Abstract
Eucalypts are of great ecological and economic importance. They dominate many woodland and forest landscapes in Australia and are planted in temperate to tropical areas worldwide for forestry. Population genomics research in eucalypts builds on a long history of genetics research, from quantitative trait analysis of field provenance trials to modern molecular genetics studies exploring neutral variation and population structure. It is backed by a high-quality reference genome and, whilst this rapidly expanding field is still in its infancy, it is already providing new insights into both ecological and industry-focused applications. This chapter reviews population genomics research in eucalypts, in the context of past genetics research. After describing the genomic resources available for eucalypts, we show that genomics is enabling greater resolution than ever before of species boundaries and patterns of hybridisation. Landscape genomics studies have revealed various patterns of population structure in natural populations, cryptic lineages within species and low divergence between closely related species. Genomic signatures of adaptation have been identified in several species, highlighting both climatic and edaphic factors as potential drivers of adaptation. In investigating the genetic architecture underlying complex traits, genomic tools are revealing not only associations with genes but also associations with differences in gene expression. With their worldwide importance, eucalypts are at the forefront of developments for integrating genomics into models for the genetic evaluation of forest tree breeding populations. Into the future, an increasing number of population genomics studies of eucalypts will help develop our understanding of the evolution of the genus; how species adapted to varied and changing environments; and the genetic architecture underlying adaptation and complex traits. Such knowledge will help guide species and provenance choices for conservation and ecological restoration under environmental change and will provide a valuable resource to breeding for forestry.
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References
Acuña CV, Villalba PV, Hopp HE, Marcucci Poltri SN. Transferability of microsatellite markers located in candidate genes for wood properties between Eucalyptus species. For Syst. 2014;23:506–12.
Aguilar I, Misztal I, Johnson DL, Legarra A, Tsuruta S, Lawlor TJ. Hot topic: a unified approach to utilize phenotypic, full pedigree, and genomic information for genetic evaluation of Holstein final score. J Dairy Sci. 2010;93(2):743–52.
Ahrens CW, Byrne M, Rymer PD. Standing genomic variation within coding and regulatory regions contributes to the adaptive capacity to climate in a foundation tree species. Mol Ecol. 2019;28(10):2502–16.
Ahrens CW, Murray K, Mazanec RA, Ferguson S, Bragg JG, Jones A, et al. Genomic constraints to drought adaptation. BioRxiv. 2021. https://doi.org/10.1101/2021.08.07.455511.
Ahuja MR, Neale DB. Evolution of genome size in conifers. Silvae Genet. 2005;54(3):126–37.
Alves AA, Rosado CCG, Faria DA, Guimarães LM d S, Lau D, Brommonschenkel SH, et al. Genetic mapping provides evidence for the role of additive and non-additive QTLs in the response of inter-specific hybrids of Eucalyptus to Puccinia psidii rust infection. Euphytica. 2012;183(1):27–38.
Alwadani KG, Janes JK, Andrew RL. Chloroplast genome analysis of box-ironbark Eucalyptus. Mol Phylogenet Evol. 2019;136:76–86.
Ammitzboll H, Vaillancourt RE, Potts BM, Singarasa S, Mani R, Freeman JS. Quantitative trait loci (QTLs) for intumescence severity in Eucalyptus globulus and validation of QTL detection based on phenotyping using open-pollinated families of a mapping population. Plant Dis. 2018;102(8):1566–73.
Ammitzboll H, Vaillancourt RE, Potts BM, Harrison PA, Brodribb T, Sussmilch FC, et al. Independent genetic control of drought resistance, recovery, and growth of Eucalyptus globulus seedlings. Plant Cell Environ. 2020;43(1):103–15.
Anand S, Mangano E, Barizzone N, Bordoni R, Sorosina M, Clarelli F, et al. Next generation sequencing of pooled samples: guideline for variants’ filtering. Sci Rep. 2016;6(1):33735.
Anderson MJ, Willis TJ. Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology. 2003;84(2):511–25.
Andrade MC, Perek M, Pereira FB, Moro M, Tambarussi EV. Quantity, organization, and distribution of chloroplast microsatellites in all species of Eucalyptus with available plastome sequence. Crop Breed Appl Biotechnol. 2018a;18:97–102.
Andrew RL, Peakall R, Wallis IR, Wood JT, Knight EJ, Foley WJ. Marker-based quantitative genetics in the wild?: the heritability and genetic correlation of chemical defenses in Eucalyptus. Genetics. 2005;171(4):1989–98.
Andrew RL, Wallis IR, Harwood CE, Henson M, Foley WJ. Heritable variation in the foliar secondary metabolite sideroxylonal in Eucalyptus confers cross-resistance to herbivores. Oecologia. 2007;153(4):891–901.
Andrew RL, Wallis IR, Harwood CE, Foley WJ. Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa. Ann Bot. 2010;105(5):707–17.
Arabidopsis Genome Initiative. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature. 2000;408:796–815.
Araus JL, Cairns JE. Field high-throughput phenotyping: the new crop breeding frontier. Trends Plant Sci. 2014;19(1):52–61.
Arriagada O, do Amaral Junior AT, Mora F. Thirteen years under arid conditions: exploring marker-trait associations in Eucalyptus cladocalyx for complex traits related to flowering, stem form and growth. Breed Sci. 2018;68(3):367–74.
Arumugasundaram S, Ghosh M, Veerasamy S, Ramasamy Y. Species discrimination, population structure and linkage disequilibrium in Eucalyptus camaldulensis and Eucalyptus tereticornis using SSR markers. PLoS One. 2011;6(12):e28252.
Ashton DH. The ecology of the boundary between Eucalyptus regnans F. Muell. and E. obliqua L’Herit in Victoria. Proc Ecol Soc Aust. 1981;11:75–94.
Australian Department of the Environment and Energy. Species profile and threats database. 2019. http://www.environment.gov.au/epbc/about/epbc-act-lists#species. Accessed Jan 2019.
Ballesta P, Mora F, Ruiz E, Contreras-Soto R. Marker-trait associations for survival, growth, and flowering components in Eucalyptus cladocalyx under arid conditions. Biol Plant. 2015;59(2):389–93.
Barber HN, Jackson WD. Natural selection in action in Eucalyptus. Nature. 1957;179(4573):1267–9.
Barbour RC, Potts BM, Vaillancourt RE. Gene flow between introduced and native Eucalyptus species: crossability of native Tasmanian species with exotic E. nitens. Aust J Bot. 2005;53(5):465–77.
Barbour RC, O’Reilly-Wapstra JM, Little DWD, Jordan GJ, Steane DA, Humphreys JR, et al. A geographic mosaic of genetic variation within a foundation tree species and its community-level consequences. Ecology. 2009;90(7):1762–72.
Barghi N, Hermisson J, Schlötterer C. Polygenic adaptation: a unifying framework to understand positive selection. Nat Rev Genet. 2020;21(12):769–81.
Barros E, van Staden C-A, Lezar S. A microarray-based method for the parallel analysis of genotypes and expression profiles of wood-forming tissues in Eucalyptus grandis. BMC Biotechnol. 2009;9(1):51.
Bartholomé J, Salmon F, Vigneron P, Bouvet J-M, Plomion C, Gion J-M. Plasticity of primary and secondary growth dynamics in Eucalyptus hybrids: a quantitative genetics and QTL mapping perspective. BMC Plant Biol. 2013;13(1):120.
Bartholomé J, Mandrou E, Mabiala A, Jenkins J, Nabihoudine I, Klopp C, et al. High-resolution genetic maps of Eucalyptus improve Eucalyptus grandis genome assembly. New Phytol. 2015a;206(4):1283–96.
Bartholomé J, Mabiala A, Savelli B, Bert D, Brendel O, Plomion C, et al. Genetic architecture of carbon isotope composition and growth in Eucalyptus across multiple environments. New Phytol. 2015b;206(4):1437–49.
Bartholomé J, Mabiala A, Burlett R, Bert D, Leplé J-C, Plomion C, et al. The pulse of the tree is under genetic control: Eucalyptus as a case study. Plant J. 2020;103(1):338–56.
Bay RA, Rose N, Barrett R, Bernatchez L, Ghalambor CK, Lasky JR, et al. Predicting responses to contemporary environmental change using evolutionary response architectures. Am Nat. 2017;189(5):463–73.
Bayer PE, Golicz AA, Scheben A, Batley J, Edwards D. Plant pan-genomes are the new reference. Nat Plants. 2020;6(8):914–20.
Bayly MJ, Rigault P, Spokevicius A, Ladiges PY, Ades PK, Anderson C, et al. Chloroplast genome analysis of Australian eucalypts – Eucalyptus, Corymbia, Angophora, Allosyncarpia and Stockwellia (Myrtaceae). Mol Phylogenet Evol. 2013;69(3):704–16.
Bezemer N, Krauss SL, Roberts DG, Hopper SD. Conservation of old individual trees and small populations is integral to maintain species’ genetic diversity of a historically fragmented woody perennial. Mol Ecol. 2019;28(14):3339–57.
Binks RM, Steane DA, Byrne M. Genomic divergence in sympatry indicates strong reproductive barriers and cryptic species within Eucalyptus salubris. Ecol Evol. 2021;11(10):5096–110.
Blackburn D, Vega M, Yong R, Britton D, Nolan G. Factors influencing the production of structural plywood in Tasmania, Australia from Eucalyptus nitens rotary peeled veneer. South For J For Sci. 2018;80(4):319–28.
Bloomfield JA, Nevill P, Potts BM, Vaillancourt RE, Steane DA. Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania. Aust J Bot. 2011a;59(3):226–37.
Booth TH. Eucalypt plantations and climate change. For Ecol Manag. 2013;301:28–34.
Booth TH, Broadhurst LM, Pinkard E, Prober SM, Dillon SK, Bush D, et al. Native forests and climate change: lessons from eucalypts. For Ecol Manag. 2015;347:18–29.
Borralho N. The impact of individual tree mixed models (BLUP) in tree breeding strategies. In: Potts B, Borralho N, Reid J, Cromer R, Tibbits W, Raymond C, editors. Eucalypt plantations: improving fibre yield and quality. CRC for Temperate Hardwood Forestry; 1995. p. 141–5.
Bouvet JM, Makouanzi G, Cros D, Vigneron P. Modeling additive and non-additive effects in a hybrid population using genome-wide genotyping: prediction accuracy implications. Heredity. 2016;116(2):146–57.
Boyle EA, Li YI, Pritchard JK. An expanded view of complex traits: from polygenic to omnigenic. Cell. 2017;169(7):1177–86.
Bradbury D, Smithson A, Krauss SL. Signatures of diversifying selection at EST-SSR loci and association with climate in natural Eucalyptus populations. Mol Ecol. 2013;22(20):5112–29.
Bradbury D, Binks RM, Byrne M. Genomic data inform conservation of rare tree species: clonality, diversity and hybridity in Eucalyptus series in a global biodiversity hotspot. Biodivers Conserv. 2021;30(3):619–41.
Brawner JT, Dillon SK, Lee DJ, Meder AR, Dieters MJ, Southerton SG. The use of genetic correlations to evaluate associations between SNP markers and quantitative traits. Tree Genet Genomes. 2012;8(6):1423–35.
Breed MF, Harrison PA, Blyth C, Byrne M, Gaget V, Gellie NJC, et al. The potential of genomics for restoring ecosystems and biodiversity. Nat Rev Genet. 2019;20(10):615–28.
Bresadola L, Caseys C, Castiglione S, Buerkle CA, Wegmann D, Lexer C. Admixture mapping in interspecific Populus hybrids identifies classes of genomic architectures for phytochemical, morphological and growth traits. New Phytol. 2019;223(4):2076–89.
Broadhurst L, Breed M, Lowe A, Bragg J, Catullo R, Coates D, et al. Genetic diversity and structure of the Australian flora. Divers Distrib. 2017a;23(1):41–52.
Broadhurst LM, Mellick R, Knerr N, Li L, Supple MA. Land availability may be more important than genetic diversity in the range shift response of a widely distributed eucalypt, Eucalyptus melliodora. For Ecol Manag. 2018a;409:38–46.
