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1.  Quantitative genetic parameters for yield, plant growth and cone chemical traits in hop (Humulus lupulus L.) 
BMC Genetics  2014;15:22.
Most traits targeted in the genetic improvement of hop are quantitative in nature. Improvement based on selection of these traits requires a comprehensive understanding of their inheritance. This study estimated quantitative genetic parameters for 20 traits related to three key objectives for the genetic improvement of hop: cone chemistry, cone yield and agronomic characteristics.
Significant heritable genetic variation was identified for α-acid and β-acid, as well as their components and relative proportions. Estimates of narrow-sense heritability for these traits (h 2  = 0.15 to 0.29) were lower than those reported in previous hop studies, but were based on a broader suite of families (108 from European, North American and hybrid origins). Narrow-sense heritabilities are reported for hop growth traits for the first time (h 2  = 0.04 to 0.20), relating to important agronomic characteristics such as emergence, height and lateral morphology. Cone chemistry and growth traits were significantly genetically correlated, such that families with more vigorous vegetative growth were associated with lower α-acid and β-acid levels. This trend may reflect the underlying population structure of founder genotypes (European and North American origins) as well as past selection in the Australian environment. Although male and female hop plants are thought to be indistinguishable until flowering, sex was found to influence variation in many growth traits, with male and female plants displaying differences in vegetative morphology from emergence to cone maturity.
This study reveals important insights into the genetic control of quantitative hop traits. The information gained will provide hop breeders with a greater understanding of the additive genetic factors which affect selection of cone chemistry, yield and agronomic characteristics in hop, aiding in the future development of improved cultivars.
PMCID: PMC3927220  PMID: 24524684
Humulus lupulus L; Narrow-sense heritability; Genetic correlation; Hop acid; Dioecy; Quantitative genetics
2.  Quantitative trait loci in hop (Humulus lupulus L.) reveal complex genetic architecture underlying variation in sex, yield and cone chemistry 
BMC Genomics  2013;14:360.
Hop (Humulus lupulus L.) is cultivated for its cones, the secondary metabolites of which contribute bitterness, flavour and aroma to beer. Molecular breeding methods, such as marker assisted selection (MAS), have great potential for improving the efficiency of hop breeding. The success of MAS is reliant on the identification of reliable marker-trait associations. This study used quantitative trait loci (QTL) analysis to identify marker-trait associations for hop, focusing on traits related to expediting plant sex identification, increasing yield capacity and improving bittering, flavour and aroma chemistry.
QTL analysis was performed on two new linkage maps incorporating transferable Diversity Arrays Technology (DArT) markers. Sixty-three QTL were identified, influencing 36 of the 50 traits examined. A putative sex-linked marker was validated in a different pedigree, confirming the potential of this marker as a screening tool in hop breeding programs. An ontogenetically stable QTL was identified for the yield trait dry cone weight; and a QTL was identified for essential oil content, which verified the genetic basis for variation in secondary metabolite accumulation in hop cones. A total of 60 QTL were identified for 33 secondary metabolite traits. Of these, 51 were pleiotropic/linked, affecting a substantial number of secondary metabolites; nine were specific to individual secondary metabolites.
Pleiotropy and linkage, found for the first time to influence multiple hop secondary metabolites, have important implications for molecular selection methods. The selection of particular secondary metabolite profiles using pleiotropic/linked QTL will be challenging because of the difficulty of selecting for specific traits without adversely changing others. QTL specific to individual secondary metabolites, however, offer unequalled value to selection programs. In addition to their potential for selection, the QTL identified in this study advance our understanding of the genetic control of traits of current economic and breeding significance in hop and demonstrate the complex genetic architecture underlying variation in these traits. The linkage information obtained in this study, based on transferable markers, can be used to facilitate the validation of QTL, crucial to the success of MAS.
PMCID: PMC3680207  PMID: 23718194
Linkage map; Transferable marker; Diversity arrays technology DArT; Pleiotropy; Sex-linked marker; Dry cone weight; Plant secondary metabolite; Hop acid; Essential oil
3.  Multiple evolutionary processes drive the patterns of genetic differentiation in a forest tree species complex 
Ecology and Evolution  2013;3(1):1-17.
Forest trees frequently form species complexes, complicating taxonomic classification and gene pool management. This is certainly the case in Eucalyptus, and well exemplified by the Eucalyptus globulus complex. This ecologically and economically significant complex comprises four taxa (sspp. bicostata, globulus, maidenii, pseudoglobulus) that are geographically and morphologically distinct, but linked by extensive “intergrade” populations. To resolve their genetic affinities, nine microsatellites were used to genotype 1200 trees from throughout the natural range of the complex in Australia, representing 33 morphological core and intergrade populations. There was significant spatial genetic structure (FST = 0.10), but variation was continuous. High genetic diversity in southern ssp. maidenii indicates that this region is the center of origin. Genetic diversity decreases and population differentiation increases with distance from this area, suggesting that drift is a major evolutionary process. Many of the intergrade populations, along with other populations morphologically classified as ssp. pseudoglobulus or ssp. globulus, belong to a “cryptic genetic entity” that is genetically and geographically intermediate between core ssp. bicostata, ssp. maidenii, and ssp. globulus. Geography, rather than morphology, therefore, is the best predictor of overall genetic affinities within the complex and should be used to classify germplasm into management units for conservation and breeding purposes.
