# Publications

2008
Davis TM, Folta KM, Shields M, Zhang Q. Gene pair markers: An innovative tool for comparative linkage mapping. Proceedings of the 6th North American Strawberry Symposium. North American Strawberry Growers Association, Kemptville, Canada. 2008.
Quintana A, Freyre R, Davis TM, Griesbach RJ. Genetic studies of flower color in Anagallis monelli L. . HortScience. 2008;43 (6) :1680-1685. Publisher's VersionAbstract

Wild Anagallis monelli exhibits blue or orange flower colors in geographically isolated populations. A new red flower color was developed through breeding, and a three-gene model was proposed for the inheritance of flower color in this species. In this study, blue and orange wild diploid accessions were used as parents to develop six F2 populations (n = 19 to 64). Sexual compatibility between blue and orange wild individuals was low with only 29% of the hybridizations producing F1 individuals. Six of 14 cross combinations between F1 siblings produced fruits, and fruiting success ranged from 55% to 90%. The number of seeds per fruit averaged 14.1 and germination rates for the F2s were low (16.8% to 30.7%). In three of six F2 populations obtained, flower color segregation ratios for orange, blue, and red were not significantly different from the expected ratios under a previously proposed three-gene model. White flower color was obtained as a fourth color variant in two of the remaining F2populations. For one of these populations, segregation ratios were not significantly different from expected ratios for an expanded four-gene model. White flowers did not contain anthocyanidins, suggesting that there was a mutation in the early stage of the anthocyanin pathway. Orange flower color was found to be primarily the result of pelargonidin, blue to malvidin, and red to delphinidin. These three pigments may be present simultaneously, and their ratios play a significant role in determining flower color. Other factors such as copigments, metal ions, or a different molecular conformation of the anthocyanin could also be involved in flower color determination.

Shulaev V, Korban SS, Sosinski B, et al. Multiple models for Rosaceae genomics. Plant Physiol. 2008;147 (3) :985-1003. Publisher's VersionAbstract

The plant family Rosaceae consists of over 100 genera and 3,000 species that include many important fruit, nut, ornamental, and wood crops. Members of this family provide high-value nutritional foods and contribute desirable aesthetic and industrial products. Most rosaceous crops have been enhanced by human intervention through sexual hybridization, asexual propagation, and genetic improvement since ancient times, 4,000 to 5,000 B.C. Modern breeding programs have contributed to the selection and release of numerous cultivars having significant economic impact on the U.S. and world markets. In recent years, the Rosaceae community, both in the United States and internationally, has benefited from newfound organization and collaboration that have hastened progress in developing genetic and genomic resources for representative crops such as apple (Malus spp.), peach (Prunus spp.), and strawberry (Fragaria spp.). These resources, including expressed sequence tags, bacterial artificial chromosome libraries, physical and genetic maps, and molecular markers, combined with genetic transformation protocols and bioinformatics tools, have rendered various rosaceous crops highly amenable to comparative and functional genomics studies. This report serves as a synopsis of the resources and initiatives of the Rosaceae community, recent developments in Rosaceae genomics, and plans to apply newly accumulated knowledge and resources toward breeding and crop improvement.

2007
Vining KJ, Zhang Q, Smith CA, Davis TM. Identification of resistance gene analogs and Verticillium wilt resistance-like sequences in Mentha longifolia . Journal of the American Society for Horticultural Science. 2007;132 (4) :541-550. Publisher's VersionAbstract

