1932

Abstract

My research focuses on elucidating the chemical communication systems linking plants, herbivores, and natural enemies. My interests in integrating chemistry and agriculture led to my graduate studies in the emerging field of chemical ecology. My thesis research resulted in the identification, synthesis, and application of boll weevil sex pheromones. My research group subsequently developed chemical lures for more than 20 species of pest insects. I then shifted my focus to some of the first studies of the chemical signals produced by plants being attacked by herbivores. When insects feed, elicitors in the insects’ oral secretions, such as volicitin, a fatty acid–amino acid conjugate elicitor, stimulate plants to release volatile organic compounds. Parasitoid wasps learn to associate these species-specific volatiles with their herbivore hosts. These volatiles also prime nearby plants to activate a faster and higher defense response upon attack. Throughout my career, I have collaborated with scientists from diverse disciplines to tackle fundamental questions in chemical ecology and create innovative solutions for insect management. Our collaborative research has fundamentally changed and improved our understanding of the ongoing coevolution of plants, their herbivores, and the natural enemies that attack those herbivores.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ento-021622-111028
2023-01-23
2024-05-10
Loading full text...

Full text loading...

/deliver/fulltext/ento/68/1/annurev-ento-021622-111028.html?itemId=/content/journals/10.1146/annurev-ento-021622-111028&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Alborn HT, Hansen TV, Jones TH, Bennett DC, Tumlinson JH et al. 2007. Disulfooxy fatty acids from the American bird grasshopper Schistocerca americana, elicitors of plant volatiles. PNAS 104:3212976–81
    [Google Scholar]
  2. 2.
    Alborn HT, Turlings TCJ, Jones TH, Stenhagen G, Loughrin JH et al. 1997. An elicitor of plant volatiles from beet armyworm oral secretion. Science 276:5314945–49
    [Google Scholar]
  3. 3.
    Böröczky K, Crook DJ, Jones TH, Kenny JC, Zylstra KE et al. 2009. Monoalkenes as contact sex pheromone components of the woodwasp Sirex noctilio. J. Chem. Ecol. 35:101202–11
    [Google Scholar]
  4. 4.
    Böröczky K, Zylstra KE, McCartney NB, Mastro VC, Tumlinson JH. 2012. Volatile profile differences and the associated Sirex noctilio activity in two host tree species in the northeastern United States. J. Chem. Ecol. 38:2213–21
    [Google Scholar]
  5. 5.
    Bosak EJ, Seidl-Adams IH, Zhu J, Tumlinson JH. 2013. Maize developmental stage affects indirect and direct defense expression. Environ. Entomol. 42:61309–21
    [Google Scholar]
  6. 6.
    Butenandt A, Beckmann R, Stamm D, Hecker E. 1959. Über den Sexuallockstoff des Seidenspinners Bombyx mori. Reindarstellung und Konstitutionsermittlung. Z. Naturforsch. 14b:283–84
    [Google Scholar]
  7. 7.
    Carson R. 1962. Silent Spring New York: Houghton Mifflin Co400 pp.
  8. 8.
    Cooperband MF, Böröczky K, Hartness A, Jones TH, Zylstra KE et al. 2012. Male-produced pheromone in the European woodwasp, Sirex noctilio. J. Chem. Ecol. 38:152–62
    [Google Scholar]
  9. 9.
    Cross WH, Mitchell HC. 1966. Mating behavior of the female boll weevil. J. Econ. Entomol. 59:61503–7
    [Google Scholar]
  10. 10.
    De Moraes CM, Lewis WJ, Paré PW, Alborn HT, Tumlinson JH. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:6685570–73
    [Google Scholar]
  11. 11.
    Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH. 2004. Airborne signals prime plants against insect herbivore attack. PNAS 101:61781–85
    [Google Scholar]
  12. 12.
    Engelberth J, Seidl-Adams I, Schultz JC, Tumlinson JH. 2007. Insect elicitors and exposure to green leafy volatiles differentially upregulate major octadecanoids and transcripts of 12-oxo phytodienoic acid reductases in Zea mays. Mol. Plant-Microbe Interact. 20:6707–16
    [Google Scholar]
  13. 13.
    Gueldner RC, Tumlinson JH, Hardee DD, Thompson AC, Hedin PA, Minyard JP. 1971. Identification and synthesis of the four compounds comprising the boll weevil sex attractant. J. Org. Chem. 36:182616–21
    [Google Scholar]
  14. 14.
    Jones AC, Cofer TM, Engelberth J, Tumlinson JH. 2022. Herbivorous caterpillars and the green leaf volatile (GLV) quandary. J. Chem. Ecol. 48:337–45
    [Google Scholar]
  15. 15.
    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. 48:2419–25
    [Google Scholar]
  16. 16.
    Lewis WJ, Tumlinson JH. 1988. Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331:6153257–59
    [Google Scholar]
  17. 17.
    Loughrin JH, Manukian A, Heath RR, Tumlinson JH. 1995. Volatiles emitted by different cotton varieties damaged by feeding beet armyworm larvae. J. Chem. Ecol. 21:81217–27
    [Google Scholar]
  18. 18.
