The Strawberry DNA Testing Handbook

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  • 1 Department of Horticultural Sciences, IFAS Gulf Coast Research and Education Center, University of Florida, Wimauma, FL 33598
  • 2 U.S. Department of Agriculture-Agricultural Research Service, National Clonal Germplasm Repository, Corvallis, OR 97333
  • 3 Department of Horticulture, Michigan State University, East Lansing, MI 48824
  • 4 Department of Plant Sciences, University of California Davis, Davis, CA 95616
  • 5 Department of Horticultural Sciences, IFAS Gulf Coast Research and Education Center, University of Florida, Wimauma, FL 33598

The availability of strawberry (Fragaria ×ananassa) genomic resources has increased dramatically in recent years. Some of these resources are readily applicable to strawberry breeding programs for use in DNA-informed breeding. Information about these tests and how to interpret them is dispersed through numerous manuscripts or in the laboratories that use them routinely. To assist breeders in identifying tests available to their breeding program and in implementing them in their program, a compendium of strawberry DNA tests was created. This compendium is available for download from the Genome Database for Rosaceae (https://www.rosaceae.org/organism/Fragaria/x-ananassa?pane=resource-4). This resource will be updated continually as old tests are modified and new tests are created.

Abstract

The availability of strawberry (Fragaria ×ananassa) genomic resources has increased dramatically in recent years. Some of these resources are readily applicable to strawberry breeding programs for use in DNA-informed breeding. Information about these tests and how to interpret them is dispersed through numerous manuscripts or in the laboratories that use them routinely. To assist breeders in identifying tests available to their breeding program and in implementing them in their program, a compendium of strawberry DNA tests was created. This compendium is available for download from the Genome Database for Rosaceae (https://www.rosaceae.org/organism/Fragaria/x-ananassa?pane=resource-4). This resource will be updated continually as old tests are modified and new tests are created.

The development of new strawberry (Fragaria ×ananassa) cultivars with improved flowering, fruit quality, and disease resistance is an ultimate goal for fruit breeders worldwide. Selective breeding has resulted in tremendous crop improvement, but even greater progress can be achieved with the use of new technologies, such as molecular markers (Peace, 2017). As genome sequences and modern genetic resources for fruit crops have become available, it is critical that these resources be used to develop practical tools for crop improvement. DNA tests are tools that help breeders predict traits of interest in parents and offspring, and how they will be inherited in future generations.

The RosBREED project (https://www.rosbreed.org), funded by U.S. Department of Agriculture (USDA)-Specialty Crop Research Initiative, focused on leveraging genetic information to improve eight rosaceous crops: apple, blackberry, peach, pear, rose, strawberry, sweet cherry, and tart cherry. For strawberry, these improvement efforts included the development of genomic resources, the discovery of quantitative trait loci (QTL), and the facilitation of DNA-informed breeding (DIB, also known as marker-assisted breeding). DNA-informed breeding helps breeders select potential cultivars while reducing the need to maintain plants long term and perform phenotypic trials for traits that are expensive or difficult to measure (Peace, 2017; van Geest, 2017). The DIB process involves extracting DNA from parents or offspring and running DNA tests that have been associated with desirable traits. The DNA tests implemented in DIB may be for a closely linked rare allele or a functional mutation within the causal gene for a trait, as exemplified in the work by Perrotte et al. (2016) and Zorrilla-Fontanesi et al. (2012). Ideally, the DNA tests are high throughput, accurate, low cost, and user friendly. These factors are especially important when a large number of samples need to be genotyped with limited resources and time. When implemented in a breeding program, DIB can enhance the efficiency, accuracy, and pace of breeding while reducing the cost. Implementing DIB enables breeders to identify and exploit the genetic potential in their programs and use their resources effectively.

