Recent advances in the molecular genetics of resin biosynthesis and genetic engineering strategies to improve defenses in conifers

Abstract

Since the first terpenoid synthase cDNA was obtained by the reverse genetic approach from grand fir, great progress in the molecular genetics of terpenoid formation has been made with angiosperms and genes encoding a monoterpene synthase, a sesquiterpene synthase, and a diterpene synthase. Tree killing bark beetles and their vectored fungal pathogens are the most destructive agents of conifer forests worldwide. Conifers defend against attack by the constitutive and inducible production of oleoresin that accumulates at the wound site to kill invaders and both flush and seal the injury. Although toxic to the bark beetle and fungal pathogen, oleoresin also plays a central role in the chemical ecology of these boring insects. Recent advances in the molecular genetics of terpenoid biosynthesis provide evidence for the evolutionary origins of oleoresin and permit consideration of genetic engineering strategies to improve conifer defenses as a component of modern forest biotechnology. This review described enzymes of resin biosynthesis, structural feathers of genes genomic intron and exon organization, pathway organization and evolution, resin production and accumulation, interactions between conifer and bark beetle, and engineering strategies to improve conifer defenses.

Keywords

Genetic engineering strategies / Resin biosynthesis / Bark beetles / Genomics / Molecular genetics / Q341 / TQ322.4 / A

References

[1] Aubourg S., Takvorian A., Cheron A., Kreis M., Lecharny A. Structure, organization and putative function of the genes identified within a 23.9kb fragment fromArabidopsis thaliana chromosome IV [J]. Gene, 1997, 199: 241-53.

[2] Bedard W.E., Tilden P.E., Wood D.L., Silverstein R.M., Brownlee RG et al. Western pine beetle: field response to its sex pheromone and a synergistic host terpene, myrcene [J]. Science, 1969, 164: 1284-85.

[3] Berryman AA Resistance of conifers to invasion by bark beetlefungus associations [J]. BioScience, 1972, 22: 598-602.

[4] Bohlmann J., Meyer-Gauen G, Croteau R. Plant terpenoid synthases: molecular biology and phylogenetic analysis [J]. Proc. Natl. Acad. Sci. USA, 1998, 95: 4126-33.

[5] Bohlmann J., Phillips M., Ramachandiran V., Katoh S., Croteau R. cDNA cloning, characterization, and functional expression of four new monoterpene synthase members of theTpsd gene family from grand fir (Abies grandis) [J]. Arch. Biochem. Biophys., 1999, 368: 232-43.

[6] Cook S.P., Hain F.P. Toxicity of host monoterpenes to Dendroctonus frontalis andIps calligraphus (Coleoptera: Scolytidae) [J]. J. Entomol. Sci., 1988, 23: 287-92.

[7] Croteau R. Kung S-D, Yang S-F The discovery of terpenes [C] Discoveries in Plant Biology, 1998 Singapore: World Sci. 329-43.

[8] Davis EM, Croteau R Leeper F, Vederas JC Cyclization enzymes in the biosynthesis of monoterpenes, sesquiterpenes and diterpenes [C] Topics in Current Chemistry: Biosynthesis, 2000 Heidelberg: Northeast Forestry University and Ecological Society of China 53-95.

[9] Facchini P.J., Chappell J. Gene family for an elicitor-induced sesquiterpene cyclase in tobacco [J]. Proc. Natl. Acad. Sci. USA, 1992, 89: 11088-11092.

[10] Francke W., Vite J.P.Z. Oxygenated terpenes in pheromone systems of bark beetles (Polygraphus poligraphus, ips amitinus, ips typographus) [J]. Z. Angew. Entomol., 1983, 96: 146-56.

[11] Fryxell K.J. The coevolution of gene family trees [J]. Trends Genet., 1996, 12: 356-69.

[12] Funk C., Croteau R. Diterpenoid resin acid biosynthesis in conifers: characterization of two cytochrome P450-dependent monooxygenases and an aldehyde dehydrogenase involved in abletic acid biosynthesis [J]. Arch. Biochem. Biophys., 1994, 308: 258-66.