Resistance gene analog (RGA) sequences were obtained from four Mentha longifolia (L.) Huds. accessions using degenerate polymerase chain reaction (PCR) primers targeting the conserved nucleotide binding site domain found in many plant disease resistance genes. Seven distinct RGA families were identified. All M. longifolia RGAs showed similarity to sequences of the non-toll-interleukin 1 receptor R gene class. In addition, degenerate PCR primers based on the tomato (Solanum lycopersicum L.) verticillium wilt resistance (Ve) genes were used to PCR-amplify a 445-base pair (bp) Ve-like sequence from M. longifolia that had ≈57% predicted amino acid identity with Ve. Mint-specific primers based on the original mint Ve sequence were used to obtain mint-specific Ve sequences from four M. longifolia accessions and from peppermint (Mentha ×piperita L.) cultivar ‘Black Mitcham’ that had 95% to 100% predicted amino acid identity to the original mint Ve sequence. Inverse PCR was then used to obtain flanking mint Ve sequence from one M. longifolia accession extending the mint Ve sequence to 1077 bp. This is the first report of RGA sequences in the Lamiaceae and the first report of Ve-like sequences obtained with degenerate PCR primers.

Davis TM, Denoyes-Rothan B, Lerceteau-Kohler E. Strawberry. In: Genome mapping and molecular breeding in plants IV: Fruits and Nuts. . Vol 4. Heidelberg, Berlin, New York. Springer ; 2007. Publisher's Version
2006
Davis TM, Dimeglio LM, Yang R, Styan SMN, Lewers KS. Assessment of SSR Marker Transfer from the Cultivated Strawberry to Diploid Strawberry Species: Functionality, Linkage Group Assignment, and Use in Diversity Analysis. Journal of the American Society for Horticultural Science. 2006;131 (4) :506-512. Publisher's VersionAbstract
The cultivated strawberry, Fragaria ×ananassa Duchesne ex Rozier, originated via hybridization between octoploids F. chiloensis (L.) Mill. and F. virginiana Mill. These three octoploid species are thought to share a putative genome composition of AAAA'BBBB'. Diploid F. vesca L., is considered to have donated the A genome. Current attention to the development of a diploid model system for strawberry genomics warrants the assessment of simple sequence repeat (SSR) marker transferability between the octoploid and diploid species in Fragaria L. In the present study, 23 SSR primer pairs derived from F. ×ananassa Earliglow' by genomic library screening were evaluated for their utility in six diploid Fragaria species, including eight representatives of F. vesca, four of F. viridis Weston, and one each of F. nubicola (Hook. f.) Lindl. ex Lacaita, F. mandshurica Staudt, F. iinumae Makino, and F. nilgerrensis Schltdl. ex J. Gay. SSR primer pair functionality, as measured by amplification success rate (= 100% - failure rate) in each species, was ranked (from highest to lowest) as follows: F. vesca (98.4%) > F. iinumae (93.8%) = F. nubicola (93.8%) > F. mandshurica (87.5%) > F. nilgerrensis (75%) > F. viridis (73.4%). The extent to which these octoploid-derived SSR primer pairs generated markers that could be added to the F. vesca linkage map also was assessed. Of the 13 F. ×ananassa SSR markers that segregated codominantly in the F. vesca mapping population, 11 were assigned to linkage groups based upon close linkages to previously mapped loci. These markers were distributed over six of the seven F. vesca linkage groups, and can serve as anchor loci defining these six groups for purposes of comparative mapping between F. vesca and F. ×ananassa.
Monfort A, Vilanova S, Davis TM, Arús P. A new set of polymorphic simple sequence repeat (SSR) markers from a wild strawberry (Fragaria vesca) are transferable to other diploid Fragaria species and to Fragaria ×ananassa . Molecular Ecology Notes. 2006;6 (1) :197-200. Publisher's VersionAbstract

A set of 41 polymorphic microsatellite markers were developed using a CT/AG-enriched genomic library of Fragaria vesca cv. Reine des Vallées. Thirty-five of them were polymorphic in F. vesca and were tested in one accession each of six additional diploid Fragaria species and the octoploid Fragaria× ananassa. A mean of 5.3 alleles per locus and a low level of observed heterozygosity were generally detected in the 32 single-locus simple sequence repeats of F. vesca. Most of these loci amplify in the other diploid species and in F. × ananassa.