The first RosBREED project, “RosBREED: Enabling Marker-assisted Breeding in Rosaceae” (Iezzoni et al., 2010), was initiated in 2009 and identified many important QTL for flowering, fruit quality, and disease resistance traits. The first 90K Axiom® single nucleotide polymorphism (SNP) array (Bassil et al., 2015), developed as part of the first RosBREED project, has been used as a high-throughput genotyping tool for QTL discovery in numerous strawberry programs worldwide (Anciro et al., 2018; Nellist et al., 2019; Roach et al., 2016; Verma et al., 2017). The second RosBREED project, “RosBREED: Combining Disease Resistance and Horticultural Quality in New Rosaceous Cultivars” (Iezzoni et al., 2016, 2017), built on the initial work by identifying disease-resistant QTL and combining them with horticultural quality QTL. This was accomplished through the development and use of many DNA tests. Moreover, the genomic resources developed by the RosBREED projects also facilitated the development of many DNA tests by the international community. This article describes briefly the development of an online compendium of DNA markers for DIB called the Strawberry DNA Testing Handbook, created with RosBREED support for the benefit of strawberry breeders and geneticists worldwide.

Rationale

In recent years, a number of chromosome regions (loci) in strawberry have been identified that control flowering, fruit quality, and disease resistance traits in strawberry. DNA tests have been developed for many of these loci in octoploid strawberry. Many breeding programs have adopted DIB as part of their breeding process by either running the tests internally or outsourcing the work to companies providing diagnostic testing services. The initial optimization process, as well as the performance and interpretation of DNA tests, often require a skill set that might not be readily available in all laboratories (Peace, 2017). As such, we created the Strawberry DNA Testing Handbook as an easy-to-use resource. The purpose of the handbook is to distill information from primary literature related to the DNA tests, provide a starting point for test optimization, and assist in the interpretation of tests for informed breeding decisions. Overall, we hope this resource can serve as a training tool and troubleshooting guide for the implementation of existing DNA tests in strawberry breeding programs. To ensure availability, the handbook has been published at the Genome Database for Rosaceae (Jung et al., 2019) and can be downloaded as a Microsoft Word document (https://www.rosaceae.org/organism/Fragaria/x-ananassa?pane=resource-4). As new DNA tests are published or old tests are modified or replaced, the authors will continually update the handbook to maintain its relevance and usefulness to the strawberry breeding community.

Technical Information

In the Strawberry DNA Testing Handbook, tests are organized by trait (e.g., fruit quality and disease resistance), the gene/locus being tested, and the test being used. Numerous SNP-based high-resolution melting markers are available for both horticultural quality and disease resistance traits (Table 1). Electrophoresis-based tests are also listed for breeding programs without access to a real-time thermocycler (Table 1). Each test in the Strawberry DNA Testing Handbook is described in the same format: 1) background information, 2) technical details, 3) test interpretation, and 4) additional notes. The background information describes the trait and gene/QTL with which the test is associated, as well as the primary literature describing the test development and validation. Suggested reaction mixtures, primer sequences, and polymerase chain reaction protocols provided as a starting point for test optimization and troubleshooting are presented in the technical section. A description of how to interpret the test, positive and negative control cultivars (Table 2), and a picture of positive and negative results are shown in the interpretation section. Many of the strawberry cultivars that can serve as positive and negative controls for the tests are part of the USDA-Agriculture Research Service National Clonal Germplasm Repository (NCGR) Fragaria collection in Corvallis, OR. Leaves or runners of plants are available for distribution through the U.S. National Plant Germplasm System (https://npgsweb.ars-grin.gov/gringlobal/search.aspx?). The final section consists of additional notes and caveats surrounding the test. These notes consist of items such as known false-positive or false-negative strawberry cultivars, pathogen virulence information, or tips to help in optimization or multiplexing. To get the most out of each test, users should read the entire protocol before use to identify any caveats related to their testing needs.

Table 1.

DNA tests in cultivated strawberry, including traits and the corresponding genes/quantitative trait loci (QTL), tests, platforms used for the tests, marker types, and citations.

Table 1.
Table 2.

Strawberry varieties found in the U.S. National Strawberry Collection at the National Clonal Germplasm Repository in Corvallis, OR, that can serve as positive (+) and negative (–) controls for some of the genes/quantitative trait loci presented in the DNA test handbook.

