A forensic perspective on the genetic identification of grapevine ( Vitis vinifera L.) varieties using STR markers

Electrophoresis 2014, 35, 3201–3207 3201

Sara Santos1,2 ∗Manuela Oliveira1 ∗Antonio Amorim1,2

Barbara van Asch1

1Instituto de Patologia eImunologia Molecular daUniversidade do Porto(IPATIMUP), Porto, Portugal

2Faculdade de Ciencias daUniversidade do Porto, Porto,Portugal

Received March 4, 2014Revised August 10, 2014Accepted August 12, 2014

Review

A forensic perspective on the geneticidentification of grapevine (Vitis vinifera L.)varieties using STR markers

The grapevine (Vitis vinifera subsp. vinifera) is one of the most important agriculturalcrops worldwide. A long interest in the historical origins of ancient and cultivated cur-rent grapevines, as well as the need to establish phylogenetic relationships and parentage,solve homonymies and synonymies, fingerprint cultivars and clones, and assess the au-thenticity of plants and wines has encouraged the development of genetic identificationmethods. STR analysis is currently the most commonly used method for these purposes.A large dataset of grapevines genotypes for many cultivars worldwide has been producedin the last decade using a common set of recommended dinucleotide nuclear STRs. Thistype of marker has been replaced by long core-repeat loci in standardized state-of-the-arthuman forensic genotyping. The first steps toward harmonized grapevine genotypinghave already been taken to bring the genetic identification methods closer to humanforensic STR standards by previous authors. In this context, we bring forward a set ofbasic suggestions that reinforce the need to (i) guarantee trueness-to-type of the sample;(ii) use the long core-repeat markers; (iii) verify the specificity and amplification consis-tency of PCR primers; (iv) sequence frequent alleles and use these standardized alleleladders; (v) consider mutation rates when evaluating results of STR-based parentage andpedigree analysis; (vi) genotype large and representative samples in order to obtain allelefrequency databases; (vii) standardize genotype data by establishing allele nomenclaturebased on repeat number to facilitate information exchange and data compilation.

Keywords:

Genetic identification / Grapevine / STR / Vitis viniferaDOI 10.1002/elps.201400107

1 Origin and domestication of cultivatedgrapevines

Vitis vinifera subsp. vinifera (or sativa), a diploid plant com-monly known as the cultivated grapevine, is one of the mostvaluable and oldest domesticated plants, used to produce ta-ble fruit, wine and spirits, juice, and raisins. It is estimatedthat the primo-domestication of the cultivated grapevine oc-curred from its wild ancestor (Vitis vinifera subsp. sylvestris) atbetween 6000 and 8000 years ago [1–3], starting in the regionspanning from the Fertile Crescent to South Caucasus andsubsequently expanded westward, reaching Europe at around2800 years ago [4]. In the course of its geographic dispersion,the cultivated grapevine has suffered introgressions with lo-cal V. sylvestris, although the extent of the wild gene poolcontribution remains unclear [5]. The domestication process

Correspondence: Dr. Barbara van Asch, IPATIMUP, Rua Dr. RobertoFrias s/n, 4200–465 Porto, PortugalE-mail: [email protected]: *351-225570799

appears to have been slow and to have recurrently incorpo-rated plants originating from sexual reproduction, whereasmodern grape cultivation essentially relies on vegetative prop-agation [6]. A recent work surveyed a representative sample ofworldwide grapevine diversity (INRA Vassal AmpelographicCollection) including samples from previously understudiedlocations (e.g. Caucasus, Spain, and North Africa) [7]. In ac-cordance with previous studies, the authors found high levelsof diversity and heterozygosity [1, 5, 8–10]. Thus, the domes-tication of the grapevine may only have involved a limited ge-netic bottleneck, because modern cultivated grapevines seemto have captured much of the haplotype diversity found inV. sylvestris. The results were also in agreement with eco-geographic groupings previously proposed [11] and it waspossible to further subdivide them into putative geographicregions of origin (West and Central Europe; East Mediter-ranean, Caucasus, Middle and Far East, the most diverse andheterozygous cluster with the latter having the lowest pro-portion of admixture; and Balkans and East Europe). Twonew groups were also identified: Central Europe, and theIberian and Italian Peninsulas as two regions of admixtures

∗These authors contributed equally to this work.

