Abstract
The establishment of intergeneric hybrids for horticultural and agricultural crops is still a demanding task for breeding programmes. The aim of such approaches is to introduce new quality and resistance traits and to enlarge the gene pool. Recently, an F1 hybrid between Malus × domestica and Pyrus communis became available which arose from a breeding approach undertaken in the late 1980s by the breeder Max Zwintzscher (Cologne-Vogelsang). Unlike previous reports, viable and fertile F2 plants were obtained from this F1 hybrid line by author HS, providing a unique perspective not only for genomic, transcriptomic and metabolomic studies but also for advanced breeding strategies. Here, we give the first report on the confirmation and characterization of the F1 hybrid by phenotypic, genetic and biochemical means. The intergeneric hybrid shows an intermediary phenotype of leaves, flowers and fruits, and some disorder of secondary shoot growth. Nuclear DNA content is also intermediary and corresponds to a diploid state. Apple and pear type rDNA as well as SI alleles from each genus were found. At the metabolic level, parallel biosynthesis of the apple dihydrochalcone phloridzin and of arbutin, a p-hydroquinone-glucoside typical for pear, take place leading to considerable concentrations of both in leaves. The overall data allow secure confirmation of the hybrid character and give a first insight into the hybrids genetics and physiology.
Similar content being viewed by others
Abbreviations
- h :
-
Hybrid index
- f :
-
Inbreeding coefficient
- ITS:
-
Internally transcribed spacer (of rDNA)
- PIC:
-
Polymorphism information content
- rDNA:
-
Ribosomal DNA
- SI:
-
Self-incompatibility (genes)
- SSR:
-
Simple sequence repeat (marker)
References
Baird WV, Estager AS, Wells JK (1994) Estimating nuclear DNA content in peach related diploid species using laser flow cytometry and DNA hybridization. J Am Soc Hortic Sci 119:1312–1316
Baldwin BG (1992) Phylogenetic utility of the internal transcribed spacers of nuclear ribosomal DNA in plants: an example from the compositae. Mol Phylogenet Evol 1:3–16
Biswal DK, Debnath M, Kumar S, Pramod P, Tandon P (2012) Phylogenetic reconstruction in the order Nymphaeales: ITS2 secondary structure analysis and in silico testing of maturase k (matK) as a potential marker for DNA bar coding. BMC Bioinform 13:S26
Broothaerts W (2003) New findings in apple S-genotype analysis resolve previous confusion and request the re-numbering of some S-alleles. Theor Appl Genet 106:703–714
Cornille A, Giraud T, Smulders MJM, Roldán-Ruiz I, Gladieux P (2014) The domestication and evolutionary ecology of apples. Trends Genet 30:57–65
Crane MB, Marks E (1952) Pear-apple hybrids. Nature 170:1017
De Franceschi P, Dondini L, Sanzol J (2012) Molecular bases and evolutionary dynamics of self-incompatability in the Pyrinae (Rosaceae). J Exp Bot 63:4015–4032
Dickson EE, Arumuganathan K, Kresovich S, Doyle JJ (1992) Nuclear DNA content variation within the Rosaceae. Am J Bot 79:1081–1086
Dreesen RSG, Vanholme BTM, Luyten K, Van Wynsberghe L, Fazio G, Roldán-Ruiz I, Keulemans J (2010) Analysis of Malus S-RNase gene diversity based on a comparative study of old and modern apple cultivars and European wild apple. Mol Breed 26:693–709
Espley R, Martens S (2013) Health properties of apple and pear. In: Skinner M, Hunter D (eds) Bioactives in fruit: health benefits and functional foods. Wiley, West Sussex, pp 81–100
Forte AV et al (2002) Phylogeny of the Malus (apple tree) species, inferred from the morphological traits and molecular DNA analysis. Russ J Genet 38:1357–1369
Germplasm Resources Information Network. United States Department of Agriculture. http://www.ars-grin.gov/cgi-bin/npgs/html/family.pl?2377. Assessed Apr 2013
Gessler C, Pertot I (2012) Vf scab resistance of Malus. Trees 26:95–108
Gonai T, Manabe T, Inoue E, Hayashi M, Yamamoto T, Hayashi T, Sakuma F, Kasumi M (2006) Overcoming hybrid lethality in a cross between Japanese pear and apple using gamma irradiation and confirmation of hybrid status using flow cytometry and SSR markers. Sci Hortic 109:43–47
