Haplotype diversity of VvTFL1A gene and association with cluster traits ingrapevine (V. vinifera)
© Fernandez et al. 2014
Received: 28 March 2014
Accepted: 23 July 2014
Published: 5 August 2014
Interaction between TERMINAL FLOWER 1 (TFL1) and LEAFY(LFY) seem to determine the inflorescence architecture inArabidopsis. In a parallel way, overexpression of VvTFL1A, agrapevine TFL1 homolog, causes delayed flowering and production of aramose cluster in the reiterated reproductive meristem (RRM) somatic variant ofcultivar Carignan. To analyze the possible contribution of this gene to clusterphenotypic variation in a diversity panel of cultivated grapevine (Vitisvinifera L. subsp. vinifera) its nucleotide diversity wascharacterized and association analyses among detected sequence polymorphisms andphenology and cluster traits was carried out.
A total of 3.6 kb of the VvTFL1A gene, including its promoter, wassequenced in a core collection of 140 individuals designed to maximize phenotypicvariation at agronomical relevant traits. Nucleotide variation forVvTFL1A within this collection was higher in the promoter and intronsequences than in the exon regions; where few polymorphisms were located inagreement with a high conservation of coding sequence. Characterization of theVvTFL1A haplotype network identified three major haplogroups,consistent with the geographic origins and the use of the cultivars that couldcorrespond to three major ancestral alleles or evolutionary branches, based on theexistence of mutations in linkage disequilibrium. Genetic association studies withcluster traits revealed the presence of major INDEL polymorphisms, explaining 16%,13% and 25% of flowering time, cluster width and berry weight, respectively, andalso structuring the three haplogroups.
At least three major VvTFL1A haplogroups are present in cultivatedgrapevines, which are defined by the presence of three main polymorphism LD blocksand associated to characteristic phenotypic values for flowering time, clusterwidth and berry size. Phenotypic differences between haplogroups are consistentwith differences observed between Eastern and Western grapevine cultivars andcould result from the use of different genetic pools in the domestication processas well as different selection pressures on the development of table and winecultivars, respectively. Altogether, these results are coherent with previousclassifications of grapevine phenotypic diversity mainly based on cluster andberry morphotypes as well as with recent results on the structure of geneticdiversity in cultivated grapevine.
KeywordsPlant reproductive development Inflorescence structure Flowering time Berry size Grape domestication Grapevine
Grapevine (Vitis vinifera subsp. vinifera) was domesticated in theNeolithic period (ca. 8500–4000 BC)  from wild populations of Vitis vinifera subsp. sylvestris. Archaeological data traced back the location of the earliest evidence forlarge-scale winemaking, likely linked to the use of domesticated plants, to the north ofZagros Mountains and in the Caucasian region  around 6000–5000 BC which supports that geographic area as the locationfor primo domestication events. From there, grapevine cuttings were widely spread: firstfrom North to South; and later from East to West around the Mediterranean basin pathway . Vegetative propagation and dissemination, spontaneous events ofhybridization among cultivars, breeding with local wild plants and likely secondarydomestication events generated the pattern of admixture that is observed in currentcultivars –. The use of different genetic pools along the process of grapevinedomestication and human selection for different uses such as fresh consumption, raisinor wine production have resulted in large variation for cluster size, compactness andarchitecture among cultivars from different geographic locations .
The size and shape of grapevine clusters is determined by the development and growth ofinflorescences as well as the efficiency of pollination, fruit set and berry growth.Generally, wine grape cultivars present small (150-250 g) and compact clusters withsmall berries, while table grapes generally have large (300-400 g) and less compactclusters with large berries. Some of them can even be extremely big weighting up to1000-1500 g . Negrul  distinguished different grape morphotypes based in part on cluster and berrytraits. Cluster architecture has implications on disease susceptibility, since cultivarswith compact clusters are more susceptible to rot by Botrytis cinerea thanthose of loose clusters ,,. In spite of the relevance of cluster structure and compactness, very littleis known about its genetic control probably due in part to the complexity of the trait,which depends on many different variables along the growth of the plant as well as theenvironmental interactions during its reproductive development. There is a need todefine cluster shape and size in terms of quantitative variables to understand itsgenetic determination. So far, only a few studies have tried to identify the mainvariables responsible for variation in bunch compactness in grapevine. In this sense,Vail and Marois  identified cluster weight as the main factor to explain its variation whileShavrukov et al.  proposed total cluster length and node number per rachis as two of the mainones. Recently, Tello and Ibañez  evaluated 19 indexes to estimate cluster compactness highlighting the role ofvarious cluster parameters such as branch length and number. The study proposed a fastand good estimator for cluster compactness based on cluster weight and length.
Genetic and molecular analyses in model plants, such as Arabidopsis thaliana,demonstrated the interaction between TERMINAL FLOWER 1 (TFL1) andLEAFY (LFY) , in the establishment of inflorescence architecture. Their interactionssupported a simple model explaining the evolution of plants inflorescence architecture . TFL1 belongs to a small gene family first identified in mammals asencoding phosphatidyl ethanolamine-binding proteins (PEBP) , which participates in a wide variety of biological functions in eukaryotes.In Arabidopsis, TFL1 has been shown to function in the transcriptionalrepression of flower meristem identity genes . LFY encodes a plant specific transcription factor , which serves as a flower meristem identity regulator activating thetranscription of other flower meristem identity genes . Recently, the existence of a common genetic pathway controllinginflorescence architecture in Arabidopsis and rice has been demonstratedindicating that this pathway could be highly conserved in angiosperms . Following this report, four MADS-box genes are required to suppressTFL1 in emerging floral meristems; what seems to be indispensable toinitiate their differentiation.
