Abstract
Conifer-produced oleoresin is mainly composed of monoterpenoids, sesquiterpenoids, and diterpenoids that can protect conifers against herbivores and pathogens. Pinus massoniana Lamb. is an important economic species in southern China. However, the traumatic resin duct (TD) formation and terpenoid accumulation induced by adult Monochamus alternatus (Coleoptera: Cerambycidae) of P. massoniana have not been clearly reported. Here, we infested P. massoniana with M. alternatus and characterized the induced terpene defenses by microscopy, gas chromatography-mass spectrometry (GC-MS) and GCflame ionization detector (GC-FID), and quantitative reverse transcriptase PCR (qRT-PCR). The induced responses involve TD formation, tissue-specific terpenoid accumulation differentiation, and temporal related gene changes. Formation of TDs was observed in secondary xylem 7 days after feeding. GC-MS and GC-FID results showed terpenoid composition varied in bark and xylem tissue in response to infestation. Following feeding damage, most of the terpenoid synthase genes were up-regulated, which is consistent with the changes in terpenoid constitution. The genes were activated before terpenoid changes were detected indicating that this complex physiological and biochemical process requires time. This study provides evidence of the temporal sequence of changes in terpenoid defenses against herbivory in P. massoniana.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alfaro RI (1995) An induced defense reaction in white spruce to attack by the white pine weevil, Pissodes strobe. Can J For Res 25:1725–1730. https://doi.org/10.1139/x95-186
Burke JL, Carroll AL (2016) The influence of variation in host tree monoterpene composition on secondary attraction by an invasive bark beetle: implications for range expansion and potential host shift by the mountain pine beetle. Forest Ecol Manag 359:59–64. https://doi.org/10.1016/j.foreco.2015.09.044
Burney OT, Jacobs DF (2012) Terpene production and growth of three Pacific Northwest conifers in response to simulated browse and nutrient availability. Trees 26:1331–1342. https://doi.org/10.1007/s00468-012-0709-4
Chang FC, Lu CM, Sha S (2007) The plant biology experiment. Nanjing Normal University Press, Nanjing, pp 209–225
Chen RX, Wang LJ, Lin T, Wei ZQ, Wang Y, Hao DJ (2017) Rearing techniques of Monochamus alternatus Hope (Coleoptera: Cerambycidae) on artificial diets. J Nanjing For Univ 1:199–202
Crook DJ, Lance DR, Mastro VC (2014) Identification of a potential third component of the male-produced pheromone of Anoplophora glabripennis and its effect on behavior. J Chem Ecol 40:1241–1250. https://doi.org/10.1007/s10886-014-0520-3
Davies FK, Jinkerson RE, Posewitz MC (2015) Toward a photosynthetic microbial platform for terpenoid engineering. Photosynth Res 123:265–284. https://doi.org/10.1007/s11120-014-9979-6
Dudareva N, Negre F, Nagegowda DA, Orlova I (2006) Plant volatiles: recent advances and future perspectives. CRC Crit Rev Plant Sci 25:417–440. https://doi.org/10.1080/07352680600899973
Erbilgin N, Ma C, Whitehouse C, Shan B, Najar A, Evenden M (2013) Chemical similarity between historical and novel host plants promotes range and host expansion of the mountain pine beetle in a naïve host ecosystem. New Phytol 201:940–950. https://doi.org/10.1111/nph.12573
Eyles A, Bonello P, Ganley R, Mohammed C (2010) Induced resistance to pests and pathogens in trees. New Phytol 185:893–908
Fan J, Kang L, Sun J (2007a) Role of host volatiles in mate location by the Japanese pine sawyer, Monochamus alternatus Hope (Coleoptera: Cerambycidae). Environ Entomol 36:58–63
