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Specificity of Herbivore-Induced Hormonal Signaling and Defensive Traits in Five Closely Related Milkweeds (Asclepias spp.)

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Abstract

Despite the recognition that phytohormonal signaling mediates induced responses to herbivory, we still have little understanding of how such signaling varies among closely related species and may generate herbivore-specific induced responses. We studied closely related milkweeds (Asclepias) to link: 1) plant damage by two specialist chewing herbivores (milkweed leaf beetles Labidomera clivicolis and monarch caterpillars Danaus plexippus); 2) production of the phytohormones jasmonic acid (JA), salicylic acid (SA), and abscisic acid (ABA); 3) induction of defensive cardenolides and latex; and 4) impacts on Danaus caterpillars. We first show that A. syriaca exhibits induced resistance following monarch herbivory (i.e., reduced monarch growth on previously damaged plants), while the defensively dissimilar A. tuberosa does not. We next worked with a broader group of five Asclepias, including these two species, that are highly divergent in defensive traits yet from the same clade. Three of the five species showed herbivore-induced changes in cardenolides, while induced latex was found in four species. Among the phytohormones, JA and ABA showed specific responses (although they generally increased) to insect species and among the plant species. In contrast, SA responses were consistent among plant and herbivore species, showing a decline following herbivore attack. Jasmonic acid showed a positive quantitative relationship only with latex, and this was strongest in plants damaged by D. plexippus. Although phytohormones showed qualitative tradeoffs (i.e., treatments that enhanced JA reduced SA), the few significant individual plant-level correlations among hormones were positive, and these were strongest between JA and ABA in monarch damaged plants. We conclude that: 1) latex exudation is positively associated with endogenous JA levels, even among low-latex species; 2) correlations among milkweed hormones are generally positive, although herbivore damage induces a divergence (tradeoff) between JA and SA; 3) induction of cardenolides and latex are not necessarily physiologically linked; and 4) even very closely related species show highly divergent induction, with some species showing strong defenses, hormonally-mediated induction, and impacts on herbivores, while other milkweed species apparently use alternative strategies to cope with insect attack.

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References

  • Agrawal AA (2001) Phenotypic plasticity in the interactions and evolution of species. Science 294:321–326

    Article  CAS  PubMed  Google Scholar 

  • Agrawal AA (2005) Natural selection on common milkweed (Asclepias syriaca) by a community of specialized insect herbivores. Evol Ecol Res 7:651–667

    Google Scholar 

  • Agrawal AA (2011) Current trends in the evolutionary ecology of plant defence. Funct Ecol 25:420–432

    Article  Google Scholar 

  • Agrawal AA, Fishbein M (2006) Plant defense syndromes. Ecology 87:S132–S149

    Article  PubMed  Google Scholar 

  • Agrawal AA, Fishbein M (2008) Phylogenetic escalation and decline of plant defense strategies. Proc Natl Acad Sci U S A 105:10057–10060

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Agrawal AA, Konno K (2009) Latex: a model for understanding mechanisms, ecology, and evolution of plant defense against herbivory. Annu Rev Ecol Evol Syst 40:311–331

    Google Scholar 

  • Agrawal AA, Fishbein M, Halitschke R, Hastings AP, Rabosky DL, Rasmann S (2009) Evidence for adaptive radiation from a phylogenetic study of plant defenses. Proc Natl Acad Sci U S A 106:18067–18072

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Agrawal AA, Kearney EE, Hastings AP, Ramsey TE (2012a) Attenuation of the jasmonate burst, plant defensive traits, and resistance to specialist monarch caterpillars on shaded common milkweed (Asclepias syriaca). J Chem Ecol 38:893–901

    Article  CAS  PubMed  Google Scholar 

  • Agrawal AA, Petschenka G, Bingham RA, Weber MG, Rasmann S (2012b) Toxic cardenolides: chemical ecology and coevolution of specialized plant-herbivore interactions. New Phytol 194:28–45

    Article  CAS  PubMed  Google Scholar 

  • Agrawal AA, Ali JG, Rasmann S, Fishbein M (2014) Macroevolutionary trends in the defense of milkweeds against monarchs: latex, cardenolides, and tolerance of herbivory. In: Oberhauser K, Altizer S, Nail K (eds) Monarchs in a changing world: biology and conservation of an iconic insect. Cornell University Press (in press)

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17:293–302

    Article  CAS  PubMed  Google Scholar 

  • Ali JG, Agrawal AA (2014) Asymmetry of plant-mediated interactions between insects from two feeding guilds. Funct Ecol. doi:10.1111/1365-2435.12271

  • Avanci NC, Luche DD, Goldman GH, Goldman MHS (2010) Jasmonates are phytohormones with multiple functions, including plant defense and reproduction. Genet Mol Res 9:484–505

    Article  CAS  PubMed  Google Scholar 

  • Bingham RA, Agrawal AA (2010) Ecological genetics of herbivore-specific induced defenses in common milkweed. J Ecol 98:1014–1022

