skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus

Abstract

Terpenes are economically and ecologically important phytochemicals. Their synthesis is controlled by the terpene synthase (TPS) gene family, which is highly diversified throughout the plant kingdom. The plant family Myrtaceae are characterised by especially high terpene concentrations, and considerable variation in terpene profiles. Many Myrtaceae are grown commercially for terpene products including the eucalypts Corymbia and Eucalyptus. Eucalyptus grandis has the largest TPS gene family of plants currently sequenced, which is largely conserved in the closely related E. globulus. However, the TPS gene family has been well studied only in these two eucalypt species. The recent assembly of two Corymbia citriodora subsp. variegata genomes presents an opportunity to examine the conservation of this important gene family across more divergent eucalypt lineages. Manual annotation of the TPS gene family in C. citriodora subsp. variegata revealed a similar overall number, and relative subfamily representation, to that previously reported in E. grandis and E. globulus. Many of the TPS genes were in physical clusters that varied considerably between Eucalyptus and Corymbia, with several instances of translocation, expansion/contraction and loss. Notably, there was greater conservation in the subfamilies involved in primary metabolism than those involved in secondary metabolism, likely reflecting different selective constraints. Themore » variation in cluster size within subfamilies and the broad conservation between the eucalypts in the face of this variation are discussed, highlighting the potential contribution of selection, concerted evolution and stochastic processes. These findings provide the foundation to better understand terpene evolution within the ecologically and economically important Myrtaceae.« less

Authors:
ORCiD logo [1];  [1]; ORCiD logo [1];  [1];  [2];  [2];  [3];  [3];  [4];  [5];  [6]; ORCiD logo [7];  [8]; ORCiD logo [8]; ORCiD logo [8]
  1. School of Natural Sciences, University of Tasmania, Hobart, TAS, 7001, Australia
  2. EMBRAPA Genetic Resources and Biotechnology, EPqB Final W5 Norte, Brasilia, 70770-917, Brazil
  3. DOE Joint Bioenergy Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, United States
  4. Hudson-Alpha Institute for Biotechnology, Huntsville, AL, United States
  5. DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, CA, United States
  6. Forest Industries Research Centre, University of the Sunshine Coast, Maroochydore DC, QLD, 4558, Australia
  7. University of Queensland/QAAFI, Brisbane, QLD, 4072, Australia
  8. Southern Cross Plant Science, Southern Cross University, Lismore, NSW, 2480, Australia
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1543741
DOE Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article
Journal Name:
Heredity
Additional Journal Information:
Journal Volume: 121; Journal Issue: 1; Journal ID: ISSN 0018-067X
Country of Publication:
United States
Language:
English
Subject:
Environmental Sciences & Ecology; Evolutionary Biology; Genetics & Heredity