In grapevine, the family of PEBP encoding genes includes at least five genes; three ofthem have deduced protein sequences related to Arabidopsis TFL1, beingVvTFL1A the closest homologous sequence . In fact, over-expression of VvTFL1A in transgenic Arabidopsisplants generates phenotypes of large and late flowering inflorescences reminding thoseobserved when over-expressing the endogenous Arabidopsis gene . Likewise, recent findings show that the extreme cluster proliferation anddelayed anthesis observed in the reiterated reproductive meristems (RRM) somatic variantof grapevine cultivar Carignan was caused by a single dominant mutation in theVvTFL1A gene. This dominant mutation was identified as the insertion of aclass II transposable element, Hatvine1-rrm, in the VvTFL1A promoter,triggering up-regulation of the corresponding VvTFL1A allele in reproductiveand vegetative organs of the shoot apex . These results suggested a role for VvTFL1A in the determination ofinflorescence structure as well as on the branching pattern of the grapevine fruitclusters and the time of anthesis.
To further analyze the contribution of VvTFL1A to the phenotypic variationobserved for reproductive and inflorescence traits in grapevine, the nucleotidediversity shown by this gene in a core collection of grapevine accessions was analysedand a candidate gene association approach on the variation observed for fertility index,phenological variables as well as several inflorescence and berry related traits wascarried out. Herein the identification of VvTFL1A sequence polymorphismsassociated with flowering and cluster traits is reported, being the most relevant onescorresponding to several INDELs in two intron regions. These INDELs are in LD withadditional SNPs defining three LD blocks, which correspond to three major haplogroups.Interestingly, these haplogroups are characteristic of either wine or table cultivars inagreement with the cluster and flowering phenotype to which they are associated to.
The plant material consisted of 140 grapevine cultivars corresponding to a corecollection of Vitis vinifera L. subsp. vinifera intended tomaximize agro-morphological diversity for 50 qualitative and quantitative traits . All the cultivars are maintained at the INRA experimental station ofDomaine de Vassal, Marseillan-plage, France(http://www1.montpellier.inra.fr/vassal/). The list of cultivars,pedigree when available, classification according to use (wine, table or wine/table),geographical group according to Bacilieri et al. , Lacombe et al.  and available data of the Vitis International Variety Catalogue(http://www.vivc.de/) are shown in Additional file 1. Classification according to Eastern and Western origin was obtainedconsidering cultivars from the Iberian Peninsula (IBER), Western and Central Europe(WCEUR) and the Italian Peninsula (ITAP) as occidental cultivars; whereas cultivarsfrom the Balkans (BALK), Russia and Ukraine (RUUK), Eastern Mediterranean andCaucasus (EMCA), Middle and Far East (MFEAS) were considered as oriental cultivars.For newly bred grape varieties, their pedigree was used to assess Western or Easternorigin to classify them according to their genetic origin and not according tobreeding location. When genetic origin of pedigree was questionable, the cultivar wasconsidered to present mixed origin.
List of traits analysed
Mean budburst time compared with Chasselas cultivar of reference
Mean flowering time (50% of open flowers) compared with Chasselascultivar of reference
Mean veraison time (50% of turn berries) compared withChasselas cultivar of reference
Mean maturity time compared with Chasselas cultivar of reference
Yield = Fertility index
(Number of inflorescence / number of shoot ) per plant
Average berry weight at maturity (20°Brix)
Average maximum cluster length at maturity (20°Brix)
Average maximum cluster width at maturity (20°Brix)
Average cluster weight at maturity (20°Brix)
Cluster weight/(cluster length)2
For each genotype, 3.6 kb of the VvTFL1A gene (GSVIVT01036145001,chr6_20199669-20203319, Genoscope 12X) were amplified and sequenced using primerslisted in Fernandez et al. . DNA was extracted from young leaves of each genotype as described inAdam-Blondon et al. . Amplifications were carried out using Taq DNA Polymerase (Qiagen) asrecommended by manufacturer. PCR products were treated with Exosap-IT reagent asrecommended by manufacturer and sequenced at the Genomic Service of the ParqueCientifico de Madrid in an ABI prism 3730 (Applied Biosystems) DNA sequencer. Basecalling, quality trimming and alignment of ABI chromatograms was performed usingSeqScape v2.5 (Applied Biosystems). Sequence polymorphisms were manually verified toestablish genotypes. The nomenclature system used to name polymorphisms correspondedto letters followed by numbers: single letter correspond to the involved nucleotidesubstitution using the IUB’s conventional nomenclature and “Ins” isused to designed INDEL; positive or negative numbers corresponded to polymorphismposition from the first base of the “ATG start codon”. Linkagedisequilibrium (LD) calculations between polymorphisms were carried out using the LDoption implemented in TASSEL v.2.1 .
