High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus
Abstract
Summary Terpenoid‐based essential oils are economically important commodities, yet beyond their biosynthetic pathways, little is known about the genetic architecture of terpene oil yield from plants. Transport, storage, evaporative loss, transcriptional regulation and precursor competition may be important contributors to this complex trait. Here, we associate 2.39 million single nucleotide polymorphisms derived from shallow whole‐genome sequencing of 468 Eucalyptus polybractea individuals with 12 traits related to the overall terpene yield, eight direct measures of terpene concentration and four biomass‐related traits. Our results show that in addition to terpene biosynthesis, development of secretory cavities, where terpenes are both synthesized and stored, and transport of terpenes were important components of terpene yield. For sesquiterpene concentrations, the availability of precursors in the cytosol was important. Candidate terpene synthase genes for the production of 1,8‐cineole and α‐pinene, and β‐pinene (which comprised > 80% of the total terpenes) were functionally characterized as a 1,8‐cineole synthase and a β/α‐pinene synthase. Our results provide novel insights into the genomic architecture of terpene yield and we provide candidate genes for breeding or engineering of crops for biofuels or the production of industrially valuable terpenes.
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States); The Australian National Univ., Canberra, ACT (Australia)
- The Australian National Univ., Canberra, ACT (Australia); Michigan Technological Univ., Houghton, MI (United States)
- The Australian National Univ., Canberra, ACT (Australia)
- The Australian National Univ., Canberra, ACT (Australia); CSIRO, Canberra, ACT (Australia)
- Martin-Luther Univ. Halle-Wittenberg, Halle (Saale) (Germany)
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE
- OSTI Identifier:
- 1542234
- Alternate Identifier(s):
- OSTI ID: 1560214
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- New Phytologist
- Additional Journal Information:
- Journal Volume: 223; Journal Issue: 3; Journal ID: ISSN 0028-646X
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; 1,8‐cineole; essential oil; eucalypt; genome‐wide association study (GWAS); pinene; terpene oil yield; terpene synthase; terpenes
Citation Formats
Kainer, David, Külheim, Carsten, Foley, William J., Padovan, Amanda, Degenhardt, Joerg, Krause, Sandra, and Mondal, Prodyut. High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus. United States: N. p., 2019.
Web. doi:10.1111/nph.15887.
Kainer, David, Külheim, Carsten, Foley, William J., Padovan, Amanda, Degenhardt, Joerg, Krause, Sandra, & Mondal, Prodyut. High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus. United States. https://doi.org/10.1111/nph.15887
Kainer, David, Külheim, Carsten, Foley, William J., Padovan, Amanda, Degenhardt, Joerg, Krause, Sandra, and Mondal, Prodyut. Tue .
"High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus". United States. https://doi.org/10.1111/nph.15887. https://www.osti.gov/servlets/purl/1542234.
@article{osti_1542234,
title = {High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus},
author = {Kainer, David and Külheim, Carsten and Foley, William J. and Padovan, Amanda and Degenhardt, Joerg and Krause, Sandra and Mondal, Prodyut},
abstractNote = {Summary Terpenoid‐based essential oils are economically important commodities, yet beyond their biosynthetic pathways, little is known about the genetic architecture of terpene oil yield from plants. Transport, storage, evaporative loss, transcriptional regulation and precursor competition may be important contributors to this complex trait. Here, we associate 2.39 million single nucleotide polymorphisms derived from shallow whole‐genome sequencing of 468 Eucalyptus polybractea individuals with 12 traits related to the overall terpene yield, eight direct measures of terpene concentration and four biomass‐related traits. Our results show that in addition to terpene biosynthesis, development of secretory cavities, where terpenes are both synthesized and stored, and transport of terpenes were important components of terpene yield. For sesquiterpene concentrations, the availability of precursors in the cytosol was important. Candidate terpene synthase genes for the production of 1,8‐cineole and α‐pinene, and β‐pinene (which comprised > 80% of the total terpenes) were functionally characterized as a 1,8‐cineole synthase and a β/α‐pinene synthase. Our results provide novel insights into the genomic architecture of terpene yield and we provide candidate genes for breeding or engineering of crops for biofuels or the production of industrially valuable terpenes.},
doi = {10.1111/nph.15887},
journal = {New Phytologist},
number = 3,
volume = 223,
place = {United States},
year = {Tue May 07 00:00:00 EDT 2019},
month = {Tue May 07 00:00:00 EDT 2019}
}
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Works referenced in this record:
Methylerythritol 4-phosphate (MEP) pathway metabolic regulation
journal, January 2014
- Banerjee, A.; Sharkey, T. D.