C© 2014 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim www.electrophoresis-journal.com

3202 S. Santos et al. Electrophoresis 2014, 35, 3201–3207

genotypes. These latter had been pointed before to haveplayed a particular role after the last glaciation [12], and Ital-ian cultivars had been pointed as dually originating fromcultivars introduced from the primary center of domestica-tion and from local domestication of wild vines [13]. Thenotion that wild grapevines have recurrently contributed tothe present diversity of domestic cultivars has prompted theinclusion of a growing number of samples in studies that aimat shedding light on the history of this important agriculturalcrop [5, 10, 14]. Overall, the arising picture of the dissemi-nation of viticulture around the Mediterranean is consistentwith historical data, that is, one route connecting Eastern toWestern Europe through the Balkans and Central Europe,and a Southern route to the Maghreb and Iberian Peninsula.Nevertheless, the precise processes, time, and place of oneor several domestications are still uncertain and the complexpicture presently arising including archaeobotanical, cultural,historical, and genetic evidence [1] will in the near future befurther clarified by the use ancient DNA analyses on grapeseeds in multidisciplinary approaches [15–18].

At present, the cultivated grapevine is highly diverse, with6000–11 000 cultivars recorded worldwide [19] (and probablyas many remaining unrecorded), although only a relativelysmall number of these are used commercially and the global-ization of markets is strongly contributing to a drastic reduc-tion in the number of exploited cultivars.

The vast number of high-order pedigree relationships(e.g. second and third degree) among grapevine cultivars re-sults in one large complex pedigree [5]. Therefore, parentageand pedigree investigation of cultivars from many world re-gions has offered an intricate view of putative genetic relation-ships and has often challenged previous conceptions [20–24].For example, a cultivar that was considered inferior, GouaisBlanc, was shown to be the ancestral of at least nine varieties,including the popular Chardonnay and Gamay [25]. Caber-net Sauvignon was shown to result from crosses betweenSauvignon Blanc and Cabernet Franc [26], and the usuallyassumed independent origin of the important commercialcultivars Pinot and Syrah was challenged [27].

2 Applications of genetic identification ofcultivated grapevines

A possible application of forensic genetic grapevine identi-fication could presently be in the context of the control andcertification of planting material available to growers in theform of grafted woody canes. This identification is impor-tant with regard to the productive part of the plant (scion),as well as for the rootstocks because they also influence thegrowth of the grafted scion and the quality of the grapes pro-duced. Genetic authentication of grapevine planting materialcould be used to protect the viticulturist from misidentifi-cation, mislabeling, or counterfeit and, in cases where thematerial is proprietary (i.e. protected by patents, trademarks,or contracts), protect the owner of the rights from illegitimatecommercialization or propagation.

Viticultural, winemaking, and wine labeling regulationstend to be more stringent in the Old World than in the NewWorld. Depending on the production region, only specificcultivars may be legally allowed in the vineyards, and the in-clusion of others may only be permitted under legally definedpercentages, thus demanding accurate cultivar identificationin planted areas. Wines are also generally marketed with la-beling information regarding cultivar, cultivation area, andyear of production. The European Union has developed winelegislation that includes origin and geographical indications,traditional terms, and labeling and presentation of wine. Asfrom 2011, wine quality categories are separated into PDO(Protected Designation of Origin) and PGI (Protected Geo-graphical Indication), with country synonyms (e.g. AOC andVDP, respectively, in France), and differences in regionalspecification are frequent. Although cultivar information inthe labeling of wine is not mandatory by European law, ithas become an important aspect of the perceived value ofwines from the point of view of the consumer, in a mar-ket characterized by fierce competition. Again, accurate culti-var identification upstream and downstream the vinificationprocess would be a distinguishing factor that would benefitconsumers and compliant producers.