Molecular diversity parameter estimates were calculated using DnaSP v4.50.2 . Per site nucleotide diversity (π) , Watterson θ estimate  and Tajima’s D  were calculated for the whole haplotype set and separately for the threestructured sub-populations (K1, K2, K3).
Comparison of the naïve General Linear Model (GLM) test, the structuredassociation test (GLM-Q) and the structured Mixed Linear Model (MLM-Q) using TASSELv.3 identified the last one as the most conservative model and was therefore selectedto perform the association tests. MLM-Q association tests were carried out using theR v.2.15  and TASSEL v.3 software. Polymorphic sites carrying rare alleles(frequencies <5% within the total sample) and unbalanced genotypic classes(frequencies <5% within the total sample) were discarded to avoid biasedassociations. Rare genotypic classes were in this last case replaced by missing data.Polymorphisms were codified to test both additive and dominant effects using R to besimilar with marker model tested using TASSEL. For traits showing significantassociations after Bonferroni correction (P ≤ 0.05) usingeither TASSEL or R, multi-locus mixed-models using forward-backward stepwiseregression (MLMM) were implemented using the R software to identify majornon-redundant associated markers . Population structure and kinship were both included in the multi-locusanalysis. Best models were selected according to the extended Bayesian informationcriteria (EBIC) and the multiple Bonferroni criteria (mBonf) according to Segura etal. .
Haplotype reconstruction and networks
As V. vinifera genotypes are generally highly heterozygous , the unphased genotypic dataset was analysed to identify the succession oflinked polymorphisms along the sequenced DNA region. Haplotypes were reconstructedusing a PLEM algorithm  implemented in PHASE v2.1 applying default values of the iterative scheme . Reconstructed haplotypes were submitted separately and simultaneously tothree recombination detection tests implemented in the Recombination DetectionProgram v3beta41 . Those were the MaxChi method with a window size of 12, 20, 25 or 30variables sites , the Chimaera method with a window size of 12, 20, 25 or 30 variablessites  and the 3SEQ method . To ensure consistency, haplotypes showing a significant probability ofbeing the result of recombination (P ≤0.05) in at least two tests wereconsidered as recombinants and excluded from further analysis as previously done byFournier-Level et al. .
Network analysis was carried out using the median-joining method  implemented in Network v126.96.36.199 (Fluxus Technology, Sudbury, UK) andfixing a weight of 99 for the polymorphisms showing best associations with traits(Ins883, Ins422, K-737 and M-196). Three haplogroups HGA, HGB and HGC were definedaccording to the three LD blocks.
VvTFL1Astructure and sequence polymorphisms
Pattern of diversity and neutrality tests for VvTFL1A gene
Haplotypes 32 and 3 were the most frequent (frequency >0.15 on the total haplotypepool and >0.19 when excluding the recombinants) and belonged to HGA and HGB,respectively. Most of the cultivars of the core collection were heterozygous for twodifferent haplotypes (86%) with 20% of them being heterozygous for a combination ofHGA and HGB haplotypes (Additional file 1). Only 20cultivars were homozygous (14%) with eight and five varieties homozygous for HGA andHGB haplotypes, respectively. Two cultivars were homozygous for haplotype 54 of HGCand the remaining homozygous accessions presented putative recombinanthaplotypes.
Regarding the recombinant haplotypes, haplotype 18, which was the most frequent(frequency = 0.05), corresponded to a recombination between haplotypesfrom HGA and HGB (Additional file 6). Indeed, no allelespecifically assigned to HGC was present in this haplotype, which was always combinedwith alleles typical of both HGA and HGB haplotypes. Interestingly; haplotype 18 waspresent only in cultivars of K1 (40%) and K3 (60%) sub-populations classified mainlyas Eastern table grapes, with two cultivars being homozygous for this haplotype(Additional file 1). Furthermore, among the individualsthat presented at least one HGC haplotype mainly composed by cultivars of the K2sub-population, the only one Eastern table cultivar belonging to the K3sub-population was a combination with haplotype 18.
Candidate gene association
List of VvTFLlA polymorphisms showing significant association after Bonferroni correction(<0.05) with flowering time, cluster width and berry weight throughstructured MLM tests using either R or TASSEL
Bonf corr < 0.05
Bonf corr < 0.05
The strongest association was found between berry weight and SNP M-196(P = 1.4E−8) explaining 16% of the traitvariation. The highest association for flowering time and cluster width was foundwith Ins883 (P = 2.7E−4,P = 1.6E−5, respectively) that explained 10%and 13% of trait variation, respectively. Interestingly, Ins883 characteristic of HGAalso associated significantly (P ≤0.01) with berry weight(P = 5.7E−7). At a lesser extent, Ins422from HGC associated with the three traits explaining 9%, 6% and 7% of flowering time,berry weight and cluster width variations, respectively.