- Nat. Prod. Rep., Vol. 31, Issue 8
High-resolution genetic maps of Eucalyptus improve Eucalyptus grandis genome assembly
journal, November 2014
- Bartholomé, Jérôme; Mandrou, Eric; Mabiala, André
- New Phytologist, Vol. 206, Issue 4
The Oil Mallee Project: A Multifaceted Industrial Ecology Case Study
journal, March 1999
- Barton, Allan
- Journal of Industrial Ecology, Vol. 3, Issue 2-3
Terpenoid biomaterials
journal, May 2008
- Bohlmann, Jörg; Keeling, Christopher I.
- The Plant Journal, Vol. 54, Issue 4
Intraspecific variation in leaf oils of Melaleuca alternifolia (Myrtaceae)
journal, June 1994
- Butcher, Penelope A.; Doran, John C.; Slee, Michael U.
- Biochemical Systematics and Ecology, Vol. 22, Issue 4
Impacts of Population Structure and Analytical Models in Genome-Wide Association Studies of Complex Traits in Forest Trees: A Case Study in Eucalyptus globulus
journal, November 2013
- Cappa, Eduardo P.; El-Kassaby, Yousry A.; Garcia, Martín N.
- PLoS ONE, Vol. 8, Issue 11
Discovery of New Biocatalysts for the Glycosylation of Terpenoid Scaffolds
journal, July 2008
- Caputi, Lorenzo; Lim, Eng-Kiat; Bowles, Dianna J.
- Chemistry - A European Journal, Vol. 14, Issue 22
Second-generation PLINK: rising to the challenge of larger and richer datasets
journal, February 2015
- Chang, Christopher C.; Chow, Carson C.; Tellier, Laurent CAM
- GigaScience, Vol. 4, Issue 1
Characterization of a Root-Specific Arabidopsis Terpene Synthase Responsible for the Formation of the Volatile Monoterpene 1,8-Cineole
journal, August 2004
- Chen, Feng; Ro, Dae-Kyun; Petri, Jana
- Plant Physiology, Vol. 135, Issue 4
Model-free Estimation of Recent Genetic Relatedness
journal, January 2016
- Conomos, Matthew P.; Reiner, Alexander P.; Weir, Bruce S.
- The American Journal of Human Genetics, Vol. 98, Issue 1
Toward a photosynthetic microbial platform for terpenoid engineering
journal, February 2014
- Davies, Fiona K.; Jinkerson, Robert E.; Posewitz, Matthew C.
- Photosynthesis Research, Vol. 123, Issue 3
A framework for variation discovery and genotyping using next-generation DNA sequencing data
journal, April 2011
- DePristo, Mark A.; Banks, Eric; Poplin, Ryan
- Nature Genetics, Vol. 43, Issue 5
FLEXBAR—Flexible Barcode and Adapter Processing for Next-Generation Sequencing Platforms
journal, December 2012
- Dodt, Matthias; Roehr, Johannes; Ahmed, Rina
- Biology, Vol. 1, Issue 3
Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
journal, August 2014
- Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
- Nature Genetics, Vol. 46, Issue 10
Phylogenetic approaches reveal biodiversity threats under climate change
journal, September 2016
- González-Orozco, Carlos E.; Pollock, Laura J.; Thornhill, Andrew H.
- Nature Climate Change, Vol. 6, Issue 12
Foliar Essential Oil Glands of Eucalyptus Subgenus Eucalyptus (Myrtaceae) Are a Rich Source of Flavonoids and Related Non-Volatile Constituents
journal, March 2016
- Goodger, Jason Q. D.; Seneratne, Samiddhi L.; Nicolle, Dean
- PLOS ONE, Vol. 11, Issue 3
Genetic determinants of oil yield in Eucalyptus polybractea R.T. Baker
journal, July 2012
- Goodger, Jason Q. D.; Woodrow, Ian E.
- Trees, Vol. 26, Issue 6
Cytochrome P450 mono-oxygenases in conifer genomes: discovery of members of the terpenoid oxygenase superfamily in spruce and pine
journal, October 2006
- Hamberger, B.; Bohlmann, J.
- Biochemical Society Transactions, Vol. 34, Issue 6
Post-translational events and modifications regulating plant enzymes involved in isoprenoid precursor biosynthesis
journal, April 2013
- Hemmerlin, Andréa
- Plant Science, Vol. 203-204
Identification of quantitative trait loci influencing foliar concentrations of terpenes and formylated phloroglucinol compounds in Eucalyptus nitens
journal, October 2007
- Henery, Martin L.; Moran, Gavin F.; Wallis, Ian R.