PMCID: PMC3568837  PMID: 23403692
Blue gum; clinal variation; conservation genetics; evolution; gene pool management; genetic diversity; hybridization; microsatellite DNA; speciation
4.  Low but structured chloroplast diversity in Atherosperma moschatum (Atherospermataceae) suggests bottlenecks in response to the Pleistocene glacials 
Annals of Botany  2011;108(7):1247-1256.
Background and Aims
The cool temperate rainforests of Australia were much reduced in range during the cold and dry glacial periods, although genetic evidence indicates that two key rainforest species, Nothofagus cunninghamii and Tasmannia lanceolata, survived within multiple locations and underwent only local range expansions at the end of the Last Glacial. To better understand the glacial response of a co-occurring but wind-dispersed and less cold-tolerant rainforest tree species, Atherosperma moschatum, a chloroplast phylogeographic study was undertaken.
A total of 3294 bp of chloroplast DNA sequence was obtained for 155 samples collected from across the species' range.
Key Results
The distribution of six haplotypes observed in A. moschatum was geographically structured with an inferred ancestral haplotype restricted to Tasmania, while three non-overlapping and endemic haplotypes were found on the mainland of south-eastern Australia. Last glacial refugia for A. moschatum are likely to have occurred in at least one location in western Tasmania and in Victoria and within at least two locations in the Great Dividing Range of New South Wales. Nucleotide diversity of A. moschatum was lower (π = 0·00021) than either N. cunninghamii (0·00101) or T. lanceolata (0·00073), and was amongst the lowest recorded for any tree species.
This study provides evidence for past bottlenecks having impacted the chloroplast diversity of A. moschatum as a result of the species narrower climatic niche during glacials. This hypothesis is supported by the star-like haplotype network and similar estimated rates of chloroplast DNA substitution for A. moschatum and the two more cold tolerant and co-occurring species that have higher chloroplast diversity, N. cunninghamii and T. lanceolata.
PMCID: PMC3197450  PMID: 21856633
Atherosperma moschatum; A. moschatum subsp. integrifolium; Atherospermataceae; bottleneck; comparative phylogeography; glacial refugia; Nothofagus cunninghamii; Pleistocene glacials; south-eastern Australia; Tasmannia lanceolata; cool temperate rainforest
5.  What does population structure analysis reveal about the Pterostylis longifolia complex (Orchidaceae)? 
Ecology and Evolution  2012;2(11):2631-2644.
Morphologically similar groups of species are common and pose significant challenges for taxonomists. Differences in approaches to classifying unique species can result in some species being overlooked, whereas others are wrongly conserved. The genetic diversity and population structure of the Pterostylis longifolia complex (Orchidaceae) in Tasmania was investigated to determine if four species, and potential hybrids, could be distinguished through genomic AFLP and chloroplast restriction-fragment-length polymorphism (RFLP) markers. Analysis of molecular variance (AMOVA) results indicated that little genetic variation was present among taxa, whereas PCoA analyses revealed genetic variation at a regional scale irrespective of taxa. Population genetic structure analyses identified three clusters that correspond to regional genetic and single taxon-specific phenotypic variation. The results from this study suggest that “longifolia” species have persisted throughout the last glacial maximum in Tasmania and that the complex may be best treated as a single taxon with several morphotypes. These results could have serious evolutionary and conservation implications as taxonomic changes could result in the instatement of a single, widespread taxon in which rarer morphotypes are not protected.
PMCID: PMC3501618  PMID: 23170201
AFLP; conservation; hybridization; refugia; speciation; taxonomy
6.  Genomic Characterization of DArT Markers Based on High-Density Linkage Analysis and Physical Mapping to the Eucalyptus Genome 
PLoS ONE  2012;7(9):e44684.
