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. 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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. Aharoni A, Giri AP, Deuerlein S, Griepink F, de Kogel W-J, Verstappen FWA et al. (2003) Terpenoid metabolism in wild-type and transgenic Arabidopsis plants. Plant Cell 15:2866–2884

  2. Ammon DG, Barton AF, Clarke DA, Tjandra J (1985) Rapid and accurate determination of terpenes in the leaves of Eucalyptus species. Analyst 110:921–924

  3. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815

  4. Asante KS, Brophy JJ, Doran JC, Goldsack RJ, Hibbert DB, Larmour JS (2001) A comparative study of the seedling leaf oils of the spotted gums: species of the Corymbia (Myrtaceae), section Politaria. Aust J Botany 49:55–66

  5. Aubourg S, Lecharny A, Bohlmann J (2002) Genomic analysis of the terpenoid synthase (AtTPS) gene family of Arabidopsis thaliana Mol Genet Genomics 267:730–745

  6. Batish DR, Singh HP, Kohli RK, Kaur S (2008) Eucalyptus essential oil as a natural pesticide. Forest Ecol Manag 256:2166–2174

  7. Birney E, Durbin R (2000) Using GeneWise in the Drosophila annotation experiment. Genome Res 10:547–548

  8. Busch M, Seuter A, Hain R (2002) Functional analysis of the early steps of carotenoid biosynthesis in tobacco. Plant Physiol 128:439–453

  9. Bushnell B (2016) BBMap. http://www.sourceforge.net/projects/bbmap/

  10. Butler JB, Vaillancourt RE, Potts BM, Lee DJ, King GJ, Baten A et al. (2017) Comparative genomics of Eucalyptus and Corymbia reveals low rates of genome structural rearrangement. BMC Genomics 18:397

  11. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4:10

  12. Carr D, Carr S (1970) Oil glands and ducts in Eucalyptus L’Héit. II. Development and structure of oil glands in the embryo. Aust J Botany 18:191–212

  13. Chaw S-M, Chang C-C, Chen H-L, Li W-H (2004) Dating the monocot–dicot divergence and the origin of core eudicots using whole chloroplast genomes. J Mol Evol 58:424–441

  14. Chen F, Tholl D, Bohlmann J, Pichersky E (2011) The family of terpene synthases in plants: a mid‐size family of genes for specialized metabolism that is highly diversified throughout the kingdom. Plant J 66:212–229

  15. Chen J-M, Cooper DN, Chuzhanova N, Ferec C, Patrinos GP (2007) Gene conversion: mechanisms, evolution and human disease Nature Rev Genet 8:762–775

  16. Chu HY, Wegel E, Osbourn A (2011) From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants Plant J 66:66–79

  17. Crisp MD, Burrows GE, Cook LG, Thornhill AH, Bowman DMJS (2011) Flammable biomes dominated by eucalypts originated at the Cretaceous-Palaeogene boundary Nat Commun 2:193

  18. del Moral R, Muller CH (1970) The allelopathic effects of Eucalyptus camaldulensis Am Midl Nat 83:254–282

  19. Demuth JP, Hahn MW (2009) The life and death of gene families. Bioessays 31:29–39

  20. Douglas MH, van Klink JW, Smallfield BM, Perry NB, Anderson RE, Johnstone P et al. (2004) Essential oils from New Zealand manuka: triketone and other chemotypes of Leptospermum scoparium. Phytochemistry 65:1255–1264

  21. Ee S-F, Mohamed-Hussein Z-A, Othman R, Shaharuddin NA, Ismail I, Zainal Z (2014) Functional characterization of sesquiterpene synthase from Polygonum minus Sci World J 2014:11

  22. Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477

  23. Field B, Fiston-Lavier A-S, Kemen A, Geisler K, Quesneville H, Osbourn AE (2011) Formation of plant metabolic gene clusters within dynamic chromosomal regions Proc Natl Acad Sci USA 108:16116–16121

  24. Field B, Osbourn AE (2008) Metabolic diversification - independent assembly of operon-like gene clusters in different plants. Science 320:543–547

  25. Flagel LE, Wendel JF (2009) Gene duplication and evolutionary novelty in plants New Phytol 183:557–564

  26. Fray RG, Wallace A, Fraser PD, Valero D, Hedden P, Bramley PM et al. (1995) Constitutive expression of a fruit phytoene synthase gene in transgenic tomatoes causes dwarfism by redirecting metabolites from the gibberellin pathway Plant J 8:693–701