Folta KM, Davis TM. Strawberry genes and genomics. Critical Reviews in Plant Sciences. 2006;25 (5) :399-415. Publisher's VersionAbstract

Despite its value as a crop and potential utility as an experimental system, relatively little is known about the molecular-genetic aspects of inheritance or physiology in the cultivated strawberry (Fragaria xananassa). This lack of information exists at a time when biotechnology may offer important remedies to address traditional and contemporary challenges that growers face. An improved understanding of genome structure will hasten the development of molecular markers and unveil clues to the composition of this unique, octoploid genome. Definition of gene function will guide the generation of transgenic resources for research use and possibly toward cultivar development. This review seeks to compile and present the current knowledge state of the molecular-genetic basis of cultivated strawberry genomic form and function. Ongoing studies promise to expand the use of genomic tools and appropriate model systems to rapidly discern the structural and functional basis for traits of interest to agriculture, such as those associated with disease, ripening, and volatile production. Together these studies bring new molecular tools to dissect complex traits, implement marker-assisted selection and address important physiological questions in the cultivated strawberry, the Fragariagenus, and the Rosaceae family.

2005
Vining KJ, Zhang Q, Tucker AO, Smith C, Davis TM. Mentha longifolia (L.) L.: a model species for mint genetic research . HortScience. 2005;40 (5) :1225-1229. Publisher's VersionAbstract

Mentha longifolia, a wild relative of the polyploid, cultivated Mentha (mint) species, was evaluated as a potential model system for genetic research relevant to the cultivated mints. Fourteen Mentha longifolia accessions maintained by the US Department of Agriculture (USDA), Agricultural Research Service, National Clonal Germplasm Repository (NCGR), were highly diverse with respect to geographic origin, oil composition, verticillium wilt resistance, aspects of morphology, and molecular marker polymorphism. Accession CMEN 584 was the only carvone chemotype, while CMEN 682 was the only accession with high menthol content. Trans-piperitone oxide was the primary oil component of accessions CMEN 17 and CMEN 18, while pulegone was most abundant in CMEN 20, CMEN 500, CMEN 501, and CMEN 585. Four accessions—CMEN 585, CMEN 17, CMEN 501, and CMEN 81—were consistently resistant to verticillium wilt, while CMEN 584 and CMEN 516 were highly susceptible. Pairwise similarity coefficients were calculated and a UPGMA (unweighted pair-group analysis) tree was constructed on the basis of 63 informative randomly amplified polymorphic DNA (RAPD) marker bands. CMEN 585 and CMEN 584 shared the greatest number of bands (16), and formed a distinct cluster in the UPGMA tree. Seven pairs of accessions had no bands in common, emphasizing the high degree of molecular diversity represented by these accessions. The favorable features of diploid (2n = 2x = 24) genome constitution, comparatively small genome size (400 to 500 Mb), self-fertility, fecundity, and diversity with respect to economically relevant traits, contribute to M. longifolia's potential usefulness as a model system for the cultivated mints. As a perennial species amenable to vegetative propagation, M. longifolia's spectrum of susceptibility/resistance to an important vascular wilt disease encourages its further evaluation as a system for broader studies of plant–microbe interactions and disease resistance mechanisms.

2004
Sargent DJ, Davis TM, Tobutt KR, et al. A genetic linkage map of microsatellite, gene-specific and morphological markers in diploid Fragaria . Theoretical and Applied Genetics. 2004;109 (7) :1385-1391. Publisher's VersionAbstract

Diploid Fragaria provide a potential model for genomic studies in the Rosaceae. To develop a genetic linkage map of diploid Fragaria, we scored 78 markers (68 microsatellites, one sequence-characterised amplified region, six gene-specific markers and three morphological traits) in an interspecific F2 population of 94 plants generated from a cross of F.vesca f. semperflorens × F. nubicola. Co-segregation analysis arranged 76 markers into seven discrete linkage groups covering 448 cM, with linkage group sizes ranging from 100.3 cM to 22.9 cM. Marker coverage was generally good; however some clustering of markers was observed on six of the seven linkage groups. Segregation distortion was observed at a high proportion of loci (54%), which could reflect the interspecific nature of the progeny and, in some cases, the self-incompatibility of F. nubicola. Such distortion may also account for some of the marker clustering observed in the map. One of the morphological markers, pale-green leaf (pg) has not previously been mapped in Fragaria and was located to the mid-point of linkage group VI. The transferable nature of the markers used in this study means that the map will be ideal for use as a framework for additional marker incorporation aimed at enhancing and resolving map coverage of the diploid Fragaria genome. The map also provides a sound basis for linkage map transfer to the cultivated octoploid strawberry.