Fan J, Sun J, Shi J (2007b) Attraction of the Japanese pine sawyer, Monochamus alternatus, to volatiles from stressed host in China. Ann For Sci 64:67–71. https://doi.org/10.1051/forest:2006089
Gijzen M, Lewinsohn E, Savage TJ, Croteau RB (1993) Conifer monoterpenes: biochemistry and bark beetle chemical ecology. ACS Symp Ser 525:8–22. https://doi.org/10.1021/bk-1993-0525.ch002
Gray DW, Breneman SR, Topper LA, Sharkey TD (2011) Biochemical characterization and homology modeling of methylbutenol synthase and implications for understanding hemiterpene synthase evolution in plants. J Biol Chem 286:20582–20590. https://doi.org/10.1074/jbc.M111.237438
Hall DE, Yuen MM, Jancsik S, Quesada AL, Dullat HK, Li M, Henderson H, Arango-Velez A, Liao NY, Docking RT (2013a) Transcriptome resources and functional characterization of monoterpene synthases for two host species of the mountain pine beetle, lodgepole pine (Pinus contorta) and jack pine (Pinus banksiana). BMC Plant Biol 13:80. https://doi.org/10.1186/1471-2229-13-80
Hall DE, Zerbe P, Jancsik S, Quesada AL, Dullat H, Madilao LL, Yuen M, Bohlmann J (2013b) Evolution of conifer diterpene synthases: diterpene resin acid biosynthesis in lodgepole pine and jack pine involves monofunctional and bifunctional diterpene synthase. Plant Physiol 161:600–616. https://doi.org/10.1104/pp.112.208546
Hao DJ, Ma FL, Wang Y, Dai HG, Zhang YH (2007) Electroantennogram and behavioural responses of Monochamus alternatus to volatiles from Pinus massoniana. Chin Bull Entomol 44:541–544. https://doi.org/10.3969/j.issn.0452-8255.2007.04.019
Hudgins JW, Christiansen E, Franceschi VR (2004) Induction of anatomically based defense responses in stems of diverse conifers by methyl jasmonate: a phylogenetic perspective. Tree Physiol 4:251–264. https://doi.org/10.1093/treephys/24.3.251
Kahl J, Siemens DH, Aerts RJ, Gäbler R, Kühnemann F, PrestonIan CA, Baldwin T (2000) Herbivore-induced ethylene suppresses a direct defense but not a putative indirect defense against an adapted herbivore. Planta 210:336–442. https://doi.org/10.1007/PL00008142
Keeling CI, Bohlmann J (2006a) Diterpene resin acids in conifers. Phytochemistry 67:2415–2423. https://doi.org/10.1016/j.phytochem.2006.08.019
Keeling CI, Bohlmann J (2006b) Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens. New Phytol 170:657–675. https://doi.org/10.1111/j.1469-8137.2006.01716.x
Keeling CI, Weisshaar S, Ralph SG, Jancsik S, Hamberger B, Dullat HK, Bohlmann J (2011) Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol 11:43. https://doi.org/10.1186/1471-2229-11-43
Kessler A, Baldwin IT (2001) Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–2144. https://doi.org/10.1126/science.291.5511.2141
Kikuchi T, Cotton JA, Dalzell JJ, Hasegawa K, Kanzaki N, Mcveigh P, Takanashi T, Tsai IJ, Assefa SA, Cock PJ (2011) Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathog 7:e1002219. https://doi.org/10.1371/journal.ppat.1002219
Kovats E (1965) Gas chromatographic characterization of organic substances in the retention index system. Adv Chromatogr 1:229–247
Lewinsohn E, Gijzen M, Savage TJ, Croteau R (1991) Defense mechanisms of conifers-relationship of monoterpene cyclase activity to anatomical specialization and oleoresin monoterpene content. Plant Physiol 96:38–43. https://doi.org/10.1104/pp.96.1.38
Lewinsohn E, Gijzen M, Muzika RM, Barton K, Croteau R (1993) Oleoresinosis in grand fir (Abies grandis) saplings and mature trees’ modulation of this wound response by light and water stresses. Plant Physiol 101:1021–1028. https://doi.org/10.1104/pp.101.3.1021
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262
