Association genetics of oleoresin flow in loblolly pine: Discovering genes and predicting phenotype for improved resistance to bark beetles and bioenergy potential

New Phytologist

Volumn 199, Issue 1, 2013, Pages 89-100

  Westbrook, Jared W ^a   Resende, Marcio F R ^a   Munoz, Patricio ^a   Walker, Alejandro R ^a   Wegrzyn, Jill L ^b   Nelson, C Dana ^c   Neale, David B ^b   Kirst, Matias ^a   Huber, Dudley A ^a   Gezan, Salvador A ^a   Peter, Gary F ^a   Davis, John M ^a  

^a UNIVERSITY OF FLORIDA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c USDA FOREST SERVICE   (United States)

Author keywords

Association genetics; Genomic selection; Genotype environment interactions; Herbivory defense; Pinus; Terpenoid

Indexed keywords

OLEORESINS; PLANT EXTRACT; TERPENE;

ANTIHERBIVORE DEFENSE; BARK; BEETLE; BIOENERGY; BIOMASS POWER; BIOTECHNOLOGY; CONIFEROUS TREE; GENE EXPRESSION; GENETIC ENGINEERING; GENETIC VARIATION; GENOTYPE-ENVIRONMENT INTERACTION; HERBIVORY; PEST RESISTANCE; PHENOTYPIC PLASTICITY; PLANT BREEDING; RESIN; TERPENE;

ANIMAL; ARTICLE; BEETLE; BIOLOGICAL MODEL; BREEDING; CLIMATE; GENETIC MARKER; GENETIC VARIABILITY; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; GROWTH, DEVELOPMENT AND AGING; LOBLOLLY PINE; METABOLISM; METHODOLOGY; PHENOTYPE; PHYSIOLOGY; POPULATION GENETICS; SINGLE NUCLEOTIDE POLYMORPHISM; SOIL; UNITED STATES;

ANIMALS; BEETLES; BREEDING; CLIMATE; GENE-ENVIRONMENT INTERACTION; GENETIC MARKERS; GENETIC VARIATION; GENETICS, POPULATION; MODELS, GENETIC; PHENOTYPE; PINUS TAEDA; PLANT EXTRACTS; POLYMORPHISM, SINGLE NUCLEOTIDE; SOIL; SOUTHEASTERN UNITED STATES; TERPENES;

UNITED STATES;

COLEOPTERA; CONIFEROPHYTA; PINUS TAEDA; SCOLYTINAE;

EID: 84878372518     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12240     Document Type: Article

References (78)

