resistance toward Manduca sexta larvae. Proc Natl Acad Sci U S A 90:8273–8276
Pearce G, Ryan CA (2003) Systemic signaling in tomato plants for defense against herbivores. Isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J Biol Chem 278:30044–30050
Pearce G, Moura D, Stratmann J, Ryan CA (2001) Production of multiple plant hormones from a single polyprotein precursor. Nature 411:817–820
Peiffer M, Felton GW (2009) Do caterpillars secrete “oral secretions”? J Chem Ecol 35:326–335. https://doi.org/10.1007/s10886-009-9604-x
Ryan CA (1967) Quantitative determination of soluble cellular proteins by radial diffusion in agar gels containing antibodies. Anal Biochem 19:434–440
Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214. https://doi.org/10.1186/1471-2148-13-214
Schmelz EA, Engelberth J, Alborn HT, Tumlinson JH, Teal PEA (2009) Phytohormone-based activity mapping of insect herbivore-produced elicitors. Proc Natl Acad Sci U S A 106:653–657. https://doi.org/10.1073/pnas.0811861106
Schmidt S, Baldwin IT (2006) Systemin in Solanum nigrum. The tomato-homologous polypeptide does not mediate direct defense responses. Plant Physiol 142:1751–1758. https://doi.org/10.1104/pp.106.089755
Schuman MC, Baldwin IT (2016) The layers of plant responses to insect herbivores. Annu Rev Entomol 61:373–394. https://doi.org/10.1146/annurev-ento-010715-023851
Stratmann JW, Ryan CA (1997) Myelin basic protein kinase activity in tomato leaves is induced systemically by wounding and increases in response to systemin and oligosaccharide elicitors. Proc Natl Acad Sci USA 94:11085–11089. https://doi.org/10.1073/pnas.94.20.11085
Stratmann J, Scheer J, Ryan CA (2000) Suramin inhibits initiation of defense signaling by systemin, chitosan and pmg-elicitor in suspension cultured Lycopersicon peruvianum cells. Proc Natl Acad Sci USA 97:8862–8867. https://doi.org/10.1073/pnas.97.16.8862
Tian DL, Peiffer M, Shoemaker E, Tooker J, Haubruge E, Francis F, Luthe DS, Felton GW (2012) Salivary glucose oxidase from caterpillars mediates the induction of rapid and delayed-induced defenses in the tomato plant. PloS One 7 https://doi.org/10.1371/journal.pone.0036168
Truitt CL, Wei H-X, Pare PW (2004) A plasma membrane protein from Zea mays binds with the herbivore elicitor Volicitin. Plant Cell 16:523–532. https://doi.org/10.1105/tpc.017723
Turlings TCJ, Alborn HT, Loughrin JH, Tumlinson JH (2000) Volicitin, an elicitor of maize volatiles in oral secretion of Spodoptera exigua: isolation and bioactivity. J Chem Ecol 26:189–202. https://doi.org/10.1023/a:1005449730052
Vadassery J, Reichelt M, Mithofer A (2012) Direct proof of ingested food regurgitation by spodoptera littoralis caterpillars during feeding on arabidopsis. J Chem Ecol 38:865–872. https://doi.org/10.1007/s10886-012-0143-5
Vandoorn A, Bonaventure G, Rogachev I, Aharoni A, Baldwin IT (2011) JA-Ile signalling in Solanum nigrum is not required for defence responses in nature. Plant Cell Environ 34:2159–2171. https://doi.org/10.1111/j.1365-3040.2011.02412.x
von Dahl CC, Winz RA, Halitschke R, Kuhnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuata. Plant J 51:293–307. https://doi.org/10.1111/j.1365-313X.2007.03142.x
Wang L, Einig E, Almeida-Trapp M, Albert M, Fliegmann J, Mithofer A, Kalbacher H, Felix G (2018) The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nature Plants 4:152–156. https://doi.org/10.1038/s41477-018-0106-0
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
Wu J, Hettenhausen C, Meldau S, Baldwin IT (2007) Herbivory rapidly activates MAPK signaling in attacked and unattacked leaf regions but not between leaves of Nicotiana attenuata. Plant Cell 19:1096–1122. https://doi.org/10.1105/tpc.106.049353
Xu SQ, Zhou WW, Pottinger S, Baldwin IT (2015) Herbivore associated elicitor-induced defences are highly specific among closely related Nicotiana species. BMC Plant Biol 15,2. https://doi.org/10.1186/s12870-014-0406-0
Yoshinaga N (2016) Physiological function and ecological aspects of fatty acid-amino acid conjugates in insects. Biosci Biotechnol Biochem 80:1274–1282. https://doi.org/10.1080/09168451.2016.1153956
Yoshinaga N, Aboshi T, Abe H, Nishida R, Alborn HT, Tumlinson JH, Mori N (2008) Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. Proc Natl Acad Sci U S A 105:18058–18063. https://doi.org/10.1073/pnas.0809623105
Yoshinaga N, Alborn HT, Nakanishi T, Suckling DM, Nishida R, Tumlinson JH, Mori N (2010) Fatty acid-amino acid conjugates diversification in lepidopteran caterpillars. J Chem Ecol 36:319–325. https://doi.org/10.1007/s10886-010-9764-8
Yoshinaga N, Abe H, Morita S, Yoshida T, Aboshi T, Fukui M, Tumlinson J, Mori N (2014a) Plant volatile eliciting FACs in lepidopteran caterpillars, fruit flies, and crickets: a convergent evolution or phylogenetic inheritance? Frontiers Physiol 5. https://doi.org/10.3389/fphys.2014.00121
Yoshinaga N, Ishikawa C, Seidl-Adams I, Bosak E, Aboshi T, Tumlinson JH, Mori N (2014b) N-(18-Hydroxylinolenoyl)-l-glutamine: a newly discovered analog of volicitin in Manduca sexta and its elicitor activity in plants. J Chem Ecol 40:484–490. https://doi.org/10.1007/s10886-014-0436-y
Zhou WW, Brockmoller T, Ling ZH, Omdahl A, Baldwin IT, Xu SQ (2016) Evolution of herbivore-induced early defense signaling was shaped by genome wide duplications in Nicotiana Elife:5. https://doi.org/10.7554/eLife.19531
Acknowledgements
The seeds of wild tomato species were developed by and/or obtained from the UC Davis/C.M. Rick Tomato Genetics Resource Center and maintained by the Department of Plant Sciences, University of California, Davis, CA 95616.
LG was supported by funds from the South Carolina Association for Minority Participation (SCAMP), a Trio-McNair fellowship, a Magellan Guarantee award from the University of SC VP for Research, and from the South Carolina Honors College (SCHC); AA was supported by supplemental REU funding (to NSF-IOS-0745545), funds from SCHC, a Magellan grant, and the Howard Hughes Undergraduate Research Fellowship; AMC was supported by the SCHC; KL was supported by funds from SCAMP and a Trio-McNair fellowship; BW was supported by funds from SCAMP; JWS, CJB, SRH, and CH were supported by National Science Foundation grant IOS-0745545 and by funds from the College of Arts and Sciences; EAS acknowledges support from USDA NIFA-AFRI (award #t 2018-67013-28125).
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
ESM 1
(PPTX 15.8 mb)
Rights and permissions
About this article
Cite this article
Grissett, L., Ali, A., Coble, AM. et al. Survey of Sensitivity to Fatty Acid-Amino Acid Conjugates in the Solanaceae. J Chem Ecol 46, 330–343 (2020). https://doi.org/10.1007/s10886-020-01152-y
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10886-020-01152-y