Brown AHD, Matheson AC, Eldridge KG. Estimation of the mating system of Eucalyptus obliqua L’Herit. by using allozyme polymorphisms. Aust J Bot. 1975;23(6):931–49.
Brown AG, Eldridge KG, Green JW, Matheson AC. Genetic variation of Eucalyptus obliqua in field trials. New Phytol. 1976;77(1):193–203.
Budde KB, Heuertz M, Hernández-Serrano A, Pausas JG, Vendramin GG, Verdú M, et al. In situ genetic association for serotiny, a fire-related trait, in Mediterranean maritime pine (Pinus pinaster). New Phytol. 2014;201(1):230–41.
Bui EN, Thornhill AH, González-Orozco CE, Knerr N, Miller JT. Climate and geochemistry as drivers of eucalypt diversification in Australia. Geobiology. 2017;15:427–40.
Bush D, Kain D, Matheson C, Kanowski P. Marker-based adjustment of the additive relationship matrix for estimation of genetic parameters—an example using Eucalyptus cladocalyx. Tree Genet Genomes. 2011;7:23–35.
Bush D, Kain D, Kanowski P, Matheson C. Genetic parameter estimates informed by a marker-based pedigree: a case study with Eucalyptus cladocalyx in southern Australia. Tree Genet Genomes. 2015;11(1):798.
Butcher PA, McDonald MW, Bell JC. Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis. Tree Genet Genomes. 2009a;5(1):189–210.
Butler JB, Freeman JS, Vaillancourt RE, Potts BM, Glen M, Lee DJ, et al. Evidence for different QTL underlying the immune and hypersensitive responses of Eucalyptus globulus to the rust pathogen Puccinia psidii. Tree Genet Genomes. 2016;12(3):39.
Butler JB, Vaillancourt RE, Potts BM, Lee DJ, King GJ, Baten A, et al. Comparative genomics of Eucalyptus and Corymbia reveals low rates of genome structural rearrangement. BMC Genomics. 2017;18(1):397.
Butler JB, Freeman JS, Potts BM, Vaillancourt RE, Grattapaglia D, Silva-Junior OB, et al. Annotation of the Corymbia terpene synthase gene family shows broad conservation but dynamic evolution of physical clusters relative to Eucalyptus. Heredity. 2018;121(1):87–104.
Butler JB, Potts BM, Vaillancourt RE, Lee DJ, Pegg GS, Freeman JS. Independent QTL underlie resistance to the native pathogen Quambalaria pitereka and the exotic pathogen Austropuccinia psidii in Corymbia. Tree Genet Genomes. 2019;15(5):72.
Byrne M. High genetic identities between three oil mallee taxa, Eucalyptus kochii ssp. kochii, ssp. plenissima and E. horistes, based on nuclear RFLP analysis. Heredity. 1999a;82(2):205–11.
Byrne M. Phylogeny, diversity and evolution of eucalypts. In: Sharma AK, Sharma A, editors. Plant genome: biodiversity and evolution – Volume 1, Part E, Phanerogams – angiosperm. Science Publishers; 2008a. p. 303–46.
Byrne M, Hines B. Phylogeographical analysis of cpDNA variation in Eucalyptus loxophleba (Myrtaceae). Aust J Bot. 2004a;52(4):459–70.
Byrne M, Hopper SD. Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biol J Linn Soc. 2008a;93(1):177–88.
Byrne M, Macdonald B. Phylogeography and conservation of three oil mallee taxa, Eucalyptus kochii ssp. kochii, ssp. plenissima and E. horistes. Aust J Bot. 2000a;48(3):305–12.
Byrne M, Parrish TL, Moran GF. Nuclear RFLP diversity in Eucalyptus nitens. Heredity. 1998a;81(2):225–33.
Byrne M, Elliott CP, Yates CJ, Coates DJ. Maintenance of high pollen dispersal in Eucalyptus wandoo, a dominant tree of the fragmented agricultural region in Western Australia. Conserv Genet. 2008;9(1):97–105.
Callister AN, Bradshaw BP, Elms S, Gillies RAW, Sasse JM, Brawner JT. Single-step genomic BLUP enables joint analysis of disconnected breeding programs: an example with Eucalyptus globulus Labill. G3 (Bethesda). 2021;11(10):jkab253.
Campbell A, Alexandra J, Curtis D. Reflections on four decades of land restoration in Australia. Rangel J. 2017;39(6):405–16.
Cappa EP, El-Kassaby YA, Garcia MN, Acuna C, Borralho NMG, Grattapaglia D, et al. Impacts of population structure and analytical models in genome-wide association studies of complex traits in forest trees: a case study in Eucalyptus globulus. PLoS One. 2013;8(11):e81267.
Cappa EP, Klápště J, Garcia MN, Villalba PV, Marcucci Poltri SN. SSRs, SNPs and DArTs comparison on estimation of relatedness and genetic parameters’ precision from a small half-sib sample population of Eucalyptus grandis. Mol Breed. 2016;36(7):97.
Cappa EP, El-Kassaby YA, Munoz F, Garcia MN, Villalba PV, Klapste J, et al. Improving accuracy of breeding values by incorporating genomic information in spatial-competition mixed models. Mol Breed. 2017;37(10):125.
Cappa EP, El-Kassaby YA, Muñoz F, Garcia MN, Villalba PV, Klápště J, et al. Genomic-based multiple-trait evaluation in Eucalyptus grandis using dominant DArT markers. Plant Sci. 2018;271:27–33.
Cappa EP, de Lima BM, da Silva-Junior OB, Garcia CC, Mansfield SD, Grattapaglia D. Improving genomic prediction of growth and wood traits in Eucalyptus using phenotypes from non-genotyped trees by single-step GBLUP. Plant Sci. 2019;284:9–15.
Carvalho GMA, Carvalho CR. The eucalypt karyogram resolved. Botany. 2016;94(5):411–6.
Carvalho GMA, Carvalho CR, Soares FAF. Flow cytometry and cytogenetic tools in eucalypts: genome size variation × karyotype stability. Tree Genet Genomes. 2017;13(5):106.
Cavalett O, Norem Slettmo S, Cherubini F. Energy and environmental aspects of using Eucalyptus from Brazil for energy and transportation services in Europe. Sustainability. 2018;10(11):4068.
Christensen OF, Lund MS. Genomic prediction when some animals are not genotyped. Genet Sel Evol. 2010;42(1):2.
Christie N, Mannapperuma C, Ployet R, van der Merwe K, Mähler N, Delhomme N, et al. qtlXplorer: an online systems genetics browser in the Eucalyptus Genome Integrative Explorer (EucGenIE). BMC Bioinformatics. 2021;22(1):595.
Christmas MJ, Breed MF, Lowe AJ. Constraints to and conservation implications for climate change adaptation in plants. Conserv Genet. 2016;17(2):305–20.
Collins TL, Andrew RL, Bruhl JJ. Morphological, phytochemical and molecular analyses define species limits in Eucalyptus magnificata (Myrtaceae) and lead to the discovery of a new rare species. Aust Syst Bot. 2019;32(1):12–28.
Costa e Silva J, Potts BM, Dutkowski GW. Genotype by environment interaction for growth of Eucalyptus globulus in Australia. Tree Genet Genomes. 2006;2(2):61–75.
Costa e Silva J, Hardner C, Tilyard P, Pires AM, Potts BM. Effects of inbreeding on population mean performance and observational variances in Eucalyptus globulus. Ann For Sci. 2010a;67(6):605.
Costa e Silva J, Hardner C, Potts BM. Genetic variation and parental performance under inbreeding for growth in Eucalyptus globulus. Ann For Sci. 2010b;67(6):606.
Costa e Silva J, Hardner C, Tilyard P, Potts BM. The effects of age and environment on the expression of inbreeding depression in Eucalyptus globulus. Heredity. 2011;107(1):50–60.
Costa e Silva J, Potts BM, Tilyard P. Epistasis causes outbreeding depression in eucalypt hybrids. Tree Genet Genomes. 2012;8(2):249–65.
Costa e Silva J, Potts BM, Lopez GA. Heterosis may result in selection favouring the products of long-distance pollen dispersal in Eucalyptus. PLoS One. 2014;9(4):e93811.
Costa e Silva J, Potts BM, Gilmour AR, Kerr RJ. Genetic-based interactions among tree neighbors: identification of the most influential neighbors, and estimation of correlations among direct and indirect genetic effects for leaf disease and growth in Eucalyptus globulus. Heredity. 2017;119(3):125–35.
Costa e Silva J, Harrison PA, Wiltshire R, Potts BM. Evidence that divergent selection shapes a developmental cline in a forest tree species complex. Ann Bot. 2018;122(1):181–94.
Costa e Silva J, Potts B, Bijma P, Kerr R, Pilbeam D. Genetic control of interactions among individuals: contrasting outcomes of indirect genetic effects arising from neighbour disease infection and competition in a forest tree. New Phytol. 2013;197(2):631–41.
Courtois B, Audebert A, Dardou A, Roques S, Ghneim-Herrera T, Droc G, et al. Genome-wide association mapping of root traits in a japonica rice panel. PLoS One. 2013;8(11):e78037.
Crandall S, Gold K, Jiménez-Gasco M, Filgueiras C, Willett D. A multi-omics approach to solving problems in plant disease ecology. PLoS One. 2020;15:e0237975.
Crisp M, Cook L, Steane D. Radiation of the Australian flora: what can comparisons of molecular phylogenies across multiple taxa tell us about the evolution of diversity in present-day communities? Philos Trans R Soc Lond B Biol Sci. 2004;359(1450):1551–71.
Crisp MD, Burrows GE, Cook LG, Thornhill AH, Bowman DMJS. Flammable biomes dominated by eucalypts originated at the Cretaceous-Palaeogene boundary. Nat Commun. 2011;2(1):1–8.
Dasgupta MG, Dharanishanthi V, Agarwal I, Krutovsky KV. Development of genetic markers in Eucalyptus species by target enrichment and exome sequencing. PLoS One. 2015;10(1):e0116528.
Dasgupta MG, Bari MPA, Shanmugavel S, Dharanishanthi V, Muthupandi M, Kumar N, et al. Targeted re-sequencing and genome-wide association analysis for wood property traits in breeding population of Eucalyptus tereticornis × E. grandis. Genomics. 2021;113(6):4276–92.
Davidson N, Bailey TG, Burgess S. Restoring the Midlands of Tasmania: an introduction. Ecol Manag Restor. 2021;22(S2):3–10.
Denis M, Favreau B, Ueno S, Camus-Kulandaivelu L, Chaix G, Gion J-M, et al. Genetic variation of wood chemical traits and association with underlying genes in Eucalyptus urophylla. Tree Genet Genomes. 2013;9(4):927–42.
Dillon SK, Brawner JT, Meder R, Lee DJ, Southerton SG. Association genetics in Corymbia citriodora subsp. variegata identifies single nucleotide polymorphisms affecting wood growth and cellulosic pulp yield. New Phytol. 2012;195(3):596–608.
Dillon S, McEvoy R, Baldwin DS, Rees GN, Parsons Y, Southerton S. Characterisation of adaptive genetic diversity in environmentally contrasted populations of Eucalyptus camaldulensis Dehnh. (River Red Gum). PLoS One. 2014;9(8):e103515.
Dillon S, McEvoy R, Baldwin DS, Southerton S, Campbell C, Parsons Y, et al. Genetic diversity of Eucalyptus camaldulensis Dehnh. following population decline in response to drought and altered hydrological regime. Austral Ecol. 2015;40(5):558–72.
Dillon S, Quentin A, Ivković M, Furbank RT, Pinkard E. Photosynthetic variation and responsiveness to CO2 in a widespread riparian tree. PLoS One. 2018;13(1):e0189635.
Doughty RW. The Eucalyptus: a natural and commercial history of the gum tree: Johns Hopkins University Press; 2000.
Downham R, Gavran M. Australian plantation statistics 2018 update: Australian Bureau of Agricultural and Resource Economics and Sciences (ABARES); 2018.
