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A Unique haplotype found in apple accessions exhibiting early bud-break could serve as a marker for breeding apples with low chilling requirements

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Abstract

Most commercial apple cultivars have high to medium chilling requirements and consequently are not grown in regions with warm winters. Furthermore, global climate changes raise the concern that some regions where apples are currently being produced will become unsuitable in the future. Therefore, mapping and understanding the factors governing chilling requirements are important goals towards the breeding of new apple varieties. In this study, we characterized 73 apple accessions: old local accessions, modern cultivars, and selected hybrids, all grown in the Newe Ya’ar germplasm collection in Israel under moderate winter conditions. We measured the time of vegetative bud-break as an indicator of chilling requirements and genotyped the accessions for known genetic markers and for markers we developed by re-sequencing the genome of ‘Anna’, a cultivar with very low chilling requirements. Our results show that while most of the accessions that were characterized as having early bud-break are genetically different from each other, they all share a unique haplotype in a region of ∼190 kb, within a previously identified QTL for bud-break time, on chromosome 9. The alleles in the early bud-break-associated haplotype were not found in any of the late accessions tested, suggesting that the causative difference leading to the variation in bud-break time lays within or near this region, and that there is a common ancestor carrying early bud-break trait of the early accessions tested. Moreover, the markers of the unique haplotype can serve as genetic markers to accelerate the breeding of apple cultivars better adapted to warm climates.

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References

  • Abbott AG, Zhebentyayeva T, Barakat A, Liu Z (2015) Chapter six—the genetic control of bud-break in trees. In: Christophe P, Anne-Françoise A-B (eds) Advances in Botanical Research, Volume 74. Academic Press, pp 201–228. doi:10.1016/bs.abr.2015.04.002

  • Allard A et al (2016) Detecting QTLs and putative candidate genes involved in budbreak and flowering time in an apple multiparental population. J Exp Bot 67:2875–2888. doi:10.1093/jxb/erw130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520. doi:10.1104/pp.110.161653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Atkinson CJ, Brennan RM, Jones HG (2013) Declining chilling and its impact on temperate perennial crops. Environ Exp Bot 91:48–62. doi:10.1016/j.envexpbot.2013.02.004

    Article  Google Scholar 

  • Belon P (2012) Travels in the Levant: the observations of Pierre Belon of Le Mans on many singularities and memorable things found in Greece, Turkey. Judaea, Hardinge Simpole Limited

    Google Scholar 

  • Bianco L et al (2014) Development and validation of a 20K single nucleotide polymorphism (SNP) whole genome genotyping array for apple (Malus × domestica Borkh). PLoS One 9:e110377. doi:10.1371/journal.pone.0110377

    Article  PubMed  PubMed Central  Google Scholar 

  • Bielenberg D et al (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507. doi:10.1007/s11295-007-0126-9

    Article  Google Scholar 

  • Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL (1994) High resolution of human evolutionary trees with polymorphic microsatellites. Nature 368:455–457

    Article  CAS  PubMed  Google Scholar 

  • Brooks RM, Olmo HP (1972) Register of new fruit and nut varieties: second edition, 2 edn. Univ of California Press, Berkeley

    Google Scholar 

  • Campoy JA, Ruiz D, Egea J (2011) Dormancy in temperate fruit trees in a global warming context: a review. Sci Hortic-Amsterdam 130:357–372. doi:10.1016/j.scienta.2011.07.011

    Article  Google Scholar 

  • Celton JM, Martinez S, Jammes MJ, Bechti A, Salvi S, Legave JM, Costes E (2011) Deciphering the genetic determinism of bud phenology in apple progenies: a new insight into chilling and heat requirement effects on flowering dates and positional candidate genes. New Phytol 192:378–392. doi:10.1111/j.1469-8137.2011.03823.x

    Article  PubMed  Google Scholar 

  • Chen M et al (2016) Genome-wide identification of WRKY family genes in peach and analysis of WRKY expression during bud dormancy. Mol Gen Genomics 292:1319–1332. doi:10.1007/s00438-016-1171-6

    Article  Google Scholar 

  • DePristo MA et al (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nature Genet 43:491–498 http://www.nature.com/ng/journal/v43/n5/abs/ng.806.html#supplementary-information

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791. doi:10.2307/2408678

    Article  Google Scholar 

  • Felsenstein J (1993) PHYLIP: phylogenetic inference package, version 3.5 c. Department of Genetics, University of Washington, Seattle

    Google Scholar 

  • Goor A, Spiegel P, Barak D (1962) The apple (in Hebrew). Government of Israel, Ministry of Agriculture, Publication devision, Tel Aviv

