BMC Genomics | |
Activation of defence pathways in Scots pine bark after feeding by pine weevil (Hylobius abietis) | |
Fred O Asiegbu1  Jarmo K Holopainen3  Jeffrey FD Dean2  W Walter Lorenz2  Rajendra Ghimire3  Susanna Keriö1  Emad Jaber1  Tommaso Raffaello1  Andriy Kovalchuk1  | |
[1] Department of Forest Sciences, University of Helsinki, Helsinki, FIN-00014, Finland;Warnell School of Forestry and Natural Resources, The University of Georgia, Athens 30602, GA, USA;Department of Environmental Science, University of Eastern Finland, Kuopio, FIN-70211, Finland | |
关键词: PR proteins; Protease inhibitors; Terpenoid pathway; Phenylpropanoid pathway; Transcriptomics; VOC emission; Herbivory; | |
Others : 1204051 DOI : 10.1186/s12864-015-1546-9 |
|
received in 2014-09-04, accepted in 2015-04-17, 发布年份 2015 | |
【 摘 要 】
Background
During their lifetime, conifer trees are exposed to numerous herbivorous insects. To protect themselves against pests, trees have developed a broad repertoire of protective mechanisms. Many of the plant’s defence reactions are activated upon an insect attack, and the underlying regulatory mechanisms are not entirely understood yet, in particular in conifer trees. Here, we present the results of our studies on the transcriptional response and the volatile compounds production of Scots pine (Pinus sylvestris) upon the large pine weevil (Hylobius abietis) feeding.
Results
Transcriptional response of Scots pine to the weevil attack was investigated using a novel customised 36.4 K Pinus taeda microarray. The weevil feeding caused large-scale changes in the pine transcriptome. In total, 774 genes were significantly up-regulated more than 4-fold (p ≤ 0.05), whereas 64 genes were significantly down-regulated more than 4-fold. Among the up-regulated genes, we could identify genes involved in signal perception, signalling pathways, transcriptional regulation, plant hormone homeostasis, secondary metabolism and defence responses. The weevil feeding on stem bark of pine significantly increased the total emission of volatile organic compounds from the undamaged stem bark area. The emission levels of monoterpenes and sesquiterpenes were also increased. Interestingly, we could not observe any correlation between the increased production of the terpenoid compounds and expression levels of the terpene synthase-encoding genes.
Conclusions
The obtained data provide an important insight into the transcriptional response of conifer trees to insect herbivory and illustrate the massive changes in the host transcriptome upon insect attacks. Moreover, many of the induced pathways are common between conifers and angiosperms. The presented results are the first ones obtained by the use of a microarray platform with an extended coverage of pine transcriptome (36.4 K cDNA elements). The platform will further facilitate the identification of resistance markers with the direct relevance for conifer tree breeding.
【 授权许可】
2015 Kovalchuk et al.; licensee BioMed Central.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20150523044244285.pdf | 1005KB | download | |
Figure 4. | 90KB | Image | download |
Figure 3. | 66KB | Image | download |
Figure 2. | 72KB | Image | download |
Figure 1. | 46KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
Figure 4.
【 参考文献 】
- [1]Maleev VP. Genus Pinus L. - Pine. In: Trees and Shrubs of the Soviet Union. Volume 1. Sokolov SY, Shishkin BK, editors. Academy of Science of the Soviet Union, Moscow, Leningrad; 1949: p.184-266. [in Russian]
- [2]Långström B, Day KR: Damage, control and management of weevil pests, especially Hylobius abietis. In: Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Edited by Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF. Dordrecht: Springer Netherlands; 2004: 415–444.
- [3]Leather SR, Day KR, Salisbury AN. The biology and ecology of the large pine weevil, Hylobius abietis (Coleoptera: Curculionidae): a problem of dispersal? Bulletin of Entomological Research. 1999; 89(01):3-16.
- [4]Wainhouse D: Hylobius abietis – host utilisation and resistance. In: Bark and Wood Boring Insects in Living Trees in Europe, a Synthesis. Edited by Lieutier F, Day KR, Battisti A, Grégoire J-C, Evans HF. Dordrecht: Springer Netherlands; 2004: 365–379.
- [5]Franceschi VR, Krokene P, Christiansen E, Krekling T. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytol. 2005; 167(2):353-75.
- [6]Howe GA, Jander G. Plant immunity to insect herbivores. Annu Rev Plant Biol. 2008; 59:41-66.
- [7]Sallas L, Luomala EM, Ultriainen J, Kainulainen P, Holopainen JK. 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(2):97-108.
- [8]Hilker M, Kobs C, Varama M, Schrank K. Insect egg deposition induces Pinus sylvestris to attract egg parasitoids. J Exp Biol. 2002; 205(Pt 4):455-61.
- [9]Virtanen A, Joutsensaari J, Koop T, Kannosto J, Yli-Pirila P, Leskinen J et al.. An amorphous solid state of biogenic secondary organic aerosol particles. Nature. 2010; 467(7317):824-7.