Citation Formats

Butler, Jakob B., Freeman, Jules S., Potts, Brad M., Vaillancourt, René E., Grattapaglia, Dario, Silva-Junior, Orzenil B., Simmons, Blake A., Healey, Adam L., Schmutz, Jeremy, Barry, Kerrie W., Lee, David J., Henry, Robert J., King, Graham J., Baten, Abdul, and Shepherd, Mervyn. Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus. United States: N. p., 2018. Web. doi:10.1038/s41437-018-0058-1.
Butler, Jakob B., Freeman, Jules S., Potts, Brad M., Vaillancourt, René E., Grattapaglia, Dario, Silva-Junior, Orzenil B., Simmons, Blake A., Healey, Adam L., Schmutz, Jeremy, Barry, Kerrie W., Lee, David J., Henry, Robert J., King, Graham J., Baten, Abdul, & Shepherd, Mervyn. Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus. United States. doi:10.1038/s41437-018-0058-1.
Butler, Jakob B., Freeman, Jules S., Potts, Brad M., Vaillancourt, René E., Grattapaglia, Dario, Silva-Junior, Orzenil B., Simmons, Blake A., Healey, Adam L., Schmutz, Jeremy, Barry, Kerrie W., Lee, David J., Henry, Robert J., King, Graham J., Baten, Abdul, and Shepherd, Mervyn. Sat . "Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus". United States. doi:10.1038/s41437-018-0058-1.
@article{osti_1543741,
title = {Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus},
author = {Butler, Jakob B. and Freeman, Jules S. and Potts, Brad M. and Vaillancourt, René E. and Grattapaglia, Dario and Silva-Junior, Orzenil B. and Simmons, Blake A. and Healey, Adam L. and Schmutz, Jeremy and Barry, Kerrie W. and Lee, David J. and Henry, Robert J. and King, Graham J. and Baten, Abdul and Shepherd, Mervyn},
abstractNote = {Terpenes are economically and ecologically important phytochemicals. Their synthesis is controlled by the terpene synthase (TPS) gene family, which is highly diversified throughout the plant kingdom. The plant family Myrtaceae are characterised by especially high terpene concentrations, and considerable variation in terpene profiles. Many Myrtaceae are grown commercially for terpene products including the eucalypts Corymbia and Eucalyptus. Eucalyptus grandis has the largest TPS gene family of plants currently sequenced, which is largely conserved in the closely related E. globulus. However, the TPS gene family has been well studied only in these two eucalypt species. The recent assembly of two Corymbia citriodora subsp. variegata genomes presents an opportunity to examine the conservation of this important gene family across more divergent eucalypt lineages. Manual annotation of the TPS gene family in C. citriodora subsp. variegata revealed a similar overall number, and relative subfamily representation, to that previously reported in E. grandis and E. globulus. Many of the TPS genes were in physical clusters that varied considerably between Eucalyptus and Corymbia, with several instances of translocation, expansion/contraction and loss. Notably, there was greater conservation in the subfamilies involved in primary metabolism than those involved in secondary metabolism, likely reflecting different selective constraints. The variation in cluster size within subfamilies and the broad conservation between the eucalypts in the face of this variation are discussed, highlighting the potential contribution of selection, concerted evolution and stochastic processes. These findings provide the foundation to better understand terpene evolution within the ecologically and economically important Myrtaceae.},
doi = {10.1038/s41437-018-0058-1},
journal = {Heredity},
issn = {0018-067X},
number = 1,
volume = 121,
place = {United States},
year = {2018},
month = {3}
}

Works referenced in this record:

Terpenoid Metabolism in Wild-Type and Transgenic Arabidopsis Plants
journal, November 2003

  • Aharoni, Asaph; Giri, Ashok P.; Deuerlein, Stephan
  • The Plant Cell, Vol. 15, Issue 12
  • DOI: 10.1105/tpc.016253

Rapid and accurate determination of terpenes in the leaves of Eucalyptus species
journal, January 1985

  • Ammon, Donald G.; Barton, Allan F. M.; Clarke, Douglas A.
  • The Analyst, Vol. 110, Issue 8
  • DOI: 10.1039/an9851000921

Genomic analysis of the terpenoid synthase ( AtTPS ) gene family of Arabidopsis thaliana
journal, August 2002


Eucalyptus essential oil as a natural pesticide
journal, December 2008

  • Batish, Daizy R.; Singh, Harminder Pal; Kohli, Ravinder Kumar
  • Forest Ecology and Management, Vol. 256, Issue 12
  • DOI: 10.1016/j.foreco.2008.08.008

Using GeneWise in the Drosophila Annotation Experiment
journal, April 2000


Functional Analysis of the Early Steps of Carotenoid Biosynthesis in Tobacco
journal, February 2002

  • Busch, Marco; Seuter, Anja; Hain, Rüdiger
  • Plant Physiology, Vol. 128, Issue 2
  • DOI: 10.1104/pp.010573

Comparative genomics of Eucalyptus and Corymbia reveals low rates of genome structural rearrangement
journal, May 2017


Oil glands and ducts in Eucalyptus L'Hérit. II. Development and structure of oil glands in the embryo
journal, January 1970

  • Carr, Dj; Carr, Sgm
  • Australian Journal of Botany, Vol. 18, Issue 2
  • DOI: 10.1071/BT9700191

Dating the Monocot?Dicot Divergence and the Origin of Core Eudicots Using Whole Chloroplast Genomes
journal, April 2004

  • Chang, Chien-Chang; Chen, Hsin-Liang; Li, Wen-Hsiung
  • Journal of Molecular Evolution, Vol. 58, Issue 4
  • DOI: 10.1007/s00239-003-2564-9