Drake JE, Aspinwall MJ, Pfautsch S, Rymer PD, Reich PB, Smith RA, et al. The capacity to cope with climate warming declines from temperate to tropical latitudes in two widely distributed Eucalyptus species. Glob Chang Biol. 2015;21(1):459–72.
Dungey HS, Potts BM, Carnegie AJ, Ades PK. Mycosphaerella leaf disease: genetic variation in damage to Eucalyptus nitens, Eucalyptus globulus, and their F1 hybrid. Can J For Res. 1997;27(5):750–9.
Dutkowski GW, Potts BM. Geographic patterns of genetic variation in Eucalyptus globulus ssp. globulus and a revised racial classification. Aust J Bot. 1999;47(2):237–63.
Dutkowski GW, Potts BM. Genetic variation in the susceptibility of Eucalyptus globulus to drought damage. Tree Genet Genomes. 2012;8(4):757–73.
Dutkowski G, McRae T, Powell M, Pilbeam D, Joyce K, Tier B, et al. Benefits from data and pedigree integration in genetic evaluation. In: Mercer C, editor. Breeding for success: diversity in action. Proceedings of the 13th Australiasian plant breeding conference. CD ROM Communication; 2006.
Eldridge K, Davidson J, Harwood C, van Wyk G. Eucalypt domestication and breeding: Clarendon Press; 1994.
Elissetche JP, Salas-Burgos A, Garcia R, Iturra C, Teixeira R, Rodriguez J, et al. Generation and analysis of expressed sequence tags (ESTs) from cambium tissue cDNA libraries of contrasting genotypes of Eucalyptus globulus Labill. BMC Proc. 2011;5(7):P108.
Ellegren H, Smeds L, Burri R, Olason PI, Backström N, Kawakami T, et al. The genomic landscape of species divergence in Ficedula flycatchers. Nature. 2012;491(7426):756–60.
Elshire RJ, Glaubitz J, Sun Q, Poland J, Kawamoto K, Buckler E, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6:e19379.
Field DL, Ayre DJ, Whelan RJ, Young AG. Relative frequency of sympatric species influences rates of interspecific hybridization, seed production and seedling performance in the uncommon Eucalyptus aggregata. J Ecol. 2008;96(6):1198–210.
Field DL, Ayre DJ, Whelan RJ, Young AG. Molecular and morphological evidence of natural interspecific hybridization between the uncommon Eucalyptus aggregata and the widespread E. rubida and E. viminalis. Conserv Genet. 2009;10(4):881–96.
Field DL, Ayre DJ, Whelan RJ, Young AG. Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida. Heredity. 2011a;106(5):841–53.
Field DL, Ayre DJ, Whelan RJ, Young AG. The importance of pre-mating barriers and the local demographic context for contemporary mating patterns in hybrid zones of Eucalyptus aggregata and Eucalyptus rubida. Mol Ecol. 2011b;20(11):2367–79.
Fishman L, Kelly AJ, Morgan E, Willis JH. A genetic map in the Mimulus guttatus species complex reveals transmission ratio distortion due to heterospecific interactions. Genetics. 2001;159(4):1701–16.
Flanagan SP, Forester BR, Latch EK, Aitken SN, Hoban S. Guidelines for planning genomic assessment and monitoring of locally adaptive variation to inform species conservation. Evol Appl. 2018;11(7):1035–52.
Florence RG. Ecology and silviculture of eucalypt forests: CSIRO Publishing; 2004.
Flowers JM, Molina J, Rubinstein S, Huang P, Schaal BA, Purugganan MD. Natural selection in gene-dense regions shapes the genomic pattern of polymorphism in wild and domesticated rice. Mol Biol Evol. 2012;29(2):675–87.
Foll M, Gaggiotti O. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics. 2008;180(2):977–93.
Foster SA, McKinnon GE, Steane DA, Potts BM, Vaillancourt RE. Parallel evolution of dwarf ecotypes in the forest tree Eucalyptus globulus. New Phytol. 2007a;175(2):370–80.
Freeman JS, Potts BM, Shepherd M, Vaillancourt RE. Parental and consensus linkage maps of Eucalyptus globulus using AFLP and microsatellite markers. Silvae Genet. 2006;55(1–6):202–17.
Freeman JS, Potts BM, Vaillancourt RE. Few Mendelian genes underlie the quantitative response of a forest tree, Eucalyptus globulus, to a natural fungal epidemic. Genetics. 2008;178(1):563–71.
Freeman JS, Potts BM, Downes GM, Pilbeam D, Thavamanikumar S, Vaillancourt RE. Stability of quantitative trait loci for growth and wood properties across multiple pedigrees and environments in Eucalyptus globulus. New Phytol. 2013;198(4):1121–34.
Freeman JS, Hamilton MG, Lee DJ, Pegg GS, Brawner JT, Tilyard PA, et al. Comparison of host susceptibilities to native and exotic pathogens provides evidence for pathogen-imposed selection in forest trees. New Phytol. 2019;221(4):2261–72.
FSC. Strategic review on the future of forest plantations. Helsinki: Forest Stewardship Council; 2012.
Garnier-Géré PH, Ades PK. Environmental surrogates for predicting and conserving adaptive genetic variability in tree species. Conserv Biol. 2001;15(6):1632–44.
Gauli A, Steane DA, Vaillancourt RE, Potts BM. Molecular genetic diversity and population structure in Eucalyptus pauciflora subsp. pauciflora (Myrtaceae) on the island of Tasmania. Aust J Bot. 2014;62(3):175–88.
Gauli A, Vaillancourt RE, Bailey TG, Steane DA, Potts BM. Evidence for local climate adaptation in early-life traits of Tasmanian populations of Eucalyptus pauciflora. Tree Genet Genomes. 2015;11(5):104.
Gea LD, McConnochie R, Wynyard S. Parental reconstruction for breeding, deployment, and seed-orchard management of Eucalyptus nitens. N Z J For Sci. 2007;37(1):23–36.
Gion J-M, Carouché A, Deweer S, Bedon F, Pichavant F, Charpentier J-P, et al. Comprehensive genetic dissection of wood properties in a widely-grown tropical tree: Eucalyptus. BMC Genomics. 2011;12(1):301.
Gompert Z, Lucas LK, Nice CC, Fordyce JA, Forister ML, Buerkle CA. Genomic regions with a history of divergent selection affect fitness of hybrids between two butterfly species. Evolution. 2012;66(7):2167–81.
González-Orozco CE, Thornhill AH, Knerr N, Laffan S, Miller JT. Biogeographical regions and phytogeography of the eucalypts. Divers Distrib. 2014;20(1):46–58.
Gonzalez-Orozco CE, Pollock LJ, Thornhill AH, Mishler BD, Knerr N, Laffan SW, et al. Phylogenetic approaches reveal biodiversity threats under climate change. Nat Clim Chang. 2016;6(12):1110–4.
Gosney BJ, Potts BM, O’Reilly-Wapstra JM, Vaillancourt RE, Fitzgerald H, Davies NW, et al. Genetic control of cuticular wax compounds in Eucalyptus globulus. New Phytol. 2016;209(1):202–15.
Gosper CR, Yates CJ, Cook GD, Harvey JM, Liedloff AC, McCaw WL, et al. A conceptual model of vegetation dynamics for the unique obligate-seeder eucalypt woodlands of south-western Australia. Austral Ecol. 2018;43(6):681–95.
Gourbiere S, Mallet J. Are species real? The shape of the species boundary with exponential failure, reinforcement, and the ‘missing snowball’. Evolution. 2010;64(1):1–24.
Grattapaglia D. Molecular breeding of Eucalyptus – state of the art, operational applications and technical challenges. In: Jain S, Minocha S, editors. Molecular biology of woody plants. Kluwer Academic Publishers; 2000. p. 451–74.
Grattapaglia D. Integrating genomics into Eucalyptus breeding. Genet Mol Res. 2004;3(3):369–79.
Grattapaglia D. Status and perspectives of genomic selection in forest tree breeding. In: Varshney R, Roorkiwal M, Sorrells M, editors. Genomic selection for crop improvement. Springer; 2017. p. 199–249.
Grattapaglia D, Bradshaw HD Jr. Nuclear DNA content of commercially important Eucalyptus species and hybrids. Can J For Res. 1994;24(5):1074–8.
Grattapaglia D, Kirst M. Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytol. 2008;179(4):911–29.
Grattapaglia D, Resende MDV. Genomic selection in forest tree breeding. Tree Genet Genomes. 2011;7(2):241–55.
Grattapaglia D, Silva Junior OB, Kirst M, de Lima BM, Faria DA, Pappas GJ Jr. High-throughput SNP genotyping in the highly heterozygous genome of Eucalyptus: assay success, polymorphism and transferability across species. BMC Plant Biol. 2011;11:65.
Grattapaglia D, Vaillancourt RE, Shepherd M, Thumma BR, Foley W, Külheim C, et al. Progress in Myrtaceae genetics and genomics: Eucalyptus as the pivotal genus. Tree Genet Genomes. 2012;8(3):463–508.
Griffin AR, Williams ER, Johnson KW. Early height growth and frost hardiness of Eucalyptus regnans provenances in twelve field trials in south-east Australia. Aust For Res. 1982;12(4):263–79.
Griffin AR, Burgess IP, Wolf L. Patterns of natural and manipulated hybridisation in the genus Eucalyptus L’hérit – a review. Aust J Bot. 1988;36(1):41–66.
Griffin AR, Potts BM, Vaillancourt RE, Bell JC. Life cycle expression of inbreeding depression in Eucalyptus regnans and inter-generational stability of its mixed mating system. Ann Bot. 2019;124(1):179–87.
Guo F, Altaner CM. Properties of rotary peeled veneer and laminated veneer lumber (LVL) from New Zealand grown Eucalyptus globoidea. N Z J For Sci. 2018;48(1):3.
Habier D, Fernando RL, Dekkers J. The impact of genetic relationship information on genome-assisted breeding values. Genetics. 2007;177(4):2389–97.
Hamilton MG, Dutkowski GW, Joyce KR, Potts BM. Meta-analysis of racial variation in Eucalyptus nitens and E. denticulata. N Z J For Sci. 2011;41:217–30.
Hamilton MG, Freeman JS, Blackburn DP, Downes GM, Pilbeam DJ, Potts BM. Independent lines of evidence of a genetic relationship between acoustic wave velocity and kraft pulp yield in Eucalyptus globulus. Ann For Sci. 2017;74(1):17.
Harbard JL, Griffin AR, Espejo J. Mass controlled pollination of Eucalyptus globulus: a practical reality. Can J For Res. 1999;29(10):1457–63.
Hardner CM, Potts BM, Gore PL. The relationship between cross success and spatial proximity of Eucalyptus globulus ssp. globulus parents. Evolution. 1998;52(2):614–8.
Harrison PA, Vaillancourt RE, Harris RMB, Potts BM. Integrating climate change and habitat fragmentation to identify candidate seed sources for ecological restoration. Restor Ecol. 2017;25(4):524–31.
Harwood CE. Frost resistance of subalpine Eucalyptus species. I. Experiments using a radiation frost room. Aust J Bot. 1980;28(6):587–99.
Harwood C. New introductions: doing it right. In: Walker J, editor. Developing a eucalypt resource: learning from Australia and elsewhere. Wood Technology Research Centre, University of Canterbury; 2011. p. 43–54.
Hasin Y, Seldin M, Lusis A. Multi-omics approaches to disease. Genome Biol. 2017;18:83.
He T, Lamont BB, Enright NJ, D’Agui HM, Stock W. Environmental drivers and genomic architecture of trait differentiation in fire-adapted Banksia attenuata ecotypes. J Integr Plant Biol. 2019;61(4):417–32.
Healey AL, Shepherd M, King GJ, Butler JB, Freeman JS, Lee DJ, et al. Pests, diseases, and aridity have shaped the genome of Corymbia citriodora. Commun Biol. 2021;4(1):537.
