Advertisement

Disease Resistance in Polyploid Strawberry

  • Charlotte F. Nellist
Chapter
Part of the Compendium of Plant Genomes book series (CPG)

Abstract

The cultivated strawberry (Fragaria × ananassa Duchesne) is grown globally, from subarctic regions through to subantarctic regions and is host to a vast array of economically important disease-causing pathogens. Diseases are a significant limiting factor to crop production worldwide, resulting in high costs caused not only by yield losses but also by the expense of pesticide applications to try to prevent or manage the diseases. Traditionally, the major strategy for disease control in strawberry production relied heavily upon pre-plant fumigation and chemicals. The withdrawal of many of these active chemicals, including fungicides and soil fumigants, is increasing the challenges in strawberry production, resulting in a rise of occurrences and severities of some once well-controlled diseases. There is an absence of commercial cultivars that possess high levels of resistance to multiple pathogens. Breeding for disease resistance is a high priority for many breeding programmes across the world. This chapter will discuss some of the major diseases of the cultivated strawberry, the current status of resistance and future prospects.

Keywords

Fragaria × ananassa Disease resistance Quantitative trait loci Plant–pathogen interactions 

References

  1. Ajwa HA, Klose S, Nelson SD, Minuto A, Lodovica Gullino M et al (2004) Alternatives to methyl bromide in strawberry production in the United States of America and the Mediterranean region. Phytopathol Mediterr 42:220–244Google Scholar
  2. Amselem J, Cuomo CA, van Kan JAL, Viaud M, Benito EP et al (2011) Genomic analysis of the necrotrophic fungal pathogens Sclerotinia sclerotiorum and Botrytis cinerea. PLoS Genet 7:e1002230PubMedPubMedCentralCrossRefGoogle Scholar
  3. Antanaviciute L, Šurbanovski N, Harrison N, McLeary K, Simpson DW et al (2015) Mapping QTL associated with Verticillium dahliae resistance in the cultivated strawberry (Fragaria × ananassa). Hortic Res 2:15009PubMedPubMedCentralCrossRefGoogle Scholar
  4. Asalf B, Gadoury DM, Tronsmo AM, Seem RC, Dobson A et al (2014) Ontogenic resistance of leaves and fruit, and how leaf folding influences the distribution of powdery mildew on strawberry plants colonized by Podosphaera aphanis. Phytopathology 104:954–963PubMedCrossRefPubMedCentralGoogle Scholar
  5. Asalf B, Gadoury DM, Tronsmo AM, Seem RC, Stensvand A (2016) Effects of development of ontogenic resistance in strawberry leaves upon pre- and postgermination growth and sporulation of Podosphaera aphanis. Plant Dis 100:72–78CrossRefGoogle Scholar
  6. Ayoubi N, Soleimani MJ (2016) Strawberry fruit rot caused by Neopestalotiopsis iranensis sp. nov., and N. mesopotamica. Curr Microbiol 72:329–336PubMedPubMedCentralGoogle Scholar
  7. Bassil NV, Davis TM, Zhang H, Ficklin S, Mittmann M et al (2015) Development and preliminary evaluation of a 90 K Axiom® SNP array for the allo-octoploid cultivated strawberry Fragaria × ananassa. BMC Genomics, 1–30Google Scholar
  8. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32:76–84PubMedCrossRefPubMedCentralGoogle Scholar
  9. Bestfleisch M, Luderer-Pflimpfl M, Höfer M, Schulte E, Wünsche JN et al (2014) Evaluation of strawberry (Fragaria L.) genetic resources for resistance to Botrytis cinerea. Plant Pathol 64:396–405CrossRefGoogle Scholar
  10. Bhat RG, Subbarao KV (1999) Host range specificity in Verticillium dahliae. Phytopathology 89:1218–1225PubMedCrossRefPubMedCentralGoogle Scholar
  11. Brun H, Chèvre A-M, Fitt BD, Powers S, Besnard A-L et al (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185:285–299PubMedCrossRefPubMedCentralGoogle Scholar