1. Aharoni A, Jongsma MA, Kim TY, Ri MB, Giri AP, Verstappen FWA, Schwab W, Bouwmeester HJ. 2006. Metabolic engineering of terpenoid biosynthesis in plants. Phytochemistry Reviews 5: 49-58.
2. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR. 1999. EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284: 2148-2152.
3. Aspinwall MJ, King JS, Booker FL, McKeand SE. 2011. Genetic effects on total phenolics, condensed tannins and non-structural carbohydrates in loblolly pine (Pinus taeda L.) needles. Tree Physiology 31: 831-842.
4. Baltunis BS, Huber DA, White TL, Goldfarb B, Stelzer HE. 2007. Genetic analysis of early field growth of loblolly pine clones and seedlings from the same full-sib families. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 37: 195-205.
5. Bentz BJ, Regniere J, Fettig CJ, Hansen EM, Hayes JL, Hicke JA, Kelsey RG, Negron JF, Seybold SJ. 2010. Climate change and bark beetles of the western United States and Canada: direct and indirect effects. BioScience 60: 602-613.
6. Bohlmann J, Meyer-Gauen G, Croteau R. 1998. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proceedings of the National Academy of Sciences, USA 95: 4126-4133.
7. Boone CK, Aukema BH, Bohlmann J, Carroll AL, Raffa KF. 2011. Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 41: 1174-1188.
8. Box GEP, Cox DR. 1964. An analysis of transformations. Journal of the Royal Statistical Society. Series B 26: 211-252.
9. Bridgen MR. 1980. Genetic variation of Scotch pine oleoresin physiology. Dissertation Abstracts International, B 40: 4047B.
10. Calder WJ, Horn KJ, St Clair SB. 2011. Conifer expansion reduces the competitive ability and herbivore defense of aspen by modifying light environment and soil chemistry. Tree Physiology 31: 582-591.
11. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
12. Eckert AJ, van Heerwaarden J, Wegrzyn JL, Nelson CD, Ross-Ibarra J, Gonzalez-Martinez SC, Neale DB. 2010. Patterns of population structure and environmental associations to aridity across the range of loblolly pine (Pinus taeda l., Pinaceae). Genetics 185: 969-982.
13. Eckert AJ, Wegrzyn JL, Cumbie WP, Goldfarb B, Huber DA, Tolstikov V, Fiehn O, Neale DB. 2012. Association genetics of the loblolly pine (Pinus taeda, Pinaceae) metabolome. New Phytologist 193: 890-902.
14. Evans JM, Cohen MJ. 2009. Regional water resource implications of bioethanol production in the southeastern United States. Global Change Biology 15: 2261-2273.
15. Franceschi VR, Krokene P, Christiansen E, Krekling T. 2005. Anatomical and chemical defenses of conifer bark against bark beetles and other pests. New Phytologist 167: 353-375.
16. Garrick DJ, Taylor JF, Fernando RL. 2009. Deregressing estimated breeding values and weighting information for genomic regression analyses. Genetics Selection Evolution 41: 1-8.
17. Gezan SA, White TL, Huber DA. 2006. Comparison of experimental designs for clonal forestry using simulated data. Forest Science 52: 108-116.
18. Gillespie JH, Turelli M. 1989. Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121: 129-138.
19. Gilmour AR, Gogel BJ, Cullis BR, Thompson R. 2009. ASReml user guide release 3.0. Hemel Hempstead, UK: VSN International Ltd.
20. Gopal V, Li Z, Casella G. 2011. BAMD: Bayesian association model for genomic data with missing covariates. [WWW document] URL http://cran.r-project.org/web/packages/BAMD/index.html [accessed on 31 December 2011].
21. Grattapaglia D, Resende MDV. 2011. Genomic selection in forest tree breeding. Tree Genetics & Genomes 7: 241-255.
22. Habier D, Fernando RL, Kizilkaya K, Garrick DJ. 2011. Extension of the Bayesian alphabet for genomic selection. BMC Bioinformatics 12: 186.
23. Hamberger B, Ohnishi T, Hamberger B, Séguin A, Bohlmann J. 2011. Evolution of diterpene metabolism: Sitka spruce CYP720B4 catalyzes multiple oxidations in resin acid biosynthesis of conifer defense against insects. Plant Physiology 157: 1677-1695.
24. Harvey BG, Wright ME, Quintana RL. 2010. High-density renewable fuels based on the selective dimerization of pinenes. Energy & Fuels 24: 267-273.
25. Hudgins JW, Franceschi VR. 2004. Methyl jasmonate-induced ethylene production is responsible for conifer phloem defense responses and reprogramming of stem cambial zone for traumatic resin duct formation. Plant Physiology 135: 2134-2149.
26. Jasinski M, Stukkens Y, Degand H, Purnelle B, Marchand-Brynaert J, Boutry M. 2001. A plant plasma membrane ATP binding cassette-type transporter is involved in antifungal terpenoid secretion. Plant Cell 13: 1095-1107.
27. Jennewein S, Rithner CD, Williams RM, Croteau RB. 2000. Taxol biosynthesis: taxane 13α-hydroxylase is a cytochrome P450-dependent monooxygenase. Proceedings of the National Academy of Sciences, USA 98: 13595-13600.
28. Jirschitzka J, Mattern DJ, Gershenzon J, D'Auria JC. 2012. Learning from nature: new approaches to the metabolic engineering of plant defense pathways. Current Opinion in Biotechnology 24: 1-9.