Table 2.

Future Strawberry Community Involvement

As mentioned previously, the handbook will be updated as new tests are developed and validated. As such, there is much potential for future community involvement to maintain the usefulness of the handbook. The recent publication of the F. ×ananassa genome (Edger et al., 2019) will likely spur the development of new DNA tests. Moreover, breeding programs are likely to have regional positive and negative control cultivars they will discover as part of the testing process. Some of these cultivars might be publicly available as part of NCGR collection. To facilitate continued use of the handbook, we encourage feedback about use of these tests as well as information about new tests and potential control cultivars that the strawberry breeding and testing community can provide.

Literature Cited

  • Anciro, A., Mangandi, J., Verma, S., Peres, N., Whitaker, V.M. & Lee, S. 2018 FaRCg1: A quantitative trait locus conferring resistance to Colletotrichum crown rot caused by Colletotrichum gloeosporioides in octoploid strawberry Theor. Appl. Genet. 131 2167 2177

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  • Bassil, N.V., Davis, T.M., Zhang, H., Ficklin, S., Mittmann, M., Webster, T., Mahoney, L., Wood, D., Alperin, E.S., Rosyara, U.R., Putten, H.K., Monfort, A., Sargent, D.J., Amaya, I., Denoyes, B., Bianco, L., van Dijk, T., Pirani, A., Iezzoni, A., Main, D., Peace, C., Yang, Y., Whitaker, V., Verma, S., Bellon, L., Brew, F., Herrera, R. & van de Weg, E. 2015 Development and preliminary evaluation of a 90K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria ×ananassa BMC Genomics 16 155

    • Search Google Scholar
    • Export Citation
  • Chambers, A.H., Pillet, J., Plotto, A., Bai, J., Whitaker, V.M. & Folta, K.M. 2014 Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach BMC Genomics 15 217

    • Search Google Scholar
    • Export Citation
  • Denoyes-Rothan, B., Guérin, G., Lerceteau-Köhler, E. & Risser, G. 2005 Inheritance of a race-specific resistance to Colletotrichum acutatum in Fragaria ×ananassa Phytopathology 95 405 412

    • Search Google Scholar
    • Export Citation
  • Edger, P.P., Poorten, T.J., Van Buren, R., Hardigan, M.A., Colle, M., McKain, M.R., Smith, R.D., Teresi, S.J., Nelson, A.D.D., Wai, C.M., Alger, E.I., Bird, K.A., Yocca, A.E., Pumplin, N., Ou, S., Ben-Zvi, G., Brodt, A., Baruch, K., Swale, T., Shiue, L., Acharya, C.B., Cole, G.S., Mower, J.P., Childs, K.L., Jiang, N., Lyons, E., Freeling, M., Puzey, J.R. & Knapp, S.J. 2019 Origin and evolution of the octoploid strawberry genome Nat. Genet. 51 541 547

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    • Export Citation
  • Gaston, A., Perrotte, J., Lerceteau-Köhler, E., Rousseau-Gueutin, M., Petit, A., Hernould, M., Rothan, C. & Denoyes, B. 2013 PFRU, a single dominant locus regulates the balance between sexual and asexual plant reproduction in cultivated strawberry J. Expt. Bot. 64 1837 1848

    • Search Google Scholar
    • Export Citation
  • Haymes, K.M., Henken, B., Davis, T.M. & Van de Weg, W.E. 1997 Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry Theor. Appl. Genet. 94 1097 1101

    • Search Google Scholar
    • Export Citation
  • Haymes, K.M., Van de Weg, W.E., Arens, P., Maas, J.L., Vosman, B. & Den Nijs, A.P.M. 2000 Development of SCAR markers linked to a Phytophthora fragariae resistance gene and their assessment in European and North American strawberry genotypes J. Amer. Soc. Hort. Sci. 125 330 339

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A, Peace, C., Main, D., Bassil, N., Coe, M., Finn, C., Gasic, K., Luby, J., Hokanson, S., McFerson, J., Norelli, J., Olmstead, M., Whitaker, V. & Yue, C. 2017 RosBREED 2: Progress and future plans to enable DNA-informed breeding in the Rosaceae In: XIV EUCARPIA Symposium on Fruit Breeding and Genetics 1172 115 118