Diversity Arrays Technology (DArT) provides a robust, high throughput, cost-effective method to query thousands of sequence polymorphisms in a single assay. Despite the extensive use of this genotyping platform for numerous plant species, little is known regarding the sequence attributes and genome-wide distribution of DArT markers. We investigated the genomic properties of the 7,680 DArT marker probes of a Eucalyptus array, by sequencing them, constructing a high density linkage map and carrying out detailed physical mapping analyses to the Eucalyptus grandis reference genome. A consensus linkage map with 2,274 DArT markers anchored to 210 microsatellites and a framework map, with improved support for ordering, displayed extensive collinearity with the genome sequence. Only 1.4 Mbp of the 75 Mbp of still unplaced scaffold sequence was captured by 45 linkage mapped but physically unaligned markers to the 11 main Eucalyptus pseudochromosomes, providing compelling evidence for the quality and completeness of the current Eucalyptus genome assembly. A highly significant correspondence was found between the locations of DArT markers and predicted gene models, while most of the 89 DArT probes unaligned to the genome correspond to sequences likely absent in E. grandis, consistent with the pan-genomic feature of this multi-Eucalyptus species DArT array. These comprehensive linkage-to-physical mapping analyses provide novel data regarding the genomic attributes of DArT markers in plant genomes in general and for Eucalyptus in particular. DArT markers preferentially target the gene space and display a largely homogeneous distribution across the genome, thereby providing superb coverage for mapping and genome-wide applications in breeding and diversity studies. Data reported on these ubiquitous properties of DArT markers will be particularly valuable to researchers working on less-studied crop species who already count on DArT genotyping arrays but for which no reference genome is yet available to allow such detailed characterization.
PMCID: PMC3439404  PMID: 22984541
7.  A reference linkage map for Eucalyptus 
BMC Genomics  2012;13:240.
Genetic linkage maps are invaluable resources in plant research. They provide a key tool for many genetic applications including: mapping quantitative trait loci (QTL); comparative mapping; identifying unlinked (i.e. independent) DNA markers for fingerprinting, population genetics and phylogenetics; assisting genome sequence assembly; relating physical and recombination distances along the genome and map-based cloning of genes. Eucalypts are the dominant tree species in most Australian ecosystems and of economic importance globally as plantation trees. The genome sequence of E. grandis has recently been released providing unprecedented opportunities for genetic and genomic research in the genus. A robust reference linkage map containing sequence-based molecular markers is needed to capitalise on this resource. Several high density linkage maps have recently been constructed for the main commercial forestry species in the genus (E. grandis, E. urophylla and E. globulus) using sequenced Diversity Arrays Technology (DArT) and microsatellite markers. To provide a single reference linkage map for eucalypts a composite map was produced through the integration of data from seven independent mapping experiments (1950 individuals) using a marker-merging method.
The composite map totalled 1107 cM and contained 4101 markers; comprising 3880 DArT, 213 microsatellite and eight candidate genes. Eighty-one DArT markers were mapped to two or more linkage groups, resulting in the 4101 markers being mapped to 4191 map positions. Approximately 13% of DArT markers mapped to identical map positions, thus the composite map contained 3634 unique loci at an average interval of 0.31 cM.
The composite map represents the most saturated linkage map yet produced in Eucalyptus. As the majority of DArT markers contained on the map have been sequenced, the map provides a direct link to the E. grandis genome sequence and will serve as an important reference for progressing eucalypt research.
PMCID: PMC3436727  PMID: 22702473
9.  Genetic Variation in the Chemical Components of Eucalyptus globulus Wood 
G3: Genes|Genomes|Genetics  2011;1(2):151-159.
Despite the ecological and economic importance of lignin and other wood chemical components, there are few studies of the natural genetic variation that exists within plant species and its adaptive significance. We used models developed from near infra-red spectroscopy to study natural genetic variation in lignin content and monomer composition (syringyl-to-guaiacyl ratio [S/G]) as well as cellulose and extractives content, using a 16-year-old field trial of an Australian tree species, Eucalyptus globulus. We sampled 2163 progenies of 467 native trees from throughout the native geographic range of the species. The narrow-sense heritability of wood chemical traits (0.25–0.44) was higher than that of growth (0.15), but less than wood density (0.51). All wood chemical traits exhibited significant broad-scale genetic differentiation (QST = 0.34–0.43) across the species range. This differentiation exceeded that detected with putatively neutral microsatellite markers (FST = 0.09), arguing that diversifying selection has shaped population differentiation in wood chemistry. There were significant genetic correlations among these wood chemical traits at the population and additive genetic levels. However, population differentiation in the S/G ratio of lignin in particular was positively correlated with latitude (R2 = 76%), which may be driven by either adaptation to climate or associated biotic factors.
PMCID: PMC3276126  PMID: 22384327
tree improvement; wood chemicals; adaptation; lignin; cellulose; extractives; syringyl; guaiacyl
10.  Sources of variation in self-incompatibility in the Australian forest tree, Eucalyptus globulus 
Annals of Botany  2010;105(5):737-745.
Background and Aims
One of the major factors affecting the outcrossing rate in Eucalyptus globulus is thought to be the inherent self-incompatibility (SI) level of the female tree. SI in this species is mainly due to late-acting pre- and post-zygotic mechanisms operating in the ovary, and not S alleles. This study aimed to assess the phenotypic variation in SI levels within E. globulus and determine its genetic control and stability across pollination techniques, sites and seasons.