Gene conversion: mechanisms, evolution and human disease
journal, September 2007

  • Chen, Jian-Min; Cooper, David N.; Chuzhanova, Nadia
  • Nature Reviews Genetics, Vol. 8, Issue 10
  • DOI: 10.1038/nrg2193

Flammable biomes dominated by eucalypts originated at the Cretaceous–Palaeogene boundary
journal, February 2011

  • Crisp, Michael D.; Burrows, Geoffrey E.; Cook, Lyn G.
  • Nature Communications, Vol. 2, Issue 1
  • DOI: 10.1038/ncomms1191

The Allelopathic Effects of Eucalyptus camaldulensis
journal, January 1970

  • del Moral, Roger; Muller, Cornelius H.
  • American Midland Naturalist, Vol. 83, Issue 1
  • DOI: 10.2307/2424020

The life and death of gene families
journal, January 2009


Essential oils from New Zealand manuka: triketone and other chemotypes of Leptospermum scoparium☆
journal, May 2004


Functional Characterization of Sesquiterpene Synthase from Polygonum minus
journal, January 2014

  • Ee, Su-Fang; Mohamed-Hussein, Zeti-Azura; Othman, Roohaida
  • The Scientific World Journal, Vol. 2014
  • DOI: 10.1155/2014/840592

NB-LRR proteins: pairs, pieces, perception, partners, and pathways
journal, August 2010


Formation of plant metabolic gene clusters within dynamic chromosomal regions
journal, August 2011

  • Field, B.; Fiston-Lavier, A. -S.; Kemen, A.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 38
  • DOI: 10.1073/pnas.1109273108

Metabolic Diversification--Independent Assembly of Operon-Like Gene Clusters in Different Plants
journal, April 2008


Gene duplication and evolutionary novelty in plants
journal, August 2009


Terpenoid synthase structures: a so far incomplete view of complex catalysis
journal, January 2012

  • Gao, Yang; Honzatko, Richard B.; Peters, Reuben J.
  • Natural Product Reports, Vol. 29, Issue 10
  • DOI: 10.1039/c2np20059g

Runaway repeats force expansion of the Phytophthora infestans genome
journal, January 2009


Contrasting ontogenetic trajectories for phenolic and terpenoid defences in Eucalyptus froggattii
journal, February 2013

  • Goodger, Jason Q. D.; Heskes, Allison M.; Woodrow, Ian E.
  • Annals of Botany, Vol. 112, Issue 4
  • DOI: 10.1093/aob/mct010

Nuclear DNA content of commercially important Eucalyptus species and hybrids
journal, May 1994

  • Grattapaglia, D.; Bradshaw Jr., H. D.
  • Canadian Journal of Forest Research, Vol. 24, Issue 5
  • DOI: 10.1139/x94-142

Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus
journal, April 2012

  • Grattapaglia, Dario; Vaillancourt, René E.; Shepherd, Merv
  • Tree Genetics & Genomes, Vol. 8, Issue 3
  • DOI: 10.1007/s11295-012-0491-x

Importance of Lineage-Specific Expansion of Plant Tandem Duplicates in the Adaptive Response to Environmental Stimuli
journal, August 2008

  • Hanada, Kousuke; Zou, Cheng; Lehti-Shiu, Melissa D.
  • Plant Physiology, Vol. 148, Issue 2
  • DOI: 10.1104/pp.108.122457

The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily
journal, February 2017

  • Hansen, Nikolaj L.; Heskes, Allison M.; Hamberger, Britta
  • The Plant Journal, Vol. 89, Issue 3
  • DOI: 10.1111/tpj.13410

Identification and functional analysis of bifunctional ent -kaurene synthase from the moss Physcomitrella patens
journal, October 2006


Systematic studies in the eucalypts. 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae) [English]
journal, December 1995


Whole Genome and Tandem Duplicate Retention Facilitated Glucosinolate Pathway Diversification in the Mustard Family
journal, October 2013

  • Hofberger, Johannes A.; Lyons, Eric; Edger, Patrick P.
  • Genome Biology and Evolution, Vol. 5, Issue 11
  • DOI: 10.1093/gbe/evt162

A Complex Interplay of Tandem- and Whole-Genome Duplication Drives Expansion of the L-Type Lectin Receptor Kinase Gene Family in the Brassicaceae
journal, January 2015