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A., Weebadde, C., Luby, J., Yue, C.Y., Peace, C.P., Bassil, N. & McFerson, J. 2010 RosBREED: Enabling marker-assisted breeding in Rosaceae Acta Hort. 859 389 394

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A., Weebadde, C., Peace, C., Main, D., Bassil, N., Coe, M., Fazio, G., Gallardo, K., Gasic, K., Luby, J., McFerson, J., van de Weg, E. & Yue, C. 2016 Where are we now as we merge genomics into plant breeding and what are our limitations? Experiences from RosBREED Acta Hort. 1117 1 6

    • Search Google Scholar
    • Export Citation
  • Jung, S., Lee, T., Cheng, C., Buble, K., Zheng, P., Yu, J., Humann, J., Ficklin, S.P., Gasic, K., Scott, K., Frank, M., Ru, S., Hough, H., Evans, K., Peace, C., Olmstead, M., DeVetter, L.W., McFerson, J., Coe, M., Wegrzyn, J.L., Staton, M.E., Abbott, A.G. & Main, D. 2019 15 Years of GDR: New data and functionality in the genome database for Rosaceae Nucl. Acids Res. 47 D1137 D1145

    • Search Google Scholar
    • Export Citation
  • Lerceteau-Köhler, E., Guerin, G. & Denoyes-Rothan, B. 2005 Identification of SCAR markers linked to Rca2 anthracnose resistance gene and their assessment in strawberry germplasm Theor. Appl. Genet. 111 862 870

    • Search Google Scholar
    • Export Citation
  • Mangandi, J., Verma, S., Osorio, L., Peres, N.A., van de Weg, E. & Whitaker, V.M. 2017 Pedigree-based analysis in a multiparental population of octoploid strawberry reveals QTL alleles conferring resistance to Phytophthora cactorum G3 (Bethesda) 7 1707 1719

    • Search Google Scholar
    • Export Citation
  • Mathey, M.M. 2013 Phenotyping diverse strawberry (Fragaria spp.) germplasm for aid in marker-assisted breeding, and marker-trait association for red stele (Phytophthora fragariae) resistance marker Rpf1. Master’s thesis, Oregon State University, Corvallis, OR

  • Nellist, C.F., Vickerstaff, R.J., Sobczyk, M.K., Marina-Montes, C., Wilson, F.M., Simpson, D.W., Whitehouse, A.D. & Harrison, R.J. 2019 Quantitative trait loci controlling Phytophthora cactorum resistance in the cultivated octoploid strawberry (Fragaria ×ananassa) Hort. Res. 6 60

    • Search Google Scholar
    • Export Citation
  • Noh, Y.H., Lee, S., Whitaker, V.M., Cearley, K.R. & Cha, J.S. 2017 A high-throughput marker-assisted selection system combining rapid DNA extraction high-resolution melting and simple sequence repeat analysis: Strawberry as a model for fruit crops J. Berry Res. 7 23 31

    • Search Google Scholar
    • Export Citation
  • Noh, Y.H., Oh, Y., Mangandi, J., Verma, S., Zurn, J.D., Lu, Y.T., Fan, Z., Bassil, N., Peres, N., Cole, G. & Acharya, C. 2018 High-throughput marker assays for FaRPc2-mediated resistance to Phytophthora crown rot in octoploid strawberry Mol. Breed. 38 104

    • Search Google Scholar
    • Export Citation
  • Peace, J. 2017 DNA-informed breeding of rosaceous crops: Promises, progress and prospects Hort. Res. 4 17006

  • Perrotte, J., Gaston, A., Potier, A., Petit, A., Rothan, C. & Denoyes, B. 2016 Narrowing down the single homoeologous FaPFRU locus controlling flowering and fruit production in the cultivated octoploid strawberry using a selective mapping strategy Plant Biotechnol. J. 14 2176 2189