SI levels were estimated for 105 genotypes originating from across the geographical range of E. globulus over multiple years of crossing. Separate grafted trees of some genotypes growing at the same and different sites allowed the genetic basis of the variation in SI to be tested and its stability across sites and seasons to be determined. The SI level of a tree was measured as the relative reduction in seeds obtained per flower pollinated following selfing compared with outcross pollinations. Thus, if seed set is the same, SI is 0 %, and if no self seed is set, SI is 100 %.
Key Results
The average SI in E. globulus was 91 % and genotypes ranged from 8 to 100 % SI. Most genotypes (>75 %) had SI levels >90 %. There were highly significant differences between genotypes and the within-site broad-sense heritability of percentage SI was high (H2 = 0·80 ± 0·13). However, there was evidence that growing site, and to a lesser extent season, can affect the expression of SI levels. Trees with low reproductive loads produced relatively more seed from selfed flowers.
There is a strong genetic basis to the phenotypic variation in SI in E. globulus within a site. However, the level of SI was affected, but to a lesser extent, by the environment, which in part may reflect the higher probability of selfed zygotes surviving on sites or in seasons where competition for resources is less.
PMCID: PMC2859912  PMID: 20228085
Heritability; plasticity; resource allocation; SI; mating systems; forest tree
11.  A high-density Diversity Arrays Technology (DArT) microarray for genome-wide genotyping in Eucalyptus 
Plant Methods  2010;6:16.
A number of molecular marker technologies have allowed important advances in the understanding of the genetics and evolution of Eucalyptus, a genus that includes over 700 species, some of which are used worldwide in plantation forestry. Nevertheless, the average marker density achieved with current technologies remains at the level of a few hundred markers per population. Furthermore, the transferability of markers produced with most existing technology across species and pedigrees is usually very limited. High throughput, combined with wide genome coverage and high transferability are necessary to increase the resolution, speed and utility of molecular marker technology in eucalypts. We report the development of a high-density DArT genome profiling resource and demonstrate its potential for genome-wide diversity analysis and linkage mapping in several species of Eucalyptus.
After testing several genome complexity reduction methods we identified the PstI/TaqI method as the most effective for Eucalyptus and developed 18 genomic libraries from PstI/TaqI representations of 64 different Eucalyptus species. A total of 23,808 cloned DNA fragments were screened and 13,300 (56%) were found to be polymorphic among 284 individuals. After a redundancy analysis, 6,528 markers were selected for the operational array and these were supplemented with 1,152 additional clones taken from a library made from the E. grandis tree whose genome has been sequenced. Performance validation for diversity studies revealed 4,752 polymorphic markers among 174 individuals. Additionally, 5,013 markers showed segregation when screened using six inter-specific mapping pedigrees, with an average of 2,211 polymorphic markers per pedigree and a minimum of 859 polymorphic markers that were shared between any two pedigrees.
This operational DArT array will deliver 1,000-2,000 polymorphic markers for linkage mapping in most eucalypt pedigrees and thus provide high genome coverage. This array will also provide a high-throughput platform for population genetics and phylogenetics in Eucalyptus. The transferability of DArT across species and pedigrees is particularly valuable for a large genus such as Eucalyptus and will facilitate the transfer of information between different studies. Furthermore, the DArT marker array will provide a high-resolution link between phenotypes in populations and the Eucalyptus reference genome, which will soon be completed.
PMCID: PMC2903579  PMID: 20587069
12.  Glacial refugia and reticulate evolution: the case of the Tasmanian eucalypts. 
Tasmania is a natural laboratory for investigating the evolutionary processes of the Quaternary. It is a large island lying 40-44 degrees S, which was repeatedly glaciated and linked to southeastern continental Australia during the Quaternary. Climate change promoted both the isolation of species in glacial refugia, and an exchange between Tasmanian and mainland floras. Eucalyptus is a complex and diverse genus, which has increased in abundance in Australia over the past 100 kyr, probably in response to higher fire frequency. Morphological evidence suggests that gene flow may have occurred between many eucalypt species after changes in their distribution during the Quaternary. This paper summarizes recent genetic evidence for migration and introgressive hybridization in Tasmanian Eucalyptus. Maternally inherited chloroplast DNA reveals a long-term persistence of eucalypts in southeastern Tasmanian refugia, coupled with introgressive hybridization involving many species. Detailed analysis of the widespread species Eucalyptus globulus suggests that migration from mainland Australia was followed by introgression involving a rare Tasmanian endemic. The data support the hypothesis that changes in distribution of interfertile species during the Quaternary have promoted reticulate evolution in Eucalyptus.
PMCID: PMC1693314  PMID: 15101583

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