  12. CABI E (1997) Quarantine pests for Europe, 2nd edn. CABI, Wallingford, U.K.Google Scholar
  13. Chamorro M, Aguado A, De los Santos B (2016) First report of root and crown rot caused by Pestalotiopsis clavispora (Neopestalotiopsis clavispora) on strawberry in Spain. Plant Dis 100:1495CrossRefGoogle Scholar
  14. Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814PubMedPubMedCentralCrossRefGoogle Scholar
  15. Cooke DEL, Drenth A, Duncan JM, Wagels G, Brasier CM (2000) A molecular phylogeny of Phytophthora and related oomycetes. Fungal Genet Biol 30:17–32PubMedCrossRefPubMedCentralGoogle Scholar
  16. Coombe L, Warren RL, Jackman SD, Yang C, Vandervalk BP et al (2016) Assembly of the complete Sitka spruce chloroplast genome using 10X Genomics’ GemCode sequencing data. PLoS ONE 11:e0163059–13Google Scholar
  17. Crosse JE, Pitcher RS (1952) Studies in the relationship of eelworms and bacteria to certain plant diseases. I. The etiology of Strawberry cauliflower disease. Ann App Biol 39:475–486CrossRefGoogle Scholar
  18. Darrow GM (1966) The strawberry. History, breeding and physiology. Holt, Rinehart & Winston, New YorkGoogle Scholar
  19. Daubeny HA, Pepin HS (1965) The relative resistance of various Fragaria chiloensis clones to Phyophthora fargariae. Can J Plant Sci 45:365–368CrossRefGoogle Scholar
  20. Daugaard H (1999) Cultural methods for controlling Botrytis cinerea Pers. in strawberry. Biol Agric Hortic 16:351–361CrossRefGoogle Scholar
  21. Dávalos-González PA, Jofre-Garfias AE, Hernández-Razo AR, Narro-Sánchez J, Castro-Franco J et al (2006) Strawberry breeding for the central plateau of México. Acta Hortic 708:547–549CrossRefGoogle Scholar
  22. Davik J, Eikemo H, Brurberg MB, Sargent DJ (2015) Mapping of the RPc-1 locus for Phytophthora cactorum resistance in Fragaria vesca. Mol Breeding 35:1–11CrossRefGoogle Scholar
  23. Denoyes B, Baudry A (1995) Species identification and pathogenicity study of French Colletotrichum strains isolated from Strawberry using morphological and cultural characteristics. Phytopathology 85:53–57CrossRefGoogle Scholar
  24. Denoyes-Rothan B, Lerceteau-Köhler E, Guerin G, Bosseur S, Bariac J et al (2004) QTL analysis for resistances to Colletotrichum acutatum and Phytophthora cactorum in octoploid strawberry (Fragaria × ananassa). Acta Hortic 663:147–152CrossRefGoogle Scholar
  25. Denoyes-Rothan B, Guerin G, Lerceteau-Köhler E, Risser G (2005) Inheritance of Resistance to Colletotrichum acutatum in Fragaria × ananassa. Phytopathology 95:405–412PubMedPubMedCentralCrossRefGoogle Scholar
  26. Deutschmann VF (1954) Eine Wurzelfäule an Erdbeeren, hervorgerufen durch Phytophthora cactorum (Leb. et Cohn) Schröt. Nachrichtenblatt des Deutschen Pflanzenschutzdienstes 6:7–9Google Scholar
  27. Eikemo H, Stensvand A (2015) Resistance of strawberry genotypes to leather rot and crown rot caused by Phytophthora cactorum. Eur J Plant Pathol 143:407–413CrossRefGoogle Scholar
  28. Eikemo H, Stensvand A, Davik J, Tronsmo AM (2003) Resistance to crown rot (Phytophthora cactorum) in strawberry cultivars and in offspring from crosses between cultivars differing in susceptibility to the disease. Ann App Biol, 1–8Google Scholar
  29. Eikemo H, Klemsdal SS, Riisberg I, Bonants P, Stensvand A et al (2004) Genetic variation between Phytophthora cactorum isolates differing in their ability to cause crown rot in strawberry. Mycol Res 108:317–324PubMedCrossRefPubMedCentralGoogle Scholar
  30. Ellis MA, Grove GG (1983) Leather rot in Ohio strawberries. Plant Dis 67:549CrossRefGoogle Scholar