    • Search Google Scholar
    • Export Citation
  • Roach, J.A., Verma, S., Peres, N.A., Jamieson, A.R., van de Weg, W.E., Bink, M.C., Bassil, N.V., Lee, S. & Whitaker, V.M. 2016 FaRXf1: A locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry Theor. Appl. Genet. 129 1191 1201

    • Search Google Scholar
    • Export Citation
  • Rugienius, R., Siksnianas, T., Stanys, V., Gelvonauskiene, D. & Bendokas, V. 2006 Use of RAPD and SCAR markers for identification of strawberry genotypes carrying red stele (Phytophtora fragariae) resistance gene Rpf1 Agron. Res. 4 335 339

    • Search Google Scholar
    • Export Citation
  • Salinas, N., Verma, S., Peres, N. & Whitaker, V.M. 2018 FaRCa1: A major subgenome-specific locus conferring resistance to Colletotrichum acutatum in strawberry Theor. Appl. Genet. 132 4 2267 2270

    • Search Google Scholar
    • Export Citation
  • Salinas, N.R., Zurn, J.D., Mathey, M., Mookerjee, S., Denoyes, B., Perrotte, J., Potier, A., Finn, C.E., Hancock, J.F., Stewart, P. & Bassil, N.V. 2017 Validation of molecular markers associated with perpetual flowering in octoploid Fragaria germplasm Mol. Breed. 37 70

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  • Sánchez-Sevilla, J.F., Cruz-Rus, E., Valpuesta, V., Botella, M.A. & Amaya, I. 2014 Deciphering gamma-decalactone biosynthesis in strawberry fruit using a combination of genetic mapping, RNA-Seq and eQTL analyses BMC Genomics 15 218

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  • van Geest, G. 2017 Disentangling hexaploid genetics: Towards DNA-informed breeding for postharvest performance in chrysanthemum. PhD Diss. Gelderland, Netherlands

  • Verma, S., Zurn, J.D., Salinas, N., Mathey, M.M., Denoyes, B., Hancock, J.F., Finn, C.E., Bassil, N.V. & Whitaker, V.M. 2017 Clarifying sub-genomic positions of QTLs for flowering habit and fruit quality in U.S. strawberry (Fragaria ×ananassa) breeding populations using pedigree-based QTL analysis Hort. Res. 4 17062

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  • Zorrilla-Fontanesi, Y., Rambla, J., Cabeza, A., Medina, J.J., Sánchez-Sevilla, J.F., Valpuesta, V., Botella, M.A., Granell, A. & Amaya, I. 2012 Genetic analysis of strawberry fruit aroma and identification of o-methyltransferase FaOMT as the locus controlling natural variation in mesifurane content Plant Physiol. 159 851 870

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Contributor Notes

This work was supported by the Florida Strawberry Research and Education Foundation (FSREF), the U.S. Department of Agriculture/National Institute of Food and Agriculture Specialty Crop Research Initiative project (“RosBREED: Combining Disease Resistance with Horticultural Quality in New Rosaceous Cultivars” under award no. 2014-51181-22378 and “Next-generation Disease Resistance Breeding and Management Solutions for Strawberry” under award no. 2017-51181-26833).

We thank all members of the strawberry genetics and breeding programs, and strawberry molecular genetics and genomics colleagues for their technical assistance.

Y.O. and J.D.Z. contributed equally to this manuscript.

S.L. is the corresponding author. E-mail: seonghee105@ufl.edu.