2003
Staudt G, Dimeglio LM, Davis TM, Gerstberger P. Fragaria ×bifera Duch.: Origin and taxonomy . Botanische Jahrbücher. 2003;125 (1) :53-72. Publisher's VersionAbstract

In 1788 DUCHESNE described strawberry plants from the environs of Bargemon (France) as Fragaria bifera. These plants appeared to him as varying between the Wood Strawberry (Fragaria vesca L.) and the Breslinges (Fragaria viridis Weston). Since then, putative hybrids between wild-growing strawberries in Europe, especially between F. vesca and F. viridis, have been reported variously. Fragaria hagenbachiana described by KOCH in 1842 from the environs of Zunzingen (Germany) is probably one of these putative hybrids. Studies on 13 accessions of putative hybrids, a great many herbarium specimens representing the whole area, and molecular investigations have led us to propose that all these plants represent hybrids of the diploid (2n = 2x = 14) species Fragaria vesca and F. viridis. The valid name is F. × bifera Duch. Morphologically F. × bifera is a highly varying hybrid species that has probably originated many times and occurs throughout the area where the two parent species commonly occur. Up to now, 12 accessions are known to be diploid (2n = 14) and one triploid (2n = 21). From molecular studies, we have identified markers for the nuclear and chloroplast genomes of F. vesca and F. viridis in all of the hybrids investigated. In all cases F. vesca has acted as the female parent. Also, the triploid's nuclear genome constitution evidently includes two genome copies from F. viridis and one from F. vesca.

2001
Deng C, Davis TM. Molecular identification of the yellow fruit color (c) locus in diploid strawberry: a candidate gene approach. Theoretical and Applied Genetics. 2001;103 (2-3) :316-322. Publisher's VersionAbstract

A candidate gene approach was used to determine the likely molecular identity of the c locus (yellow fruit color) in Fragaria vesca, a diploid (2n=2x=14) strawberry. Using PCR with degenerate primer pairs, intron-containing segments of structural genes coding for chalcone synthase (CHS), chalcone isomerase (CHI), flavanone 3-hydroxylase (F3H), dihydroflavonol 4-reductase (DFR), anthocyanidin synthase (ANS) and one Del-like regulatory gene in the anthocyanin biosynthetic pathway, were amplified, cloned and sequenced. Intron length polymorphisms for each of these genes were detected among three diploid varieties: F. vesca Alpine variety ’Yellow Wonder’ (YW) (Europe); DN1C, a F. vesca clone collected from Northern California; and Fragaria nubicola FRA520, a U.S.D.A. accession collected in Pakistan. Using F2generations of the crosses DN1C×YW and YW×FRA520 as mapping populations, the six candidate genes were mapped in relation to previously mapped randomly amplified polymorphic DNA (RAPD) markers and morphological markers. The F3H gene was linked without recombination to the c locus in linkage group I, while the other five candidate genes mapped to different linkage groups. These results suggest that the wild-type allele (C) of the c (yellow fruit color) locus encodes an F3H necessary for red fruit color in F. vesca.