    Loughrin JH, Manukian A, Heath RR, Turlings TC, Tumlinson JH. 1994. Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plant. PNAS 91:2511836–40
    [Google Scholar]
  19. 19.
    Matsui K, Sugimoto K, Mano J, Ozawa R, Takabayashi J. 2012. Differential metabolisms of green leaf volatiles in injured and intact parts of a wounded leaf meet distinct ecophysiological requirements. PLOS ONE 7:4e36433
    [Google Scholar]
  20. 20.
    Muli E, Patch H, Frazier M, Frazier J, Torto B et al. 2014. Evaluation of the distribution and impacts of parasites, pathogens, and pesticides on honey bee (Apis mellifera) populations in East Africa. PLOS ONE 9:4e94459
    [Google Scholar]
  21. 21.
    Paré PW, Tumlinson JH. 1997. De novo biosynthesis of volatiles induced by insect herbivory in cotton plants. Plant Physiol 114:41161–67
    [Google Scholar]
  22. 22.
    Paudel Timilsena B 2021. Reducing crop loss to herbivore pests: from modeling risk of herbivore invasion and establishment to harnessing plant defenses via priming PhD Thesis Penn State194 pp.
  23. 23.
    Richter A, Seidl-Adams I, Köllner TG, Schaff C, Tumlinson JH, Degenhardt J. 2015. A small, differentially regulated family of farnesyl diphosphate synthases in maize (Zea mays) provides farnesyl diphosphate for the biosynthesis of herbivore-induced sesquiterpenes. Planta 241:61351–61
    [Google Scholar]
  24. 24.
    Rose USR, Manukian A, Heath RR, Tumlinson JH. 1996. Volatile semiochemicals released from undamaged cotton leaves (a systemic response of living plants to caterpillar damage). Plant Physiol 111:2487–95
    [Google Scholar]
  25. 25.
    Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J et al. 2006. Fragments of ATP synthase mediate plant perception of insect attack. PNAS 103:238894–99
    [Google Scholar]
  26. 26.
    Seidl-Adams I, Richter A, Boomer KB, Yoshinaga N, Degenhardt J, Tumlinson JH. 2015. Emission of herbivore elicitor-induced sesquiterpenes is regulated by stomatal aperture in maize (Zea mays) seedlings. Plant Cell Environ. 38:123–34
    [Google Scholar]
  27. 27.
    Silverstein RM, Rodin JO, Wood DL. 1966. Sex attractants in frass produced by male Ips confusus in Ponderosa pine. Science 154:3748509–10
    [Google Scholar]
  28. 28.
    Torto B, Boucias DG, Arbogast RT, Tumlinson JH, Teal PEA. 2007. Multitrophic interaction facilitates parasite–host relationship between an invasive beetle and the honey bee. PNAS 104:208374–78
    [Google Scholar]
  29. 29.
    Tumlinson JH, Hardee DD, Gueldner RC, Thompson AC, Hedin PA, Minyard JP. 1969. Sex pheromones produced by male boll weevil: isolation, identification, and synthesis. Science 166:39081010–12
    [Google Scholar]
  30. 30.
    Tumlinson JH, Hardee DD, Minyard JP, Thompson AC, Gast RT, Hedin PA. 1968. Boll weevil sex attractant: isolation studies. J. Econ. Entomol. 61:2470–74
    [Google Scholar]
  31. 31.
    Tumlinson JH, Klein MG, Doolittle RE, Ladd TL, Proveaux AT. 1977. Identification of the female Japanese beetle sex pheromone: inhibition of male response by an enantiomer. Science 197:4305789–92
    [Google Scholar]
  32. 32.
    Tumlinson JH, Silverstein RM, Moser JC, Brownlee RG, Ruth JM. 1971. Identification of the trail pheromone of a leaf-cutting ant, Atta texana. Nature 234:5328348–49
    [Google Scholar]
  33. 33.
    Turlings TC, Tumlinson JH, Lewis WJ. 1990. Exploitation of herbivore-induced plant odors by host-seeking parasitic wasps. Science 250:49851251–53
    [Google Scholar]
  34. 34.
    Yoshinaga N, Abe H, Morita S, Yoshida T, Aboshi T et al. 2014. Plant volatile eliciting FACs in lepidopteran caterpillars, fruit flies, and crickets: a convergent evolution or phylogenetic inheritance?. Front. Physiol. 5:e121
    [Google Scholar]
  35. 35.
    Yoshinaga N, Aboshi T, Abe H, Nishida R, Alborn HT et al. 2008. Active role of fatty acid amino acid conjugates in nitrogen metabolism in Spodoptera litura larvae. PNAS 105:4618058–63
    [Google Scholar]
  36. 36.
    Yoshinaga N, Aboshi T, Ishikawa C, Fukui M, Shimoda M et al. 2007. Fatty acid amides, previously identified in caterpillars, found in the cricket Teleogryllus taiwanemma and fruit fly Drosophila melanogaster larvae. J. Chem. Ecol. 33:71376–81
    [Google Scholar]
  37. 37.
    Yoshinaga N, Alborn HT, Nakanishi T, Suckling DM, Nishida R et al. 2010. Fatty acid-amino acid conjugates diversification in lepidopteran caterpillars. J. Chem. Ecol. 36:3319–25
    [Google Scholar]
  38. 38.
    Yoshinaga N, Ishikawa C, Seidl-Adams I, Bosak E, Aboshi T et al. 2014. N-(18-hydroxylinolenoyl)-l-glutamine: a newly discovered analog of volicitin in Manduca sexta and its elicitor activity in plants. J. Chem. Ecol. 40:5484–90
    [Google Scholar]
/content/journals/10.1146/annurev-ento-021622-111028
Loading
/content/journals/10.1146/annurev-ento-021622-111028
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error