[13] Funk C., Lewinsohn E., Vogel B.S., Steele C.L., Croteau R. Regulation of oleoresinosis in grand fir (Abies grandis): coordinate induction of monoterpene and diterpene cyclases and two cytochrome P450-dependent diterpene hydroxylases by stem wounding [J]. Plant Physiol., 1994, 106: 999-1005.

[14] Gifford E.M., Foster A.S. Coniferophyta [C] Morphology and Evolution of Vascular Plants, 1988 Harbin: Freeman 401-453.

[15] Gijzen M., Lewinsohn E., Croteau R. Characterization of the constitutive and wound-inducible monoterpene cyclases of grand fir (Abies grandis) [J]. Arch. Biochem. Biophys., 1991, 289: 267-73.

[16] Gijzen M., Lewinsohn E., Croteau R. Antigenic cross-reactivity among monoterpene cyclases from grand fir and induction of these enzymes upon stem wounding [J]. Arch. Biochem. Biophys., 1992, 294: 670-74.

[17] Gijzen M., Lewinsohn E., Savage T.J., Croteau R.B. Teranishi R, Buttery RG, Sugisawa H Conifer monoterpenes: biochemistry and bark beetle chemical ecology [C] Bioactive VolatileCompounds from Plants, 1993 Washington, DC: Am. Chem. Soc. 8-22.

[18] Jain K.K. Evolution of wood structure in Pinaceae [J]. Isr. J. Bot., 1976, 25: 28-33.

[19] James R.R. Utilizing a social ethic toward the environment in assessing genetically engineered insect-resistance in trees [J]. Agr. Hum. Values, 1997, 14: 237-49.

[20] Katoh S., Croteau R. Individual variation in constitutive and induced monoterpene biosynthesis in grand fir (Abies grandis) [J]. Phytochemistry, 1998, 47: 577-82.

[21] Keegstra K., Olsen L.J., Theg S.M. Chloroplastic precursors and their transport across the envelope membrane [J]. Annu. Rev. Plant Physiol. Plant Mol. Biol., 1989, 40: 471-501.

[22] Kuroda K., Shimaji K. Traumatic resin canal formation as a marker of xylem growth For. Sci., 1983, 29: 653-659.

[23] LaFever R.E., Stofer, Vogel B., Croteau R. Diterpenoid resin acid biosynthesis in conifers: enzymatic cyclization of geranylgeranyl pyrophosphate to abletadiene, the precursor of abietic acid [J]. Arch. Biochem. Biophys., 1994, 313: 139-149.

[24] Lewinsohn E., Gijzen M., Croteau R. Nes WD, Parish EJ, Trzaskos JM Regulation of monoterpene biosynthesis in conifer defense [C] Regulation of Isopentenoid Metabolism, 1992 Washington, DC: Am. Chem. Soc. 8-17.

[25] Lewinsohn E., Gijzen M., Muzika R.M., Barton K., Croteau R. Oleoresinosis in grand fir (Abies grandis) saplings and mature trees: modulation of this wound response by light and water stresses [J]. Plant Physiol., 1993, 101: 1021-1028.

[26] Lewinsohn E., Gijzen M., Savage T.J., Croteau R. Defense mechanisms of conifers: relationship of monoterpene cyclase activity to anatomical specialization and cleoresin monoterpene content [J]. Plant Physiol., 1991, 96: 38-43.

[27] Lewinsohn E., Katoh S., Croteau R. Lerner HR Conifer chemical defenses against bark beetles: the modulation of monoterpene biosynthesis by wounding, environmental stress, and ethylene [C] Plant Responses to Environmental Stresses: From Phytohormones to Genome Reorganization, 1999 Harbin: Marcel Dekker 659-706.