  27. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453

  28. Gao Y, Honzatko RB, Peters RJ (2012) Terpenoid synthase structures: a so far incomplete view of complex catalysis. Nat Prod Rep 29:1153–1175

  29. Gijzen M (2009) Runaway repeats force expansion of the Phytophthora infestans genome. Genome Biol 10:241

  30. Goodger JQ, Heskes AM, Woodrow IE (2013) Contrasting ontogenetic trajectories for phenolic and terpenoid defences in Eucalyptus froggattii. Ann Bot (Lond) 112:651–659

  31. Grattapaglia D, Bradshaw Jr HD (1994) Nuclear DNA content of commercially important Eucalyptus species and hybrids Can J For Res 24:1074–1078

  32. Grattapaglia D, Vaillancourt RE, Shepherd M, Thumma BR, Foley W, Külheim C et al. (2012) Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus Tree Genet Genomes 8:463–508

  33. Haas BJ, Papanicolaou A, Yassour M, Grabherr M, Blood PD, Bowden J et al. (2013) De novo transcript sequence reconstruction from RNA-Seq: reference generation and analysis with Trinity. Nat Protoc 8:https://doi.org/10.1038/nprot.2013.1084

  34. Hanada K, Zou C, Lehti-Shiu MD, Shinozaki K, Shiu S-H (2008) Importance of lineage-specific expansion of plant tandem duplicates in the adaptive response to environmental stimuli. Plant Physiol 148:993–1003

  35. Hansen NL, Heskes AM, Hamberger B, Olsen CE, Hallström BM, Andersen-Ranberg J et al. (2017) The terpene synthase gene family in Tripterygium wilfordii harbors a labdane-type diterpene synthase among the monoterpene synthase TPS-b subfamily Plant J 89:429–441

  36. Hayashi K-i, Kawaide H, Notomi M, Sakigi Y, Matsuo A, Nozaki H (2006) Identification and functional analysis of bifunctional ent-kaurene synthase from the moss Physcomitrella patens. FEBS Lett 580:6175–6181

  37. Healey A, Shepherd M, Baten A, King GJ, Lee DJ, Furtado A et al. (2017) Sequencing the branches of the eucalypt tree: comparison between Eucalyptus and Corymbia genomes. In: Plant & Animal Genome Conference XXV, San Diego, United States of America.

  38. Heiling S, Schuman MC, Schoettner M, Mukerjee P, Berger B, Schneider B et al. (2010) Jasmonate and ppHsystemin regulate key malonylation steps in the biosynthesis of 17-hydroxygeranyllinalool diterpene glycosides, an abundant and effective direct defense against herbivores in Nicotiana attenuata. Plant Cell 22:273–292

  39. Hill KD, Johnson LA (1995) Systematic studies in the eucalypts 7. A revision of the bloodwoods, genus Corymbia (Myrtaceae). Telopea 6:185–504

  40. Hofberger JA, Lyons E, Edger PP, Chris Pires J, Eric Schranz M (2013) Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family Genome Biol Evol 5:2155–2173

  41. Hofberger JA, Nsibo DL, Govers F, Bouwmeester K, Schranz ME (2015) A complex interplay of tandem- and whole-genome duplication drives expansion of the L-type lectin receptor kinase gene family in the Brassicaceae Genome Biol Evol 7:720–734

  42. Hosfield DJ, Zhang Y, Dougan DR, Broun A, Tari LW, Swanson RV et al. (2004) Structural basis for bisphosphonate-mediated inhibition of isoprenoid biosynthesis J Biol Chem 279:8526–8529

  43. Hurles M (2004) Gene duplication: the genomic trade in spare parts. PLoS Biol 2:e206

  44. Irmisch S, Jiang Y, Chen F, Gershenzon J, Köllner TG (2014) Terpene synthases and their contribution to herbivore-induced volatile emission in western balsam poplar (Populus trichocarpa). BMC Plant Biol 14:270

  45. Iskow RC, Gokcumen O, Lee C (2012) Exploring the role of copy number variants in human adaptation Trends Genet 28:245–257

  46. Keszei A, Brubaker CL, Foley WJ (2008) A molecular perspective on terpene variation in Australian Myrtaceae Aust J Bot 56:197–213

  47. Keszei A, Brubaker CL, Carter R, Köllner T, Degenhardt J, Foley WJ (2010a) Functional and evolutionary relationships between terpene synthases from Australian Myrtaceae Phytochemistry 71:844–852