Markers in the model
Phenotypic values related to major haplotypes
Arabidopsis TFL1 plays a critical role in the specification of theinflorescence meristem and inflorescence architecture ,. This role seems to be conserved in other plant species  likely through a conserved regulatory pathway . In grapevine, the previous identification of misexpression of theArabidopsis homolog VvTFL1A as the molecular cause of thereiteration of reproductive meristems (RRM) mutant , also supported the possible conservation of its biological function in thisspecies in agreement with previous results ,. Phenotypic characterization of the RRM plants showed that VvTFL1Aoverexpression was related to a delay in the time of anthesis and to an increase in thesize and branching pattern of the inflorescences , similar to the effects of TFL1 overexpression in transgenicArabidopsis . To provide additional evidence on the involvement of VvTFL1A innatural variation for flowering time and inflorescence development and to identifynucleotide sequence polymorphisms that could be partially responsible for those traitsin grapevine, a genetic diversity analysis of this gene sequence and genetic associationstudies with those traits were carried out.
Nucleotide variations for VvTFL1A in the grapevine core collection analysed isrelatively high with an average of one polymorphic site every 50 nucleotides. However,only five out of the 70 polymorphisms detected are located in exonic regions and onlythree of them result in non-synonymous amino acid substitutions. This result is inagreement with the slight negative Tajima’s D values observed alongVvTFL1A coding sequences and suggests that the protein structure admits fewvariations. Reduction in overall level of nucleotide variation was also reported for theArabidopsis TFL1 gene when compared with other flowering genes . Among the three non-synonymous polymorphisms identified in VvTFL1A,W13, located in first exon, had a very low frequency and was not considered for theassociation analyses. The two other, W1087 and M1094, are located in the fourth exon ina region of the protein responsible for the functional divergence between FT and TFL1 ; although the substituted amino acids do not correspond to conserved residues  and the SNP did not associate with inflorescence related traits undersingle-locus models. However, W1087 was selected by the multi-locus mixed-model analysisto explain part of flowering time variation together with Ins883 suggesting a possiblefunctional effect of this SNP in this trait. Regarding the 17 polymorphisms found inintron regions, two INDEL (Ins422 and Ins883) showed significant association withflowering and cluster trait variation. INDEL Ins422 is located in intron 2 andcorresponds to a microsatellite sequence of GA repetitions; while INDEL Ins883 islocated in intron 3 and corresponds to a G nucleotide repetition. The 48 remainingVvTFL1A polymorphisms identified in the core collection were locatedupstream of the translation start codon and included four INDEL. No traces of theHatvine1-rrm transposon were detected in the promoter of VvTFL1A inthe whole core collection which demonstrates the specificity of the insertion eventcausing the Carignan RRM mutant phenotype .
Nucleotide polymorphisms in VvTFL1A LD blocks that discriminate the threehaplogroups displayed differential association with cluster traits under linearregression models. Among all traits analysed, polymorphic sites characteristic of HGAand HGC haplogroups explained part of the phenotypic variation for flowering time, berryweight and cluster width. In the same way, polymorphisms specific of HGB associated withcluster width as well as polymorphisms from HGA. These results suggest that variation atVvTFL1A has an effect on flowering time, berry weight and cluster width withdifferent alleles having differential effects on the traits. Interestingly, bothflowering time delay and cluster width increase were observed in the phenotypiccharacterization of the RRM somatic variant related to VvTFL1A overexpression.Unfortunately, berry size was not measured in that study .
Among all the polymorphic sites tested, insertion Ins883 discriminating HGA from HGB andHGC explained alone part of flowering time, berry weight and cluster width variations.According to the multi-locus analysis, Ins833 explained up to 16%, 13% and 25% offlowering time, cluster width and berry weight variation in the best models, being theonly polymorphism contributing to berry weight variation. INDEL occurring infunctionally important regions of genes could affect gene function, through geneexpression modification  or RNA structure alterations . However, a preliminary VvTLF1A RT qPCR expression analysis carriedout in young inflorescences of the cultivars of the core collection did not reveal anyassociation between gene expression variation and the VvTFL1A polymorphisms(data not shown). Likewise, no clear correlation (Pearson’s r <0.28) betweenVvTFL1A expression and phenotypic traits was identified (data not shown).Nevertheless, these negative results do not discard a possible role of this intronsequences in transcriptional or posttranscriptional processes given the difficulties incarrying out transcriptional comparisons among different genotypes with differentflowering behaviour. Analysis of maize TFL1 homologs expression in differenttissues and developmental stages showed the existence of differential transcriptprocessing . In fact, in a preliminary study, the existence of alternatively spliced RNAforms was detected for the first and the second introns of VvTFL1A (data notshown). Further research will be required to demonstrate any functional role of thisalternative splicing as well as its relationship with the described VvTFL1AIns833 polymorphism. In any case, further association analyses using larger samples andspecific segregation analyses will be required to confirm the detected associations.
Together with Ins883, M-196 and W1087 without LD with other VvTFL1Apolymorphisms explain part of berry weight and flowering time variation according tomulti-locus analysis, respectively. In contrast to Ins883 that discriminates haplotypesof HGA from those of HGB and HGC, M-196 and W1087 corresponded to mutationsdifferentiating haplotypes within the HGA haplogroup (Figure 4). The M-196 base change located in the proximal promoter and the W1087non-synonymous substitution in the fourth exon of VvTFL1A might representrelevant structural modifications at the promoter and the protein sequence,respectively, likely affecting VvTFL1A function in a non-redundant way withIns883. Moreover, in silico analysis using SIFT program(http://sift.jcvi.org/) predicts that substitution of T by S at position144 of the VvTFL1A sequence affects protein function with a score of 0.04 based on thealignment of 240 closely related sequences.