  31. English AC, Richards S, Han Y, Wang M, Vee V et al (2012) Mind the gap: upgrading genomes with pacific biosciences RS long-read sequencing technology. PLoS ONE 7:e47768PubMedPubMedCentralCrossRefGoogle Scholar
  32. Faedi W, Mourgues F, Rosati C (2002) Strawberry breeding and varieties: situation and perspectives. Acta Hortic 567:51–59CrossRefGoogle Scholar
  33. Fang X, Barbetti MJ (2014) Differential protein accumulations in isolates of the strawberry wilt pathogen Fusarium oxysporum f. sp. fragariae differing in virulence. J Proteomics 108:223–237PubMedCrossRefPubMedCentralGoogle Scholar
  34. Fang X, Phillips D, Verheyen G, Li H, Sivasithamparam K, Barbetti MJ (2012a) Yields and resistance of strawberry cultivars to crown and root diseases in the field, and cultivar responses to pathogens under controlled environment conditions. Phytopathol Mediterr 51:69–84Google Scholar
  35. Fang X, Kuo J, You MP, Finnegan PM, Barbetti MJ (2012b) Comparative root colonisation of strawberry cultivars. Camarosa and festival by Fusarium oxysporum f. sp. fragariae. Plant Soil 358:75–89CrossRefGoogle Scholar
  36. Fang X, Jost R, Finnegan PM, Barbetti MJ (2013) Comparative proteome analysis of the strawberry- Fusarium oxysporum f. sp. fragariae pathosystem reveals early activation of defense responses as a crucial determinant of host resistance. J Proteome Res 12:1772–1788.  https://doi.org/10.1021/pr301117aCrossRefPubMedPubMedCentralGoogle Scholar
  37. Gao R, Cheng Y, Wang Y, Wang Y, Guo L et al (2015) Genome sequence of Phytophthora fragariae var. fragariae, a quarantine plant-pathogenic fungus. Genome Announc 3:e00034–15PubMedPubMedCentralCrossRefGoogle Scholar
  38. Gołębniak B, Jarosz A, Olechnowicz J (2006) Susceptibility of strawberry cultivars to leather rot (Phytophthora cactorum and P. citricola). Phytopathol Pol 39:149–153Google Scholar
  39. González G, Moya M, Sandoval C, Herrera R (2009) Genetic diversity in Chilean strawberry (Fragaria chiloensis): differential response to Botrytis cinerea infection. Span J Agric Res 7:886–895CrossRefGoogle Scholar
  40. Goto M, Shiramatsu T, Nozaki K, Kawagughi K (1978) Studies on bacterial wilt of strawberry caused by Pseudomonas solanacearum (Smith) Smith. Jpn J Phytopathol 44:270–276CrossRefGoogle Scholar
  41. Han J-H, Chon J-K, Ahn J-H, Choi I-Y, Lee Y-H et al (2016) Whole genome sequence and genome annotation of Colletotrichum acutatum, causal agent of anthracnose in pepper plants in South Korea. GDATA 8:45–46Google Scholar
  42. Hancock JF, Luby JJ, Dale A, Callow PW, Serçe S et al (2002) Utilizing wild Fragaria virginiana in strawberry cultivar development: inheritance of photoperiod sensitivity, fruit size, gender, female fertility and disease resistance. Euphytica 126:177–184CrossRefGoogle Scholar
  43. Harrison RE, Luby JJ, Furnier GR (1997) Chloroplast DNA restriction fragment variation among strawberry (Fragaria spp.) Taxa. J Am Soc Hort Sci 122:63–68Google Scholar
  44. Hartung JS, Gouin CC, Lewers KS, Maas JL, Hokanson SC (2003) Identification of sources of resistance to bacterial angular leafspot disease of strawberry. Acta Hortic 26:155–159CrossRefGoogle Scholar
  45. Haymes KM, Henken B, Davis TM, van de Weg WE (1997) Identification of RAPD markers linked to a Phytophthora fragariae resistance gene (Rpf1) in the cultivated strawberry. Theor App Genet 94:1097–1101CrossRefGoogle Scholar
  46. Haymes KM, Hokanson S, van de Weg EW, Maas JL (1998) AFLP and RAPD markers linked to Phytophthora fragariae resistance genes in Strawberry. In: Plant and animal genome conferenceGoogle Scholar
  47. Henry PM, Leveau JHJ (2016) Finished genome sequences of Xanthomonas fragariae, the cause of bacterial angular leaf spot of strawberry. Genome Announc 4:e01271–16PubMedPubMedCentralCrossRefGoogle Scholar