    Google Scholar 

  • Grasovsky A, Weitz J (1933) Apple growing in Palestine, Agriculteral leaflets, vol 30. Department of Agriculture and Forests, Palestine

    Google Scholar 

  • Gur-Arieh J (1995) Abba Shel Anna. The work of Abba Stein in breeding of deciduous fruit varieties in Israel (in Hebrew). Fruit Board of Israel, Tel Aviv

    Google Scholar 

  • Hauagge R, Cummins JN (1991) Genetics of length of dormancy period in Malus vegetative buds. J Am Soc Hortic Sci 116:121–126

    Google Scholar 

  • Hauagge R, Cummins JN (2000) Pome fruit genetic pool for production in warm climates. In: Erez A (ed) Temperate Fruit Crops in Warm Climates. Springer, pp 267–303

  • Heide OM, Prestrud AK (2005) Low temperature, but not photoperiod, controls growth cessation and dormancy induction and release in apple and pear. Tree Physiol 25:109–114. doi:10.1093/treephys/25.1.109

    Article  CAS  PubMed  Google Scholar 

  • Holland D, Bar-Ya’akov I, Hatib K (2015) Apple genetic resources in Israel. J Am Pomol Soc 69:186–200

    Google Scholar 

  • Jerzmanowski A (2007) SWI/SNF chromatin remodeling and linker histones in plants. Biochem Biophys Acta 1769:330–345. doi:10.1016/j.bbaexp.2006.12.003

    CAS  PubMed  Google Scholar 

  • Kitamura Y, Takeuchi T, Yamane H, Tao R (2016) Simultaneous down-regulation of DORMANCY-ASSOCIATED MADS-box6 and SOC1 during dormancy release in Japanese apricot (Prunus mume) flower buds. J Hortic Sci Biotechnol 91:476–482. doi:10.1080/14620316.2016.1173524

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359. doi:10.1038/nmeth.1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lassois L et al (2016) Genetic diversity, population structure, parentage analysis, and construction of core collections in the French apple germplasm based on SSR markers. Plant Mol Biol Rep 34:827–844. doi:10.1007/s11105-015-0966-7

    Article  CAS  Google Scholar 

  • Legave J-M, Guédon Y, Malagi G, El Yaacoubi A, Bonhomme M (2015) Differentiated responses of apple tree floral phenology to global aarming in contrasting climatic regions. Front Plant Sci 6:1054. doi:10.3389/fpls.2015.01054

    Article  PubMed  PubMed Central  Google Scholar 

  • Matityahu A, Stern RA, Schneider D, Goldway M (2005) Molecular identification of a new apple S-RNase—S29—cloned from ‘Anna’, a low-chilling-requirement cultivar. Hortscience 40:850–851

    CAS  Google Scholar 

  • Micheletti D, Troggio M, Zharkikh A, Costa F, Malnoy M, Velasco R, Salvi S (2011) Genetic diversity of the genus Malus and implications for linkage mapping with SNPs. Tree Genet Genomes 7:857–868. doi:10.1007/s11295-011-0380-8

    Article  Google Scholar 

  • Miller E Sherman W (1980) Origin and description of ‘Dorsett Golden’ apple. In: Proc Fl St Hortic Soc. pp 108–109

  • Minch E, Ruiz-Linares A, Goldstein D, Feldman M, Cavalli-Sforza L (1997) MICROSAT: a computer program for calculating various statistics on microsatellite allele data. Stanford University, Palo Alto

    Google Scholar 

  • Oppenheimer C, Slor E (1968) Breeding of apples for a subtropical climate. Theor Appl Genet 38:97–102. doi:10.1007/bf00934198

    Article  CAS  PubMed  Google Scholar 

  • Pommer CV, Barbosa W (2009) The impact of breeding on fruit production in warm climates of Brazil. Rev Bras Frutic 31:612–634

    Article  Google Scholar 

  • Porebski S, Bailey LG, Baum BR (1997) Modification of a CTAB DNA extraction protocol for plants containing high polysaccharide and polyphenol components. Plant Mol Biol Rep 15:8–15. doi:10.1007/bf02772108

    Article  CAS  Google Scholar 

  • Porto DD et al (2015) Transcription profiling of the chilling requirement for bud break in apples: a putative role for FLC-like genes. J Exp Bot 66:2659–2672. doi:10.1093/jxb/erv061

    Article  CAS  PubMed  Google Scholar 

  • Ríos G, Leida C, Conejero A, Badenes ML (2014) Epigenetic regulation of bud dormancy events in perennial plants. Front Plant Sci 5:247. doi:10.3389/fpls.2014.00247

    PubMed  PubMed Central  Google Scholar 

  • Rumayor F, Martinez C, Vazquez R (2001) Breeding apples for the warm climates of Northeastern Mexico. Acta Hortic 565:63–68. doi:10.17660/ActaHortic.2001.565.9