  • Hofberger, Johannes A.; Nsibo, David L.; Govers, Francine
  • Genome Biology and Evolution, Vol. 7, Issue 3
  • DOI: 10.1093/gbe/evv020

Structural Basis for Bisphosphonate-mediated Inhibition of Isoprenoid Biosynthesis
journal, December 2003

  • Hosfield, David J.; Zhang, Yanming; Dougan, Douglas R.
  • Journal of Biological Chemistry, Vol. 279, Issue 10
  • DOI: 10.1074/jbc.C300511200

Gene Duplication: The Genomic Trade in Spare Parts
journal, July 2004


Terpene synthases and their contribution to herbivore-induced volatile emission in western balsam poplar (Populus trichocarpa)
journal, October 2014


Exploring the role of copy number variants in human adaptation
journal, June 2012


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
  • DOI: 10.1071/BT07146

Gene Duplication in the Diversification of Secondary Metabolism: Tandem 2-Oxoglutarate–Dependent Dioxygenases Control Glucosinolate Biosynthesis in Arabidopsis
journal, March 2001

  • Kliebenstein, Daniel J.; Lambrix, Virginia M.; Reichelt, Michael
  • The Plant Cell, Vol. 13, Issue 3
  • DOI: 10.1105/tpc.13.3.681

Gene duplication as a mechanism of genomic adaptation to a changing environment
journal, October 2012

  • Kondrashov, Fyodor A.
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 279, Issue 1749
  • DOI: 10.1098/rspb.2012.1108

The Eucalyptus terpene synthase gene family
journal, June 2015


Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae: Australian biogeographical connections
journal, June 2003


Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials
journal, August 1998


SMS: Smart Model Selection in PhyML
journal, May 2017

  • Lefort, Vincent; Longueville, Jean-Emmanuel; Gascuel, Olivier
  • Molecular Biology and Evolution, Vol. 34, Issue 9
  • DOI: 10.1093/molbev/msx149

Comparative Genomics Analyses Reveal Extensive Chromosome Colinearity and Novel Quantitative Trait Loci in Eucalyptus
journal, December 2015


BadiRate: estimating family turnover rates by likelihood-based methods
journal, November 2011


Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N -mediated resistance to tobacco mosaic virus
journal, June 2004


The Evolutionary Fate and Consequences of Duplicate Genes
journal, November 2000


Finding and Comparing Syntenic Regions among Arabidopsis and the Outgroups Papaya, Poplar, and Grape: CoGe with Rosids
journal, October 2008

  • Lyons, Eric; Pedersen, Brent; Kane, Josh
  • Plant Physiology, Vol. 148, Issue 4
  • DOI: 10.1104/pp.108.124867

How old are the eucalypts? A review of the microfossil and phylogenetic evidence
journal, January 2016

  • Macphail, Mike; Thornhill, Andrew H.
  • Australian Journal of Botany, Vol. 64, Issue 8
  • DOI: 10.1071/BT16124

Ultrafast Approximation for Phylogenetic Bootstrap
journal, February 2013

  • Minh, B. Q.; Nguyen, M. A. T.; von Haeseler, A.
  • Molecular Biology and Evolution, Vol. 30, Issue 5
  • DOI: 10.1093/molbev/mst024

The genome of Eucalyptus grandis
journal, June 2014

  • Myburg, Alexander A.; Grattapaglia, Dario; Tuskan, Gerald A.
  • Nature, Vol. 510, Issue 7505
  • DOI: 10.1038/nature13308

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species
journal, October 2004


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
  • DOI: 10.1007/s11295-010-0350-6

The evolution of foliar terpene diversity in Myrtaceae
journal, October 2013

  • Padovan, Amanda; Keszei, András; Külheim, Carsten
  • Phytochemistry Reviews, Vol. 13, Issue 3
  • DOI: 10.1007/s11101-013-9331-3

Mosaic Eucalypt Trees Suggest Genetic Control at a Point That Influences Several Metabolic Pathways
journal, June 2012

  • Padovan, Amanda; Keszei, András; Wallis, Ian R.
  • Journal of Chemical Ecology, Vol. 38, Issue 7
  • DOI: 10.1007/s10886-012-0149-z

Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions
journal, March 2005


The formation and function of plant volatiles: perfumes for pollinator attraction and defense
journal, June 2002