  48. Herrington ME, Chandler CK, Moisander JA, Reid CE (2007) “Rubygem” strawberry. HortScience 42:1482–1483Google Scholar
  49. Hirakawa H, Shirasawa K, Kosugi S, Tashiro K, Nakayama S et al (2014) Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria Species. DNA Res 21:169–181PubMedPubMedCentralCrossRefGoogle Scholar
  50. Horn NL, Carver RB, Burnside KR (1972) Powdery mildew of strawberry. Plant Dis Rep 56:368Google Scholar
  51. Hummer KE, Bassil N, Njuguna W (2011) Fragaria. Springer Berlin Heidelberg, Berlin, Heidelberg, pp 17–44Google Scholar
  52. Islam MS, Haque MS, Islam MM, Emdad EM, Halim A et al (2012) Tools to kill: genome of one of the most destructive plant pathogenic fungi Macrophomina phaseolina. BMC Genom 13:493CrossRefGoogle Scholar
  53. Jamieson AR, Hildebrand PD, Renderos WE (2013) Breeding strawberry plants resistant to angular leaf disease. Int J Fruit Sci 13:28–35CrossRefGoogle Scholar
  54. Jamieson AR, Hildebrand PD, Renderos WE, Fillmore SAE (2014) Resistance to angular leafspot disease of strawberry: influence of seedling age. Acta Hortic 1049:187–191CrossRefGoogle Scholar
  55. Janse JD, Rossi MP, Gorkink RFJ, Derks JHJ, Swing J et al (2001) Bacterial leaf blight of strawberry (Fragaria (×) ananassa) caused by a pathovar of Xanthomonas arboricola, not similar to Xanthomonas fragariae Kennedy & King. Description of the causal organism as Xanthomonas arboricola pv. fragariae (pv. nov., comb. nov.). Plant Pathol 50:653–665CrossRefGoogle Scholar
  56. Jørgensen JH (1992) Discovery, characterization and exploitation of Mlo powdery mildew resistance in barley. Euphytica 63:141–152CrossRefGoogle Scholar
  57. Jupe F, Witek K, Verweij W, Śliwka J, Pritchard L et al (2013) Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J 76:530–544PubMedPubMedCentralCrossRefGoogle Scholar
  58. Kennedy DM, King TH (1962) Angular leaf spot of Strawberry caused by Xanthomonas fragariae sp. nov. Phytopathology 52:873–875Google Scholar
  59. Kim CH, Seo HD, Cho WD, Kim SB (1982) Studies on varietal resistance and chemical control of the wilt of strawberry caused by Fusarium oxysporum. Korean J Plant Prot 21:61–67Google Scholar
  60. Klosterman SJ, Subbarao KV, Kang S, Veronese P, Gold SE et al (2011) Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7:e1002137–19CrossRefGoogle Scholar
  61. Koike ST, Arias RS, Hogan CS, Martin FN, Gordon TR (2016) Status of Macrophomina phaseolina on strawberry in California and preliminary characterization of the pathogen. Int J Fruit Sci 16:148–159CrossRefGoogle Scholar
  62. Laver T, Harrison J, O’Neill PA, Moore K, Farbos A et al (2015) Assessing the performance of the Oxford Nanopore Technologies MinION. BDQ 3:1–8PubMedPubMedCentralGoogle Scholar
  63. Lerceteau-Köhler E, Guérin G, Denoyes-Rothan B (2005) Identification of SCAR markers linked to Rca2 anthracnose resistance gene and their assessment in strawberry germplasm. Theor Appl Genet 111:862–870CrossRefPubMedGoogle Scholar
  64. Levy-Sakin M, Ebenstein Y (2013) Beyond sequencing: optical mapping of DNA in the age of nanotechnology and nanoscopy. Curr Opin Biotechnol 24:690–698PubMedCrossRefPubMedCentralGoogle Scholar
  65. Lewers KS, Maas JL, Hokanson SC, Hartung JS (2003) Inheritance of resistance in strawberry to bacterial angular leafspot disease caused by Xanthomonas fragariae. J Am Soc Hort Sci 128:209–212Google Scholar
  66. Liang L, Lin Z (2014) Genetic study on resistance to Powdery Mildew in Strawberry. Acta Hortic 1049:255–258CrossRefGoogle Scholar