    Article  Google Scholar 

  • Sherman W, Lyrene P (2003) Low chill breeding of deciduous fruits at the University of Florida. In: XXVI IHC- Genetics and Breeding of Tree Fruits and Nuts. Ed. J. Janick. Acta Hortic 622:599–605

  • Stino G (1995) Aspects related to temperate zone fruit production in Egypt. Acta Hortic 409:203–206

    Article  Google Scholar 

  • Thiel T, Michalek W, Varshney R, Graner A (2003) Exploiting EST databases for the development and characterization of gene-derived SSR-markers in barley (Hordeum vulgare L.). Theor Appl Genetics 106:411–422. doi:10.1007/s00122-002-1031-0

    Article  CAS  Google Scholar 

  • Thomson WM (1880) The land and the book: or biblical illustrations drawn from the manners and customs, the scenes and scenery of the Holy Land. Harper & brothers, New York

    Google Scholar 

  • Trainin T, Bar-Ya’akov I, Holland D (2013) ParSOC1, a MADS-box gene closely related to Arabidopsis AGL20/SOC1, is expressed in apricot leaves in a diurnal manner and is linked with chilling requirements for dormancy break. Tree Genet Genomes 9:753–766. doi:10.1007/s11295-012-0590-8

    Article  Google Scholar 

  • Trainin T, Bar-Ya’akov I, Holland D (2015) The genetic components involved in sensing chilling requirements in apricot. In: Anderson JV(ed) Advances in plant dormancy. Springer, pp 159–168

  • van Dyk MM, Soeker MK, Labuschagne IF, Rees DJG (2010) Identification of a major QTL for time of initial vegetative budbreak in apple (Malus x domestica Borkh.). Tree Genet Genomes 6:489–502. doi:10.1007/s11295-009-0266-1

    Article  Google Scholar 

  • Velasco R et al (2010) The genome of the domesticated apple (Malus x domestica Borkh.). Nature Genet 42:833–839

    Article  CAS  PubMed  Google Scholar 

  • Voogd C, Wang T, Varkonyi-Gasic E (2015) Functional and expression analyses of kiwifruit SOC1-like genes suggest that they may not have a role in the transition to flowering but may affect the duration of dormancy. J Exp Bot 66:4699–4710. doi:10.1093/jxb/erv234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wisniewski M, Artlip T, Norelli J (2015) Overexpression of a peach CBF gene in apple: a model for understanding the integration of growth, dormancy, and cold hardiness in woody plants. Front Plant Sci 6:85. doi:10.3389/fpls.2015.00085

    Article  PubMed  PubMed Central  Google Scholar 

  • Yordanov YS, Ma C, Strauss SH, Busov VB (2014) EARLY BUD-BREAK 1 (EBB1) is a regulator of release from seasonal dormancy in poplar trees. Proc Natl Acad Sci U S A 111:10001–10006. doi:10.1073/pnas.1405621111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang S et al (2014) Genomic variants of genes associated with three horticultural traits in apple revealed by genome re-sequencing. Horticulture Research 1:14045. doi:10.1038/hortres.2014.45

    Article  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We would like to thank Charles-Eric Durel and Caroline Denance for their help with genotypic characterization with the universal SSR markers, and Allesandro Cestaro for providing a list of heterozygous positions in the Golden Delicious genome v3.0. This work was funded by grant number 203-0947-12 from the Chief Scientist of the Ministry of Agriculture and Rural Development of Israel.

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Authors and Affiliations

  1. Department of Fruit Tree Sciences, Agricultural Research Organization, Newe Ya’ar Research Center, P.O. Box 1021, 30095, Ramat Yishay, Israel

    Taly Trainin, Matat Zohar, Einav Shimoni-Shor, Irit Bar-Ya’akov, Kamel Hatib, Doron Holland & Tal Isaacson

  2. Institute of Plant Sciences, Agricultural Research Organization, HaMaccabim Road 68, P.O.B 15159, 7528809, Rishon LeZion, Israel

    Adi Doron-Faigenboim & Noa Sela

  3. Department of Plant Pathology and Weed Research, Institute of Plant Protection, Agricultural Research Organization, HaMaccabim Road 68, P.O.B 15159, 7528809, Rishon LeZion, Israel

    Noa Sela

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  1. Taly Trainin
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Correspondence to Tal Isaacson.

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Trainin, T., Zohar, M., Shimoni-Shor, E. et al. A Unique haplotype found in apple accessions exhibiting early bud-break could serve as a marker for breeding apples with low chilling requirements. Mol Breeding 36, 158 (2016). https://doi.org/10.1007/s11032-016-0575-7

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