Heer K, Behringer D, Piermattei A, Bässler C, Brandl R, Fady B, Jehl H, Liepelt S, Lorch S, Piotti A, Vendramin GG. Linking dendroecology and association genetics in natural populations: Stress responses archived in tree rings associate with SNP genotypes in silver fir (Abies alba Mill.). Mol Ecol. 2018;27(6):1428–38.
Hedrick PW, Hellsten U, Grattapaglia D. Examining the cause of high inbreeding depression: analysis of whole-genome sequence data in 28 selfed progeny of Eucalyptus grandis. New Phytol. 2016;209(2):600–11.
Hefer C, Mizrachi E, Joubert F, Myburg A. The Eucalyptus genome integrative explorer (EucGenIE): a resource for Eucalyptus genomics and transcriptomics. BMC Proc. 2011;5(7):O49.
Hendre PS, Kamalakannan R, Varghese M. High-throughput and parallel SNP discovery in selected candidate genes in Eucalyptus camaldulensis using Illumina NGS platform. Plant Biotechnol J. 2012;10(6):646–56.
Henry RJ, Kole C (Eds) Genetics, genomics and breeding of eucalypts: CRC Press; 2015.
Hirakawa H, Nakamura Y, Kaneko T, Isobe S, Sakai H, Kato T, et al. Survey of the genetic information carried in the genome of Eucalyptus camaldulensis. Plant Biotechnol. 2011a;28(5):471–80.
Hobbs RJ. Where to from here? Challenges for restoration and revegetation in a fast-changing world. Rangel J. 2017;39(6):563–6.
Hodge GR, Volker PW, Potts BM, Owen JV. A comparison of genetic information from open-pollinated and control-pollinated progeny tests in two eucalypt species. Theor Appl Genet. 1996;92(1):53–63.
Hoffmann AA, Weeks AR, Sgrò CM. Opportunities and challenges in assessing climate change vulnerability through genomics. Cell. 2021;184(6):1420–5.
Holman JE, Hughes JM, Fensham RJ. Origins of a morphological cline between Eucalyptus melanophloia and Eucalyptus whitei. Aust J Bot. 2011a;59(3):244–52.
House SM. Reproductive biology of eucalypts. In: Williams JE, Woinarski J, editors. Eucalypt ecology: individuals to ecosystems. Cambridge University Press; 1997. p. 30–56.
Hudson CJ, Kullan ARK, Freeman JS, Faria DA, Grattapaglia D, Kilian A, et al. High synteny and colinearity among Eucalyptus genomes revealed by high-density comparative genetic mapping. Tree Genet Genomes. 2012;8(2):339–52.
Hudson CJ, Freeman JS, Jones RC, Potts BM, Wong MML, Weller JL, et al. Genetic control of heterochrony in Eucalyptus globulus. G3 (Bethesda). 2014;4(7):1235–45.
Hudson CJ, Freeman JS, Myburg AA, Potts BM, Vaillancourt RE. Genomic patterns of species diversity and divergence in Eucalyptus. New Phytol. 2015;206(4):1378–90.
Iglesias-Trabado G, Arballeira-Tenreiro R, Folgueira-Lozana J. Eucalyptus universalis: global cultivated eucalypt forests map. Version 1.2. In: Eucalyptologics information resources on eucalypt cultivation worldwide. 2009. http://www.git-forestry.com. Accessed 19 Oct 2009.
Jackson HD, Steane DA, Potts BM, Vaillancourt RE. Chloroplast DNA evidence for reticulate evolution in Eucalyptus (Myrtaceae). Mol Ecol. 1999;8(5):739–51.
Jacobs M. Eucalypts for planting, FAO forestry series, vol. 11: FAO; 1981.
Janes JK, Hamilton JA. Mixing it up: the role of hybridization in forest management and conservation under climate change. Forests. 2017;8(7):237.
Jarvis SF, Borralho NMG, Potts BM. Implementation of a multivariate BLUP model for genetic evaluation of Eucalyptus globulus in Australia. In: Potts B, Borralho N, Reid J, Cromer R, Tibbits W, Raymond C, editors. Eucalypt plantations: improving fibre yield and quality. CRC for Temperate Hardwood Forestry; 1995. p. 212–6.
Jones RC, McKinnon GE, Potts BM, Vaillancourt RE. Genetic diversity and mating system of an endangered tree Eucalyptus morrisbyi. Aust J Bot. 2005a;53(4):367–77.
Jordan GJ, Potts BM, Kirkpatrick JB, Gardiner C. Variation in the Eucalyptus globulus complex revisited. Aust J Bot. 1993;41(6):763–85.
Jordan GJ, Potts BM, Chalmers P, Wiltshire RJE. Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp. globulus is an adaptive trait. Aust J Bot. 2000;48(5):561–7.
Jordan R, Dillon SK, Prober SM, Hoffmann AA. Landscape genomics reveals altered genome wide diversity within revegetated stands of Eucalyptus microcarpa (Grey Box). New Phytol. 2016;212(4):992–1006.
Jordan R, Hoffmann AA, Dillon SK, Prober SM. Evidence of genomic adaptation to climate in Eucalyptus microcarpa: implications for adaptive potential to projected climate change. Mol Ecol. 2017;26(21):6002–20.
Kainer D, Stone EA, Padovan A, Foley WJ, Külheim C. Accuracy of genomic prediction for foliar terpene traits in Eucalyptus polybractea. G3 (Bethesda). 2018;8(8):2573–83.
Kainer D, Padovan A, Degenhardt J, Krause S, Mondal P, Foley WJ, et al. High marker density GWAS provides novel insights into the genomic architecture of terpene oil yield in Eucalyptus. New Phytol. 2019;223(3):1489–504.
Keith DA. Australian vegetation. 3rd ed: Cambridge University Press; 2017.
Keller G, Marchal T, SanClemente H, Navarro M, Ladouce N, Wincker P, et al. Development and functional annotation of an 11,303-EST collection from Eucalyptus for studies of cold tolerance. Tree Genet Genomes. 2009;5(2):317–27.
Kerr R, Thumma B, Southerton S, Tier B, Dutkowski G, McRae T, et al. Operational testing of molecular breeding to improve pulpwood value in Eucalyptus nitens (Technical report 209): CRC for Forestry; 2011.
Kerr RJ, McRae TA, Dutkowski GW, Tier B. Managing the rate of increase in average co-ancestry in a rolling front tree breeding strategy. J Anim Breed Genet. 2015;132(2):109–20.
Kerr R, Tibbits J, Dutkowski G, McRae T. Single-step genomic selection methods and its integration with current quantitative breeding methods. In: Jones R, Steane D, Tilyard P, Vaillancourt R, Andrew R, Rymer P, Potts B, editors. Abstracts of conference presentations and posters. University of Tasmania; 2019. p. 47.
Kirst M, Myburg AA, De Leon JPG, Kirst ME, Scott J, Sederoff R. Coordinated genetic regulation of growth and lignin revealed by quantitative trait locus analysis of cDNA microarray data in an interspecific backcross of Eucalyptus. Plant Physiol. 2004;135(4):2368–78.
Klápště J, Ashby RL, Telfer EJ, Graham NJ, Dungey HS, Brauning R, et al. The use of ‘genotyping-by-sequencing’ to recover shared genealogy in genetically diverse Eucalyptus populations. Forests. 2021;12(7):904.
Kramer AT, Ison JL, Ashley MV, Howe HF. The paradox of forest fragmentation genetics. Conserv Biol. 2008;22(4):878–85.
Kremer A, Potts BM, Delzon S. Genetic divergence in forest trees: understanding the consequences of climate change. Funct Ecol. 2014;28(1):22–36.
Külheim C, Yeoh SH, Maintz J, Foley WJ, Moran GF. Comparative SNP diversity among four Eucalyptus species for genes from secondary metabolite biosynthetic pathways. BMC Genomics. 2009;10(1):452.
Külheim C, Yeoh SH, Wallis IR, Laffan S, Moran GF, Foley WJ. The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus. New Phytol. 2011;191(4):1041–53.
Külheim C, Padovan A, Hefer C, Krause ST, Köllner TG, Myburg AA, et al. The Eucalyptus terpene synthase gene family. BMC Genomics. 2015;16(1):450.
Kullan ARK, van Dyk MM, Hefer CA, Jones N, Kanzler A, Myburg AA. Genetic dissection of growth, wood basic density and gene expression in interspecific backcrosses of Eucalyptus grandis and E. urophylla. BMC Genet. 2012;13:60.
Ladiges PY, Ashton DH. A comparison of some populations of Eucalyptus viminalis Labill. growing on calcareous and acid soils in Victoria, Australia. Aust J Ecol. 1977;2(2):161–78.
Ladiges PY, Udovicic F, Nelson G. Australian biogeographical connections and the phylogeny of large genera in the plant family Myrtaceae. J Biogeogr. 2003;30(7):989–98.
Larcombe MJ, Holland B, Steane DA, Jones RC, Nicolle D, Vaillancourt RE, et al. Patterns of reproductive isolation in Eucalyptus – a phylogenetic perspective. Mol Biol Evol. 2015;32(7):1833–46.
Larcombe MJ, Barbour RC, Jones RC, Vaillancourt RE, Potts BM. Postmating barriers to hybridization between an island’s native eucalypts and an introduced congener. Tree Genet Genomes. 2016a;12(2):26.
Larcombe MJ, Silva JCE, Tilyard P, Gore P, Potts BM. On the persistence of reproductive barriers in Eucalyptus: the bridging of mechanical barriers to zygote formation by F1 hybrids is counteracted by intrinsic post-zygotic incompatibilities. Ann Bot. 2016b;118(3):431–44.
Lebedev V, Lebedeva T, Chernodubov A, Shestibratov K. Genomic selection for forest tree improvement: methods, achievements and perspectives. Forests. 2020;11:1190.
Legarra A, Aguilar I, Misztal I. A relationship matrix including full pedigree and genomic information. J Dairy Sci. 2009;92(9):4656–63.
Lenz PR, Nadeau S, Mottet MJ, Perron M, Isabel N, Beaulieu J, Bousquet J. Multi-trait genomic selection for weevil resistance, growth, and wood quality in Norway spruce. Evol Appl. 2020;13(1):76–94.
Lezar S, Myburg AA, Berger DK, Wingfield MJ, Wingfield BD. Development and assessment of microarray-based DNA fingerprinting in Eucalyptus grandis. Theor Appl Genet. 2004;109(7):1329–36.
Li F, Zhou C, Weng Q, Li M, Yu X, Guo Y, et al. Comparative genomics analyses reveal extensive chromosome colinearity and novel quantitative trait loci in Eucalyptus. PLoS One. 2015;10(12):e0145144.
Li T, Kainer D, Foley WJ, Rodrigo A, Külheim C. The draft genome sequence of Eucalyptus polybractea based on hybrid assembly with short- and long-reads reads. BioRxiv. 2021. https://doi.org/10.1101/2021.05.18.444652.
Lindenmayer D, Blair D, McBurney L, Banks S. Mountain ash: fire, logging and the future of Victoria’s giant forests: CSIRO Publishing; 2015.
Lotterhos KE, Whitlock MC. The relative power of genome scans to detect local adaptation depends on sampling design and statistical method. Mol Ecol. 2015;24(5):1031–46.
Maldonado C, Contreras-Soto RI, Gerhardt IFS, do Amaral A, Mora F. Stable marker-trait associations for growth across different ages in Eucalyptus cladocalyx through the use of microsatellites. Sci For. 2018;46:367–76.
Mantere T, Kersten S, Hoischen A. Long-read sequencing emerging in medical genetics. Front Genet. 2019;10:426.
Marie D, Brown SC. A cytometric exercise in plant DNA histograms, with 2C values for 70 species. Biol Cell. 1993;78(1–2):41–51.
Mazanec RA, Mason ML. Genetic variation in Eucalyptus diversicolor F. Muell. in Western Australia and potential gains from selection. For Ecol Manag. 1993;62(1–4):285–301.
McDonald T, Jonson J, Dixon K. National standards for the practice of ecological restoration in Australia. Restor Ecol. 2016;24:S4–S32.