  67. Luby JJ, Hancock JF, Dale A, Serçe S (2008) Reconstructing Fragaria × ananassa utilizing wild F. virginiana and F. chiloensis: inheritance of winter injury, photoperiod sensitivity, fruit size, female fertility and disease resistance in hybrid progenies. Euphytica 163:57–65CrossRefGoogle Scholar
  68. Maas JL (1998) Compendium of strawberry diseases, 2nd edn. The American Phytopathological Society, Minnesota, USAGoogle Scholar
  69. Maas JL (2004) Strawberry disease management. In: Naqvi SAMH (ed) Diseases of fruits and vegetables. Kluwer Academic Publishers, pp 441–483Google Scholar
  70. Maas JL (2014) Strawberry diseases and pests—progress and problems. Acta Hortic 1049:133–142CrossRefGoogle Scholar
  71. Maas JL, Galletta GJ, Draper AD (1989) Resistance in strawberry to races of Phytophthora fragariae and to isolates of Verticillium from North America. Acta Hortic 265:521–526CrossRefGoogle Scholar
  72. Maas JL, Gouin-Behe C, Hartung JS, Hokanson SC (2000) Sources of resistance for two differentially pathogenic strains of Xanthomonas fragariae in Fragaria genotypes. HortScience 35:128–131Google Scholar
  73. Maas JL, Gouin CC, Hokanson SC, Hartung JS (2002) Strawberry parent clones US 4808 and US 4809 resistant to bacterial angular leafspot disease caused by Xanthomonas fragariae. HortScience 37:716–717Google Scholar
  74. MacKenzie SJ, Legard DE, Timmer LW, Chandler CK, Peres NA (2006) Resistance of strawberry cultivars to crown rot caused by Colletotrichum gloeosporioides isolates from florida is nonspecific. Plant Dis 90:1091–1097CrossRefGoogle Scholar
  75. Mangandi J, Peres NA, Whitaker VM (2015) Identifying resistance to crown rot caused by Colletotrichum gloeosporioides in strawberry. Plant Dis 99:954–961CrossRefGoogle Scholar
  76. Mangandi J, Verma S, Osorio LF, van de Weg EW, Whitaker VM (2017) Pedigree-based analysis in a multiparental population of octoploid strawberry reveals QTL alleles conferring resistance to Phytophthora cactorum. Genes, Genomes and Genet 7:1707–1719Google Scholar
  77. Nagarajan G, Nam MH, Song JY, Yoo SJ, Kim HG (2004) Genetic variation in Fusarium oxysporum f. sp. fragariae populations based on RAPD and rDNA RFLP analyses. Plant Pathol 20:264–270CrossRefGoogle Scholar
  78. Nagarajan G, Kang SW, Nam MH, Song JY, Yoo SJ et al (2006) Characterisation of Fusarium oxysporum f. sp. fragariae based on vegetative compatibility group, random amplified polymorphic DNA and pathogenicity. Plant Pathol 22:222–229CrossRefGoogle Scholar
  79. Nelson MD, Gubler WD, Shaw DV (1995) Inheritance of powdery mildew resistance in greenhouse-grown versus field-grown California strawberry progenies. Phytopathology 85:421–424CrossRefGoogle Scholar
  80. Nelson MD, Gubler WD, Shaw DV (1996) Relative resistance of 47 strawberry cultivars to Powdery mildew in California greenhouse and field environments. Plant Dis 80:326–328CrossRefGoogle Scholar
  81. Pattison JA, Samuelian SK, Weber CA (2007) Inheritance of Phytophthora root rot resistance in red raspberry determined by generation means and molecular linkage analysis. Theor Appl Genet 115:225–236CrossRefPubMedGoogle Scholar
  82. Paulus AO (1990) Fungal diseases of strawberry. HortScience 25:885–889Google Scholar
  83. Pavan S, Jacobsen E, Visser RGF, Bai Y (2010) Loss of susceptibility as a novel breeding strategy for durable and broad-spectrum resistance. Mol Breed 25:1–12PubMedCrossRefPubMedCentralGoogle Scholar
  84. Pedersen WL, Leath S (1988) Pyramiding major genes for resistance to maintain residual effects. Ann Rev Phytopathol 26:369–378CrossRefGoogle Scholar
  85. Pessina S, Pavan S, Catalano D, Gallotta A, Visser RGF et al (2014) Characterization of the MLO gene family in Rosaceae and gene expression analysis in Malus domestica. BMC Genom 15:1–12CrossRefGoogle Scholar