29. Kane JM, Kolb TE. 2010. Importance of resin ducts in reducing ponderosa pine mortality from bark beetle attack. Oecologia 164: 601-609.
30. 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 Biology 11: 1-14.
31. Kenward MG, Roger JH. 1997. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53: 983-997.
32. Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H. 2005. CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant Journal 41: 710-721.
33. Kim YB, Kim SM, Kang MK, Kuzuyama T, Lee JK, Park SC, Shin SC, Kim SU. 2009. Regulation of resin acid synthesis in Pinus densiflora by differential transcription of genes encoding multiple 1-deoxy-d-xylulose 5-phosphate synthase and 1-hydroxy-2-methyl-2-(e)-butenyl 4-diphosphate reductase genes. Tree Physiology 29: 737-749.
34. Kim SM, Kuzuyama T, Kobayashi A, Sando T, Chang YJ, Kim SU. 2008. 1-hydroxy-2-methyl-2-(e)-butenyl 4-diphosphate reductase (IDS) is encoded by multicopy genes in gymnosperms Ginkgo biloba and Pinus taeda. Planta 227: 287-298.
35. Kopper BJ, Illman BL, Kersten PJ, Klepzig KD, Raffa KF. 2005. Effects of diterpene acids on components of a conifer bark beetle-fungal interaction: tolerance by Ips pini and sensitivity by its associate Ophiostoma ips. Environmental Entomology 34: 486-493.
36. Kurz WA, Dymond CC, Stinson G, Rampley GJ, Neilson ET, Carroll AL, Ebata T, Safranyik L. 2008. Mountain pine beetle and forest carbon feedback to climate change. Nature 452: 987-990.
37. Leonard E, Ajikumar PK, Thayer K, Xiao WH, Mo JD, Tidor B, Stephanopoulos G, Prather KLJ. 2010. Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control. Proceedings of the National Academy of Sciences, USA 107: 13654-13659.
38. Li Z, Gopal V, Li X, Davis JM, Casella G. 2012. Simultaneous SNP identification in association studies with missing data. Annals of Applied Statistics 6: 432-456.
39. Lorio PL. 1986. Growth-differentiation balance - a basis for understanding southern pine-beetle tree interactions. Forest Ecology and Management 14: 259-273.
40. Lorio PL, Sommers RA. 1986. Evidence of competition for photosynthates between growth processes and oleoresin synthesis in Pinus taeda L. Tree Physiology 2: 301-306.
41. van Mantgem PJ, Stephenson NL, Byrne JC, Daniels LD, Franklin JF, Fule PZ, Harmon ME, Larson AJ, Smith JM, Taylor AH et al. 2009. Widespread increase of tree mortality rates in the western United States. Science 323: 521-524.
42. Meuwissen THE, Hayes BJ, Goddard ME. 2001. Prediction of total genetic value using genome-wide dense marker maps. Genetics 157: 1819-1829.
43. Moreno JE, Tao Y, Chory J, Ballare CL. 2009. Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. Proceedings of the National Academy of Sciences, USA 106: 4935-4940.
44. Munoz PR, Resende MFR, Huber DA, Quesada T, Resende MDV, Neale DB, Wegrzyn JL, Kirst M, Peter GF. 2013. Genomic relationship matrix for correcting pedigree errors in breeding populations: impact on genetic parameters and genomic selection accuracy. Crop Science, in press.
45. Nicotra AB, Atkin OK, Bonser SP, Davidson AM, Finnegan EJ, Mathesius U, Poot P, Purugganan MD, Richards CL, Valladares F et al. 2010. Plant phenotypic plasticity in a changing climate. Trends in Plant Science 15: 684-692.
46. Nowak J, Asaro C, Klepzig K, Billings R. 2008. The southern pine beetle prevention initiative: working for healthier forests. Journal of Forestry 106: 261-267.
47. Ogawa T, Uchimiya H, Kawai-Yamada M. 2007. Mutual regulation of Arabidopsis thaliana ethylene-responsive element binding protein and a plant floral homeotic gene, APETELA2. Annals of Botany 99: 239-244.
48. Paine TD, Raffa KF, Harrington TC. 1997. Interactions among scolytid bark beetles, their associated fungi, and live host conifers. Annual Review of Entomology 42: 179-206.
49. Patterson HD, Williams ER. 1976. New class of resolvable incomplete block designs. Biometrika 63: 83-92.
50. Peralta-Yahya PP, Keasling JD. 2010. Advanced biofuel production in microbes. Biotechnology Journal 5: 147-162.
51. Peralta-Yahya PP, Ouellet M, Chan R, Mukhopadhyay A, Keasling JD, Lee TS. 2011. Identification and microbial production of a terpene-based advanced biofuel. Nature Communications 2: 1-8.
52. Phillips MA, Croteau RB. 1999. Resin-based defenses in conifers. Trends in Plant Science 4: 184-190.
53. Pritchard JK, Stephens M, Rosenberg NA, Donnelly P. 2000. Association mapping in structured populations. American Journal of Human Genetics 67: 170-181.
54. R Core Team. 2012. R: a language and environment for statistical computing. Vienna, Austria. [WWW document] URL http://www.R-project.org/ [accessed on 31 December 2011].
55. Raffa KF, Aukema BH, Bentz BJ, Carroll AL, Hicke JA, Turner MG, Romme WH. 2008. Cross-scale drivers of natural disturbances prone to anthropogenic amplification: the dynamics of bark beetle eruptions. BioScience 58: 501-517.