STR-based identification in cultivated grapevines ispresently becoming an important aid in the identification anddiscrimination of propagative material in order to implementeffective strategies for the management of germplasm col-lections. Virtually, all traditional grapevine-growing regionsin the Old World have their indigenous grapevine varietiesand have constituted collections to record, preserve, and man-age biodiversity. For example, the Portuguese AmpelographicCollection records approximately 720 cultivars (including 250putative autochthonous varieties), of which 341 are legallyauthorized for wine production [28]. The great number ofcultivars and their distribution throughout the country re-sulted in misnaming, synonyms (different names for thesame cultivar), and homonyms (different cultivars identifiedunder the same name). Despite the high number of culti-vars currently recognized, many of them are scarcely usedand face the risk of extinction. It is estimated that 5–10%grapevine cultivars in worldwide collections are misnamed,synonymous, or homonymous [29]. Correct resolution of syn-onyms and homonyms and verification of germplasm collec-tions can greatly aid the authentication and management ofresources for the conservation of the biodiversity of grapevinevarieties.

Genetic identification of grapevine cultivars would alsobe extremely relevant in commercial food products, partic-ularly mono-varietal wines. Presently, genetic analyses havebeen successful in experimental wine musts, although thefinal steps of production (decanting, clarification, and filtra-tion) seem to be responsible for negative DNA extraction, andinhibitors and low-quality DNA for hampering PCR and sub-sequent analysis [30–35]. As an example of the high degreeof inaccuracy that the information provided to consumersregarding grape and grape-derived products may contain,a survey of commercial table grapes and raisins in Austria


Electrophoresis 2014, 35, 3201–3207 Nucleic acids 3203

revealed that one-third of the market fruit was mislabeledwith regard to cultivar [36].

3 Grapevine identification methods

3.1 Non-DNA methods

Ampelography is a traditional identification method that re-lies on the analysis of diverse morphological vine organs(leaves, shoots, inflorescence, grape bunches, and individualgrapes), their phenology, and other features (budburst, flow-ering, the beginning of ripening, maturity, leaf fall, yield,grape and wine quality, resistance to disease and pests), andit has been the most used tool in the characterization ofgrapevine germplasm and plant collections. It has also con-tributed greatly to establishing relationships among cultivarsand the early definition of broad and regional eco-geographicgroups [11, 37–40]. However, ampelographic identificationsmay be subject to ambiguity in the cases of morphologicallysimilar cultivars. Also, the same cultivar may present dif-ferent morphological features depending on factors such ashealth status and nutritional state, terroir, and the expertiseand interpretation of the ampelographist. Furthermore, juve-nile plants are difficult to identify because they do not exhibitthe typical morphological traits of adult plants until they reachmaturity [41, 42].

Chemical and biochemical techniques allow for the char-acterization of grapevine cultivars with regard to the geo-graphical area of production. The main methods are the pro-filing of volatile compounds, amino acids, minerals, and theanalysis of stable isotopes and organic compounds. In wine,the main methods used for cultivar identification are sensoryanalysis, and profile analysis of minerals, amino acids, pro-teins, and polyphenolic and volatile compounds [43]. Theseprofiles can be used for characterizing and differentiatingmusts and wines by comparison to control samples as proofof authenticity. However, these methods do not always giveabsolute results because they are influenced by terroir, culti-vation strategies, vinification methods, and wine aging.

3.2 DNA-based methods

The past decade has witnessed the introduction of geneticmethodologies for grapevine and wine identification. Themain advantage of genetic analysis is that DNA is identi-cal in all cells of any tissue at any stage of development andits features are not altered by environmental or phytosanitaryconditions. Thus, genetic identification of grapevines can the-oretically be more objective than ampelography and chemicaland biochemical methods.

RFLP analysis was effectively employed to detect cultivar-specific DNA fingerprints for grapevine and rootstock culti-vars albeit the method is morose and requires a large quan-tity of high-quality DNA and was therefore supplanted byPCR-based methods [44]. RAPD analysis is a cost-effectivemethod that is less time consuming than RFLP. However,

different experimental conditions (e.g. thermal cycling equip-ment, Taq polymerases, and DNA and primer concentrations)often also lead to low intra- and interlaboratorial reproducibil-ity [45]. Amplified fragment length polymorphisms analysishas proven useful for discriminating among grapevine cul-tivars [46] but the method has the disadvantage of generat-ing a complex series of bands that may be difficult to inter-pret and standardize. However, this method and modifiedversions have shown to be powerful to investigate polymor-phisms among clones and assess inter- and intracultivar di-versity [47–50].