VvTFL1A haplotype network differentiates three haplogroups of closely relatedhaplotypes. Each HG is represented by a high frequency haplotype, haplotypes 32 for HGA,3 for HGB and haplotype 60 from HGC. Consistent with the results of the associationanalyses, individuals containing haplotype 32 of HGA, exhibited late flowering, largecluster width and larger berries. Interestingly, most of the cultivars of K1 and K3classified to table or table/wine uses, characterized by these phenotypic features , present HGA haplotypes. This relationship is also true for accessionscarrying the recombinant haplotype 18. Indeed, haplotype 18 contains Ins883 insertionpresent in HGA haplotypes and mostly present in Eastern table cultivars belonging to K1and K3 genetic groups. The fact that cultivars carrying haplotype 18 display lateflowering, large cluster width and larger berries supports a clear relationship betweenIns883 polymorphism and the eastern table cluster characteristics. In contrast,individuals containing haplotype 60 of HGC with Ins422 insertion exhibited earlyflowering, shorter cluster width and smaller berries. Consistently, HGC haplotypes areenriched in Western wine grape cultivars mostly belonging to K2 genetic group, which areknown to display those cluster and berry features . Finally, HGB haplotypes do not contain Ins422 or Ins883 insertions. Thephenotype of individuals containing haplotype 3 (most frequent within HGB) is similar tosome extent to that of cultivars carrying haplotype 60 (HGC). Consistently with thisphenotype, HGB haplotypes are mostly present in cultivars for wine use. Because nohomozygous individuals were observed for haplotype 60 in the core collection, thephenotypic effect of this haplotype is supposed to be much stronger in homozygous state,which suggests that haplotype 60, related to extreme phenology and clustercharacteristics, could be less favored in cultivars in homozygous state than haplotype3. Interestingly, partial sequencing of VvTFL1A in 20 V.v ssp.sylvestris plants from the Iberian Peninsula identified wild haplotypessimilar to haplotype 60 and belonging to HGC (data not shown). These data could indicatea western origin for haplotypes of HGC.
Three major VvTFL1A haplogroups were identified in cultivated grapevines basedon the presence of three main polymorphism LD blocks. These haplogroups are associatedto characteristic phenotypic values for flowering time, cluster width and berry size.Phenotypic differences between VvTFL1A haplogroups are consistent with theclassification of grapevine phenotypic diversity in three different morphotypes proposedby Negrul  and could result from the use of different genetic pools in grapevinedomestication and/or the existence of different selection pressures on the developmentof table and wine cultivars. Polymorphic markers identifying haplogroups can also berelevant in marker-assisted breeding programs addressing the improvement of clusterstructure and berry size.
We would like to thank Dr Javier Ibanez and Dr Stéphanie Mariette for helpfuldiscussions; Virginia Rodriguez for her assistance for DNA extraction; Dr CarlosAlonso Blanco for his helpful comments and critical reading of the manuscript; and DrVincent Segura is acknowledged for assistance using MLMM software and criticalreading of the manuscript. This work was funded by grant BIO2008-03892 andBIO2011-026229 from the MICINN and MINECO of Spain to JMM-Z. Networking activitieswere also funded by COST Action FA1003 “East–west Collaboration forGrapevine Diversity Exploration and Mobilization of Adaptive Traits forBreeding”. JT was recipient of a fellowship from the MICINN.
- Mc Govern PE, Glusker DL, Exner LJ, Voigt MM: Neolithic resinated wine. Nature. 1996, 381: 480-481. 10.1038/381480a0.View ArticleGoogle Scholar
- Levadoux L: Les population sauvage et cultivées deVitis viniferaL. Annales de l' Amélioration des Plantes 1956, 6:59–118.,Google Scholar
- Mc Govern PE: Ancient wine. The search for the origins of viniculture. 2003, Princeton University Press, Princeton, NJGoogle Scholar
- Aradhya MK, Dangl GS, Prins BH, Boursiquot JM, Walker MA, Meredith CP, Simon CJ: Genetic structure and differentiation in cultivated grape,Vitis viniferaL. Genet Res 2003, 81:179–192.,View ArticlePubMedGoogle Scholar