McKinnon GE, Steane DA, Potts BM, Vaillancourt RE. Incongruence between chloroplast and species phylogenies in Eucalyptus subgenus Monocalyptus (Myrtaceae). Am J Bot. 1999;86(7):1038–46.
McKinnon GE, Vaillancourt RE, Jackson HD, Potts BM. Chloroplast sharing in the Tasmanian eucalypts. Evolution. 2001;55(4):703–11.
McKinnon GE, Smith JJ, Potts BM. Recurrent nuclear DNA introgression accompanies chloroplast DNA exchange between two eucalypt species. Mol Ecol. 2010;19(7):1367–80.
McLean EH, Prober SM, Stock WD, Steane DA, Potts BM, Vaillancourt RE, et al. Plasticity of functional traits varies clinally along a rainfall gradient in Eucalyptus tricarpa. Plant Cell Environ. 2014;37(6):1440–51.
McRae TA, Pilbeam DJ, Gore PL, Dutkowski GW, Apiolaza LA. Australian cooperative tree improvement strategy for Eucalyptus globulus. In: IUFRO, editor. Developing the eucalypt of the future: proceedings IUFRO international symposium. Valdivia: IUFRO; 2001. p. 179.
McRae TA, Pilbeam DJ, Powell M, Dutkowski GW, Joyce K, Tier B. Genetic evaluation in eucalypt breeding programs. In: Borralho N, Pereira J, Marques C, Coutinho J, Madeira M, Tomé M, editors. Eucalyptus in a changing world. Proceedings of IUFRO conference. RAIZ, Instituto Investigação de Floresta e Papel; 2004. p. 189–90.
Meuwissen THE, Hayes BJ, Goddard M. Prediction of total genetic value using genome-wide dense marker maps. Genetics. 2001;157(4):1819–29.
Mhoswa L, O’Neill MM, Mphahlele MM, Oates CN, Payn KG, Slippers B, et al. A genome-wide association study for resistance to the insect pest Leptocybe invasa in Eucalyptus grandis reveals genomic regions and positional candidate defense genes. Plant Cell Physiol. 2020;61(7):1285–96.
Mizrachi E, Hefer CA, Ranik M, Joubert F, Myburg AA. De novo assembled expressed gene catalog of a fast-growing Eucalyptus tree produced by Illumina mRNA-Seq. BMC Genomics. 2010;11(1):681.
Moran GF. Patterns of genetic diversity in Australian tree species. New For. 1992;6(1):49–66.
Moran GF, Bell JC. Eucalyptus. In: Tanksley S, Orton T, editors. Isozymes in plant genetics and breeding. Part B. Amsterdam: Elsevier Science Publishers; 1983. p. 423–41.
Moran GF, Forrester RI, Rout AR. Early growth of Eucalyptus delegatensis provenances in four field trials in south-eastern Australia. N Z J For Sci. 1990;20(2):148–61.
Morgante M, De Paoli E, Radovic S. Transposable elements and the plant pan-genomes. Curr Opin Plant Biol. 2007;10(2):149–55.
Mostert-O’Neill MM, Reynolds SM, Acosta JJ, Lee DJ, Borevitz JO, Myburg AA. Genomic evidence of introgression and adaptation in a model subtropical tree species, Eucalyptus grandis. Mol Ecol. 2021;30(3):625–38.
Mphahlele MM, Isik F, Mostert-O’Neill MM, Reynolds SM, Hodge GR, Myburg AA. Expected benefits of genomic selection for growth and wood quality traits in Eucalyptus grandis. Tree Genet Genomes. 2020;16(4):49.
Müller BSF, Neves LG, de Almeida Filho JE, Resende MFR, Muñoz PR, Dos Santos PET, et al. Genomic prediction in contrast to a genome-wide association study in explaining heritable variation of complex growth traits in breeding populations of Eucalyptus. BMC Genomics. 2017;18(1):524.
Müller BSF, de Almeida Filho JE, Lima BM, Garcia CC, Missiaggia A, Aguiar AM, et al. Independent and Joint-GWAS for growth traits in Eucalyptus by assembling genome-wide data for 3373 individuals across four breeding populations. New Phytol. 2019;221(2):818–33.
Murray KD, Janes JK, Jones A, Bothwell HM, Andrew RL, Borevitz JO. Landscape drivers of genomic diversity and divergence in woodland Eucalyptus. Mol Ecol. 2019;28(24):5232–47.
Myburg AA, Vogl C, Griffin AR, Sederoff RR, Whetten RW. Genetics of postzygotic isolation in Eucalyptus: whole-genome analysis of barriers to introgression in a wide interspecific cross of Eucalyptus grandis and E. globulus. Genetics. 2004;166(3):1405–18.
Myburg AA, Potts BM, Marques CM, Kirst M, Gion JM, Grattapaglia D, et al. Eucalypts. In: Kole C, editor. Genome mapping and molecular breeding in plants. Springer; 2007. p. 115–60.
Myburg AA, Grattapaglia D, Tuskan GA, Hellsten U, Hayes RD, Grimwood J, et al. The genome of Eucalyptus grandis. Nature. 2014;510(7505):356–62.
Nascimento LC, Salazar MM, Lepikson-Neto J, Camargo ELO, Parreiras LS, Pereira GAG, et al. EUCANEXT: an integrated database for the exploration of genomic and transcriptomic data from Eucalyptus species. Database. 2017;2017:bax079.
Neves LG, Mamani EMC, Alfenas AC, Kirst M, Grattapaglia D. A high-density transcript linkage map with 1,845 expressed genes positioned by microarray-based Single Feature Polymorphisms (SFP) in Eucalyptus. BMC Genomics. 2011;12:189.
Nevill PG, Després T, Bayly MJ, Bossinger G, Ades PK. Shared phylogeographic patterns and widespread chloroplast haplotype sharing in Eucalyptus species with different ecological tolerances. Tree Genet Genomes. 2014;10(4):1079–92.
Nickolas H, Harrison PA, Tilyard P, Vaillancourt RE, Potts BM. Inbreeding depression and differential maladaptation shape the fitness trajectory of two co-occurring Eucalyptus species. Ann For Sci. 2019;76:10.
Nicolle D. A classification and census of regenerative strategies in the eucalypts (Angophora, Corymbia and Eucalyptus—Myrtaceae), with special reference to the obligate seeders. Aust J Bot. 2006;54(4):391–407.
Nicolle D. Classification of the eucalypts (Angophora, Corymbia and Eucalyptus) version 3. 2019. http://www.dn.com.au/Classification-Of-The-Eucalypts.pdf. Accessed Nov 2019.
Novaes E, Drost DR, Farmerie WG, Pappas GJ, Grattapaglia D, Sederoff RR, et al. High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. BMC Genomics. 2008;9(1):312.
NVIS. Native vegetation information system. 2019. https://www.awe.gov.au/agriculture-land/land/native-vegetation/national-vegetation-information-system. Accessed June 2019
O’Brien EK, Krauss SL. Testing the home-site advantage in forest trees on disturbed and undisturbed sites. Restor Ecol. 2010;18(3):359–72.
O’Brien EK, Mazanec RA, Krauss SL. Provenance variation of ecologically important traits of forest trees: implications for restoration. J Appl Ecol. 2007;44(3):583–93.
O’Reilly-Wapstra JM, Freeman JS, Davies NW, Vaillancourt RE, Fitzgerald H, Potts BM. Quantitative trait loci for foliar terpenes in a global eucalypt species. Tree Genet Genomes. 2011;7(3):485–98.
O’Reilly-Wapstra JM, Freeman JS, Barbour R, Vaillancourt RE, Potts BM. Genetic analysis of the near-infrared spectral phenome of a global Eucalyptus species. Tree Genet Genomes. 2013;9(4):943–59.
Obudulu O, Mähler N, Skotare T, Bygdell J, Abreu IN, Ahnlund M, et al. A multi-omics approach reveals function of secretory carrier-associated membrane proteins in wood formation of Populus trees. BMC Genomics. 2018;19(1):11
Orr HA. The population genetics of speciation: the evolution of hybrid incompatibilities. Genetics. 1995;139(4):1805–13.
Oudjehih B, Abdellah B. Chromosome numbers of the 59 species of Eucalyptus L’Herit. (Myrtaceae). Caryologia. 2006;59(3):207–12.
Padovan A, Webb H, Mazanec R, Grayling P, Bartle J, Foley WJ, et al. Association genetics of essential oil traits in Eucalyptus loxophleba: explaining variation in oil yield. Mol Breed. 2017;37(6):73.
Paiva JAP, Prat E, Vautrin S, Santos MD, San-Clemente H, Brommonschenkel S, et al. Advancing Eucalyptus genomics: identification and sequencing of lignin biosynthesis genes from deep-coverage BAC libraries. BMC Genomics. 2011;12(1):137.
Paludeto JGZ, Grattapaglia D, Estopa RA, Tambarussi EV. Genomic relationship-based genetic parameters and prospects of genomic selection for growth and wood quality traits in Eucalyptus benthamii. Tree Genet Genomes. 2021;17(4):38.
Paux E, Carocha V, Marques C, de Sousa A, Borralho N, Sivadon P, et al. Transcript profiling of Eucalyptus xylem genes during tension wood formation. New Phytol. 2005;167(1):89–100.
Payn KG, Dvorak WS, Janse BJH, Myburg AA. Microsatellite diversity and genetic structure of the commercially important tropical tree species Eucalyptus urophylla, endemic to seven islands in eastern Indonesia. Tree Genet Genomes. 2008a;4(3):519–30.
Petit RJ, Hampe A. Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst. 2006;37:187–214.
Petroli CD, Sansaloni CP, Carling J, Steane DA, Vaillancourt RE, Myburg AA, et al. Genomic characterization of DArT markers based on high-density linkage analysis and physical mapping to the Eucalyptus genome. PLoS One. 2012;7(9):e44684.
Pfeilsticker TR, Jones RC, Steane DA, Harrison PA, Vaillancourt RE, Potts BM. Expansion of the rare Eucalyptus risdonii under climate change through hybridization with a closely related species despite hybrid inferiority. Ann Bot. 2022;129(1):1–14.
Pinosio S, Giacomello S, Faivre-Rampant P, Taylor G, Jorge V, Le Paslier MC, et al. Characterization of the poplar pan-genome by genome-wide identification of structural variation. Mol Biol Evol. 2016;33(10):2706–19.
Poke FS, Vaillancourt RE, Potts BM, Reid JB. Genomic research in Eucalyptus. Genetica. 2005;125(1):79–101.
Potts BM. Variation in the Eucalyptus gunnii-archeri complex. III. Reciprocal transplant trials. Aust J Bot. 1985;33(6):687–704.
Potts BM. Genetic improvement of eucalypts. In: Burley J, Evans J, Youngquist J, editors. Encyclopedia of forest science. Elsevier Science; 2004. p. 1480–90.
Potts BM, Jackson WD. Evolutionary processes in the Tasmanian high altitude eucalypts. In: Barlow B, editor. Flora and fauna of alpine Australasia. Ages and origins. CSIRO; 1986. p. 511–27.
Potts BM, Reid JB. Variation in the Eucalyptus gunnii-archeri complex. II. The origin of variation. Aust J Bot. 1985;33(5):519–41.
Potts BM, Reid JB. Hybridization as a dispersal mechanism. Evolution. 1988;42(6):1245–55.
Potts BM, Wiltshire R. Eucalypt genetics and genecology. In: Williams JE, Woinarski J, editors. Eucalypt ecology: individuals to ecosystems. Cambridge University Press; 1997. p. 56–91.
Potts BM, Barbour RC, Hingston AB, Vaillancourt RE. Genetic pollution of native eucalypt gene pools – identifying the risks. Aust J Bot. 2003;51(1):1–25.
Potts BM, Vaillancourt RE, Jordan GJ, Dutkowski GW, Silva JCE, McKinnon GE, et al. Exploration of the Eucalyptus globulus gene pool. In: Borralho N, Pereira J, Marques C, Coutinho J, Madeira M, Tomé M, editors. Eucalyptus in a changing world. Proceedings of IUFRO conference. RAIZ, Instituto Investigação de Floresta e Papel; 2004. p. 46–61.