3.2.1 Mitochondrial and chloroplast markers

Contrarily to its animal counterpart, grapevine mitochondrialDNA has an extremely low mutation rate and polymorphism[51], therefore is generally not used in intraspecific genetic di-versity, phylogenetics, and phylogeography research. Chloro-plast DNA is exclusively maternally inherited in grapevinesand has a lower evolutionary rate than the nuclear genomeand thus can be used to address interspecific phylogeneticand phylogeographic questions, albeit the level of chloroplastDNA polymorphism is lower than nuclear [2, 52, 53].

3.2.2 STRs

The search for suitable genetic markers for identification,parentage, and assessment of genetic diversity has led to thepresent development of STR, also known as simple sequencerepeat, or microsatellites. STRs consist of abundantly dis-tributed tandem-repeated DNA sequences with a repeatedcore-unit of 1–6 bp that have a high level of variability (poly-morphism) in the number of repeats of the core motif at eachlocus in populations. STRs constitute an almost unlimitedsource of polymorphic sites that can be exploited as neutralgenetic markers when not located inside or close to a codingsequence, that is, not affected by selective pressures.

STR genotype information can be given objectively byprofiles represented by the allele sizes detected at the analyzedloci and expressed in base pairs or number of repeated unitsthat can be easily compared between laboratories, after thenecessary adjustments for minor methodological differences.Laboratory procedures for STR genotyping rely on the PCRamplification of specific loci from template DNA and the elec-trophoretic separation of alleles. High-quality and high-purityplant DNA can be obtained from a biological source using avariety of commercial kits and noncommercial methods, al-though it is usually more difficult to isolate than mammalianDNA, particularly due to the presence of polyphenols andpolysaccharides [54]. PCR amplification can be performed in-dividually for each locus or several loci can be simultaneouslyamplified using multiple primer pairs (multiplex PCR) in asingle reaction. PCR-amplified STR alleles are separated byelectrophoresis according to their size and compared to DNAreferences or allelic ladders to obtain genotypes. The mul-tiplex PCR strategy requires considerable optimization and



is generally coupled with the use of dye-labeled primers andautomated CE.

Human forensic genotyping protocols currently relyon PCR amplification of long core-repeat (mostly tetranu-cleotide) STR loci with dye-labeled primers, followed by CEseparation and automatic sizing of the alleles by comparisonto reference allelic ladders constructed for each locus. Dinu-cleotide repeats (e.g. [CA]n, with n representing the numberof repeated units of an allele) are the most abundant STRsand have been widely used in a variety of applications suchas genetic mapping, assessment of genetic diversity and ori-gin of populations, and individual identification and kinship.However, PCR amplification of dinucleotide STRs generatesa high level of amplification by-products smaller than the trueallele (stuttering) that render the identification of the true al-lele difficult [55]. Narrow distances between adjacent allelesalso present additional difficulties in binning (the process thatconverts raw allele lengths into allele classes). Finally, dinu-cleotide repeats are extremely problematic to sequence thusimpeding the establishment of standardized allele nomencla-tures based on the number of repeated core units. These fac-tors contribute to low reproducibility in intra- and interlabora-torial analysis, and hamper the comparison and compilationof genotype data from different sources. Dinucleotides werereplaced by longer core-repeat STRs (tri-, tetra-, and pentanu-cleotide) in human genetic forensics because the latter offera good level of polymorphism, are relatively easy to score,and alleviate the problems with allele calling and binningcharacteristic of dinucleotides [56]. Robust long core-repeatSTR-based protocols are increasingly being developed for an-imals, such as domestic dogs (e.g. [57]), but such proceduresare still scarcely reported for plant DNA analysis [8, 58].