    Article  Google Scholar 

  • Broekaert W, Lee HI, Kush A, Chua NH, Raikhel N (1990) Wound-induced accumulation of messenger-RNA containing a hevein sequence in laticifers of rubber tree (Hevea brasiliensis). Proc Natl Acad Sci U S A 87:7633–7637

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cipollini D (2004) Stretching the limits of plasticity: can a plant defend against both competitors and herbivores? Ecology 85:28–37

    Article  Google Scholar 

  • De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH (1998) Herbivore-infested plants selectively attract parasitoids. Nature 393:570–573

    Article  Google Scholar 

  • Erb M, Flors V, Karlen D, de Lange E, Planchamp C, D’Alessandro M, Turlings TCJ, Ton J (2009) Signal signature of aboveground-induced resistance upon belowground herbivory in maize. Plant J 59:292–302

    Article  CAS  PubMed  Google Scholar 

  • Erb M, Meldau S, Howe GA (2012) Role of phytohormones in insect-specific plant reactions. Trends Plant Sci 17:250–259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fishbein M, Chuba D, Ellison C, Mason-Gamer RJ, Lynch SP (2011) Phylogenetic relationships of asclepias (Apocynaceae) inferred from non-coding chloroplast DNA sequences. Syst Bot 36:1008–1023

    Article  Google Scholar 

  • Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807

    Article  CAS  PubMed  Google Scholar 

  • Haribal M, Renwick JAA (1998) Identification and distribution of oviposition stimulants for monarch butterflies in hosts and nonhosts. J Chem Ecol 24:891–904

    Article  CAS  Google Scholar 

  • Heil M, Greiner S, Meimberg H, Kruger R, Noyer JL, Heubl G, Linsenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

    Article  CAS  PubMed  Google Scholar 

  • Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC, Pieterse CMJ (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Lackman P, Gonzalez-Guzman M, Tilleman S, Carqueijeiro I, Perez AC, Moses T, Seo M, Kanno Y, Hakkinen ST, Van Montagu MCE and others (2011) Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci U S A 108:5891–5896

  • Leon-Reyes A, Spoel SH, De Lange ES, Abe H, Kobayashi M, Tsuda S, Millenaar FF, Welschen RAM, Ritsema T, Pieterse CMJ (2009) Ethylene modulates the role of nonexpressor of pathogenesis-related genes1 in cross talk between salicylate and jasmonate signaling. Plant Physiol 149:1797–1809

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Leon-Reyes A, Du YJ, Koornneef A, Proietti S, Korbes AP, Memelink J, Pieterse CMJ, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Mol Plant Microbe Interact 23:187–197

    CAS  PubMed  Google Scholar 

  • Malcolm SB, Zalucki MP (1996) Milkweed latex and cardenolide induction may resolve the lethal plant defence paradox. Entomol Exp Appl 80:193–196

    Article  CAS  Google Scholar 

  • Malcolm SB, Cockrell BJ, Brower LP (1989) Cardenolide fingerprint of monarch butterflies reared on common milkweed, Asclepias syriaca L. J Chem Ecol 15:819–853

    Article  CAS  PubMed  Google Scholar 

  • Mooney KA, Jones P, Agrawal AA (2008) Coexisting congeners: demography, competition, and interactions with cardenolides for two milkweed-feeding aphids. Oikos 117:450–458

    Article  CAS  Google Scholar 

  • Moreno JE, Tao Y, Chory J, Ballare CL (2009) Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proc Natl Acad Sci U S A 106:4935–4940

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Mur LAJ, Kenton P, Atzorn R, Miersch O, Wasternack C (2006) The outcomes of concentration-specific interactions between salicylate and jasmonate signaling include synergy, antagonism, and oxidative stress leading to cell death. Plant Physiol 140:249–262

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Musser RO, Cipollini DF, Hum-Musser SM, Williams SA, Brown JK, Felton GW (2005) Evidence that the caterpillar salivary enzyme glucose oxidase provides herbivore offense in Solanaceous plants. Arch Insect Biochem Physiol 58:128–137

    Article  CAS  PubMed  Google Scholar 

  • Rasmann S, Agrawal AA (2009) Plant defense against herbivory: progress in identifying synergism, redundancy, and antagonism between resistance traits. Cur Opin Plant Biol 12(4):473–478

    Article  CAS  Google Scholar 

  • Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecol Lett 14:476–483

    Article  PubMed  Google Scholar 

  • Rasmann S, Johnson MD, Agrawal AA (2009) Induced responses to herbivory and jasmonate in three milkweed species. J Chem Ecol 35:1326–1334

    Article  CAS  PubMed  Google Scholar 

  • Reymond P, Farmer EE (1998) Jasmonate and salicylate as global signals for defense gene expression. Cur Opin Plant Biol 1:404–411

    Article  CAS  Google Scholar 

  • Reymond P, Weber H, Damond M, Farmer EE (2000) Differential gene expression in response to mechanical wounding and insect feeding in Arabidopsis. Plant Cell 12:707–719