Potts B, Hamilton M, Pilbeam D. Mejoramiento genético de eucaliptos de zonas templadas en Australia [Genetic improvement of temperate eucalypts in Australia]. In: Ipinza R, Barros S, Gutierrez B, Borralho N, editors. Mejoramiento Genético de Eucaliptos de en Chile. INFOR Instituto Forestal (chapter translated into Spanish by editors); 2014. p. 411–44.
Praça MM, Carvalho CR, Novaes CRDB. Nuclear DNA content of three Eucalyptus species estimated by flow and image cytometry. Aust J Bot. 2009;57(6):524–31.
Prober SM, Brown AHD. Conservation of the grassy white box woodlands: population genetics and fragmentation of Eucalyptus albens. Conserv Biol. 1994a;8(4):1003–13.
Prober SM, Byrne M, McLean EH, Steane DA, Potts BM, Vaillancourt RE, et al. Climate-adjusted provenancing: a strategy for climate-resilient ecological restoration. Front Ecol Evol. 2015;3:65.
Prober SM, Potts BM, Bailey T, Byrne M, Dillon S, Harrison PA, et al. Climate adaptation and ecological restoration in eucalypts. Proc R Soc Victoria. 2016;128(1):40–53.
Pryor L. A genetic analysis of some Eucalyptus species. Proc Linnean Soc NSW. 1951;76:140–8.
Pryor LD. Anther shape in Eucalyptus genetics and systematics. Proc Linnean Soc NSW. 1953;78:43–8.
Pryor LD. Variation in snow gum (Eucalyptus pauciflora Sieb.). Proc Linnean Soc NSW. 1957;81:299–305.
Pryor LD, Johnson LAS. A classification of the eucalypts: Australian National University Press; 1971.
Pryor L, Johnson L. Eucalyptus, the universal Australian. In: Keast A, editor. Ecological biogeography of Australia. W. Junk; 1981. p. 499–536.
Rajora OP, Eckert AJ, Zinck JWR. Single-locus versus multilocus patterns of local adaptation to climate in eastern white pine (Pinus strobus, Pinaceae). PLoS One. 2016;11(7):e0158691.
Rasmussen-Poblete S, Valdes J, Gamboa MC, Valenzuela PDT, Krauskopf E. Generation and analysis of an Eucalyptus globulus cDNA library constructed from seedlings subjected to low temperature conditions. Electron J Biotechnol. 2008;11(2):56–68.
Raymond CA, Volker PW, Williams ER. Provenance variation, genotype by environment interactions and age-age correlations for Eucalyptus regnans on nine sites in south eastern Australia. For Genet. 1997;4(4):235–51.
Rellstab C, Dauphin B, Exposito-Alonso M. Prospects and limitations of genomic offset in conservation management. Evol Appl. 2021;14(5):1202–12.
Rengel D, Clemente HS, Servant F, Ladouce N, Paux E, Wincker P, et al. A new genomic resource dedicated to wood formation in Eucalyptus. BMC Plant Biol. 2009;9:36.
Resende MDV, Resende Marcio FR Jr, Sansaloni CP, Petroli CD, Missiaggia AA, Aguiar AM, et al. Genomic selection for growth and wood quality in Eucalyptus: capturing the missing heritability and accelerating breeding for complex traits in forest trees. New Phytol. 2012;194(1):116–28.
Resende RT, Vilela Resende MD, Silva FF, Azevedo CF, Takahashi EK, Silva-Junior OB, et al. Regional heritability mapping and genome-wide association identify loci for complex growth, wood and disease resistance traits in Eucalyptus. New Phytol. 2017a;213(3):1287–300.
Resende RT, Resende MDV, Silva FF, Azevedo CF, Takahashi EK, Silva-Junior OB, et al. Assessing the expected response to genomic selection of individuals and families in Eucalyptus breeding with an additive-dominant model. Heredity. 2017b;119(4):245–55.
Ribeiro T, Barrela RM, Berges H, Marques C, Loureiro J, Morais-Cecílio L, et al. Advancing Eucalyptus genomics: cytogenomics reveals conservation of Eucalyptus genomes. Front Plant Sci. 2016;7:510.
Rosado CCG, da Silva Guimarães LM, Faria DA, de Resende MDV, Cruz CD, Grattapaglia D, et al. QTL mapping for resistance to Ceratocystis wilt in Eucalyptus. Tree Genet Genomes. 2016;12(4):72.
Rossetto M, Lucarotti F, Hopper SD, Dixon KW. DNA fingerprinting of Eucalyptus graniticola: a critically endangered relict species or a rare hybrid? Heredity. 1997;79(3):310–8.
Rubilar R, Hubbard R, Emhart V, Mardones O, Quiroga J, Medina A, et al. Climate and water availability impacts on early growth and growth efficiency of Eucalyptus genotypes: the importance of GxE interactions. For Ecol Manag. 2020;458:117763.
Rutherford S. Insights into speciation and species delimitation of closely related eucalypts using an interdisciplinary approach. Aust Syst Bot. 2020;33(1):110–27.
Rutherford S, Rossetto M, Bragg JG, McPherson H, Benson D, Bonser SP, et al. Speciation in the presence of gene flow: population genomics of closely related and diverging Eucalyptus species. Heredity. 2018;121:126–41.
Rutherford S, van der Merwe M, Wilson PG, Kooyman RM, Rossetto M. Managing the risk of genetic swamping of a rare and restricted tree. Conserv Genet. 2019;20(5):1113–31.
Rutherford S, Wan JSH, Cohen JM, Benson D, Rossetto M. Looks can be deceiving: speciation dynamics of co-distributed Angophora (Myrtaceae) species in a varying landscape. Evolution. 2021;75(2):310–29.
Sansaloni CP, Petroli CD, Carling J, Hudson CJ, Steane DA, Myburg AA, et al. A high-density Diversity Arrays Technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Methods. 2010;6:16.
Sansaloni C, Petroli C, Jaccoud D, Carling J, Detering F, Grattapaglia D, et al. Diversity Arrays Technology (DArT) and next-generation sequencing combined: genome-wide, high throughput, highly informative genotyping for molecular breeding of Eucalyptus. BMC Proc. 2011;5:54.
Santos SA, Vidigal PMP, Guimaraes L, Mafia RG, Templeton MD, Alfenas AC. Transcriptome analysis of Eucalyptus grandis genotypes reveals constitutive overexpression of genes related to rust (Austropuccinia psidii) resistance. Plant Mol Biol. 2020;104(4):339–57.
Schuster TM, Setaro SD, Tibbits JFG, Batty EL, Fowler RM, McLay TGB, et al. Chloroplast variation is incongruent with classification of the Australian bloodwood eucalypts (genus Corymbia, family Myrtaceae). PLoS One. 2018;13(4):e0195034.
Sexton TR, Lima BM, Thavamanikumar S. Molecular mapping of complex traits in Eucalyptus. In: Henry R, Kole C, editors. Genetics, genomics and breeding of eucalypts. CRC Press; 2014. p. 75–102.
Shepherd M, Bartle J, Lee DJ, Brawner J, Bush D, Turnbull P, et al. Eucalypts as a biofuel feedstock. Biofuels. 2011;2(6):639–57.
Silva-Junior OB, Grattapaglia D. Genome-wide patterns of recombination, linkage disequilibrium and nucleotide diversity from pooled resequencing and single nucleotide polymorphism genotyping unlock the evolutionary history of Eucalyptus grandis. New Phytol. 2015;208(3):830–45.
Silva-Junior OB, Faria DA, Grattapaglia D. A flexible multi-species genome-wide 60K SNP chip developed from pooled resequencing of 240 Eucalyptus tree genomes across 12 species. New Phytol. 2015;206(4):1527–40.
Singh D, Wang X, Kumar U, Gao L, Noor M, Imtiaz M, et al. High-throughput phenotyping enabled genetic dissection of crop lodging in wheat. Front Plant Sci. 2019;10:394.
Slayter RO. Altitudinal variation in the photosynthetic characteristics of snow gum, Eucalyptus pauciflora Sieb. ex Spreng. IV. Temperature response of four populations grown at different temperatures. Funct Plant Biol. 1977;4(4):583–94.
Slotte T. The impact of linked selection on plant genomic variation. Brief Funct Genomics. 2014;13(4):268–75.
Smith S, Hughes J, Wardell-Johnson G. High population differentiation and extensive clonality in a rare mallee eucalypt: Eucalyptus curtisii. Conserv Genet. 2003;4(3):289–300.
Song Z, Zhang M, Li F, Weng Q, Zhou C, Li M, et al. Genome scans for divergent selection in natural populations of the widespread hardwood species Eucalyptus grandis (Myrtaceae) using microsatellites. Sci Rep. 2016;6:34941.
Southerton SG, MacMillan CP, Bell JC, Bhuiyan N, Dowries G, Ravenwood IC, et al. Association of allelic variation in xylem genes with wood properties in Eucalyptus nitens. Aust For. 2010;73(4):259–64.
Sow MD, Allona I, Ambroise C, Conde D, Fichot R, Gribkova S, et al. Epigenetics in forest trees: state of the art and potential implications for breeding and management in a context of climate change. Adv Bot Res. 2018;88:387–453.
Steane DA, Byrne M, Vaillancourt RE, Potts BM. Chloroplast DNA polymorphism signals complex interspecific interactions in Eucalyptus (Myrtaceae). Aust Syst Bot. 1998;11(1):25–40.
Steane DA, Nicolle D, McKinnon GE, Vaillancourt RE, Potts BM. Higher-level relationships among the eucalypts are resolved by ITS-sequence data. Aust Syst Bot. 2002;15(1):49–62.
Steane DA, Jones RC, Vaillancourt RE. A set of chloroplast microsatellite primers for Eucalyptus (Myrtaceae). Mol Ecol Notes. 2005a;5(3):538–41.
Steane DA, Nicolle D, Sansaloni CP, Petroli CD, Carling J, Kilian A, et al. Population genetic analysis and phylogeny reconstruction in Eucalyptus (Myrtaceae) using high-throughput, genome-wide genotyping. Mol Phylogenet Evol. 2011;59(1):206–24.
Steane DA, Potts BM, McLean E, Prober SM, Stock WD, Vaillancourt RE, et al. Genome-wide scans detect adaptation to aridity in a widespread forest tree species. Mol Ecol. 2014;23(10):2500–13.
Steane DA, Potts BM, McLean E, Collins L, Prober SM, Stock WD, et al. Genome-wide scans reveal cryptic population structure in a dry-adapted eucalypt. Tree Genet Genomes. 2015;11(3):33.
Steane DA, Mclean EH, Potts BM, Prober SM, Stock WD, Stylianou VM, et al. Evidence for adaptation and acclimation in a widespread eucalypt of semi-arid Australia. Biol J Linn Soc. 2017a;121(3):484–500.
Steane DA, Potts BM, McLean EH, Collins L, Holland BR, Prober SM, et al. Genomic scans across three eucalypts suggest that adaptation to aridity is a genome-wide phenomenon. Genome Biol Evol. 2017b;9(2):253–65.
Su G, Christensen OF, Janss L, Lund MS. Comparison of genomic predictions using genomic relationship matrices built with different weighting factors to account for locus-specific variances. J Dairy Sci. 2014;97(10):6547–59.
Sumathi M, Yasodha R. Microsatellite resources of Eucalyptus: current status and future perspectives. Bot Stud. 2014;55:73.
Sumathi M, Bachpai VKW, Mayavel A, Dasgupta MG, Nagarajan B, Rajasugunasekar D, et al. Genetic linkage map and QTL identification for adventitious rooting traits in red gum eucalypts. 3 Biotech. 2018a;8(5):242.
Sumathi M, Bachpai VKW, Deeparaj B, Mayavel A, Dasgupta MG, Nagarajan B, et al. Quantitative trait loci mapping for stomatal traits in interspecific hybrids of Eucalyptus. J Genet. 2018b;97(1):323–9.