4 Commonly used STRs for grapevinegenotyping

Analysis of nuclear STRs in grapevines began three decadesago and is presently the most used method, despite recentefforts to develop other types of genetic markers such asSNPs [59–61]. Along with the codominant Mendelian inheri-tance mode, an abundance of STR sequences in the nucleargenome of V. vinifera suitable for identifying cultivars wasearly demonstrated, as well as their suitability for geneticmapping and potential use for identification of genetic diver-sity and relatedness [62].

In 2004, a collaborative study including ten partners inseven countries representing the major European grapevinecollections was performed with the purpose to assess thecomparability and reproducibility of STR-based genotyping ofgrapevines and to standardize allele calling by defining refer-ence alleles [41]. A set of six specific dinucleotide STRs alreadywidely used (VVMD5, VVMD7, VVDM27, VVS2, VrZAG62,and VrZAG79) was agreed upon by the members for futureanalyses (Table 1). After converting raw data into normalizeddata through a coding method, the authors reported discrep-ancies of the results among the members: genotyping errors,

Table 1. List of six dinucleotide STR markers recommended by“The European Vitis Database” for grapevine profilingand bibliographic references

Marker Reference

VVS2 [17, 20, 23, 24, 28, 32, 33, 35, 41, 49, 50, 65, 69–93]VVMD5 [17, 20, 23, 24, 28, 32, 33, 35, 41, 49, 50, 65, 69–72, 74–80, 83,

85–92, 94–96]VVMD7 [17,20,23,24,28,32,33,35,41,49,50,65,69–72,74–92,94–96]VVMD27 [17, 20, 24, 28, 41, 49, 50, 65, 69, 71, 72, 74–86, 92, 94, 95]ssrVrZAG62 [17,20,23,24,28,33,35,41,49,50,65,69–72,74–86,89,91,92]SsrVrZAG79 [17,20,23,24,28,33,35,41,49,50,65,69–72,74–86,89,91,92]

1–2 bp shifts for several alleles, and discrepancies in the caseof single alleles that were only 2 bp apart. All these discrep-ancies can be explained by the characteristics of dinucleotideSTRs described in the previous section. In order to overcomethis problem, a coding method based on the alleles observedin well-known reference cultivars was developed to allow forgenotype data comparison and compilation.

5 Emerging long core-repeat STRs forgrapevine genotyping

Long core-repeat STRs suitable for grapevine genotyping havebeen recently started to be explored. A list of 38 new long-coreSTR markers (tri-, tetra-, and pentanucleotides) was proposedand ranked based on the amplification of a single locus, neg-ligible frequency of null alleles, quality of the electrophoreticsignal, and independent segregation [58]. Of these, the 19loci with the highest power of discrimination (distributedone per chromosome, with combined nonexclusion proba-bility for unrelated and full-sib individuals of 1.23 × 10−15

and 8.6 × 10−7, respectively) were proposed for grapevinegenotyping (Table 2).

In the same study, this 19 loci STR panel was alsocompared with the panel of 6 commonly used dinucleotideloci [41] in terms of information content and power of discrim-ination, and similar results were obtained. A second study,using 34 long-repeat STRs derived from Cipriani et al. wasused to genotype a collection of 1005 grapevine accessions [8],thus providing the first database of grapevine genotypes withalleles given in terms of the number of repeated units. Ahigh level of synonymy and near synonymy was found inthe analyzed collection, resulting in 745 unique genotypes.Exploratory parentage analysis confirmed, revised, and re-ported new parentages including well-known and less-knowncultivars. A complex picture of second- and third-degree re-lationships among cultivars considered typical of differentEuropean wine making regions challenged the previous con-ception of independent origins [27, 63, 64]. The authors sug-gested that ampelography should be used to confirm bothidentity and parentage analysis, since further misnaming andmislabeling in the collection could not be excluded. Thesereports clearly demonstrate that dinucleotide STRs can beadvantageously replaced by long core-repeat loci for the



Table 2. List of 19 tetranucleotide STR markers for grapevinegenotyping, length of the sequence allele, repeat motif,and power of discrimination (PD) [58]

Marker Sequencedallele (bp)