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schmelz EA, Engelberth J, Alborn HT, O’Donnell P, Sammons M, Toshima H, Tumlinson JH (2003) Simultaneous analysis of phytohormones, phytotoxins, and volatile organic compounds in plants. Proc Natl Acad Sci U S A 100:10552–10557

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schuman MC, Heinzel N, Gaquerel E, Svatos A, Baldwin IT (2009) Polymorphism in jasmonate signaling partially accounts for the variety of volatiles produced by Nicotiana attenuata plants in a native population. New Phytol 183:1134–1148

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS, Bostock RM (2004) Interactions between abscisic-acid-mediated responses and plant resistance to pathogens and insects. Ecology 85:48–58

    Article  Google Scholar 

  • Thaler JS, Karban R (1997) A phylogenetic reconstruction of constitutive and induced resistance in Gossypium. Am Nat 149:1139–1146

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS, Farag MA, Pare PW, Dicke M (2002) Jasmonate-deficient plants have reduced direct and indirect defences against herbivores. Ecol Lett 5:764–774

    Article  Google Scholar 

  • Thaler JS, Agrawal AA, Halitschke R (2010) Salicylate-mediated interactions between pathogens and herbivores. Ecology 91:1075–1082

    Article  PubMed  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  CAS  PubMed  Google Scholar 

  • Traw MB, Bergelson J (2003) Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. Plant Physiol 133:1367–1375

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Van Zandt PA, Agrawal AA (2004a) Community-wide impacts of herbivore-induced plant responses in milkweed (Asclepias syriaca). Ecology 85:2616–2629

    Article  Google Scholar 

  • Van Zandt PA, Agrawal AA (2004b) Specificity of induced plant responses to specialist herbivores of the common milkweed, Asclepias syriaca. Oikos 104:401–409

    Article  Google Scholar 

  • Vannette RL, Hunter MD (2011) Genetic variation in expression of defense phenotype may mediate evolutionary adaptation of Asclepias syriaca to elevated CO2. Glob Chang Biol 17:1277–1288

    Article  Google Scholar 

  • Viswanathan DV, Narwani AJT, Thaler JS (2005) Specificity in induced plant responses shapes patterns of herbivore occurrence on Solanum dulcamara. Ecology 86:886–896

    Article  Google Scholar 

  • von Dahl CC, Baldwin IT (2007) Deciphering the role of ethylene in plant-herbivore interactions. J Plant Growth Regul 26:201–209

    Article  CAS  Google Scholar 

  • Warashina T, Noro T (2009) 8,14-Secopregnane glycosides from the aerial parts of Asclepias tuberosa. Phytochemistry 70:1294–1304

    Article  CAS  PubMed  Google Scholar 

  • Woodson RE (1954) The North American species of Asclepias L. Ann Miss Bot Garden 41:1–211

    Article  Google Scholar 

  • Zalucki MP, Malcolm SB (1999) Plant latex and first-instar monarch larval growth and survival on three North American milkweed species. J Chem Ecol 25:1827–1842

    Article  CAS  Google Scholar 

  • Zalucki MP, Brower LP, Alonso A (2001) Detrimental effects of latex and cardiac glycosides on survival and growth of first-instar monarch butterfly larvae Danaus plexippus feeding on the sandhill milkweed Asclepias humistrata. Ecological Entomol 26:212–224

    Article  Google Scholar 

  • Zehnder CB, Hunter MD (2007) Interspecific variation within the genus Asclepias in response to herbivory by a phloem-feeding insect herbivore. J Chem Ecol 33:2044–2053

    Article  CAS  PubMed  Google Scholar 

  • Zehnder CB, Hunter MD (2008) Effects of nitrogen deposition on the interaction between an aphid and its host plant. Ecological Entomol 33:24–30

    Article  Google Scholar 

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Acknowledgements

This study was improved by discussions and input from Jared Ali, Rayko Halitschke, Monica Kersch-Becker, Georg Petschenka, Jennifer Thaler, Tobias Züst, and the Phytophagy Lab at Cornell University. We thank Mark Fishbein for help with the phylogeny of Asclepias and Marc Johnson and Peter Van Zandt for collecting A. obovata seeds. We thank T. Ramsey for help conducting the experiments, E. Kearney and C. Creneti for sample preparation, and J. Kerr for help with cardenolide analysis. Our research and lab (www.herbivory.com/) is currently supported by NSF-DEB 1118783 and the Templeton Foundation.

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  1. Department of Ecology and Evolutionary Biology, and Department of Entomology, Cornell University, Ithaca, NY, USA

    Anurag A. Agrawal, Amy P. Hastings, Eamonn T. Patrick & Anna C. Knight

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  1. Anurag A. Agrawal
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Correspondence to Anurag A. Agrawal.

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Agrawal, A.A., Hastings, A.P., Patrick, E.T. et al. Specificity of Herbivore-Induced Hormonal Signaling and Defensive Traits in Five Closely Related Milkweeds (Asclepias spp.). J Chem Ecol 40, 717–729 (2014). https://doi.org/10.1007/s10886-014-0449-6

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