  48. Keszei A, Hassan Y, Foley WJ (2010b) A biochemical interpretation of terpene chemotypes in Melaleuca alternifolia J Chem Ecol 36:652–661

  49. Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T (2001) Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate–dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:681–694

  50. Kondrashov FA (2012) Gene duplication as a mechanism of genomic adaptation to a changing environment. Proc R Soc B: Biol Sci 279:5048–5057

  51. Külheim C, Padovan A, Hefer C, Krause ST, Köllner TG, Myburg AA et al. (2015) The Eucalyptus terpene synthase gene family. BMC Genomics 16:1–18

  52. Ladiges PY, Udovicic F, Nelson G (2003) Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae. J Biogeogr 30:989–998

  53. Lawler IR, Foley WJ, Eschler BM, Pass DM, Handasyde K (1998) Intraspecific variation in Eucalyptus secondary metabolites determines food intake by folivorous marsupials. Oecologia 116:160–169

  54. Lawler IR, Stapley J, Foley WJ, Eschler BM (1999) Ecological example of conditioned flavor aversion in plant–herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. J Chem Ecol 25:401–415

  55. Lee DJ (2007) Achievements in forest tree genetic improvement in Australia and New Zealand 2: Development of Corymbia species and hybrids for plantations in eastern Australia. Aust Forestry 70:11–16

  56. Lefort V, Longueville J-E, Gascuel O (2017) SMS: Smart Model Selection in PhyML. Mol Biol Evol 34:2422–2424

  57. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes Trends Genet 20:116–122

  58. Li F, Zhou C, Weng Q, Li M, Yu X, Guo Y et al. (2015) Comparative genomics analyses reveal extensive chromosome colinearity and novel quantitative trait loci in Eucalyptus. PLoS ONE 10:e0145144

  59. Librado P, Vieira FG, Rozas J (2012) BadiRate: estimating family turnover rates by likelihood-based methods. Bioinformatics 28:279–281

  60. Liu Y, Schiff M, Dinesh-Kumar S (2004) Involvement of MEK1 MAPKK, NTF6 MAPK, WRKY/MYB transcription factors, COI1 and CTR1 in N-mediated resistance to tobacco mosaic virus. Plant J 38:800 –809

  61. Lynch M (2007) The origins of genome architecture. Sinauer Associates, Inc, Sunderland, MA

  62. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290:1151–1155

  63. Lyons E, Freeling M (2008) How to usefully compare homologous plant genes and chromosomes as DNA sequences. Plant J 53:661–673

  64. Lyons E, Pedersen B, Kane J, Alam M, Ming R, Tang H et al. (2008) Finding and comparing syntenic regions among Arabidopsis and the outgroups papaya, poplar, and grape: CoGe with rosids. Plant Physiol 148:1772–1781

  65. Macphail M, Thornhill AH (2016) How old are the eucalypts? A review of the microfossil and phylogenetic evidence Aust J Bot 64:579–599

  66. Martin DM, Aubourg S, Schouwey MB, Daviet L, Schalk M, Toub O et al. (2010) Functional annotation, genome organization and phylogeny of the grapevine (Vitis vinifera) terpene synthase gene family based on genome assembly, FLcDNA cloning, and enzyme assays. BMC Plant Biol 10:226

  67. Mendivil-Ramos O, Ferrier DEK (2012) Mechanisms of gene duplication and translocation and progress towards understanding their relative contributions to animal genome evolution. Int J Evolut Biol 2012:10

  68. Minh BQ, Nguyen MAT, von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195

  69. Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J et al. (2014) The genome of Eucalyptus grandis. Nature 510:356–362

  70. Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274

  71. O’Reilly-Wapstra JM, McArthur C, Potts BM (2004) Linking plant genotype, plant defensive chemistry and mammal browsing in a Eucalyptus species. Funct Ecol 18:677–684

  72. O’Reilly-Wapstra JM, Freeman JS, Davies NW, Vaillancourt RE, Fitzgerald H, Potts BM (2011) Quantitative trait loci for foliar terpenes in a global eucalypt species. Tree Genet Genomes 7:485–498

  73. Padovan A, Keszei A, Külheim C, Foley WJ (2014) The evolution of foliar terpene diversity in Myrtaceae. Phytochem Rev 13:695–716

  74. Padovan A, Keszei A, Wallis IR, Foley WJ (2012) Mosaic eucalypt trees suggest genetic control at a point that influences several metabolic pathways. J Chem Ecol 38:914–923