- [10]Riccobono F, Schobesberger S, Scott CE, Dommen J, Ortega IK, Rondo L et al.. Oxidation products of biogenic emissions contribute to nucleation of atmospheric particles. Science. 2014; 344(6185):717-21.
- [11]Kessler A, Baldwin IT. Plant responses to insect herbivory: The emerging molecular analysis. Annu Rev Plant Biol. 2002; 53:299-328.
- [12]Baldwin IT. Jasmonate-induced responses are costly but benefit plants under attack in native populations. Proc Natl Acad Sci U S A. 1998; 95(14):8113-8.
- [13]Karban R, Agrawal AA, Mangel M. The benefits of induced defenses against herbivores. Ecology. 1997; 78(5):1351-5.
- [14]Kovalchuk A, Keriö S, Oghenekaro AO, Jaber E, Raffaello T, Asiegbu FO. Antimicrobial defenses and resistance in forest trees: Challenges and perspectives in a genomic era. Annu Rev Phytopathol. 2013; 51:221-44.
- [15]Heidel‐Fischer HM, Musser RO, Vogel H. Plant transcriptomic responses to herbivory. Annual Plant Reviews. 2014; 47:155-96.
- [16]Ralph SG, Yueh H, Friedmann M, Aeschliman D, Zeznik JA, Nelson CC et al.. Conifer defence against insects: microarray gene expression profiling of Sitka spruce (Picea sitchensis) induced by mechanical wounding or feeding by spruce budworms (Choristoneura occidentalis) or white pine weevils (Pissodes strobi) reveals large-scale changes of the host transcriptome. Plant Cell Environ. 2006; 29(8):1545-70.
- [17]Kolosova N: Transcriptome analysis of conifer defense against bark beetle-associated blue-stain fungi and white pine weevil. PhD thesis. Vancouver, Canada: University of British Columbia; 2010.
- [18]Lippert D, Chowrira S, Ralph SG, Zhuang J, Aeschliman D, Ritland C et al.. Conifer defense against insects: Proteome analysis of Sitka spruce (Picea sitchensis) bark induced by mechanical wounding or feeding by white pine weevils (Pissodes strobi). Proteomics. 2007; 7(2):248-70.
- [19]D'Auria JC, Pichersky E, Schaub A, Hansel A, Gershenzon J. Characterization of a BAHD acyltransferase responsible for producing the green leaf volatile (Z)-3-hexen-1-yl acetate in Arabidopsis thaliana. Plant J. 2007; 49(2):194-207.
- [20]Ghimire RP, Markkanen JM, Kivimaenpaa M, Lyytikainen-Saarenmaa P, Holopainen JK. Needle removal by pine sawfly larvae increases branch-level VOC emissions and reduces below-ground emissions of Scots pine. Environ Sci Technol. 2013; 47(9):4325-32.
- [21]Kännaste A, Nordenhem H, Nordlander G, Borg-Karlson AK. Volatiles from a mite-infested spruce clone and their effects on pine weevil behavior. J Chem Ecol. 2009; 35(10):1262-71.
- [22]Singh K, Foley RC, Onate-Sanchez L. Transcription factors in plant defense and stress responses. Curr Opin Plant Biol. 2002; 5(5):430-6.
- [23]Nakashima K, Takasaki H, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K. NAC transcription factors in plant abiotic stress responses. Biochim Biophys Acta. 2012; 1819(2):97-103.
- [24]Licausi F, Ohme-Takagi M, Perata P. APETALA2/Ethylene Responsive Factor (AP2/ERF) transcription factors: mediators of stress responses and developmental programs. New Phytol. 2013; 199(3):639-49.
- [25]Schweizer F, Fernandez-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G et al.. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell. 2013; 25(8):3117-32.
- [26]Keeling CI, Weisshaar S, Ralph SG, Jancsik S, Hamberger B, Dullat HK et al.. Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.). BMC Plant Biol. 2011; 11:43. BioMed Central Full Text
- [27]Martin DM, Faldt J, Bohlmann J. Functional characterization of nine Norway Spruce TPS genes and evolution of gymnosperm terpene synthases of the TPS-d subfamily. Plant Physiol. 2004; 135(4):1908-27.
- [28]Wang Y, Chantreau M, Sibout R, Hawkins S. Plant cell wall lignification and monolignol metabolism. Front Plant Sci. 2013; 4:220.
- [29]Davin LB, Lewis NG. Dirigent phenoxy radical coupling: advances and challenges. Curr Opi Biotechnol. 2005; 16(4):398-406.
- [30]Ralph S, Park JY, Bohlmann J, Mansfield SD. Dirigent proteins in conifer defense: gene discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Mol Biol. 2006; 60(1):21-40.
- [31]Ralph SG, Jancsik S, Bohlmann J. Dirigent proteins in conifer defense II: Extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry. 2007; 68(14):1975-91.
- [32]Liu Y, Ahn JE, Datta S, Salzman RA, Moon J, Huyghues-Despointes B et al.. Arabidopsis vegetative storage protein is an anti-insect acid phosphatase. Plant Physiol. 2005; 139(3):1545-56.
