Feeding of large pine weevil on Scots pine stem triggers localised bark and systemic shoot emission of volatile organic compounds

Environmental and Experimental Botany

Volumn 71, Issue 3, 2011, Pages 390-398

  Heijari, Juha ^a,b   Blande, James D ^a   Holopainen, Jarmo K ^a  

^a UNIVERSITY OF EASTERN FINLAND   (Finland)

^b Kotka Maritime Research Centre   (Finland)

Author keywords

Induced defence; ISR; Monoterpenes; Needle; Photosynthesis; Terpenoids; VOC

Indexed keywords

AEROSOL FORMATION; BARK; BEETLE; BIOGENIC EMISSION; CONIFEROUS TREE; FOLIAGE; PEST DAMAGE; PHOTOSYNTHESIS; SHOOT; STEM; TERPENE; VOLATILE ORGANIC COMPOUND;

CONIFEROPHYTA; HEXAPODA; HYLOBIUS ABIETIS; PINUS SYLVESTRIS;

EID: 79952708734     PISSN: 00988472     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.envexpbot.2011.02.008     Document Type: Article

References (66)

1. Arimura G., Huber D.P.W., Bohlmann J. Forest tent caterpillars (Malacosoma disstria) induce local and systemic diurnal emissions of terpenoid volatiles in hybrid poplar (Populus trichocarpa×deltoides): cDNA cloning, functional characterization, and patterns of gene expression of (2)-germacrene D synthase, PtdTPS1. Plant J. 2004, 37:603-616.
2. Atkinson R., Arey J. Gas-phase tropospheric chemistry of biogenic volatile organic compounds. A review. Atmos. Environ. 2003, 37:S197-S219.
3. Baldwin I.T., Halitschke R. Volatile signaling in plant-plant interactions: "Talking trees" in the genomics era. Science. 2006, 311:812-815.
4. Blande J.D., Turunen K., Holopainen J.K. Pine weevil feeding on Norway spruce bark has a stronger impact on needle VOC emissions than enhanced ultraviolet-B radiation. Environ. Pollut. 2009, 157:174-180.
5. Bonello P., Gordon T.R., Storer A.J. Systemic induced resistance in Monterey pine. Forest Pathol. 2001, 31:99-106.
6. Bonello P., Gordon T.R., Herms D.A., Wood D.L., Erbilgin N. Nature and ecological implications of pathogen-induced systemic resistance in conifers: A novel hypothesis. Physiol. Mol. Plant Pathol. 2006, 68:95-104.
7. Bonn B., Moortgat G.K. Sesquiterpene ozonolysis: origin of atmospheric new particle formation from biogenic hydrocarbons. Geophys. Res. Lett. 2003, 30:1585. 10.1029/2003GL017000.
8. Boy M., Karl T., Turnipseed A., Mauldin R.L., Kosciuch E., Greenberg J., Rathbone J., Smith J., Held A., Barsanti K., Wehner B., Bauer S., Wiedensohler A., Bonn B., Kulmala M., Guenther A. New particle formation in the front range of the Colorado rocky mountains. Atmos. Chem. Phys. 2008, 8:1577-1590.
9. Danielsson M., Kännaste A., Lindström A., Hellqvist C., Stattin E., Långström B., Borg-Karlson A.K. Mini-seedlings of Picea abies are less attacked by Hylobius abietis than conventional ones: is plant chemistry the explanation?. Scand. J. For. Res. 2008, 23:299-306.
10. Dillon A.B., Moore C.P., Downes M.J., Griffin C.T. Evict or infect? Managing populations of the large pine weevil, Hylobius abietis, using a bottom-up and top-down approach. For. Ecol. Manage. 2008, 255:26342642.
11. Fäldt J., Martin D., Miller B., Rawat S., Bohlmann J. Traumatic resin defense in Norway spruce (Picea abies): methyl jasmonate-induced terpene synthase gene expression, and cDNA cloning and functional characterization of (δ)-3-carene synthase. Plant Mol. Biol. 2003, 51:119-133.
12. Flower-Ellis J.K.G., Olsson L. Estimation of volume, total and projected area of Scots pine needles from their regression on length. Stud. For. Suecica 1993, 190:1-19.
13. Franceschi V.R., Krekling T., Christiansen E. Application of methyl jasmonate on Picea abies (Pinaceae) stems induces defense-related responses in phloem and xylem. Am. J. Bot. 2002, 89:578-586.