- New Phytologist, Vol. 176, Issue 1
Development of schizogenous intercellular spaces in plants
journal, July 2015
- Ishizaki, Kimitsune
- Frontiers in Plant Science, Vol. 6
An efficient and scalable analysis framework for variant extraction and refinement from population-scale DNA sequence data
journal, April 2015
- Jun, Goo; Wing, Mary Kate; Abecasis, Gonçalo R.
- Genome Research, Vol. 25, Issue 6
Assessment of a non-destructive method to predict oil yield in Eucalyptus polybractea (blue mallee)
journal, August 2017
- Kainer, David; Bush, David; Foley, William J.
- Industrial Crops and Products, Vol. 102
Accuracy of Genomic Prediction for Foliar Terpene Traits in Eucalyptus polybractea
journal, June 2018
- Kainer, David; Stone, Eric A.; Padovan, Amanda
- G3: Genes|Genomes|Genetics, Vol. 8, Issue 8
Temporal regulation of terpene synthase gene expression in Eucalyptus globulus leaves upon ozone and wounding stresses: relationships with stomatal ozone uptake and emission responses
journal, November 2018
- Kanagendran, Arooran; Pazouki, Leila; Bichele, Rudolf
- Environmental and Experimental Botany, Vol. 155
Beyond six scents: defining a seventh Thymus vulgaris chemotype new to southern France by ethanol extraction
journal, May 2009
- Keefover-Ring, Ken; Thompson, John D.; Linhart, Yan B.
- Flavour and Fragrance Journal, Vol. 24, Issue 3
A molecular perspective on terpene variation in Australian Myrtaceae
journal, January 2008
- Keszei, Andras; Brubaker, Curt L.; Foley, William. J.
- Australian Journal of Botany, Vol. 56, Issue 3
Terpene deployment in Eucalyptus polybractea; relationships with leafstructure, environmental stresses, and growth
journal, January 2004
- King, Drew J.; Gleadow, Roslyn M.; Woodrow, Ian E.
- Functional Plant Biology, Vol. 31, Issue 5
The accumulation of terpenoid oils does not incur a growth cost in Eucalyptus polybractea seedlings
journal, January 2006
- King, Drew J.; Gleadow, Roslyn M.; Woodrow, Ian E.
- Functional Plant Biology, Vol. 33, Issue 5
Characterization of two functional phosphoenolpyruvate/phosphate translocator (PPT) genes in Arabidopsis-AtPPT1 may be involved in the provision of signals for correct mesophyll development
journal, November 2003
- Knappe, Silke; Lottgert, Tanja; Schneider, Anja
- The Plant Journal, Vol. 36, Issue 3
ANGSD: Analysis of Next Generation Sequencing Data
journal, November 2014
- Korneliussen, Thorfinn Sand; Albrechtsen, Anders; Nielsen, Rasmus
- BMC Bioinformatics, Vol. 15, Issue 1
The Eucalyptus terpene synthase gene family
journal, June 2015
- Külheim, Carsten; Padovan, Amanda; Hefer, Charles
- BMC Genomics, Vol. 16, Issue 1
Comparative SNP diversity among four Eucalyptus species for genes from secondary metabolite biosynthetic pathways
journal, January 2009
- Külheim, Carsten; Hui Yeoh, Suat; Maintz, Jens
- BMC Genomics, Vol. 10, Issue 1
The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus
journal, May 2011
- Külheim, Carsten; Yeoh, Suat Hui; Wallis, Ian R.
- New Phytologist, Vol. 191, Issue 4
Isoprenoid biosynthesis: The evolution of two ancient and distinct pathways across genomes
journal, November 2000
- Lange, B. M.; Rujan, T.; Martin, W.
- Proceedings of the National Academy of Sciences, Vol. 97, Issue 24
Fast and accurate short read alignment with Burrows-Wheeler transform
journal, May 2009
- Li, H.; Durbin, R.
- Bioinformatics, Vol. 25, Issue 14
The Sequence Alignment/Map format and SAMtools
journal, June 2009
- Li, H.; Handsaker, B.; Wysoker, A.
- Bioinformatics, Vol. 25, Issue 16
Low-coverage sequencing: Implications for design of complex trait association studies
journal, April 2011
- Li, Y.; Sidore, C.; Kang, H. M.
- Genome Research, Vol. 21, Issue 6
The 1-Deoxy-D-Xylulose-5-Phosphate Pathway of Isoprenoid Biosynthesis in Plants
journal, June 1999
- Lichtenthaler, Hartmut K.
- Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 50, Issue 1
Intracellular Metabolite Transporters in Plants
journal, January 2010
- Linka, Nicole; Weber, Andreas P. M.