2000
Lin J, Davis TM. S1 analysis of long PCR heteroduplexes: detection of chloroplast indel polymorphisms in Fragaria. Theoretical and Applied Genetics. 2000;101 (3) :415-420. Publisher's VersionAbstract

S1 analysis of long PCR heteroduplexes was found to be an effective method for detecting phylogenetically informative indel (insertion/deletion) polymorphisms in the highly conserved strawberry chloroplast genome. In this broadly applicable method, long-range PCR products containing heteroduplex DNA molecules generated from mixed-template amplifications are subjected to S1 nuclease digestion followed by separation and visualization on an agarose gel. The presence of fragments resulting from S1 digestion of mismatch loops in heteroduplex molecules is indicative of indel polymorphism between the template sources. Upon analysis of 13-kb heteroduplex-containing PCR products spanning the petA-psbB chloroplast genome region in Fragaria vesca and Fragaria moschata, two indels distinguishing these species were detected, and subsequently localized to the psbJ-psbL and rpl20-rps18 intergenic regions. Comparative sequencing of these regions revealed that F. moschata resembled Fragaria viridis, but differed from F. vescaFragaria nubicola, and a closely related outgroup representative, Duchesnea indica, by a 10-bp deletion in the psbJ-psbL region and a 10-bp insertion in the rpl20-rps18 region. Thus, of the three diploids (2n = 2x = 14) examined, F. viridis is favored over F. vesca and F. nubicola as the most likely chloroplast genome donor to hexaploid (2n = 6x = 42) F. moschata.

1999
Paruvangada VG, Davis TM. Brief communication. A dominant, host plant mutation conferring ineffective nodulation in the chickpea-Rhizobium symbiosis . Journal of Heredity. 1999;90 (2) :297-299. Publisher's VersionAbstract

Chickpea (Cicer arietinum L.) mutant PM638, a derivative of wild-type, desi chickpea line ICC 640, forms yellowish, ineffective root nodules and differs phenotypically from previously described chickpea nodulation mutants. To establish the mode of inheritance of the mutant nodule trait, and to eliminate independent chlorophyll and sterility mutations carried by the mutant, PM638 was crossed with ICC 640 and an F5 generation mutant was reciprocally backcrossed to ICC 640. Segregation analysis indicated that the mutant phenotype was conferred by a single, dominant nuclear gene mutation. In keeping with established nomenclature for chickpea nodulation genes, the mutant allele is tentatively designated Rn7.

1998
Haymes KM, Davis TM. Agrobacterium-mediated transformation of Alpine Fragaria vesca, and transmission of transgenes to R1 progeny . Plant Cell Reports. 1998;17 (4) :279-283. Publisher's VersionAbstract

Agrobacterium-mediated transformation was used to stably introduce β-glucuronidase (gus) and neomycin phosphotransferase (nptII) marker genes into Alpine' Fragaria vesca FRA 197, a diploid (2n = 2x = 14) strawberry. R0 generation transformants derived from a single clump of kanamycin-resistant callus were vegetatively propagated. The presence of the gus and nptII genes in five clonal R0 runner plants was confirmed by PCR. Southern analysis suggested two sites of nptII insertion. When R1 generation seedlings obtained via self-fertilization of R0 plants were tested by histochemical assay, 591 were GUS positive and 39 were GUS negative. The R1 segregation data fit a 15 : 1 ratio (0.5 > P > 0.25), consistent with the independent segregation of two transgene insertion loci. These results demonstrate the suitability of `Alpine' F. vesca for transgene research in strawberry.

1997
Haymes KM, Henken B, Davis TM, Van de Weg WE. Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry. Theoretical and Applied Genetics. 1997;94 (8) :1097-1101. Publisher's VersionAbstract

Bulked segregant analysis (BSA) was used to identify seven random amplified polymorphic DNA (RAPD) markers linked to the Rpf 1 gene. Rpf 1 confers resistance to Phytophthora fragariae var. fragariae, the causal agent of red stele root rot in Fragaria spp. The bulked DNAs represented subsets of a F1 population obtained from the cross Md683×Senga Sengana which consisted of 60 plants and segregated in a 1:1 ratio for resistance or susceptibility to race 2.3.4 isolate NS2 of P.  fragariae. Seven markers were shown to be linked to Rpf 1 and were generated from four primers; five of these markers were in coupling phase and two in repulsion phase with respect to the gene. A linkage map of this resistance gene region was generated using JoinMap 2.0TM. The manner in which Rpf 1 and the linked markers co-segregated indicated that they are inherited in a disomic fashion. These markers could enable gene pyramiding and marker-assisted selection of resistance genes in strawberry breeding programmes.