14. Frost C.J., Appel M., Carlson J.E., De Moraes C.M., Mescher M.C., Schultz J.C. Within-plant signalling via volatiles overcomes vascular constraints on systemic signalling and primes responses against herbivores. Ecol. Lett. 2007, 10:490-498.
15. Frost C.J., Mescher M.C., Dervinis C., Davis J.M., Carlson J.E., De Moraes C.M. Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytologist 2008, 180:722-733.
16. Ghirardo A., Koch K., Taipale R., Zimmer I., Schnitzler J.P., Rinne J. Determination of de novo and pool emissions of terpenes from four common boreal/alpine trees by 13CO(2) labelling and PTR-MS analysis. Plant Cell Environ. 2010, 33:781-792.
17. Gershenzon J. Plant volatiles carry both public and private messages. Proc. Natl. Acad. Sci. USA. 2007, 104:5257-5258.
18. Gershenzon J., Croteau R. Terpenoids. Herbivores, their Interactions with Secondary Plant Metabolites 1991, 165-219. Academic Press, New York. G.A. Rosenthal, M.R. Berenbaum (Eds.).
19. Guenther A., Zimmermann P.R., Harley P.C., Monson R.K., Fall R. Isoprene and monoterpene emission rate variability: model evaluations and sensitivity analyses. J. Geophys. Res. 1993, 98:12609-12617.
20. Hämet-Ahti L., Palmén A., Alanko P., Tigerstedt P.M.A. Woody Flora of Finland 1992, Yliopistopaino, Helsinki, 373p.
21. Hao L.Q., Yli-Pirilä P., Tiitta P., Romakkaniemi S., Vaattovaara P., Kajos M.K., Rinne J., Heijari J., Kortelainen A., Miettinen P., Kroll J.H., Holopainen J.K., Smith J.N., Joutsensaari J., Kulmala M., Worsnop D.R., Laaksonen A. New particle formation from the oxidation of direct emissions of pine seedlings. Atmos. Chem. Phys. 2009, 9:8121-8137.
22. Heijari J., Nerg A.M., Kainulainen P., Viiri H., Vuorinen M., Holopainen J.K. Application of methyl jasmonate reduces growth, but increases chemical defence and resistance against Hylobius abietis in Scots pine seedlings. Ent. Exp. Appl. 2005, 115:117-124.
23. Heijari J., Nerg A.M., Kainulainen P., Vuorinen M., Holopainen J.K. Long-term effects of exogenous methyl jasmonate application on Scots pine (Pinus sylvestris L.) needle chemical defence and diprionid sawfly performance. Ent. Exp. Appl. 2008, 128:162-171.
24. Helmig D., Ortega J., Guenther A., Herrick J.D., Geron C. Sesquiterpene emissions from loblolly pine and their potential contribution to biogenic aerosol formation in the Southeastern US. Atmos. Environ. 2006, 40:4150-4157.
25. Hilker M., Kobs C., Varma M., Schrank K. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J. Exp. Biol. 2002, 205:455-461.
26. Himanen S.J., Blande J.D., Klemola T., Pulkkinen J., Heijari J., Holopainen J.K. Birch (Betula spp.) leaves adsorb and re-release volatiles specific to neighbouring plants-a mechanism for associational herbivore resistance?. New Phytologist 2010, 186:722-732.
27. Holopainen J.K., Heijari J., Nerg A.-M., Vuorinen M., Kainulainen P. Potential for the use of exogenous chemical elicitors in disease and insect pest management of conifer seedling production. Open For. Sci. J. 2009, 2:17-24.
28. Janson R.W. Monoterpene emissions from Scots pine and Norwegian spruce. J. Geophys. Res. Atmos. 1993, 98:2839-2850.
29. Jimenez J.L., Canagaratna M.R., Donahue N.M., Prevot A.S.H., Zhang Q., Kroll J.H., DeCarlo P.F., Allan J.D., Coe H., Ng N.L., Aiken A.C., Docherty K.S., Ulbrich I.M., Grieshop A.P., Robinson A.L., Duplissy J., Smith J.D., Wilson K.R., Lanz V.A., Hueglin C., Sun Y.L., Tian J., Laaksonen A., Raatikainen T., Rautiainen J., Vaattovaara P., Ehn M., Kulmala M., Tomlinson J.M., Collins D.R., Cubison M.J., Dunlea E.J., Huffman J.A., Onasch T.B., Alfarra M.R., Williams P.I., Bower K., Kondo Y., Schneider J., Drewnick F., Borrmann S., Weimer S., Demerjian K., Salcedo D., Cottrell L., Griffin R., Takami A., Miyoshi T., Hatakeyama S., Shimono A., Sun J.Y., Zhang Y.M., Dzepina K., Kimmel J.R., Sueper D., Jayne J.T., Herndon S.C., Trimborn A.M., Williams L.R., Wood E.C., Middlebrook A.M., Kolb C.E., Baltensperger U., Worsnop D.R. Evolution of organic aerosols in the atmosphere. Science 2009, 326:1525-1529.
