Advertisement

Arthropod-Plant Interactions

, Volume 3, Issue 2, pp 99–104 | Cite as

Volatile communication among sagebrush branches affects herbivory: timing of active cues

  • Kaori Shiojiri
  • Richard Karban
  • Satomi Ishizaki
Original Paper

Abstract

Airborne communication can affect systemic induced resistance to herbivory on neighboring branches and individual plants. Sagebrush is the best known example of this phenomenon although the mechanisms of this communication system remain unidentified. We do not know the timing of emission or the chemical nature of the active cue. We investigated the timing of this phenomenon by using plastic bags to prevent propagation of volatile compounds and experimentally manipulated the timing of removal of these bags. We found that blocking the volatiles prevented systemic induced resistance. Experimentally allowing clipped branches to release cues for up to 3 days after clipping caused a reduction in damage in neighboring branches on the clipped plants. This indicates that active cues are released from the time we clipped for the next 3 days or that cues released immediately remained active over this time period. As we continue to evaluate potential chemicals as active cues in plant communication, this prolonged effectiveness may provide an important screen against which to evaluate any putative signals.

Keywords

Eavesdropping Induced resistance Plant behavior Plant–plant communication Signal 

Notes

Acknowledgements

This study was conducted in Tahoe National Forest adjacent to UC Sagehen Creek Reserve and we thank Jeff Brown for facilitating our work. We thank Gen-ichirou Arimura for comments, Professor Masashi Ohara for helping with all aspects of this project and Ms. Shiojiri for logistical support. We were funded by grants from JSPS and NSF.