- Molecular Plant, Vol. 3, Issue 1
The relationship between isoprene emission rate and dark respiration rate in white poplar (Populus alba L.) leaves
journal, May 2007
- Loreto, Francesco; Centritto, Mauro; Barta, Csengele
- Plant, Cell & Environment, Vol. 30, Issue 5
Nucleotide diversity and linkage disequilibrium in Populus nigra cinnamyl alcohol dehydrogenase (CAD4) gene
journal, April 2011
- Marroni, Fabio; Pinosio, Sara; Zaina, Giusi
- Tree Genetics & Genomes, Vol. 7, Issue 5
Genome-wide association implicates numerous genes underlying ecological trait variation in natural populations of Populus trichocarpa
journal, April 2014
- McKown, Athena D.; Klápště, Jaroslav; Guy, Robert D.
- New Phytologist, Vol. 203, Issue 2
Plant-Derived Terpenes: A Feedstock for Specialty Biofuels
journal, March 2017
- Mewalal, Ritesh; Rai, Durgesh K.; Kainer, David
- Trends in Biotechnology, Vol. 35, Issue 3
Efficient conversion of pure and mixed terpene feedstocks to high density fuels
journal, July 2012
- Meylemans, Heather A.; Quintana, Roxanne L.; Harvey, Benjamin G.
- Fuel, Vol. 97
Independent and Joint‐ GWAS for growth traits in Eucalyptus by assembling genome‐wide data for 3373 individuals across four breeding populations
journal, September 2018
- Müller, Bárbara S. F.; de Almeida Filho, Janeo E.; Lima, Bruno M.
- New Phytologist, Vol. 221, Issue 2
The genome of Eucalyptus grandis
journal, June 2014
- Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A.
- Nature, Vol. 510, Issue 7505
Quantitative trait loci for foliar terpenes in a global eucalypt species
journal, November 2010
- O’Reilly-Wapstra, Julianne M.; Freeman, Jules S.; Davies, Noel W.
- Tree Genetics & Genomes, Vol. 7, Issue 3
The evolution of foliar terpene diversity in Myrtaceae
journal, October 2013
- Padovan, Amanda; Keszei, András; Külheim, Carsten
- Phytochemistry Reviews, Vol. 13, Issue 3
Association genetics of essential oil traits in Eucalyptus loxophleba: explaining variation in oil yield
journal, May 2017
- Padovan, Amanda; Webb, Hamish; Mazanec, Richard
- Molecular Breeding, Vol. 37, Issue 6
Essential Oil Quantity and Composition from 10 Cultivars of Organically Grown Lavender and Lavandin
journal, July 2001
- Renaud, Erica N. C.; Charles, Denys J.; Simon, James E.
- Journal of Essential Oil Research, Vol. 13, Issue 4
Regional heritability mapping and genome-wide association identify loci for complex growth, wood and disease resistance traits in Eucalyptus
journal, November 2016
- Resende, Rafael Tassinari; Resende, Marcos Deon Vilela; Silva, Fabyano Fonseca
- New Phytologist, Vol. 213, Issue 3
Enzymatic glycosylation of terpenoids
journal, April 2013
- Rivas, Francisco; Parra, Andres; Martinez, Antonio
- Phytochemistry Reviews, Vol. 12, Issue 2
Cost-effective, high-throughput DNA sequencing libraries for multiplexed target capture
journal, January 2012
- Rohland, N.; Reich, D.
- Genome Research, Vol. 22, Issue 5
Terpene glucoside production: Improved biocatalytic processes using glycosyltransferases
journal, February 2015
- Schwab, Wilfried; Fischer, Thilo; Wüst, Matthias
- Engineering in Life Sciences, Vol. 15, Issue 4
Biotransformation of thymol, carvacrol, and eugenol by cultured cells of Eucalyptus perriniana
journal, October 2006
- Shimoda, Kei; Kondo, Yoko; Nishida, Tomohisa
- Phytochemistry, Vol. 67, Issue 20
A flexible multi-species genome-wide 60K SNP chip developed from pooled resequencing of 240 Eucalyptus tree genomes across 12 species
journal, February 2015
- Silva-Junior, Orzenil B.; Faria, Danielle A.; Grattapaglia, Dario
- New Phytologist, Vol. 206, Issue 4
A Unified Framework for Association Analysis with Multiple Related Phenotypes
journal, July 2013
- Stephens, Matthew
- PLoS ONE, Vol. 8, Issue 7
The Phosphoenolpyruvate/Phosphate Translocator Is Required for Phenolic Metabolism, Palisade Cell Development, and Plastid-Dependent Nuclear Gene Expression
journal, September 1999
- Streatfield, Stephen J.; Weber, Andreas; Kinsman, Elizabeth A.