Suontama M, Klápště J, Telfer E, Graham N, Stovold T, Low C, et al. Efficiency of genomic prediction across two Eucalyptus nitens seed orchards with different selection histories. Heredity. 2019;122(3):370–9.
Supple MA, Bragg JG, Broadhurst LM, Nicotra AB, Byrne M, Andrew RL, et al. Landscape genomic prediction for restoration of a Eucalyptus foundation species under climate change. eLife. 2018;7:e31835.
Tan B, Grattapaglia D, Martins GS, Ferreira KZ, Sundberg B, Ingvarsson PK. Evaluating the accuracy of genomic prediction of growth and wood traits in two Eucalyptus species and their F1 hybrids. BMC Plant Biol. 2017;17:110.
Tan B, Grattapaglia P, Wu HX, Ingvarsson PK. Genomic relationships reveal significant dominance effects for growth in hybrid Eucalyptus. Plant Sci. 2018;267:84–93.
Thavamanikumar S, Southerton S, Thumma B. RNA-Seq using two populations reveals genes and alleles controlling wood traits and growth in Eucalyptus nitens. PLoS One. 2014a;9(6):e101104.
Thavamanikumar S, McManus LJ, Ades PK, Bossinger G, Stackpole DJ, Kerr R, et al. Association mapping for wood quality and growth traits in Eucalyptus globulus ssp. globulus Labill identifies nine stable marker-trait associations for seven traits. Tree Genet Genomes. 2014b;10(6):1661–78.
Thavamanikumar S, Arnold RJ, Luo J, Thumma BR. Genomic studies reveal substantial dominant effects and improved genomic predictions in an open-pollinated breeding population of Eucalyptus pellita. G3 (Bethesda). 2020;10(10):3751–63.
Thiebaut F, Hemerly AS, Ferreira PCG. A role for epigenetic regulation in the adaptation and stress responses of non-model plants. Front Plant Sci. 2019;10:246.
Thumma BR, Nolan MF, Evans R, Moran GF. Polymorphisms in cinnamoyl CoA reductase (CCR) are associated with variation in microfibril angle in Eucalyptus spp. Genetics. 2005;171(3):1257–65.
Thumma BR, Sharma N, Southerton SG. Transcriptome sequencing of Eucalyptus camaldulensis seedlings subjected to water stress reveals functional single nucleotide polymorphisms and genes under selection. BMC Genomics. 2012;13(1):364.
Tng DYP, Williamson GJ, Jordan GJ, Bowman D. Giant eucalypts – globally unique fire-adapted rain-forest trees? New Phytol. 2012;196(4):1001–14.
Torres-Dini D, Nunes ACP, Aguiar A, Nikichuk N, Centurión C, Cabrera M, et al. Clonal selection of for productivity, adaptability, and stability, using SNP markers. Silvae Genet. 2016;65(2):30–8.
Turnbull JW. Economic and social importance of eucalypts. In: Keane P, Kile G, Podger F, Brown B, editors. Diseases and pathogens of eucalypts. CSIRO Publishing; 2000. p. 1–9.
Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science. 2006;313(5793):1596–604.
Tuskan GA, Groover AT, Schmutz J, DiFazio SP, Myburg A, Grattapaglia D, et al. Hardwood tree genomics: unlocking woody plant biology. Front Plant Sci. 2018;9:1799.
Valenzuela CE, Ballesta P, Ahmar S, Fiaz S, Heidari P, Maldonado C, et al. Haplotype- and SNP-based GWAS for growth and wood quality traits in Eucalyptus cladocalyx trees under arid conditions. Plan Theory. 2021;10(1):148.
Van Dijk K, Waycott M, Quarmby J, Bickerton D, Thornhill AH, Cross H, et al. Genomic screening reveals that the endangered Eucalyptus paludicola (Myrtaceae) is a hybrid. Diversity. 2020;12(12):468.
Van Raden PM, Van Tassell C, Wiggans G, Sonstegard T, Schnabel R, Schenkel F. Reliability of genomic predictions for North American dairy bulls. J Dairy Sci. 2009;92:16–24.
Villar E, Klopp C, Noirot C, Novaes E, Kirst M, Plomion C, et al. RNA-Seq reveals genotype-specific molecular responses to water deficit in Eucalyptus. BMC Genomics. 2011;12(1):538.
Vining KJ, Romanel E, Jones RC, Klocko A, Alves-Ferreira M, Hefer CA, et al. The floral transcriptome of Eucalyptus grandis. New Phytol. 2015;206(4):1406–22.
Volker PW, Potts BM, Borralho NMG. Genetic parameters of intra-and inter-specific hybrids of Eucalyptus globulus and E. nitens. Tree Genet Genomes. 2008;4(3):445–60.
von Takach Dukai B, Jack C, Borevitz J, Lindenmayer DB, Banks SC. Pervasive admixture between eucalypt species has consequences for conservation and assisted migration. Evol Appl. 2019;12(4):845–60.
Wallis IR, Keszei A, Henery ML, Moran GF, Forrester R, Maintz J, et al. A chemical perspective on the evolution of variation in Eucalyptus globulus. Perspect Plant Ecol Evol Syst. 2011;13(4):305–18.
Wang W, Das A, Kainer D, Schalamun M, Morales-Suarez A, Schwessinger B, et al. The draft nuclear genome assembly of Eucalyptus pauciflora: a pipeline for comparing de novo assemblies. Gigascience. 2020;9:giz160.
Warren CR, Tausz M, Adams MA. Does rainfall explain variation in leaf morphology and physiology among populations of red ironbark (Eucalyptus sideroxylon subsp. tricarpa) grown in a common garden? Tree Physiol. 2005;25(11):1369–78.
Wheeler MA, Byrne M, McComb JA. Little genetic differentiation within the dominant forest tree, Eucalyptus marginata (Myrtaceae) of south-western Australia. Silvae Genet. 2003a;52(5–6):254–9.
Wilkinson GR. Population differentiation within Eucalyptus obliqua: implications for regeneration success and genetic conservation in production forests. Aust For. 2008;71(1):4–15.
Williams J, Woinarski J. Eucalypt ecology: individuals to ecosystems: Cambridge University Press; 1997.
Williams DR, Potts BM, Black PG. Testing single visit pollination procedures for Eucalyptus globulus and E. nitens. Aust For. 1999;62(4):346–52.
Wrigley J, Fagg M. Eucalypts: a celebration: Allen & Unwin; 2010.
Xie Y, Arnold RJ, Wu Z, Chen S, Du A, Luo J. Advances in eucalypt research in China. Front Agric Sci Eng. 2017;4(4):380–90.
Yong WTL, Ades PK, Runa FA, Bossinger G, Sandhu KS, Potts BM, et al. Genome-wide association study of myrtle rust (Austropuccinia psidii) resistance in Eucalyptus obliqua (subgenus Eucalyptus). Tree Genet Genomes. 2021;17(3):31.
Zhou C, Wang L, Weng Q, Li F, Li M, Chen J, et al. Association of microsatellite markers with growth and wood mechanical traits in Eucalyptus cloeziana F. Muell. (Myrtaceae). Ind Crop Prod. 2020;154:112702.
Appendix References
Andrade MC, Perek M, Pereira FB, Moro M, Tambarussi EV. Quantity, organization, and distribution of chloroplast microsatellites in all species of Eucalyptus with available plastome sequence. Crop Breed Appl Biotechnol. 2018b;18:97–102.
Bezemer N. Wild seedlings of a tree endemic on granite outcrops show no evidence of inbreeding depression. Aust J Bot. 2018;66:39–47.
Bezemer N, Krauss SL, Phillips RD, Roberts DG, Hopper SD. Paternity analysis reveals wide pollen dispersal and high multiple paternity in a small isolated population of the bird-pollinated Eucalyptus caesia (Myrtaceae). Heredity. 2016;117:460–71.
Bloomfield JA, Nevill P, Potts BM, Vaillancourt RE, Steane DA. Molecular genetic variation in a widespread forest tree species Eucalyptus obliqua (Myrtaceae) on the island of Tasmania. Aust J Bot. 2011b;59:226–37.
Breed MF, Christmas MJ, Lowe AJ. Higher levels of multiple paternities increase seedling survival in the long-lived tree Eucalyptus gracilis. PLoS One. 2014;9:e90478.
Breed MF, Ottewell KM, Gardner MG, Marklund MHK, Stead MG, Harris JBC, et al. Mating system and early viability resistance to habitat fragmentation in a bird-pollinated eucalypt. Heredity. 2015;115:100–7.
Broadhurst LM. A genetic analysis of scattered Yellow Box trees (Eucalyptus melliodora A.Cunn. ex Schauer, Myrtaceae) and their restored cohorts. Biol Conserv. 2013;161:48–57.
Broadhurst L, Breed M, Lowe A, Bragg J, Catullo R, Coates D, et al. Genetic diversity and structure of the Australian flora. Divers Distrib. 2017b;23:41–52.
Broadhurst LM, Mellick R, Knerr N, Li L, Supple MA. Land availability may be more important than genetic diversity in the range shift response of a widely distributed eucalypt, Eucalyptus melliodora. For Ecol Manag. 2018b;409:38–46.
Brondani RPV, Brondani C, Tarchini R, Grattapaglia D. Development, characterization and mapping of microsatellite markers in Eucalyptus grandis and E. urophylla. Theor Appl Genet. 1998;97:816–27.
Brondani RPV, Brondani C, Grattapaglia D. Towards a genus-wide reference linkage map for Eucalyptus based exclusively on highly informative microsatellite markers. Mol Gen Genomics. 2002;267:338–47.
Brondani RPV, Williams ER, Brondani C, Grattapaglia D. A microsatellite-based consensus linkage map for species of Eucalyptus and a novel set of 230 microsatellite markers for the genus. BMC Plant Biol. 2006;6:20.
Butcher PA, McDonald MW, Bell JC. Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis. Tree Genet Genomes. 2009b;5:189–210.
Byrne M. High genetic identities between three oil mallee taxa, Eucalyptus kochii ssp. kochii, ssp. plenissima and E. horistes, based on nuclear RFLP analysis. Heredity. 1999b;82:205–11.
Byrne M. Phylogeny, diversity and evolution of eucalypts. In: Sharma AK, Sharma A, editors. Plant genome biodiversity and evolution. Science Publishers; 2008b. p. 303–46.
Byrne M, Hines B. Phylogeographical analysis of cpDNA variation in Eucalyptus loxophleba (Myrtaceae). Aust J Bot. 2004b;52:459–70.
Byrne M, Hopper SD. Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biol J Linn Soc. 2008b;93:177–88.
Byrne M, Macdonald B. Phylogeography and conservation of three oil mallee taxa, Eucalyptus kochii ssp kochii, ssp plenissima and E. horistes. Aust J Bot. 2000b;48:305–12.
Byrne M, MarquezGarcia MI, Uren T, Smith DS, Moran GF. Conservation and genetic diversity of microsatellite loci in the genus Eucalyptus. Aust J Bot. 1996;44:331–41.
Byrne M, Parrish TL, Moran GF. Nuclear RFLP diversity in Eucalyptus nitens. Heredity. 1998b;81:225–33.
Byrne M, Koenders A, Rogerson K, Sampson J, van Etten EJB. Genetic and morphological analysis of multi-stemmed plants of tuart (Eucalyptus gomphocephala). Aust J Bot. 2017a;64(8):704–14.
Byrne M, Millar MA, Coates DJ, Macdonald BM, McArthur SM, Zhou M, et al. Refining expectations for environmental characteristics of refugia: two ranges of differing elevation and topographical complexity are mesic refugia in an arid landscape. J Biogeogr. 2017b;44:2539–50.
Cook IO, Ladiges PY. Isozyme variation in Eucalyptus nitens and E. denticulata. Aust J Bot. 1998;46:35–44.
da Silva JM, de Sousa ACB, De Souza AP, Mori ES, Freitas MLM, Sebbenn AM, et al. Development and characterization of 14 microsatellite loci from an enriched genomic library of Eucalyptus camaldulensis Dehnh. Conserv Genet Resour. 2009;1:465–9.