  86. Pincot DDA, Poorten TJ, Hardigan MA, Harshman JM, Acharya CB, Cole GS, Gordon TR, Stueven M, Edger PP, Knapp SJ (2018) Genome-Wide Association Mapping Uncovers Fw1, a Dominant Gene Conferring Resistance to Fusarium Wilt in Strawberry, G3–Genes Genom Genet 8:1817-1828Google Scholar
  87. Poland J, Rutkoski J (2016) Advances and challenges in genomic selection for disease resistance. Annu Rev Phytopathol 54:79–98PubMedCrossRefPubMedCentralGoogle Scholar
  88. Putnam NH, O’Connell BL, Stites JC, Rice BJ, Blanchette M et al (2016) Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res 26:342–350PubMedPubMedCentralCrossRefGoogle Scholar
  89. Roach JA, Verma S, Peres NA, Jamieson AR, Weg WE et al (2016) FaRXf1: a locus conferring resistance to angular leaf spot caused by Xanthomonas fragariae in octoploid strawberry. Theor Appl Genet 129:1191–1201CrossRefPubMedGoogle Scholar
  90. Roberts PD, Berger RD, Jones JB, Chandler CK, Stall RE (1997) Disease progress, yield loss, and control of Xanthomonas fragariae on strawberry plants. Plant Dis 81:917–921CrossRefGoogle Scholar
  91. Rodrigues FA, Silva IT, Antunes Cruz MF, Carré-Missio V (2014) The infection process of Pestalotiopsis Longisetula leaf spot on strawberry leaves. J Phytopathol 162:690–692CrossRefGoogle Scholar
  92. Rose DH (1924) Leather rot of strawberries. J Agric Res 28:357–376Google Scholar
  93. 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 (Phytophthora fragariae) resistance gene Rpf1. Agron Res 4:335–339Google Scholar
  94. Sànchez S, Henríquez JL, Urcola LA, Scott A, Gambardella M (2016) Susceptibility of strawberry cultivars to root and crown rot caused by Macrophomina phaseolina. J Berry Res 6:345–354CrossRefGoogle Scholar
  95. Schafleitner S, Bonnet A, Pedeprat N, Rocca D, Chartier P et al (2013) Genetic variation of resistance of the cultivated strawberry to crown rot caused by Phytophthora cactorum. J Berry Res 3:79–91Google Scholar
  96. Shaw DV, Gubler WD, Larson KD, Hansen J (1996) Genetic variation for field resistance to Verticillium dahliae evaluated using genotypes and segregating progenies of California strawberries. J Am Soc Hort Sci 121:625–628Google Scholar
  97. Shaw DV, Hansen J, Browne GT (2006) Genotypic variation for resistance to Phytophthora cactorum in a California strawberry breeding population. J Amer Soc Hort Sci 131:687–690Google Scholar
  98. Shaw DV, Hansen J, Browne GT, Shaw SM (2008) Components of genetic variation for resistance of strawberry to Phytophthora cactorum estimated using segregating seedling populations and their parent genotypes. Plant Pathol 57:210–215CrossRefGoogle Scholar
  99. Shulaev V, Sargent DJ, Crowhurst RN, Mockler TC, Folkerts O et al (2011) The genome of woodland strawberry (Fragaria vesca). Nat Genet 43:109–116PubMedPubMedCentralCrossRefGoogle Scholar
  100. Smith BJ, Black LL (1986) First report of Colletotrichum acutatum on Strawberry in the United States. Plant Dis 70:1074CrossRefGoogle Scholar
  101. Sprague SJ, Marcroft SJ, Hayden HL, Howlett BJ (2006) Major gene resistance to Blackleg in Brassica napus overcome within three years of commercial production in Southeastern Australia. Plant Dis 90:190–198CrossRefGoogle Scholar
  102. Stensvand A, Herrero ML, Talgø V (1999) Crown rot caused by Phytophthora cactorum in Norwegian strawberry production. EPPO Bulletin 29:155–158CrossRefGoogle Scholar
  103. Tabima J, Kronmiller B, Press C, Tyler BM, Zasada I et al (2017) Whole genome sequences of the raspberry and strawberry pathogens Phytophthora rubi and P. fragariae. Mol Plant Microbe InteractGoogle Scholar