- The Plant Cell, Vol. 11, Issue 9
Dissection of complex traits in forest trees — opportunities for marker-assisted selection
journal, February 2013
- Thavamanikumar, Saravanan; Southerton, Simon G.; Bossinger, Gerd
- Tree Genetics & Genomes, Vol. 9, Issue 3
Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny
journal, December 2015
- Thornhill, Andrew H.; Ho, Simon Y. W.; Külheim, Carsten
- Molecular Phylogenetics and Evolution, Vol. 93
Demonstration of Genome-Wide Association Studies for Identifying Markers for Wood Property and Male Strobili Traits in Cryptomeria japonica
journal, November 2013
- Uchiyama, Kentaro; Iwata, Hiroyoshi; Moriguchi, Yoshinari
- PLoS ONE, Vol. 8, Issue 11
Metabolic engineering of volatile isoprenoids in plants and microbes: Exploiting volatile isoprenoids for biotechnology
journal, May 2014
- Vickers, Claudia E.; Bongers, Mareike; Liu, Qing
- Plant, Cell & Environment, Vol. 37, Issue 8
10 Years of GWAS Discovery: Biology, Function, and Translation
journal, July 2017
- Visscher, Peter M.; Wray, Naomi R.; Zhang, Qian
- The American Journal of Human Genetics, Vol. 101, Issue 1
Network Analysis of the MVA and MEP Pathways for Isoprenoid Synthesis
journal, April 2013
- Vranová, Eva; Coman, Diana; Gruissem, Wilhelm
- Annual Review of Plant Biology, Vol. 64, Issue 1
The genetic basis of foliar terpene yield: Implications for breeding and profitability of Australian essential oil crops
journal, January 2015
- Webb, Hamish; Foley, William J.; Külheim, Carsten
- Plant Biotechnology, Vol. 31, Issue 5
The Yield of Essential Oils in Melaleuca alternifolia (Myrtaceae) Is Regulated through Transcript Abundance of Genes in the MEP Pathway
journal, March 2013
- Webb, Hamish; Lanfear, Robert; Hamill, John
- PLoS ONE, Vol. 8, Issue 3
Emissions of isoprene, monoterpene and short-chained carbonyl compounds from Eucalyptus spp. in southern Australia
journal, June 2009
- Winters, Anthony J.; Adams, Mark A.; Bleby, Tim M.
- Atmospheric Environment, Vol. 43, Issue 19
Monoterpene Synthases from Common Sage ( Salvia officinalis ) : cDNA ISOLATION, CHARACTERIZATION, AND FUNCTIONAL EXPRESSION OF (+)-SABINENE SYNTHASE, 1,8-CINEOLE SYNTHASE, AND (+)-BORNYL DIPHOSPHATE SYNTHASE
journal, June 1998
- Wise, Mitchell L.; Savage, Thomas J.; Katahira, Eva
- Journal of Biological Chemistry, Vol. 273, Issue 24
GCTA: A Tool for Genome-wide Complex Trait Analysis
journal, January 2011
- Yang, Jian; Lee, S. Hong; Goddard, Michael E.
- The American Journal of Human Genetics, Vol. 88, Issue 1
A high-performance computing toolset for relatedness and principal component analysis of SNP data
journal, October 2012
- Zheng, X.; Levine, D.; Shen, J.
- Bioinformatics, Vol. 28, Issue 24
Identification of deleterious recessive haplotypes and candidate deleterious recessive mutations in Japanese Black cattle
journal, March 2021
- Sasaki, Shinji; Watanabe, Toshio; Ibi, Takayuki
- Scientific Reports, Vol. 11, Issue 1
The Eucalyptus terpene synthase gene family
text, January 2015
- Külheim, Carsten; Padovan, Amanda; Hefer, Charles
- BioMed Central
Low-coverage sequencing: Implications for design of complex trait association studies
text, January 2011
- M., Boehnke,; M., Kang, H.; Y., Li,
- The University of North Carolina at Chapel Hill University Libraries
The Phosphoenolpyruvate/Phosphate Translocator Is Required for Phenolic Metabolism, Palisade Cell Development, and Plastid-Dependent Nuclear Gene Expression
journal, September 1999
- Streatfield, Stephen J.; Weber, Andreas; Kinsman, Elizabeth A.
- The Plant Cell, Vol. 11, Issue 9
Second-generation PLINK: rising to the challenge of larger and richer datasets
text, January 2014
- Chang, Christopher C.; Chow, Carson C.; Tellier, Laurent C. A. M.
- arXiv
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