Elliott C, Byrne M. Genetic diversity within and between natural populations of Eucalyptus occidentalis (Myrtaceae). Silvae Genet. 2003;52:169–73.
Faria DA, Mamani EMC, Pappas GJ, Grattapaglia D. Genotyping systems for Eucalyptus based on tetra-, penta-, and hexanucleotide repeat EST microsatellites and their use for individual fingerprinting and assignment tests. Tree Genet Genomes. 2011;7:63–77.
Field DL, Ayre DJ, Whelan RJ, Young AG. Patterns of hybridization and asymmetrical gene flow in hybrid zones of the rare Eucalyptus aggregata and common E. rubida. Heredity. 2011c;106:841–53.
Foster SA, McKinnon GE, Steane DA, Potts BM, Vaillancourt RE. Parallel evolution of dwarf ecotypes in the forest tree Eucalyptus globulus. New Phytol. 2007b;175:370–80.
Freeman JS, Jackson HD, Steane DA, McKinnon GE, Dutkowski GW, Potts BM, et al. Chloroplast DNA phylogeography of Eucalyptus globulus. Aust J Bot. 2001;49:585–96.
Gaiotto FA, Bramucci M, Grattapaglia D. Estimation of outcrossing rate in a breeding population of Eucalyptus urophylla with dominant RAPD and AFLP markers. Theor Appl Genet. 1997;95:842–9.
Gauli A, Vaillancourt RE, Steane DA, Bailey TG, Potts BM. Effect of forest fragmentation and altitude on the mating system of Eucalyptus pauciflora (Myrtaceae). Aust J Bot. 2013;61:622–32.
Glaubitz JC, Emebiri LC, Moran GF. Dinucleotide microsatellites from Eucalyptus sieberi: inheritance, diversity, and improved scoring of single-base differences. Genome. 2001;44:1041–5.
Grattapaglia D, Mamani EMC, Silva OB, Faria DA. A novel genome-wide microsatellite resource for species of Eucalyptus with linkage-to-physical correspondence on the reference genome sequence. Mol Ecol Resour. 2015;15:437–48.
Harrison PA, Jones RC, Vaillancourt RE, Wiltshire RJE, Potts BM. Unravelling the evolutionary history of Eucalyptus cordata (Myrtaceae) using molecular markers. Aust J Bot. 2014;62:114–31.
Hirakawa H, Nakamura Y, Kaneko T, Isobe S, Sakai H, Kato T, et al. Survey of the genetic information carried in the genome of Eucalyptus camaldulensis. Plant Biotechnol. 2011b;28:471–80.
Holman JE, Hughes JM, Fensham RJ. A morphological cline in Eucalyptus: a genetic perspective. Mol Ecol. 2003;12:3013–25.
Holman JE, Hughes JM, Fensham RJ. Origins of a morphological cline between Eucalyptus melanophloia and Eucalyptus whitei. Aust J Bot. 2011b;59:244–52.
House APN, Bell JC. Isozyme variation and mating system in Eucalyptus urophylla St-Blake. Silvae Genet. 1994;43:167–79.
Jones ME, Stokoe RL, Cross MJ, Scott LJ, Maguire TL, Shepherd M. Isolation of microsatellite loci from spotted gum (Corymbia variegata), and cross-species amplification in Corymbia and Eucalyptus. Mol Ecol Notes. 2001;1:276–8.
Jones RC, McKinnon GE, Potts BM, Vaillancourt RE. Genetic diversity and mating system of an endangered tree Eucalyptus morrisbyi. Aust J Bot. 2005b;53:367–77.
Jones TH, Vaillancourt RE, Potts BM. Detection and visualization of spatial genetic structure in continuous Eucalyptus globulus forest. Mol Ecol. 2007;16:697–707.
Jones RC, Steane DA, Lavery M, Vaillancourt RE, Potts BM. Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex. Ecol Evol. 2013;3:1–17.
Kennington WJ, James SH. Allozyme and morphometric variation in two closely related mallee species from western Australia, Eucalyptus argutifolia and E. obtusiflora (Myrtaceae). Aust J Bot. 1998;46:173–86.
Le S, Nock C, Henson M, Shepherd M. Genetic differentiation among and within three red mahoganies (series Annulares), Eucalyptus pellita, E. resinifera and E. scias (Myrtaceae). Aust Syst Bot. 2009;22:332–43.
Li CY. RAPD analysis of genetic variation in Eucalyptus microtheca F. Muell. populations. Hereditas. 2000;132:151–6.
Mimura M, Barbour RC, Potts BM, Vaillancourt RE, Watanabe KN. Comparison of contemporary mating patterns in continuous and fragmented Eucalyptus globulus native forests. Mol Ecol. 2009;18:4180–92.
Mora F, Arriagada O, Ballesta P, Ruiz E. Genetic diversity and population structure of a drought-tolerant species of Eucalyptus, using microsatellite markers. J Plant Biochem Biotechnol. 2017;26:274–81.
Nesbitt KA, Potts BM, Vaillancourt RE, West AK, Reid JB. Partitioning and distribution of RAPD variation in a forest tree species, Eucalyptus globulus (Myrtaceae). Heredity. 1995;74:628–37.
Nevill PG, Bradbury D, Jorgensen T, Krauss S, Samaraweera S, Gardner MG. Microsatellite primers identified by 454 sequencing in the floodplain tree species Eucalyptus victrix (Myrtaceae). Appl Plant Sci. 2013;1:1200402.
Okun DO, Kenya EU, Oballa PO, Odee DW, Muluvi GM. Analysis of genetic diversity in Eucalyptus grandis (Hill ex Maiden) seed sources using inter simple sequence repeats (ISSR) molecular markers. Afr J Biotechnol. 2008;7:2119–23.
Ottewell KM, Donnellan SC, Moran GF, Paton DC. Multiplexed microsatellite markers for the genetic analysis of Eucalyptus leucoxylon (Myrtaceae) and their utility for ecological and breeding studies in other Eucalyptus species. J Hered. 2005;96:445–51.
Payn KG, Dvorak WS, Myburg AA. Chloroplast DNA phylogeography reveals the island colonisation route of Eucalyptus urophylla (Myrtaceae). Aust J Bot. 2007;55:673–83.
Payn KG, Dvorak WS, Janse BJH, Myburg AA. Microsatellite diversity and genetic structure of the commercially important tropical tree species Eucalyptus urophylla, endemic to seven islands in eastern Indonesia. Tree Genet Genomes. 2008b;4:519–30.
Poltri SNM, Zelener N, Traverso JR, Gelid P, Hopp HE. Selection of a seed orchard of Eucalyptus dunnii based on genetic diversity criteria calculated using molecular markers. Tree Physiol. 2003;23:625–32.
Prober SM, Brown AHD. Conservation of the grassy white box woodlands – population-genetics and fragmentation of Eucalyptus albens. Conserv Biol. 1994b;8:1003–13.
Rathbone DA, McKinnon GE, Potts BM, Steane DA, Vaillancourt RE. Microsatellite and cpDNA variation in island and mainland populations of a regionally rare eucalypt, Eucalyptus perriniana (Myrtaceae). Aust J Bot. 2007;55:513–20.
Sampson JF, Byrne M. Assessing genetic structure in a rare clonal eucalypt as a basis for augmentation and introduction translocations. Conserv Genet. 2016;17:293–304.
Sampson J, Tapper S, Coates D, Hankinson M, McArthur S, Byrne M. Persistence with episodic range expansion from the early Pleistocene: the distribution of genetic variation in the forest tree Corymbia calophylla (Myrtaceae) in south-western Australia. Biol J Linn Soc. 2018;123:545–60.
Shepherd M, Raymond C. Species differentiation and gene flow in the Blackbutts (genus Eucalyptus subgenus Eucalyptus section Pseudophloius). Conserv Genet. 2010;11:1965–78.
Shepherd M, Kasem S, Lee D, Henry R. Construction of microsatellite linkage maps for Corymbia. Silvae Genet. 2006;55:228–38.
Shepherd M, Kasem S, Ablett G, Ochieng J, Crawford A. Genetic structuring in the spotted gum complex (genus Corymbia, section Politaria). Aust Syst Bot. 2008;21:15–25.
Shepherd M, Sexton TR, Thomas D, Henson M, Henry RJ. Geographical and historical determinants of microsatellite variation in Eucalyptus pilularis. Can J For Res. 2010;40(6):1051–63.
Shepherd M, Henson M, Lee DJ. Revisiting genetic structuring in spotted gums (genus Corymbia section Maculatae) focusing on C. maculata, an early diverged, insular lineage. Tree Genet Genomes. 2012;8:137–47.
Skabo S, Vaillancourt RE, Potts BM. Fine-scale genetic structure of Eucalyptus globulus ssp. globulus forest revealed by RAPDs. Aust J Bot. 1998;46:583–94.
Soto A. Simple PCR markers for the study of chloroplast in Eucalyptus. Silvae Genet. 2004;53:139–40.
Steane DA, Vaillancourt RE, Russell J, Powell W, Marshall D, Potts BM. Development and characterisation of microsatellite loci in Eucalyptus globulus (Myrtaceae). Silvae Genet. 2001;50:89–91.
Steane DA, Jones RC, Vaillancourt RE. A set of chloroplast microsatellite primers for Eucalyptus (Myrtaceae). Mol Ecol Notes. 2005b;5:538–41.
Steane DA, Conod N, Jones RC, Vaillancourt RE, Potts BM. A comparative analysis of population structure of a forest tree, Eucalyptus globulus (Myrtaceae), using microsatellite markers and quantitative traits. Tree Genet Genomes. 2006;2:30–8.
Stokoe RL, Shepherd M, Lee DJ, Nikles DG, Henry RJ. Natural inter-subgeneric hybridization between Eucalyptus acmenoides Schauer and Eucalyptus cloeziana F. Muell (Myrtaceae) in southeast Queensland. Ann Bot. 2001;88:563–70.
Thamarus KA, Groom K, Murrell J, Byrne M, Moran GF. A genetic linkage map for Eucalyptus globulus with candidate loci for wood, fibre, and floral traits. Theor Appl Genet. 2002;104:379–87.
Vaillancourt RE, Jackson HD. A chloroplast DNA hypervariable region in eucalypts. Theor Appl Genet. 2000;101:473–7.
Van Der Nest MA, Steenkamp ET, Wingfield BD, Wingfield MJ. Development of simple sequence repeat (SSR) markers in Eucalyptus from amplified inter-simple sequence repeats (ISSR). Plant Breed. 2000;119:433–6.
Walker E, Byrne M, Macdonald B, Nicolle D, McComb J. Clonality and hybrid origin of the rare Eucalyptus bennettiae (Myrtaceae) in Western Australia. Aust J Bot. 2009;57:180–8.
Wheeler MA, Byrne M, McComb JA. Little genetic differentiation within the dominant forest tree, Eucalyptus marginata (Myrtaceae) of South-Western Australia. Silvae Genet. 2003b;52:254–9.
Yeoh SH, Bell JC, Foley WJ, Wallis IR, Moran GF. Estimating population boundaries using regional and local-scale spatial genetic structure: an example in Eucalyptus globulus. Tree Genet Genomes. 2012;8:695–708.
Zelener N, Poltri SNM, Bartoloni N, Lopez CR, Hopp HE. Selection strategy for a seedling seed orchard design based on trait selection index and genomic analysis by molecular markers: a case study for Eucalyptus dunnii. Tree Physiol. 2005;25:1457–67.
Acknowledgements
The authors thank Clare Holleley and David Bush for constructive feedback on an earlier draft. The authors also thank Karanjeet Sandhu, Robert Wiltshire, Shannon Dillon, Robert Barbour, J.E. Prober and Dario Grattapaglia for permission to use their photos. Publication funding is supported by the Australian Government through the Great Western Woodlands Terrestrial Ecosystems Research Network (TERN) Supersite. The contributions of Brad Potts, Dorothy Steane and RenÕ Vaillancourt to this work was part of the Australian Research Discovery (ARC) grants DP160101650 and DP190102053.
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Appendix
Appendix
Previous population genetics studies of eucalypts including molecular marker development.
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