References

  1. Ballare CL (1999) Keeping up with the neighbors: phytochrome sensing and other signalling mechanisms. Trends Plant Sci 4:97–102. doi: 10.1016/S1360-1385(99)01383-7 PubMedCrossRefGoogle Scholar
  2. Cook CW, Stoddart LA (1960) Physiological responses of big sagebrush to different types of herbage removal. J Range Manage 13:14–16. doi: 10.2307/3894891 CrossRefGoogle Scholar
  3. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785. doi: 10.1073/pnas.0308037100 PubMedCrossRefGoogle Scholar
  4. Farag MA, Pare PW (2002) C6-Green leaf volatiles trigger local and systemic VOC emissions in tomato. Phytochemistry 61:545–554. doi: 10.1016/S0031-9422(02)00240-6 PubMedCrossRefGoogle Scholar
  5. Farmer EF, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induced synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716. doi: 10.1073/pnas.87.19.7713 PubMedCrossRefGoogle Scholar
  6. Frost CJ, Appel HM, Carlson JE, De Moraes CM, Mescher MC, Schultz JC (2007) Within-plant signaling via volatiles overcomes vascular constraints on systemic signaling and primes responses against herbivores. Ecol Lett 10:490–498. doi: 10.1111/j.1461-0248.2007.01043.x PubMedCrossRefGoogle Scholar
  7. Heil M, Silva Bueno JC (2007) Within-plant signaling by volatiles leads to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472. doi: 10.1073/pnas.0610266104 PubMedCrossRefGoogle Scholar
  8. Karban R (2001) Communication between sagebrush and wild tobacco in the field. Biochem Syst Ecol 29:995–1006. doi: 10.1016/S0305-1978(01)00046-1 CrossRefGoogle Scholar
  9. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71. doi: 10.1007/PL00008892 CrossRefGoogle Scholar
  10. Karban R, Huntzinger M, McCall AC (2004) The specificity of eavesdropping on sagebrush by other plants. Ecology 85:1846–1852. doi: 10.1890/03-0593 CrossRefGoogle Scholar
  11. Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930. doi: 10.1890/0012-9658(2006)87[922:DRISVA]2.0.CO;2 PubMedCrossRefGoogle Scholar
  12. Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292. doi: 10.1007/s00442-006-0365-8 PubMedCrossRefGoogle Scholar
  13. Knudsen JT, Gershenzon J (2006) The chemical diversity of floral scent. In: Dudareva N, Pichersky E (eds) Biology of floral scent. CRC Press, Boca Raton FL, pp 27–52Google Scholar
  14. Loughrin JH, Manukian A, Heath RR, Turlings TCJ, Tumlinson JH (1994) Diurnal cycle of emission of induced volatile terpenoids by herbivore-injured cotton plants. Proc Natl Acad Sci USA 91:11836–11840. doi: 10.1073/pnas.91.25.11836 PubMedCrossRefGoogle Scholar
  15. Orians C (2005) Herbivores, vascular pathways, and systemic induction: facts and artifacts. J Chem Ecol 31:2231–2242. doi: 10.1007/s10886-005-7099-7 PubMedCrossRefGoogle Scholar
  16. Pare PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–331. doi: 10.1104/pp.121.2.325 PubMedCrossRefGoogle Scholar
  17. Pickford GD (1932) The influence of continued heavy grazing and of promiscuous burning on spring-fall ranges in Utah. Ecology 13:159–171. doi: 10.2307/1931066 CrossRefGoogle Scholar
  18. Pierik R, Whitelam GC, Voesnek LACJ, de Kroon H, Visser EJW (2004) Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant–plant signalling. Plant J 38:310–319. doi: 10.1111/j.1365-313X.2004.02044.x PubMedCrossRefGoogle Scholar
  19. Preston CA, Laue G, Baldwin IT (2004) Plant-plant signaling: application of trans- or cis-methyl jasmonate equivalent to sagebrush releases does not elicit direct defenses in native tobacco. J Chem Ecol 30:2193–2214. doi: 10.1023/B:JOEC.0000048783.64264.2a PubMedCrossRefGoogle Scholar
  20. Rodriguez-Saona CR, Rodriguez-Soana LE, Frost CJ (2009) Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signaling. J Chem Ecol 35:163–175. doi: 10.1007/s10886-008-9579-z PubMedCrossRefGoogle Scholar
  21. Schmitt J, Dudley SA, Pigliucci M (1999) Manipulative approaches to testing adaptive plasticity: phytochrome-mediated shade-avoidance responses in plants. Am Nat 154:S43–S54. doi: 10.1086/303282 CrossRefGoogle Scholar
  22. Shiojiri K, Karban R (2006) Plant age, communication and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 149:214–220. doi: 10.1007/s00442-006-0441-0 PubMedCrossRefGoogle Scholar
  23. Shiojiri K, Karban R (2008) Vascular systemic induced resistance for Artemisia cana and volatile communication for Artemisia douglasiana. Am Midl Nat 159:468–477. doi: 10.1674/0003-0031(2008)159[468:VSIRFA]2.0.CO;2 CrossRefGoogle Scholar
  24. Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591. doi: 10.1038/35036500 PubMedCrossRefGoogle Scholar
  25. Ton J, D’Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26. doi: 10.1111/j.1365-313X.2006.02935.x PubMedCrossRefGoogle Scholar
  26. Tscharntke T, Thiessen S, Dolch R, Boland W (2001) Herbivory, induced resistance, and interplant signal transfer in Alnus glutinosa. Biochem Syst Ecol 29:1025–1047. doi: 10.1016/S0305-1978(01)00048-5 CrossRefGoogle Scholar
  27. Turlings TCJ, Wackers F (2004) Recruitment of predators and parasitoids by herbivore-injured plants. In: Carde RT, Millar JG (eds) Advances in insect chemical ecology. Cambridge Press, New York, pp 21–75Google Scholar
  28. Turlings TCJ, Loughrin JH, McCall PJ, Rose USR, Lewis WJ, Tumlinson JH (1995) How caterpillar-damaged plants protect themselves by attracting parasitic wasps. Proc Natl Acad Sci USA 92:4169–4174. doi: 10.1073/pnas.92.10.4169 PubMedCrossRefGoogle Scholar
  29. Turlings TCJ, Lengwiler UB, Bernasconi ML, Wechsler D (1998) Timing of induced volatile emissions in maize seedlings. Planta 207:146–152. doi: 10.1007/s004250050466 CrossRefGoogle Scholar
  30. Wiens JA, Cates RG, Rotenberry JT, Cobb N, Van Horne B, Redak RA (1991) Arthropod dynamics on sagebrush (Artemisia tridentata): effects of plant chemistry and avian predation. Ecol Monogr 61:299–321. doi: 10.2307/2937110 CrossRefGoogle Scholar
  31. Young JA, Evans RA, Major J (1988) Sagebrush steppe. In Barbour MG, Major J (eds) Terrestrial vegetation of California, 2nd edn. California Native Plant Society Special Publication 9, pp 763–769Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Kaori Shiojiri
    • 1
  • Richard Karban
    • 2
  • Satomi Ishizaki
    • 3
  1. 1.Center for Ecological ResearchKyoto UniversityOtsuJapan
  2. 2.Department of EntomologyUniversity of CaliforniaDavisUSA
  3. 3.Graduate School of Environmental ScienceHokkaido UniversitySapporoJapan

Personalised recommendations