  • Anciro, A., Mangandi, J., Verma, S., Peres, N., Whitaker, V.M. & Lee, S. 2018 FaRCg1: A quantitative trait locus conferring resistance to Colletotrichum crown rot caused by Colletotrichum gloeosporioides in octoploid strawberry Theor. Appl. Genet. 131 2167 2177

    • Search Google Scholar
    • Export Citation
  • Bassil, N.V., Davis, T.M., Zhang, H., Ficklin, S., Mittmann, M., Webster, T., Mahoney, L., Wood, D., Alperin, E.S., Rosyara, U.R., Putten, H.K., Monfort, A., Sargent, D.J., Amaya, I., Denoyes, B., Bianco, L., van Dijk, T., Pirani, A., Iezzoni, A., Main, D., Peace, C., Yang, Y., Whitaker, V., Verma, S., Bellon, L., Brew, F., Herrera, R. & van de Weg, E. 2015 Development and preliminary evaluation of a 90K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria ×ananassa BMC Genomics 16 155

    • Search Google Scholar
    • Export Citation
  • Chambers, A.H., Pillet, J., Plotto, A., Bai, J., Whitaker, V.M. & Folta, K.M. 2014 Identification of a strawberry flavor gene candidate using an integrated genetic-genomic-analytical chemistry approach BMC Genomics 15 217

    • Search Google Scholar
    • Export Citation
  • Denoyes-Rothan, B., Guérin, G., Lerceteau-Köhler, E. & Risser, G. 2005 Inheritance of a race-specific resistance to Colletotrichum acutatum in Fragaria ×ananassa Phytopathology 95 405 412

    • Search Google Scholar
    • Export Citation
  • Edger, P.P., Poorten, T.J., Van Buren, R., Hardigan, M.A., Colle, M., McKain, M.R., Smith, R.D., Teresi, S.J., Nelson, A.D.D., Wai, C.M., Alger, E.I., Bird, K.A., Yocca, A.E., Pumplin, N., Ou, S., Ben-Zvi, G., Brodt, A., Baruch, K., Swale, T., Shiue, L., Acharya, C.B., Cole, G.S., Mower, J.P., Childs, K.L., Jiang, N., Lyons, E., Freeling, M., Puzey, J.R. & Knapp, S.J. 2019 Origin and evolution of the octoploid strawberry genome Nat. Genet. 51 541 547

    • Search Google Scholar
    • Export Citation
  • Gaston, A., Perrotte, J., Lerceteau-Köhler, E., Rousseau-Gueutin, M., Petit, A., Hernould, M., Rothan, C. & Denoyes, B. 2013 PFRU, a single dominant locus regulates the balance between sexual and asexual plant reproduction in cultivated strawberry J. Expt. Bot. 64 1837 1848

    • Search Google Scholar
    • Export Citation
  • Haymes, K.M., Henken, B., Davis, T.M. & Van de Weg, W.E. 1997 Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry Theor. Appl. Genet. 94 1097 1101

    • Search Google Scholar
    • Export Citation
  • Haymes, K.M., Van de Weg, W.E., Arens, P., Maas, J.L., Vosman, B. & Den Nijs, A.P.M. 2000 Development of SCAR markers linked to a Phytophthora fragariae resistance gene and their assessment in European and North American strawberry genotypes J. Amer. Soc. Hort. Sci. 125 330 339

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A, Peace, C., Main, D., Bassil, N., Coe, M., Finn, C., Gasic, K., Luby, J., Hokanson, S., McFerson, J., Norelli, J., Olmstead, M., Whitaker, V. & Yue, C. 2017 RosBREED 2: Progress and future plans to enable DNA-informed breeding in the Rosaceae In: XIV EUCARPIA Symposium on Fruit Breeding and Genetics 1172 115 118

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A., Weebadde, C., Luby, J., Yue, C.Y., Peace, C.P., Bassil, N. & McFerson, J. 2010 RosBREED: Enabling marker-assisted breeding in Rosaceae Acta Hort. 859 389 394

    • Search Google Scholar
    • Export Citation
  • Iezzoni, A., Weebadde, C., Peace, C., Main, D., Bassil, N., Coe, M., Fazio, G., Gallardo, K., Gasic, K., Luby, J., McFerson, J., van de Weg, E. & Yue, C. 2016 Where are we now as we merge genomics into plant breeding and what are our limitations? Experiences from RosBREED Acta Hort. 1117 1 6