- [33]Park SC, Lee JR, Shin SO, Park Y, Lee SY, Hahm KS. Characterization of a heat-stable protein with antimicrobial activity from Arabidopsis thaliana. Biochem Biophys Res Commun. 2007; 362(3):562-7.
- [34]van Zyl L, von Arnold S, Bozhkov P, Chen Y, Egertsdotter U, Mackay J et al.. Heterologous array analysis in Pinaceae: hybridization of Pinus taeda cDNA arrays with cDNA from needles and embryogenic cultures of P. taeda, P. sylvestris or Picea abies. Comp Funct Genomics. 2002; 3(4):306-18.
- [35]Felton GW, Chung SH, Hernandez MGE, Louis J, Peiffer M, Tian D. Herbivore oral secretions are the first line of protection against plant-induced defences. Annual Plant Reviews. 2014; 47:37-76.
- [36]Langenheim JH. Plant resins: chemistry, evolution, ecology, and ethnobotany. Timber Press, Portland, Cambridge; 2003.
- [37]Heijari J, Blande JD, Holopainen JK. Feeding of large pine weevil on Scots pine stem triggers localised bark and systemic shoot emission of volatile organic compounds. Environ Exp Bot. 2011; 71(3):390-8.
- [38]Blande JD, Turunen K, Holopainen JK. Pine weevil feeding on Norway spruce bark has a stronger impact on needle VOC emissions than enhanced ultraviolet-B radiation. Environ Pollut. 2009; 157(1):174-80.
- [39]Mumm R, Schrank K, Wegener R, Schulz S, Hilker M. Chemical analysis of volatiles emitted by Pinus sylvestris after induction by insect oviposition. J Chem Ecol. 2003; 29(5):1235-52.
- [40]Mumm R, Tiemann T, Schulz S, Hilker M. Analysis of volatiles from black pine (Pinus nigra): significance of wounding and egg deposition by a herbivorous sawfly. Phytochemistry. 2004; 65(24):3221-30.
- [41]Miller B, Madilao LL, Ralph S, Bohlmann J. 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. 2005; 137(1):369-82.
- [42]Mumm R, Hilker M. The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem Senses. 2005; 30(4):337-43.
- [43]Keeling CI, Weisshaar S, Lin RP, Bohlmann J. Functional plasticity of paralogous diterpene synthases involved in conifer defense. Proc Natl Acad Sci USA. 2008; 105(3):1085-90.
- [44]Guenther A, Zimmermann PR, Harley PC, Monson RK, Fall R. Isoprene and monoterpene emission rate variability: model evaluations and sensitivity analyses. J Geophys Res. 1993; 98(D7):12609-17.
- [45]Helmig D, Ortega J, Guenther A, Herrick JD, Geron C. Sesquiterpene emissions from loblolly pine and their potential contribution to biogenic aerosol formation in the Southeastern US. Atmos Environ. 2006; 40(22):4150-7.
- [46]Chang S, Puryear J, Cairney J. A simple and efficient method for isolating RNA from pine trees. Plant Mol Biol Rep. 1993; 11(2):113-6.
- [47]Lorenz WW, Ayyampalayam S, Bordeaux JM, Howe GT, Jermstad KD, Neale DB et al.. Conifer DBMagic: a database housing multiple de novo transcriptome assemblies for 12 diverse conifer species. Tree Genet Genomes. 2012; 8(6):1477-85.
- [48]R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2013.
- [49]Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S et al.. Bioconductor: Open software development for computational biology and bioinformatics. Genome Biol. 2004; 5:R80. BioMed Central Full Text
- [50]Carvalho BS, Irizarry RA. A framework for oligonucleotide microarray preprocessing. Bioinformatics. 2010; 26(19):2363-7.
- [51]Smyth GK. Limma: Linear models for microarray data. In: Bioinformatics and Computational Biology Solutions Using R and Bioconductor. Gentleman R, Carey V, Dudoit S, Irizarry R, Huber W, editors. Springer, New York; 2005: p.397-420.
- [52]Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M et al.: gplots: Various R programming tools for plotting data. 2014. http://cran.r-project.org/web/packages/gplots/index.html. Accessed 3 Sept 2014.
- [53]Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002; 30(1):207-10.
- [54]Vestman D, Larsson E, Uddenberg D, Cairney J, Clapham D, Sundberg E, et al. Important processes during differentiation and early development of somatic embryos of Norway spruce as revealed by changes in global gene expression. Tree Genet Genomes. 2011;7(2):347–62. doi:10.1038/srep05135.
- [55]Kuo HC, Hui S, Choi J, Asiegbu FO, Valkonen JPT, Lee YH. Secret lifestyles of Neurospora crassa. Sci Rep-Uk. 2014; 4:..
- [56]Pape SL. EasyqpcR : EasyqpcR for easy analysis of real-time PCR data. IRTOMIT-INSERM U1082. 2012.