  75. Peñuelas J, Llusià J, Asensio D, Munné-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28:278–286

  76. Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

  77. R Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  78. Rockwood D, Rudie A, Ralph S, Zhu J, Winandy J (2008) Energy product options for Eucalyptus species grown as short rotation woody crops. Int J Mol Sci 9:1361

  79. Sasaki K, Saito T, Lämsä M, Oksman-Caldentey K-M, Suzuki M, Ohyama K et al. (2007) Plants utilize isoprene emission as a thermotolerance mechanism. Plant Cell Physiol 48:1254–1262

  80. Schiffer PH, Gravemeyer J, Rauscher M, Wiehe T (2016) Ultra large gene families: a matter of adaptation or genomic parasites? Life 6:32

  81. Schnee C, Köllner TG, Held M, Turlings TCJ, Gershenzon J, Degenhardt J (2006) The products of a single maize sesquiterpene synthase form a volatile defense signal that attracts natural enemies of maize herbivores. Proc Natl Acad Sci USA 103:1129–1134

  82. Schwab W, Fuchs C, Huang F-C (2013) Transformation of terpenes into fine chemicals. Eur J Lipid Sci Technol 115:3–8

  83. Sharma M, Pandey GK (2015) Expansion and function of repeat domain proteins during stress and development in plants. Front Plant Sci 6:1218

  84. Shepherd M, Bartle J, Lee DJ, Brawner J, Bush D, Turnbull P et al. (2011) Eucalypts as a biofuel feedstock. Biofuels 2:639–657

  85. Shepherd M, Baten A, Junior OBdS, Lee DJ, Butler JB, Freeman J et al. (2015) Towards a Corymbia reference genome: comparative efficiencies of Illumina, PacBio and hybrid de novo assemblies of a complex heterozygous genome. In: Vettori C, Vendramin GG, Paffetti D, Travaglini D (eds) Proceedings of the IUFRO Tree Biotechnology 2015 Conference: “Forests: the importance to the planet and society”, Florence, Italy.

  86. Singsaas EL, Lerdau M, Winter K, Sharkey TD (1997) Isoprene increases thermotolerance of isoprene-emitting species. Plant Physiol 115:1413–1420

  87. Slee A, Brooker M, Duffy S, West J (2006) EUCLID eucalypts of Australia. 3rd edn. Centre for Plant Biodiversity Research - CSIRO Publishing Canberra

  88. Soler M, Camargo ELO, Carocha V, Cassan-Wang H, San Clemente H, Savelli B et al. (2015) The Eucalyptus grandis R2R3-MYB transcription factor family: evidence for woody growth-related evolution and function New Phytol 206:1364–1377

  89. Soltis DE, Visger CJ, Soltis PS (2014) The polyploidy revolution then… and now: Stebbins revisited. Am J Bot 101:1057–1078

  90. Szöllősi GJ, Daubin V (2012) Modeling gene family evolution and reconciling phylogenetic discord. Evolut Genomics: Stat Comput Methods 2:29–51

  91. Takos AM, Rook F (2012) Why biosynthetic genes for chemical defense compounds cluster. Trends Plant Sci 17:383–388

  92. Tang Y-C, Amon A (2013) Gene copy-number alterations: a cost-benefit analysis. Cell 152:394–405

  93. Thornhill AH, Ho SYW, Külheim C, Crisp MD (2015) Interpreting the modern distribution of Myrtaceae using a dated molecular phylogeny. Mol Phylogenet Evol 93:29–43

  94. Veitia RA (2004) Gene dosage balance in cellular pathways: implications for dominance and gene duplicability. Genetics 168:569

  95. Vernin GA, Parkanyi C, Cozzolino F, Fellous R (2004) GC/MS analysis of the volatile constituents of Corymbia citriodora Hook. from Réunion Island. J Essential Oil Res 16:560–565

  96. Vinckenbosch N, Dupanloup I, Kaessmann H (2006) Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci USA 103:3220–3225

  97. Wang Y, Wang X, Paterson AH (2012) Genome and gene duplications and gene expression divergence: a view from plants. Ann N Y Acad Sci 1256:1–14

  98. Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T et al. (2016) gplots: various R programming tools for plotting data. https://CRAN.R-project.org/package=gplots

  99. Wenke K, Kai M, Piechulla B (2010) Belowground volatiles facilitate interactions between plant roots and soil organisms. Planta 231:499–506

  100. Wikström N, Savolainen V, Chase MW (2001) Evolution of the angiosperms: calibrating the family tree. Proc Royal Soc B 268:2211–2220