Davis TM, Yu H. A linkage map of the diploid strawberry, Fragaria vesca. Journal of Heredity. 1997;88 (3) :215-221. Publisher's VersionAbstract

A 445 cM long genetic linkage map consisting of seven linkage groups was constructed for the diploid (2n = 2x = 14) strawberry, Fragaria vesca. Segregation data used for linkage analysis were obtained from the F2 generation of a cross between Baron Solemacher (BS), an Alpine F. vesca variety, and WC6, an F. vesca clone collected from the wild in New Hampshire. Segregation ratios were systematically skewed in five linkage groups, in all cases favoring the BS alleies over the WC6 alleles. The 80-marker map includes 64 dominant and 11 codominant randomly amplified polymorphic DNA (RAPD) markers, an alcohol dehydrogenase locus detected as a PCR-based sequence tagged site, the phosphoglucose isomerase and shikimate dehydrogenase Isozyme loci, and the runnering and fruit color loci. A notable feature of the map is the unusually large number of codominant RAPD markers, the detection of which was due In part to the use of template mixing methods for primer testing and marker analysis. Alternate alleies of a maternally inherited RAPD marker were also detected using these methods.

1996
Davis TM. The use of molecular markers to accelerate cultivar development in Fragaria. Feb. 15-17, 1995, 4th North American Strawberry Conference. 1996.
1995
Yu H, Davis TM. Genetic linkage between runnering and phosphoglucoisomerase allozymes, and systematic distortion of monogenic segregation ratios in diploid strawberry. Journal of the American Society for Horticultural Science. 1995;120 (4) :687-690. Publisher's VersionAbstract

As part of a strawberry (Fragaria sp.) genome mapping project, we studied the linkage relationship between runnering and phosphoglucoisomerase PGI-2 allozymes in diploid strawberry. The respective r and Pgi-2 loci were found linked with a recombination frequency of 18.1% ± 1.6%(a map distance of 18.9 ± 1.6 cM). This is the second reported linkage in strawberry. The linkage between runnering and phosphoglucoisomerase allozymes, if conserved at the octoploid level, might provide a means of marker-assisted selection for the nonrunnering and bushy branching growth habits in cultivated strawberry. Severe distortion of monogenic segregation ratios was observed for runnering and PGI-2, and also for an unlinked locus for shikimate dehydrogenase allozymes. Alleles from the perpetual flowering (alpine F. vesca) parents were favored in this distortion. This phenomenon should be considered in future genetic studies using crosses between alpine and nonalpine strawberries.

Davis TM, Yu H, Haymes KM. Genetic linkage group structure in the diploid strawberry: evidence for chromosome differentiation between Fragaria vesca and F. viridis . Proceedings of the IV North American Strawberry Conference. Horticultural Sciences Department, University of Florida. 1995 :213-216. Publisher's VersionAbstract

As part of a strawberry (Fragaria sp.) genome mapping project, we studied the linkage relationship between runnering and phosphoglucoisomerase PGI-2 allozymes in diploid strawberry. The respective r and Pgi-2 loci were found linked with a recombination frequency of 18.1% ± 1.6%(a map distance of 18.9 ± 1.6 cM). This is the second reported linkage in strawberry. The linkage between runnering and phosphoglucoisomerase allozymes, if conserved at the octoploid level, might provide a means of marker-assisted selection for the nonrunnering and bushy branching growth habits in cultivated strawberry. Severe distortion of monogenic segregation ratios was observed for runnering and PGI-2, and also for an unlinked locus for shikimate dehydrogenase allozymes. Alleles from the perpetual flowering (alpine F. vesca) parents were favored in this distortion. This phenomenon should be considered in future genetic studies using crosses between alpine and nonalpine strawberries.