  104. Takahashi H, Yoshida Y, Kanda H, Furuya H, Matsmoto T (2003) Breeding of Fusarium wilt-resistant strawberry cultivar susceptible for field culture in Northern Japan. Acta Hortic 626:113–118CrossRefGoogle Scholar
  105. Tennessen JA, Govindarajulu R, Ashman T-L, Liston A (2014) Evolutionary origins and dynamics of octoploid strawberry subgenomes revealed by dense targeted capture linkage maps. Genome Biol Evol 6:3295–3313PubMedPubMedCentralCrossRefGoogle Scholar
  106. Toljamo A, Blande D, Kärenlampi S, Kokko H (2016) Reprogramming of Strawberry (Fragaria vesca) root transcriptome in response to Phytophthora cactorum. PLoS ONE, 1–21PubMedPubMedCentralCrossRefGoogle Scholar
  107. Tweedy B, Powell D (1958) Charcoal rot on strawberry in Illinois. Plant Dis Rep 42:107Google Scholar
  108. van de Weg E (1997a) A gene-for-gene model to explain interactions between cultivars of strawberry and races of Phytophthora fragariae var. fragariae. Theor App Genet 94:445–451CrossRefGoogle Scholar
  109. van de Weg WE (1997b) Resistance to Phytophthora fragariae var. fragariae in strawberry: the Rpf2 gene. Theor App Genet 94:1–5CrossRefGoogle Scholar
  110. van de Weg WE (1997c) Gene-for-gene relationships between strawberry and the causal agent of red stele root rot. Wageningen University, Phytophthora fragariae var fragariaeGoogle Scholar
  111. van Dijk T, Pagliarani G, Pikunova A, Noordijk Y, Yilmaz-Temel H et al (2014) Genomic rearrangements and signatures of breeding in the allo-octoploid strawberry as revealed through an allele dose based SSR linkage map. BMC Plant Biol 14:1–16CrossRefGoogle Scholar
  112. Vellicce GR, Ricci JCD, Hernández L, Castagnaro AP (2006) Enhanced resistance to Botrytis cinerea mediated by the transgenic expression of the chitinase gene ch5B in strawberry. Transgenic Res 15:57–68PubMedCrossRefPubMedCentralGoogle Scholar
  113. Verma S, Whitaker VM (2016) A new technology enabling new advances in Strawberry genetics. J Hort 3:1Google Scholar
  114. Verma S, Bassil NV, van de Weg E, Harrison RJ, Monfort A et al (2017) Development and evaluation of the Axiom® IStraw35 384HT array for the allo-octoploid cultivated strawberry Fragaria × ananassa. Acta Hortic 1156:75–82CrossRefGoogle Scholar
  115. Vining KJ, Davis TM, Jamieson AR, Mahoney LL (2015) Germplasm resources for verticillium wilt resistance breeding and genetics in strawberry (Fragaria). J Berry Res 5:183–195CrossRefGoogle Scholar
  116. Waltz E (2016a) Gene-edited CRISPR mushroom escapes US regulation. Nature 532:293PubMedCrossRefPubMedCentralGoogle Scholar
  117. Waltz E (2016b) CRISPR-edited crops free to enter market, skip regulation. Nature Biotechnol 34:582CrossRefGoogle Scholar
  118. Watanabe T, Hashimoto K, Sato M (1977) Pythium species associated with strawberry roots in japan and their role in the strawberry stunt disease. Phytopathology 67:1324–1332CrossRefGoogle Scholar
  119. Wenneker M, Bergsma-Vlami M (2015) Erwinia pyrifoliae, a new pathogen on strawberry in the Netherlands. J Berry Res 5:17–22CrossRefGoogle Scholar
  120. Whitaker VM (2011) Applications of molecular markers in strawberry. J Berry Res 1:115–127Google Scholar
  121. Winks BL, Williams YN (1965) A wilt of strawberry caused by a new form of Fusarium oxysporum. Queensland J Agricu Anim Sci 22:475–479Google Scholar
  122. Witek K, Jupe F, Witek AI, Baker D, Clark MD et al (2016) Accelerated cloning of a potato late blight–resistance gene using RenSeq and SMRT sequencing. Nature Biotechnol 34:656–660CrossRefGoogle Scholar
  123. Zhao Y, Liu Q, Davis RE (2004) Transgene expression in strawberries driven by a heterologous phloem-specific promoter. Plant Cell Rep 23:224–230PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.NIAB EMRKentUK

Personalised recommendations