Motif PD

VChr1b 112 ATCC 0.821VChr2b 123 AGCT 0.714VChr3a 199 AAT 0.933VChr4a 197 AAAG 0.787VChr5b 198 AAAG 0.899VChr6a 184 AATC 0.733VChr7b 188 ACAT 0.866VChr8b 142 AAG 0.956VChr9a 114 AAG 0.925VChr10b 140 AAC 0.798VChr11b 163 AGAT 0.874VChr12a 136 AATT 0.814VChr13a 155 AAAAG 0.855VChr14b 195 ATC 0.834VChr15b 124 AAT 0.898VChr16a 162 AAAT 0.796VChr17a 187 AACC 0.585VChr18a 167 AAGG 0.852VChr19a 143 AAG 0.902

genotyping of grapevines in identity and parentage testing,and to investigate the genetic structure of populations.

6 Conclusions

The development of grapevine DNA analysis has not dis-placed the need for classical identification by ampelographicmethods. In fact, a close relationship between ampelogra-phers and molecular geneticists is essential for setting the ba-sis for accurate grapevine identification by securing extensivemorphological knowledge and “true-to-typeness” of individu-als [65, 66]. This collaboration is evident in the improvementand selection of OIV (Organization Internacionale de la Vi-gne et du Vin) primary and secondary descriptors carried outby ampelographic experts within the project GENRES 081(European network for grapevine genetic resources conser-vation and characterization, www.genres.de/eccdb/vitis) forthe morphological description and the assessment of agro-nomic traits of grapevine cultivars listed in the European Vi-tis Database (www.eu-vitis.de), including old and less-knownvarieties.

STR-based grapevine genotyping has already proved itsmerit to help clarifying the origins, history, and pedigree ofV. vinifera, as well as great potential to be used as a tool inforensic applications such as identification and assessmentof authenticity. Pioneering work has been performed andthe necessary steps have already been taken toward harmo-nized grapevine genotyping [8, 41, 58]. This may be viewedas an exemplary at a moment when not even broad guide-lines for forensic plant genotyping have yet been developed.In fact, only recently has the analysis of non-human DNAresulted in general recommendations by panels of experts

regarding the use of non-human DNA in forensic investi-gations [67, 68]. Although a large amount of grapevine STRdata has been published, interlaboratory variations and lackof standardized reports of genotypes render the compilationand full comparison of results extremely difficult. Consider-able international collaboration effort will be required in orderto improve the current protocols, which are presently basedon recommended set of widely used six dinucleotide STRloci that present serious disadvantages compared to longercore-repeat loci. These improvements would aid grapevinegenotyping to converge with the state-of-the-art forensic ge-netics standards already established for human analyses andcurrently in development for other animals.

In this context, we here present a basic set of sugges-tions for the further development of standardized STR-basedgenotyping in the grapevine: (i) trueness-to-type of the sam-ple must be guaranteed; (ii) long core-repeat markers (e.g.tri-, tetra-, and pentanucleotide) should be used instead ofdinucleotide STRs; (iii) PCR primers should produce con-sistent amplifications and their specificity should be testedby the sequencing of primer annealing regions in a widerange of grapevine cultivars; (iv) frequent alleles should be se-quenced and used to construct standardized allele ladders (i.e.with alleles referred to by the number of repeats determinedby sequencing; (v) STR-based parentage and pedigree analy-sis should consider mutation rates when evaluating results;(vi) large and representative numbers of individuals must begenotyped in order to obtain allele frequency databases; (vii)standardized genotype data based on repeat number nomen-clature should be publicly available in order to facilitate infor-mation exchange between laboratories.

B. A. is a grantee from Foundation for Science and Technol-ogy (FCT) (SFRH/BPD/73108/2010). M. O. is a grantee fromFCT (SFRH/BPD/66071/2009). IPATIMUP is an AssociateLaboratory of the Portuguese Ministry of Science, Technology andHigher Education and is partially supported by FCT. The authorsare grateful to three anonymous reviewers for helpful commentson the manuscript.

The authors have declared no conflict of interest.

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A forensic perspective on the genetic identification of grapevine ( Vitis vinifera L.) varieties using STR markers