[28] Mau C.J.D., West C.A. Cloning of casbene synthase cDNA: evidence for conserved structural features among terpenoid cyclases in plants [J]. Proc. Natl. Acad. Sci. USA, 1994, 91: 8497-501.

[29] Mutton D.B. Hillis WE Wood resin [C] Wood Extractives, 1962 Harbin: Academic 331-63.

[30] Payne T.L. Kulhavy DL, Miller MC Olfactory basis for insect enemies of allied species [C] Potential for Biological Control of Dendroctonus and Ips Bark Beetles, 1989 Nacogdoches, TX: Stephen F. Austin Univ. Press 55-69.

[31] Phillips M.A., Croteau R. Resin based defenses in conifers [J]. Trends Plant Sci., 1999, 4: 184-90.

[32] Puritch G.S., Nijhoit W.W. Occurrence of juvabione-related compounds in grand fir (Abies grandis) and pacific silver fir (Abies amabilis) infested by balsam wooly aphid (Adelges piceae) [J]. Can. J. Bot., 1974, 52: 585-87.

[33] Raffa K.F., Berryman A.A., Simasko J., Teal W., Wong B.L. Effects of grand fir monoterpenes on the fir engraver,Scolytus ventralis (Coleoptera: Scolytidae) and its symbiotic fungus [J]. Environ. Entomol., 1985, 14: 552-56.

[34] Robinson C. Making forest biotechnology a commercial reality [J]. Nat. Biotechnol., 1999, 17: 27-29.

[35] Savage T.J., Hatch M.W., Croteau R. Monoterpene synthases ofPinus contorta: a new class of terpenoid cyclase [J]. J. Biol. Chem., 1994, 269: 4012-20.

[36] Scagel R.F., Bandoni R.J., Rouse G.E., Schofield W.B., Stein J.R. An Evolutionary Survey of the Plant Kingdom [M], 1965 Belmont, CA: Wadsworth 491-524.

[37] Schopf R. The effect of secondary needle compounds on the development of phytophagous insects [J]. For. Ecol. Manage., 1986, 15: 55-64.

[38] Sederoff R. Building better trees with antisense [J]. Nat. Biotechnol., 1999, 17: 750-51.

[39] Starks C.M., Back K., Chappell J., Noel J.P. Structural basis for cyclic terpene biosynthesis by tobacco 5-epi-aristolochene synthase [J]. Science, 1997, 277: 1815-20.

[40] Steele C.L., Katoh S., Bohlmann J., Croteau R. Regulation of oleoresinosis in grand fir (Abies grandis). Differential transcriptional control of monoterpene, sesquiterpene and diterpene synthase genes in response to wounding [J]. Plant Physiol, 1998, 116: 1497-504.

[41] Steele C.L., Lewinsohn E., Croteau R. Induced oleoresin biosynthesis in grand fir as a defense against bark beetles [J]. Proc. Natl. Acad. Sci. USA, 1995, 92: 4164-68.

[42] Trapp S., Croteau R. Detensive resin biosynthesis in conifers [J]. Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52: 689-724.

[43] Wildung M.R., Croteau R. AcDNA clone for taxadiene synthase, the diterpene cyclase that catalyzes the committed step of Taxol biosynthesis [J]. J. Biol. Chem., 1996, 271: 9201-4.

[44] Williams D.C., McGarvey D.J., Katahira E.J., Croteau R. Truncation of limonene synthase preprotein provides a fully active ‘pseudomature’ form of this monoterpene cyclase and reveals the function of the amino-terminal arginine pair [J]. Biochemistry, 1998, 37: 12213-20.

[45] Wise M.L., Croteau R. Cane DE Monoterpene biosynthesis [C] Comprehensive Natural Products Chemistry: Isoprenoids Including Steroids and Carotenoids, 1999 Oxford: Elsevier Sci. 97-153.

[46] Wood D.L. The role of pheromones, karomones and allomones in the host selection and colonization behavior of bark beeties [J]. Annu. Rev. Entomol., 1982, 27: 411-46.