30. Joutsensaari J., Loivamäki M., Vuorinen T., Miettinen P., Nerg A.M., Holopainen J.K., Laaksonen A. Nanoparticle formation by ozonolysis of inducible plant volatiles. Atmos. Chem. Phys. 2005, 5:1489-1495.
31. Kännaste, A., 2008. Volatiles of conifer seedlings, function and resistance markers. Ph.D.: thesis. 51 pp. KTH, Stockholm, Sweden (URL: urn_nbn_se_kth_diva-4723-2__fulltext.pdf).
32. Keeling C.I., Bohlmann J. Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytologist 2006, 170:657-675.
33. Knebel L., Robison D.J., Wentworth T.R., Klepzig K.D. Resin flow responses to fertilization, wounding and fungal inoculation in loblolly pine (Pinus taeda) in North Carolina. Tree Physiol. 2008, 28:847-853.
34. Kurz W.A., Dymond C.C., Stinson G., Rampley G.J., Neilson E.T., Carroll A.L., Ebata T., Safranyik L. Mountain pine beetle and forest carbon feedback to climate change. Nature 2008, 452:987-990.
35. Luchi N., Ma R., Capretti P., Bonello P. Systemic induction of traumatic resin ducts and resin flow in Austrian pine by wounding and inoculation with Sphaeropsis sapinea and Diplodia scrobiculata. Planta 2005, 221:75-84.
36. Maldonado-Bonilla L.D., Betancourt-Jimenez M., Lozoya-Gloria E. Local and systemic gene expression of sesquiterpene phytoalexin biosynthetic enzymes in plant leaves. Eur. J. Plant Pathol. 2008, 121:439-449.
37. Manninen A.M., Pasanen P., Holopainen J.K. Comparing the VOC emissions between air-dried and heat-treated Scots pine wood. Atmos. Environ. 2002, 36:1763-1768.
38. Mäntylä E., Alessio G.A., Blande J.D., Heijari J., Holopainen J.K., Laaksonen T., Piirtola P., Klemola T. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLoS ONE 2008, 3:e2832.
39. Mentel T.F., Wildt J., Kiendler-Scharr A., Kleist E., Tillmann R., Dal Maso M., Fisseha R., Hohaus T., Spahn H., Uerlings R., Wegener R., Griffiths P.T., Dinar E., Rudich Y., Wahner A. Photochemical production of aerosols from real plant emissions. Atmos. Chem. Phys. 2009, 9:4387-4406.
40. Mercado L.M., Bellouin N., Sitch S., Boucher O., Huntingford C., Wild M., Cox P.M. Impact of changes in diffuse radiation on the global land carbon sink. Nature 2009, 458:1014-1018.
41. Mitra S., Baldwin I.T. Independently silencing two photosynthetic proteins in Nicotiana attenuata has different effects on herbivore resistance. Plant. Physiol. 2008, 148:1128-1138.
42. Moreira X., Sampedro L., Zas R. Defensive responses of Pinus pinaster seedlings to exogenous application of methyl jasmonate: concentration effect and systemic response. Environ. Exp. Bot. 2009, 67:94-100.
43. Mumm R., Hilker M. Direct and indirect chemical defence of pine against folivorous insects. Trends Plant Sci. 2006, 11:351-358.
44. Nicole M.C., Zeneli G., Lavallee R., Rioux D., Bauce E., Morency M.J., Fenning I.M., Seguin A. White pine weevil (Pissodes strobi) biological performance is unaffected by the jasmonic acid or wound-induced defense response in Norway spruce (Picea abies). Tree Physiol. 2006, 26:1377-1389.
45. Noe S.M., Copolovici L., Niinemets U., Vaino E. Foliar limonene uptake scales positively with leaf lipid content: "non-emitting" species absorb and release monoterpenes. Plant Biol. 2008, 10:129-137.
46. Nordlander G. Limonene inhibits attraction to α-pinene in pine weevil Hylobius abietis and H. pinastri. J. Chem. Ecol. 1990, 16:1307-1320.
47. Örlander G., Nilsson U. Effect of reforestation methods on pine weevil (Hylobius abietis) damage and seedling survival. Scand. J. For. Res. 1999, 14:341-354.
48. Petersson M., Nordlander G., Orlander G. Why vegetation increases pine weevil damage: bridge or shelter?. For. Ecol. Manage. 2006, 225:368-377.