Energy Product Options for Eucalyptus Species Grown as Short Rotation Woody Crops
journal, July 2008

  • Rockwood, Donald; Rudie, Alan; Ralph, Sally
  • International Journal of Molecular Sciences, Vol. 9, Issue 8
  • DOI: 10.3390/ijms9081361

Plants Utilize Isoprene Emission as a Thermotolerance Mechanism
journal, September 2007

  • Sasaki, Kanako; Saito, Takuya; Lämsä, Mari
  • Plant and Cell Physiology, Vol. 48, Issue 9
  • DOI: 10.1093/pcp/pcm104

Ultra Large Gene Families: A Matter of Adaptation or Genomic Parasites?
journal, August 2016

  • Schiffer, Philipp; Gravemeyer, Jan; Rauscher, Martina
  • Life, Vol. 6, Issue 3
  • DOI: 10.3390/life6030032

The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores
journal, January 2006

  • Schnee, C.; Kollner, T. G.; Held, M.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 4
  • DOI: 10.1073/pnas.0508027103

Transformation of terpenes into fine chemicals
journal, November 2012

  • Schwab, Wilfried; Fuchs, Christopher; Huang, Fong-Chin
  • European Journal of Lipid Science and Technology, Vol. 115, Issue 1
  • DOI: 10.1002/ejlt.201200157

Profiling the expression domains of a rice-specific microRNA under stress
journal, May 2015

  • Sharma, Neha; Tripathi, Anita; Sanan-Mishra, Neeti
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00333

Eucalypts as a biofuel feedstock
journal, November 2011

  • Shepherd, Mervyn; Bartle, John; Lee, David J.
  • Biofuels, Vol. 2, Issue 6
  • DOI: 10.4155/bfs.11.136

Isoprene Increases Thermotolerance of Isoprene-Emitting Species
journal, December 1997


The Eucalyptus grandis R2R3-MYB transcription factor family: evidence for woody growth-related evolution and function
journal, September 2014

  • Soler, Marçal; Camargo, Eduardo Leal Oliveira; Carocha, Victor
  • New Phytologist, Vol. 206, Issue 4
  • DOI: 10.1111/nph.13039

The polyploidy revolution then...and now: Stebbins revisited
journal, July 2014

  • Soltis, D. E.; Visger, C. J.; Soltis, P. S.
  • American Journal of Botany, Vol. 101, Issue 7
  • DOI: 10.3732/ajb.1400178

Why biosynthetic genes for chemical defense compounds cluster
journal, July 2012


Gene Copy-Number Alterations: A Cost-Benefit Analysis
journal, January 2013


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
  • DOI: 10.1016/j.ympev.2015.07.007

Gene Dosage Balance in Cellular Pathways: Implications for Dominance and Gene Duplicability
journal, September 2004


GC/MS Analysis of the Volatile Constituents of Corymbia citriodora Hook. from Réunion Island
journal, November 2004


Evolutionary fate of retroposed gene copies in the human genome
journal, February 2006

  • Vinckenbosch, N.; Dupanloup, I.; Kaessmann, H.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 9
  • DOI: 10.1073/pnas.0511307103

Genome and gene duplications and gene expression divergence: a view from plants: Gene duplication and expression divergence
journal, May 2012


Belowground volatiles facilitate interactions between plant roots and soil organisms
journal, December 2009


Expansion and Diversification of the Populus R2R3-MYB Family of Transcription Factors
journal, December 2008

  • Wilkins, Olivia; Nahal, Hardeep; Foong, Justin
  • Plant Physiology, Vol. 149, Issue 2
  • DOI: 10.1104/pp.108.132795

Coexpression of Neighboring Genes in the Genome of Arabidopsis thaliana
journal, May 2004


Genome-wide analysis of the terpene synthase gene family in physic nut (Jatropha curcas L.) and functional identification of six terpene synthases
journal, September 2016


Evolution and divergence of SBP-box genes in land plants
journal, October 2015


The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they?
journal, May 2007


Copy number polymorphism in plant genomes
journal, August 2013

  • Żmieńko, Agnieszka; Samelak, Anna; Kozłowski, Piotr
  • Theoretical and Applied Genetics, Vol. 127, Issue 1
  • DOI: 10.1007/s00122-013-2177-7