  101. Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

  102. Williams EJ, Bowles DJ (2004) Coexpression of neighboring genes in the genome of Arabidopsis thaliana. Genome Res 14:1060–1067

  103. Xiong W, Wu P, Jia Y, Wei X, Xu L, Yang Y et al. (2016) Genome-wide analysis of the terpene synthase gene family in physic nut (Jatropha curcas L.) and functional identification of six terpene synthases. Tree Genet Genomes 12:97

  104. Zhang S-D, Ling L-Z, Yi T-S (2015) Evolution and divergence of SBP-box genes in land plants. BMC Genomics 16:787

  105. Zheng D, Gerstein MB (2007) The ambiguous boundary between genes and pseudogenes: the dead rise up, or do they? Trends Genet 23:219–224

  106. Żmieńko A, Samelak A, Kozłowski P, Figlerowicz M (2014) Copy number polymorphism in plant genomes. Theor Appl Genet 127:1–18

Download references

Acknowledgements

The research presented here is part of a larger project working towards the creation of a reference genome for Corymbia, please see http://scu.edu.au/scps/index.php/137 for more information. The germplasm used to create the genomes referenced in this study was provided by the Queensland Department of Agriculture and Fisheries (DAF). The authors thank John Oostenbrink (DAF) for his work to produce the hybrid families, Valerie Hecht (University of Tasmania) for valuable advice regarding the creation of the phylogenies and Agnelo Furtado (University of Queensland) for consultation regarding the Corymbia genome project. This work was supported by the Australian Research Council (grant numbers DP140102552, DP110101621), and an Australian Government Research Training Program Scholarship. Sequencing and assembly data carried out by EMBRAPA as part of the Corymbia genome project was supported by FAPDF grant “Nextree” 193.000.570/2009. For the portion of the work conducted by the Joint Genome Institute and the Joint BioEnergy Institute, support was provided by the Office of Science of the U.S. Department of Energy under Contract No. DE-AC02-05CH11231.

Author information

Affiliations

  1. School of Natural Sciences, University of Tasmania, Hobart, TAS, 7001, Australia

    • Jakob B. Butler
    • , Jules S. Freeman
    • , Brad M. Potts
    •  & René E. Vaillancourt
  2. ARC Training Centre for Forest Value, University of Tasmania, Hobart, TAS, 7001, Australia

    • Brad M. Potts
    •  & René E. Vaillancourt
  3. EMBRAPA Genetic Resources and Biotechnology, EPqB Final W5 Norte, Brasilia, 70770-917, Brazil

    • Dario Grattapaglia
    •  & Orzenil B. Silva-Junior
  4. DOE Joint Bioenergy Institute, Lawrence Berkeley National Laboratory, Berkeley, CA, USA

    • Blake A. Simmons
    •  & Adam L. Healey
  5. Hudson-Alpha Institute for Biotechnology, Huntsville, AL, USA

    • Jeremy Schmutz
  6. DOE Joint Genome Institute, Lawrence Berkeley National Laboratory, Walnut Creek, CA, USA

    • Jeremy Schmutz
    •  & Kerrie W. Barry
  7. Forest Industries Research Centre, University of the Sunshine Coast, Maroochydore DC, QLD, 4558, Australia

    • David J. Lee
  8. University of Queensland/QAAFI, Brisbane, QLD, 4072, Australia

    • Robert J. Henry
  9. Southern Cross Plant Science, Southern Cross University, Lismore, NSW, 2480, Australia

    • Graham J. King
    • , Abdul Baten
    •  & Mervyn Shepherd

Authors

  1. Search for Jakob B. Butler in:

  2. Search for Jules S. Freeman in:

  3. Search for Brad M. Potts in:

  4. Search for René E. Vaillancourt in:

  5. Search for Dario Grattapaglia in:

  6. Search for Orzenil B. Silva-Junior in:

  7. Search for Blake A. Simmons in:

  8. Search for Adam L. Healey in:

  9. Search for Jeremy Schmutz in:

  10. Search for Kerrie W. Barry in:

  11. Search for David J. Lee in:

  12. Search for Robert J. Henry in:

  13. Search for Graham J. King in:

  14. Search for Abdul Baten in:

  15. Search for Mervyn Shepherd in:

Conflict of interest

The authors declare that they have no conflict of interest.

Corresponding author

Correspondence to Jakob B. Butler.

Electronic supplementary material

About this article

Publication history

Received

Revised

Accepted

Published

DOI

https://doi.org/10.1038/s41437-018-0058-1