56. Resende MFR, Munoz P, Acosta JJ, Peter GF, Davis JM, Grattapaglia D, Resende MDV, Kirst M. 2012a. Accelerating the domestication of trees using genomic selection: accuracy of prediction models across ages and environments. New Phytologist 193: 617-624.
57. Resende MFR, Munoz P, Resende MDV, Garrick DJ, Fernando RL, Davis JM, Jokela EJ, Martin TA, Peter GF, Kirst M. 2012b. Accuracy of genomic selection methods in a standard data set of loblolly pine (Pinus taeda L.). Genetics 190: 1503-1510.
58. Ro DK, Arimura GL, Lau SYW, Piers E, Bohlmann J. 2005. Loblolly pine abietadienol/abietadienal oxidase ptao (cyp720b1) is a multifunctional, multisubstrate cytochrome P450 monooxygenase. Proceedings of the National Academy of Sciences, USA 102: 8060-8065.
59. Roberds JH, Strom BL, Hain FP, Gwaze DP, McKeand SE, Lott LH. 2003. Estimates of genetic parameters for oleoresin and growth traits in juvenile loblolly pine. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 33: 2469-2476.
60. Rodriguez-Concepcion M, Boronat A. 2002. Elucidation of the methylerythritol phosphate pathway for isoprenoid biosynthesis in bacteria and plastids. A metabolic milestone achieved through genomics. Plant Physiology 130: 1079-1089.
61. Romanelli RC, Sebbenn AM. 2004. Genetic parameters and selection gains for oleoresin production in Pinus elliottii var. elliottii, in south of São Paulo state. Revista do Instituto Florestal 16: 11-23.
62. Schmidt A, Gershenzon J. 2008. Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies). Phytochemistry 69: 49-57.
63. Schmidt A, Nagel R, Krekling T, Christiansen E, Gershenzon J, Krokene P. 2011. Induction of isoprenyl diphosphate synthases, plant hormones and defense signalling genes correlates with traumatic resin duct formation in Norway spruce (Picea abies). Plant Molecular Biology 77: 577-590.
64. Schulz-Streeck T, Ogutu JO, Piepho HP. 2011. Preselection of markers for genomic selection. BMC Proceedings 5(Suppl 3): S12.
65. Squillace AE, Bengtson GW. 1961. Inheritance of gum yield and other characteristics of slash pine. In: Proceedings of the Sixth Southern Conference on Forest Tree Improvement. Gainesville, FL: School of Forestry, University of Florida, 85-96.
66. Strom BL, Goyer RA, Ingram LL, Boyd GDL, Lott LH. 2002. Oleoresin characteristics of progeny of loblolly pines that escaped attack by southern pine beetle. Forest Ecology and Management 158: 169-178.
67. Stubbs J, Roberts DR, Outcalt KW. 1984. Chemical stimulation of lightwood in Southern pines. In: General Technical Report SE-25, Asheville, NC, USA: US Forest Service, 1-50.
68. Telewski FW, Wakefield AH, Jaffe MJ. 1983. Computer-assisted image-analysis of tissues of ethrel-treated Pinus taeda seedlings. Plant Physiology 72: 177-181.
69. Trapp S, Croteau R. 2001. Defensive resin biosynthesis in conifers. Annual Review of Plant Physiology and Plant Molecular Biology 52: 689-724.
70. Visscher PM, Medland SE, Ferreira MAR, Morley KI, Zhu G, Cornes BK, Montgomery GW, Martin NG. 2006. Assumption-free estimation of heritability from genome-wide identity-by-descent sharing between full siblings. PLOS Genetics 2: 316-325.
71. Wallin KF, Kolb TE, Skov KR, Wagner M. 2008. Forest management treatments, tree resistance, and bark beetle resource utilization in ponderosa pine forests of northern Arizona. Forest Ecology and Management 255: 3263-3269.
72. Wang Y, Lim L, Robertson G, Bohlmann J, Breuil C. 2013. A specialized ABC efflux transporter GcABC-G1 confers monoterpene resistance to Grosmannia clavigera, a bark beetle-associated fungal pathogen of pine trees. New Phytologist 197: 886-898.
73. Waring KM, Reboletti DM, Mork LA, Huang CH, Hofstetter RW, Garcia AM, Fule PZ, Davis TS. 2009. Modeling the impacts of two bark beetle species under a warming climate in the southwestern USA: ecological and economic consequences. Environmental Management 44: 824-835.
74. White TL, Carson M. 2004. Breeding program of conifers. In: Walter C, Carson M, eds. Plantation forest biotechnology for the 21st century. Research Signpost, 61-85.
75. Wolter KE, Zinkel DF. 1984. Observations on the physiological-mechanisms and chemical-constituents of induced oleoresin synthesis in Pinus resinosa. Canadian Journal of Forest Research-Revue Canadienne De Recherche Forestiere 14: 452-458.
76. Yang JA, Benyamin B, McEvoy BP, Gordon S, Henders AK, Nyholt DR, Madden PA, Heath AC, Martin NG, Montgomery GW et al. 2010. Common SNPs explain a large proportion of the heritability for human height. Nature Genetics 42: 565-569.
77. Zeller SL, Kalinina O, Brunner S, Keller B, Schmid B. 2010. Transgene x environment interactions in genetically modified wheat. PLoS ONE 5: 7.
78. Zulak KG, Bohlmann J. 2010. Terpenoid biosynthesis and specialized vascular cells of conifer defense. Journal of Integrative Plant Biology 52: 86-97.