- Arroyo-Garcia R, Ruiz-Garcia L, Bolling L, Ocete R, Lopez MA, Arnold C, Ergul A, Soylemezoglu G, Uzun HI, Cabello F, Ibanez J, Aradhya MK, Atanassov A, Atanassov I, Balint S, Cenis JL, Costantini L, Goris-Lavets S, Grando MS, Klein BY, McGovern PE, Merdinoglu D, Pejic I, Pelsy F, Primikirios N, Risovannaya V, Roubelakis-Angelakis KA, Snoussi H, Sotiri P, Tamhankar S, et al: Multiple origins of cultivated grapevine (Vitis viniferaL. ssp. sativa) based on chloroplast DNA polymorphisms. Mol Ecol 2006, 15:3707–3714.,View ArticlePubMedGoogle Scholar
- Bacilieri R, Lacombe T, Le Cunff L, Di Vecchi-Staraz M, Laucou V, Genna B, Peros JP, This P, Boursiquot JM: Genetic structure in cultivated grapevines is linked to geography and humanselection. BMC Plant Biol. 2013, 13: 25-10.1186/1471-2229-13-25.PubMed CentralView ArticlePubMedGoogle Scholar
- Emanuelli F, Lorenzi S, Grzeskowiak L, Catalano V, Stefanini M, Troggio M, Myles S, Martinez-Zapater JM, Zyprian E, Moreira FM, Grando MS: Genetic diversity and population structure assessed by SSR and SNP markers in alarge germplasm collection of grape. BMC Plant Biol. 2013, 13: 39-10.1186/1471-2229-13-39.PubMed CentralView ArticlePubMedGoogle Scholar
- Myles S, Boyko AR, Owens CL, Brown PJ, Grassi F, Aradhya MK, Prins B, Reynolds A, Chia JM, Ware D, Bustamante CD, Buckler ES: Genetic structure and domestication history of the grape. Proc Natl Acad Sci U S A. 2011, 108: 3530-3535. 10.1073/pnas.1009363108.PubMed CentralView ArticlePubMedGoogle Scholar
- Myles S, Chia JM, Hurwitz B, Simon C, Zhong GY, Buckler E, Ware D: Rapid genomic characterization of the genus vitis. PLoS One. 2010, 5: e8219-10.1371/journal.pone.0008219.PubMed CentralView ArticlePubMedGoogle Scholar
- Branas J: Viticulture. 1974, Paul Dehan, MontpellierGoogle Scholar
- Boursiquot JM, Dessup M, Rennes C: Distribution des principaux caractères phénologiques, agronomiques et technologiques chezVitis viniferaL. Vitis 1995, 34:31–35.,Google Scholar
- Negrul AM: Origin and classification of cultured grape. The Ampelography of the USSR. Edited by: Baranov A, Kai YF, Lazarevski MA, Palibin TV, Prosmoserdov NN, Baranov A, KaiYF, Lazarevski MA, Palibin TV, Prosmoserdov NN. 1946, Pischepromizdat, Moscow, 159-216.Google Scholar
- Molitor D, Rothmeier M, Behr M, Fischer S, Hoffman L, Evers D: Crop cultural and chemical methods to control grey mould on grapes. Vitis. 2011, 50: 81-87.Google Scholar
- Vail ME, Marois JJ: Grape cluster architecture and the susceptibility of berries to Botrytiscinerea. Phytopatholog. 1991, 81: 188-191. 10.1094/Phyto-81-188.View ArticleGoogle Scholar
- Shavrukov YN, Dry IB, Thomas MR: Inflorescence and bunch architecture development inVitis viniferaL. Aust J Grape Wine Res 2003, 10:116–124.,View ArticleGoogle Scholar
- Tello J, Ibáñez J: Evaluation of indexes for the quantitative and objective estimation of grapevinebunch compactness. Vitis. 2014, 53: 9-16.Google Scholar
- Bradley D, Ratcliffe O, Vincent C, Carpenter R, Coen E: Inflorescence commitment and architecture in Arabidopsis. Science 1997, 275:80–83.,View ArticlePubMedGoogle Scholar
- Shannon S, Meeks-Wagner DR: A mutation in the Arabidopsis TFL1 gene affects inflorescence meristem development. Plant Cell 1991, 3:877–892.PubMed CentralView ArticlePubMedGoogle Scholar
- Prusinkiewicz P, Erasmus Y, Lane B, Harder LD, Coen E: Evolution and development of inflorescence architectures. Science. 2007, 316: 1452-1456. 10.1126/science.1140429.View ArticlePubMedGoogle Scholar
- Schoentgen F, Saccoccio F, Jolles J, Bernier I, Jolles P: Complete amino acid sequence of a basic 21-kDa protein from bovine braincytosol. Eur J Biochem. 1987, 166: 333-338. 10.1111/j.1432-1033.1987.tb13519.x.View ArticlePubMedGoogle Scholar
- Hanano S, Goto K: Arabidopsis TERMINAL FLOWER1 is involved in the regulation of flowering time andinflorescence development through transcriptional repression. Plant Cell. 2011, 23: 3172-3184. 10.1105/tpc.111.088641.PubMed CentralView ArticlePubMedGoogle Scholar
- Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM: LEAFY controls floral meristem identity in Arabidopsis. Cell 1992, 69:843–859.,View ArticlePubMedGoogle Scholar
- Parcy F, Nilsson O, Busch MA, Lee I, Weigel D: A genetic framework for floral patterning. Nature. 1998, 395: 561-566. 10.1038/26903.View ArticlePubMedGoogle Scholar
- Liu C, Teo ZW, Bi Y, Song S, Xi W, Yang X, Yin Z, Yu H: A conserved genetic pathway determines inflorescence architecture in Arabidopsisand rice. Dev Cell. 2013, 24: 612-622. 10.1016/j.devcel.2013.02.013.View ArticlePubMedGoogle Scholar
- Carmona MJ, Cubas P, Calonje M, Martinez-Zapater JM: Flowering transition in grapevine (Vitis vinifera L.). Can J Bot 2007, 85:701–711.,View ArticleGoogle Scholar