Martin DM, Tholl D, Gershenzon J, Bohlmann J (2002) Methyl jasmonate induces traumatic resin ducts, terpenoid resin biosynthesis, and terpenoid accumulation in developing xylem of Norway spruce stems. Plant Physiol 129:1003–1018. https://doi.org/10.1104/pp.011001
Martin DM, Gershenzon J, Bohlmann J (2003) Induction of volatile terpene biosynthesis and diurnal emission by methyl jasmonate in foliage of Norway spruce. Plant Physiol 132:1586–1599. https://doi.org/10.1104/pp.103.021196
Martin DM, Faldt J, Bohlmann J (2004) Functional characterization of nine Norway Spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol 135:1908–1927. https://doi.org/10.1104/pp.011001
Matson PA, Hain FP (1985) Host conifer defense strategies: a hypothesis. Proceedings of the IUFRO Conference on The role of the host in the population dynamics of forest insects. Alberta, Canada, pp 33–42
McKay SAB, Hunter WL, Godard KA, Wang SX, Martin DM, Bohlmann J, Plant AL (2003) Insect attack and wounding induce traumatic resin duct development and gene expression of (-)-pinene synthase in Sitka spruce. Plant Physiol 133:368–378. https://doi.org/10.1104/pp.103.022723
Miller B, Madilao LL, Ralph S, Bohlmann J (2005) Insect-induced conifer defense. White pine weevil and methyl jasmonate induce traumatic resinosis, de Novo formed volatile emissions, and accumulation of terpenoid synthase and putative octadecanoid pathway transcripts in Sitka spruce. Plant Physiol 137:369–382. https://doi.org/10.1104/pp.103.022723
Mitchell C, Brennan RM, Graham J, Karley AJ (2016) Plant defense against herbivorous pests: exploiting resistance and tolerance traits for sustainable crop protection. Front Plant Sci 7:1132. https://doi.org/10.3389/fpls.2016.01132
Moreira X, Zas R, Sampedro L (2012a) Differential allocation of constitutive and induced chemical defenses in pine tree juveniles: a test of the optimal defense theory. PLoS ONE 7:e34006. https://doi.org/10.1371/journal.pone.0034006
Moreira X, Zas R, Sampedro L (2012b) Quantitative comparison of chemical, biological and mechanical induction of secondary compounds in Pinus pinaster seedlings. Trees–Struct Funct 26:677–683. https://doi.org/10.1007/s00468-011-0602-6
Mur LAJ, Kenton P, loyd L, Ougham AJ, Prats H E (2008) The hypersensitive response; the centenary is upon us but how much do we know? J Exp Bot 59:501–520. https://doi.org/10.1093/jxb/erm239
Nagy NE, Franceschi VR, Solheim H, Krekling T, Christiansen E (2000) Wound-induced traumatic resin duct development in stems of Norway spruce (Pinaceae): anatomy and cytochemical traits. Am J Bot 87:302–313. https://doi.org/10.2307/2656626
Nault JR, Alfaro RI (2001) Changes in cortical and wood terpenes in Sitka spruce in response to wounding. Can J For Res 31:1561–1568. https://doi.org/10.1139/x01-082
Phillips MA, Croteau RB (1999) Resin-based defenses in conifers. Trends Plant Sci 4:184–190. https://doi.org/10.1016/S1360-1385(99)01401-6
Portman SL, Kariyat RR, Johnston M, Sthephenson AG, Marden JH (2015) Inbreeding compromises host plant defense gene expression and improves herbivore survival. Plant Signal Behav 10(5):e998548. https://doi.org/10.1080/15592324.2014.998548
Preisser EL, Gibson SE, Adler LS, Lewis EE (2007) Underground herbivory and the costs of constitutive defense in tobacco. Acta Oecol 31:210–215. https://doi.org/10.1016/j.actao.2006.09.004
Robert JA, Madilao LL, White RA, Yanchuk AD, King J, Bohlmann J (2010) Terpenoid metabolite profiling in Sitka spruce identifies association of dehydroabietic acid, (+)-3-carene, and terpinolene with resistance against white pine weevil. Botany 88:810–820. https://doi.org/10.1139/B10-049