49. Pinto D.M., Tiiva P., Miettinen P., Joutsensaari J., Kokkola H., Nerg A.M., Laaksonen A., Holopainen J.K. The effects of increasing atmospheric ozone on biogenic monoterpene profiles and the formation of secondary aerosols. Atmos. Environ. 2007, 41:4877-4887.
50. Rasmann S., Turlings T.C.J. Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol. Lett. 2007, 10:926-936.
51. Rodriguez-Saona C.R., Rodriguez-Saona L.E., Frost C.J. Herbivore-induced volatiles in the perennial shrub, Vaccinium corymbosum, and their role in inter-branch signalling. J. Chem. Ecol. 2009, 35:163-175.
52. Sallas L., Luomala E.M., Utriainen J., Kainulainen P., Holopainen J.K. Contrasting effects of elevated carbon dioxide concentration and temperature on Rubisco activity, chlorophyll fluorescence, needle ultrastructure and secondary metabolites in conifer seedlings. Tree Physiol. 2003, 23:97-108.
53. Sallas L., Vuorinen M., Kainulainen P., Holopainen J.K. Effects of planting on concentrations of terpenes, resin acids and total phenolics in Pinus sylvestris seedlings. Scand. J. For. Res. 1999, 14:218-226.
54. Schaub A., Blande J.D., Graus M., Oksanen E., Holopainen J.K., Hansel A. Real-time monitoring of herbivore induced volatile emissions in the field. Physiol. Plant. 2010, 138:123-133.
55. Schröder R., Forstreuter M., Hilker M. A plant notices insect egg deposition and changes its rate of photosynthesis. Plant Physiol. 2005, 138:470-477.
56. Schwachtje J., Minchin P.E.H., Jahnke S., van Dongen J.T., Schittko U., Baldwin I.T. SNF1-related kinases allow plants to tolerate herbivory by allocating carbon to roots. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:12935-12940.
57. Spracklen D.V., Bonn B., Carslaw K.S. Boreal forests, aerosols and the impacts on clouds and climate. Phil. Transact. Royal Soc. A: Math. Phys. Eng. Sci. 2008, 366:4613-4626.
58. Staudt M., Lhoutellier L. Volatile organic compound emission from holm oak infested by gypsy moth larvae: evidence for distinct responses in damaged and undamaged leaves. Tree Physiol. 2007, 27:1433-1440.
59. Trapp S., Croteau R. Defensive resin biosynthesis in conifers. Ann. Rev. Plant Phys. Plant Mol. Biol. 2001, 52:689-724.
60. VanReken T.M., Greenberg J.P., Harley P.C., Guenther A.B., Smith J.N. Direct measurement of particle formation and growth from the oxidation of biogenic emissions. Atmos. Chem. Phys. 2006, 6:4403-4413.
61. Virtanen A., Joutsensaari J., Koop T., Kannosto J., Yli-Pirilä P., Leskinen J., Mäkelä J.M., Holopainen J.K., Pöschl U., Kulmala M., Worsnop D.R., Laaksonen A. An amorphous solid state of biogenic secondary organic aerosol particles. Nature 2010, 467:824-827.
62. Wallin K.F., Raffa K.F. Altered constitutive and inducible phloem monoterpenes following natural defoliation of jack pine: implications to host mediated interguild interactions and plant defense theories. J. Chem. Ecol. 1999, 25:861-880.
63. Wang D., Eyles A., Mandich D., Bonello P. Systemic aspects of host-pathogen interactions in Austrian pine (Pinus nigra): a proteomics approach. Physiol. Molec. Plant Pathol. 2006, 68:149-157.
64. Yuan J.S., Himanen S.J., Holopainen J.K., Chen F., Stewart C.N. Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol. Evol. 2009, 24:323-331.
65. Zagatti P., Lemperiere G., Malosse C. Monoterpenes emitted by the large pine weevil, Hylobius abietis (L.) feeding on Scots pine, Pinus sylvestris L. Physiol. Entomol. 1997, 22:394-400.
66. Zeneli G., Krokene P., Christiansen E., Krekling T., Gershenzon J. Methyl jasmonate treatment of mature Norway spruce (Picea abies) trees increases the accumulation of terpenoid resin components and protects against infection by Ceratocystis polonica, a bark beetle-associated fungus. Tree Physiol. 2006, 26:977-988.