- Fernandez L, Torregrosa L, Segura V, Bouquet A, Martinez-Zapater JM: Transposon-induced gene activation as a mechanism generating cluster shape somaticvariation in grapevine. Plant J. 2010, 61: 545-557. 10.1111/j.1365-313X.2009.04090.x.View ArticlePubMedGoogle Scholar
- Barnaud A, Lacombe T, Doligez A: Linkage disequilibrium in cultivated grapevine,Vitis vinifera L. Theor Appl Genet 2006, 112:708–716.,View ArticlePubMedGoogle Scholar
- Lacombe T, Boursiquot JM, Laucou V, Di Vecchi-Staraz M, Peros JP, This P: Large-scale parentage analysis in an extended set of grapevine cultivars (Vitis vinifera L.). Theor Appl Genet 2013, 126:401–414.,View ArticlePubMedGoogle Scholar
- Adam-Blondon AF, Roux C, Claux D, Butterlin G, Merdinoglu D, This P: Mapping 245 SSR markers on the Vitis vinifera genome: a tool for grapegenetics. Theor Appl Genet. 2004, 109: 1017-1027. 10.1007/s00122-004-1704-y.View ArticlePubMedGoogle Scholar
- Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES: TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007, 23: 2633-2635. 10.1093/bioinformatics/btm308.View ArticlePubMedGoogle Scholar
- Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R: DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 2003, 19: 2496-2497. 10.1093/bioinformatics/btg359.View ArticlePubMedGoogle Scholar
- Nei M: Molecular Evolutionary Genetics. 1987, Columbia University Press, New York, NYGoogle Scholar
- Watterson GA: On the number of segregating sites in genetical models without recombination. Theor Pop Biol. 1975, 7: 256-276. 10.1016/0040-5809(75)90020-9.View ArticleGoogle Scholar
- Tajima F: Statistical method for testing the neutral mutation hypothesis by DNApolymorphism. Genetics. 1989, 123: 585-595.PubMed CentralPubMedGoogle Scholar
- Thornsberry JM, Goodman MM, Doebley J, Kresovich S, Nielsen D, Buckler ES: Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet. 2001, 28: 286-289. 10.1038/90135.View ArticlePubMedGoogle Scholar
- Yu J, Pressoir G, Briggs WH, Vroh Bi I, Yamasaki M, Doebley JF, McMullen MD, Gaut BS, Nielsen DM, Holland JB, Kresovich S, Buckler ES: A unified mixed-model method for association mapping that accounts for multiplelevels of relatedness. Nat Genet. 2006, 38: 203-208. 10.1038/ng1702.View ArticlePubMedGoogle Scholar
- Laucou V, Lacombe T, Dechesne F, Siret R, Bruno JP, Dessup M, Dessup T, Ortigosa P, Parra P, Roux C, Santoni S, Vares D, Peros JP, Boursiquot JM, This P: High throughput analysis of grape genetic diversity as a tool for germplasmcollection management. Theor Appl Genet. 2011, 122: 1233-1245. 10.1007/s00122-010-1527-y.View ArticlePubMedGoogle Scholar
- Pritchard JK, Stephens M, Donnely P: Inference of population structure using multilocus genotype data. Genetics. 2000, 155: 945-959.PubMed CentralPubMedGoogle Scholar
- Evanno G, Regnaut S, Goudet J: Detecting the number of clusters of individuals using the software STRUCTURE: asimulation study. Mol Ecol. 2005, 14: 2611-2620. 10.1111/j.1365-294X.2005.02553.x.View ArticlePubMedGoogle Scholar
- Vigouroux Y, Glaubitz JC, Matsuoka Y, Goodman MM, Sanchez GJ, Doebley J: Population structure and genetic diversity of New World maize races assessed byDNA microsatellites. Am J Bot. 2008, 95: 1240-1253. 10.3732/ajb.0800097.View ArticlePubMedGoogle Scholar
- Fournier-Level A, Le Cunff L, Gomez C, Doligez A, Ageorges A, Roux C, Bertrand Y, Souquet JM, Cheynier V, This P: Quantitative genetic bases of anthocyanin variation in grape (Vitis vinifera L.ssp. sativa) berry: a quantitative trait locus to quantitative trait nucleotideintegrated study. Genetics. 2009, 183: 1127-1139. 10.1534/genetics.109.103929.PubMed CentralView ArticlePubMedGoogle Scholar
- Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, Daly MJ, Eskin E: Efficient control of population structure in model organism associationmapping. Genetics. 2008, 178: 1709-1723. 10.1534/genetics.107.080101.PubMed CentralView ArticlePubMedGoogle Scholar
- Segura V, Vilhjalmsson BJ, Platt A, Korte A, Seren U, Long Q, Nordborg M: An efficient multi-locus mixed-model approach for genome-wide association studiesin structured populations. Nat Genet. 2012, 44: 825-830. 10.1038/ng.2314.PubMed CentralView ArticlePubMedGoogle Scholar
- Qin ZS, Niu T, Liu JS: Partition-ligation-expectation-maximization algorithm for haplotype inference withsingle-nucleotide polymorphisms. Am J Hum Genet. 2002, 71: 1242-1247. 10.1086/344207.PubMed CentralView ArticlePubMedGoogle Scholar