Semiz G, Erbilgin N, Holopainen JK (2017) Hylobius abietis L. feeding on the novel host Pinus brutia Ten. increases emission of volatile organic compounds. J Appl Entomol 141:133–140. https://doi.org/10.1111/jen.12310
Seybold SJ, Bohlmann J, Raffa KF (2000) Biosynthesis of coniferophagous bark beetle pheromones and conifer isoprenoids: evolutionary perspective and synthesis. Can Entomol 132:697–753. https://doi.org/10.4039/Ent132697-6
Steele CL, Crock J, Bohlmann J, Croteau R (1998a) Sesquiterpene synthase from grand fir (Abies grandis). Comparison of constitutive and wound-induced activities and cDNA isolation, characterization, and bacterial expression of δ-Selinene synthase and γ-humulene synthase. J Biol Chem 273:2078–2089. https://doi.org/10.1074/jbc.273.4.2078
Steele CL, Katoh S, Bohlmann J, Croteau R (1998b) Regulation of oleoresinosis in grand fir (Abies grandis). Differential transcriptional control of monoterpene, sesquiterpene, and diterpene synthase genes in response to wounding. Plant Physiol 116:1497–1504. https://doi.org/10.1104/pp.116.4.1497
Togashi K, Miyauchi O, Dai K, Matsushita N (2015) Commensal relation between Bursaphelenchus xylophilus (Nematoda: Aphelenchoididae) and Monochamus alternatus (Coleoptera: Cerambycidae) within pine trees. Appl Entomol Zool 51:53–62. https://doi.org/10.1007/s13355-015-0370-7
TomLin ES, Antonejevic E, Alfaro RI, Borden JH (2000) Changes in volatile terpene and diterpene resin acid composition of resistant and susceptible white spruce leaders exposed to simulated white pine weevil damage. Tree Physiol 20:1087–1095. https://doi.org/10.1093/treephys/20.16.1087
Xu LT, Lu M, Sun JH (2016) Invasive bark beetle-associated microbes degrade a host defensive monoterpene. Insect Sci 23:183–190. https://doi.org/10.1111/1744-7917.12255
Yasui H, Fujiwara-Tsujii N (2016) Host plant affects the sexual attractiveness of the female white-spotted longicorn beetle, Anoplophora malasiaca. Sci Rep 6:29526. https://doi.org/10.1038/srep29526
Zagatti P, Lemperiere G, Malosse C (1997) Monoterpenes emitted by the large pine weevil, Hylobius abietis (L.) feeding on Scots pine Pinus sylvestris L. Physiol Entomol 22:394–400. https://doi.org/10.1111/j.1365-3032.1997.tb01185.x
Zeneli G, Krokene P, Christiansen E, Krekling T, Gershenzon J (2006) 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 26:977–988. https://doi.org/10.1093/treephys/26.8.977
Zhao LL, Wei W, Kang L, Sun JH (2007) Chemotaxis of the pinewood nematode, Bursaphelenchus xylophilus, to volatiles associated with host pine, Pinus massoniana, and its vector Monochamus alternatus. J Chem Ecol 33:1207–1216. https://doi.org/10.1007/s10886-007-9289-y
Zhao BG, Futai K, Sutherland JR, Takeuchi Y (2008) Pine wilt disease. Springer, Japan
Zulak KG, Bohlmann J (2010) Terpenoid biosynthesis and specialized vascular cells of conifer defense. J Integr Plant Biol 52:86–97. https://doi.org/10.1111/j.1744-7909.2010.00910.x
Acknowledgements
We greatly thank the Doctorate Fellowship Foundation of Nanjing Forestry University, the National Natural Science Foundation of China (31170606 and 31470650), and the Priority Academic Program Development of Jiangsu Higher Education Institutions for supporting these researches.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, R., He, X., Chen, J. et al. Traumatic Resin Duct Development, Terpenoid Formation, and Related Synthase Gene Expression in Pinus massoniana Under Feeding Pressure of Monochamus alternatus. J Plant Growth Regul 38, 897–908 (2019). https://doi.org/10.1007/s00344-018-9900-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-018-9900-1