    • Search Google Scholar
    • Export Citation
  • Jung, S., Lee, T., Cheng, C., Buble, K., Zheng, P., Yu, J., Humann, J., Ficklin, S.P., Gasic, K., Scott, K., Frank, M., Ru, S., Hough, H., Evans, K., Peace, C., Olmstead, M., DeVetter, L.W., McFerson, J., Coe, M., Wegrzyn, J.L., Staton, M.E., Abbott, A.G. & Main, D. 2019 15 Years of GDR: New data and functionality in the genome database for Rosaceae Nucl. Acids Res. 47 D1137 D1145

    • Search Google Scholar
    • Export Citation
  • Lerceteau-Köhler, E., Guerin, G. & Denoyes-Rothan, B. 2005 Identification of SCAR markers linked to Rca2 anthracnose resistance gene and their assessment in strawberry germplasm Theor. Appl. Genet. 111 862 870

    • Search Google Scholar
    • Export Citation
  • Mangandi, J., Verma, S., Osorio, L., Peres, N.A., van de Weg, E. & Whitaker, V.M. 2017 Pedigree-based analysis in a multiparental population of octoploid strawberry reveals QTL alleles conferring resistance to Phytophthora cactorum G3 (Bethesda) 7 1707 1719

    • Search Google Scholar
    • Export Citation
  • Mathey, M.M. 2013 Phenotyping diverse strawberry (Fragaria spp.) germplasm for aid in marker-assisted breeding, and marker-trait association for red stele (Phytophthora fragariae) resistance marker Rpf1. Master’s thesis, Oregon State University, Corvallis, OR

  • Nellist, C.F., Vickerstaff, R.J., Sobczyk, M.K., Marina-Montes, C., Wilson, F.M., Simpson, D.W., Whitehouse, A.D. & Harrison, R.J. 2019 Quantitative trait loci controlling Phytophthora cactorum resistance in the cultivated octoploid strawberry (Fragaria ×ananassa) Hort. Res. 6 60

    • Search Google Scholar
    • Export Citation
  • Noh, Y.H., Lee, S., Whitaker, V.M., Cearley, K.R. & Cha, J.S. 2017 A high-throughput marker-assisted selection system combining rapid DNA extraction high-resolution melting and simple sequence repeat analysis: Strawberry as a model for fruit crops J. Berry Res. 7 23 31

    • Search Google Scholar
    • Export Citation
  • Noh, Y.H., Oh, Y., Mangandi, J., Verma, S., Zurn, J.D., Lu, Y.T., Fan, Z., Bassil, N., Peres, N., Cole, G. & Acharya, C. 2018 High-throughput marker assays for FaRPc2-mediated resistance to Phytophthora crown rot in octoploid strawberry Mol. Breed. 38 104

    • Search Google Scholar
    • Export Citation
  • Peace, J. 2017 DNA-informed breeding of rosaceous crops: Promises, progress and prospects Hort. Res. 4 17006

  • Perrotte, J., Gaston, A., Potier, A., Petit, A., Rothan, C. & Denoyes, B. 2016 Narrowing down the single homoeologous FaPFRU locus controlling flowering and fruit production in the cultivated octoploid strawberry using a selective mapping strategy Plant Biotechnol. J. 14 2176 2189

    • Search Google Scholar
    • Export Citation
  • Roach, J.A., Verma, S., Peres, N.A., Jamieson, A.R., van de Weg, W.E., Bink, M.C., Bassil, N.V., Lee, S. & Whitaker, V.M. 2016 FaRXf1: A locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry Theor. Appl. Genet. 129 1191 1201

    • Search Google Scholar
    • Export Citation
  • Rugienius, R., Siksnianas, T., Stanys, V., Gelvonauskiene, D. & Bendokas, V. 2006 Use of RAPD and SCAR markers for identification of strawberry genotypes carrying red stele (Phytophtora fragariae) resistance gene Rpf1 Agron. Res. 4 335 339

    • Search Google Scholar
    • Export Citation
  • Salinas, N., Verma, S., Peres, N. & Whitaker, V.M. 2018 FaRCa1: A major subgenome-specific locus conferring resistance to Colletotrichum acutatum in strawberry Theor. Appl. Genet. 132 4 2267 2270

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