- Stephens M, Donnelly P: A comparison of bayesian methods for haplotype reconstruction from populationgenotype data. Am J Hum Genet. 2003, 73: 1162-1169. 10.1086/379378.PubMed CentralView ArticlePubMedGoogle Scholar
- Martin DP, Williamson C, Posada D: RDP2: recombination detection and analysis from sequence alignments. Bioinformatics. 2005, 21: 260-262. 10.1093/bioinformatics/bth490.View ArticlePubMedGoogle Scholar
- Maynard Smith J: Analyzing the mosaic structure of genes. J Mol Evol. 1992, 34: 126-129.Google Scholar
- Posada D, Crandall KA: Evaluation of methods for detecting recombination from DNA sequences: computersimulations. Proc Natl Acad Sci U S A. 2001, 98: 13757-13762. 10.1073/pnas.241370698.PubMed CentralView ArticlePubMedGoogle Scholar
- Boni MF, Posada D, Feldman MW: An exact nonparametric method for inferring mosaic structure in sequencetriplets. Genetics. 2007, 176: 1035-1047.PubMed CentralView ArticlePubMedGoogle Scholar
- Fournier-Level A, Lacombe T, Le Cunff L, Boursiquot JM, This P: Evolution of the VvMybA gene family, the major determinant of berry colour incultivated grapevine (Vitis vinifera L.). Heredity (Edinb). 2010, 104: 351-362. 10.1038/hdy.2009.148.View ArticleGoogle Scholar
- Bandelt HJ, Forster P, Rohl A: Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999, 16: 37-48. 10.1093/oxfordjournals.molbev.a026036.View ArticlePubMedGoogle Scholar
- Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, et al: The grapevine genome sequence suggests ancestral hexaploidization in majorangiosperm phyla. Nature. 2007, 449: 463-467. 10.1038/nature06148.View ArticlePubMedGoogle Scholar
- Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES: Structure of linkage disequilibrium and phenotypic associations in the maizegenome. Proc Natl Acad Sci U S A. 2001, 98: 11479-11484. 10.1073/pnas.201394398.PubMed CentralView ArticlePubMedGoogle Scholar
- Jack T: Molecular and genetic mechanisms of floral control. Plant Cell. 2004, 16 (Suppl 1): S1-S17.PubMed CentralView ArticlePubMedGoogle Scholar
- Ratcliffe OJ, Amaya I, Vincent CA, Rothstein S, Carpenter R, Coen ES, Bradley DJ: A common mechanism controls the life cycle and architecture of plants. Development. 1998, 125: 1609-1615.PubMedGoogle Scholar
- McGarry RC, Ayre BG: Manipulating plant architecture with members of the CETS gene family. Plant Sci. 2012, 188–189: 71-81.View ArticlePubMedGoogle Scholar
- Boss PK, Sreekantan L, Thomas MR: A grapevine TFL1 homologue can delay flowering and alter floral development whenoverexpressed in heterologous species. Funct Plant Biol. 2006, 33: 31-41. 10.1071/FP05191.View ArticleGoogle Scholar
- Carmona MJ, Calonje M, Martinez-Zapater JM: The FT/TFL1 gene family in grapevine. Plant Mol Biol. 2007, 63: 637-650. 10.1007/s11103-006-9113-z.View ArticlePubMedGoogle Scholar
- Olsen KM, Womack A, Garrett AR, Suddith JI, Purugganan MD: Contrasting evolutionary forces in the Arabidopsis thaliana floral developmentalpathway. Genetics. 2002, 160: 1641-1650.PubMed CentralPubMedGoogle Scholar
- Ahn JH, Miller D, Winter VJ, Banfield MJ, Lee JH, Yoo SY, Henz SR, Brady RL, Weigel D: A divergent external loop confers antagonistic activity on floral regulators FTand TFL1. Embo J. 2006, 25: 605-614. 10.1038/sj.emboj.7600950.PubMed CentralView ArticlePubMedGoogle Scholar
- Warren ST, Zhang F, Licameli GR, Peters JF: The fragile X site in somatic cell hybrids: an approach for molecular cloning offragile sites. Science. 1987, 237: 420-423. 10.1126/science.3603029.View ArticlePubMedGoogle Scholar
- Collins FS, Drumm ML, Cole JL, Lockwood WK, Vande Woude GF, Iannuzzi MC: Construction of a general human chromosome jumping library, with application tocystic fibrosis. Science. 1987, 235: 1046-1049. 10.1126/science.2950591.View ArticlePubMedGoogle Scholar
- Danilevskaya ON, Meng X, Hou Z, Ananiev EV, Simmons CR: A genomic and expression compendium of the expanded PEBP gene family frommaize. Plant Physiol. 2008, 146: 250-264.PubMed CentralView ArticlePubMedGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative CommonsAttribution License (http://creativecommons.org/licenses/by/4.0), whichpermits unrestricted use, distribution, and reproduction in any medium, provided theoriginal work is properly credited. The Creative Commons Public Domain Dedication waiver(http://creativecommons.org/publicdomain/zero/1.0/) applies to the datamade available in this article, unless otherwise stated.