Gorshkova LI (1980) A comparative study of fruit anatomy in apple-pear hybrids. Byul Nauch Inform Tsentr Genet Lab 34:59–62
Grisdale SK, Towers GHN (1960) Biosynthesis of arbutin from some phenylpropanoid compounds in Pyrus communis. Nature 188:1130–1131
Haberer G, Fischer TC, Torres-Ruiz RA (1996) Mapping of the nucleolus organizer region on chromosome 4 in Arabidopsis thaliana. Mol Gen Genet 250:123–128
Höfer M, Meister A (2010) Genome size variation in Malus species. J Bot. doi:10.1155/2010/480873
Hofsommer H-J (1999) New Analytical Techniques for Judging the Authenticity of Fruit Juices. Fruit Process 12:471–479
Inoue E, Sakuma F, Kasumi M, Hara H, Tsukihashi T (2003) Effect of high-temperature on suppression of the lethality exhibited in the intergeneric hybrid between Japanese pear (Pyrus pyrifolia Nakai) and apple (Malus × domestica Borkh.). Sci Hortic 98:385–396
Ishimizu T, Inoue K, Shimonaka M, Saito T, Terai O, Norioka S (1999) PCR-based method for identifying the S-genotypes of Japanese pear culitvars. Theor Appl Genet 98:961–967
Johnston JS, Bennett MD, Rayburn AL, Galbraith DW, Price HJ (1999) Reference standards for determination of DNA content of plant nuclei. Am J Bot 86:609–613
Krüssmann G (1977) Handbuch der Laubgehölze. Paul Parey, Berlin
Li M, Zhu K, Bai S, Liu Z, Li T (2011) Isolation and S-genotyping application of S-allelic polymorphic MdSLFBs in apple (Malus domestica Borkh.). Mol Breed 28:171–180
Li T, Long S, Li M, Bai S, Zhang W (2012) Determination of S-genotypes and identification of five novel S-RNase alleles in wild Malus species. Plant Mol Biol Rep 30:453–461
Liebhard R, Gianfranceschi L, Koller B, Ryder CD, Tarchini R, Van de Weg E, Gessler C (2002) Development and characterisation of 140 new microsatellites in apple (Malus × domestica Borkh.). Mol Breed 10:217–241
Liu K, Muse SV (2005) PowerMarker: integrated analysis environment for genetic marker data. Bioinformatics 21:2128–2129
Malnoy M, Xu M, Borejsza-Wysocka E, Korban SS, Aldwinckle HS (2008) Two receptor-like genes, Vfa1 and Vfa2, confer resistance to the fungal pathogen Venturia inaequalis inciting apple scab disease. Mol Plant Microbe Interact 21:448–458
Meirmans PG, Van Tienderen PH (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Mol Ecol Notes 4:792–794
Nikiforova SV, Cavalieri D, Velasco R, Goremyki V (2013) Phylogenetic analysis of 47 chloroplast genomes clarifies the contribution of wild species to the domesticated apple maternal line. Mol Biol Evol 30:1751–1760
Paetkau D, Slade R, Burden M, Estoup A (2004) Genetic assignment methods for the direct, real-time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol Ecol 13:55–65
Peakall R, Smouse PE (2012) GenAlex 6.5: genetic analysis in Excel. Population genetic software for teaching and research-an update. Bioinformatics 28:2537–2539
Pierantoni L, Cho K-H, Shin I-S, Chiodini R, Tartarini S, Dondini L, Kang S-J, Sansavini S (2004) Characterisation and transferability of apple SSRs to two European pear F1 populations. Theor Appl Gen 109:1519–1524
R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Wirtschaftsuniversität Wien, Institute for Statistics and Mathematics. http://www.R-project.org/
Rayburn AL, Auger JA, McMurphy LM (1992) Estimating percentage constitutive heterochromatin by flow cytometry. Exp Cell Res 198:175–178
Robinson JP et al (2001) Taxonomy of the genus Malus Mill. (Rosaceae) with emphasis on the cultivated apple, Malus domestica Borkh. Plant Syst Evol 226:35–58
Rudenko IS, Rotaru GI (1970) (only abstract available to us) Morphological and anatomical characteristics of an intergeneric apple × pear hybrid. Strukturi Osobennosti Sochn i Myasnsi Plodov 1970:40–51
Rudenko IS, Rotaru G I (1989) (not available to us) Morphoanatomical features of seeds of apple, pear and quince hybrid forms. Izv. Akad. Nauk Moldav. SSR, Ser. Biol. Khim. Nauk 5:15–20 (in Russian)
Schieber A, Keller P, Carle R (2001) Determination of phenolic acids and flavonoids of apple and pear by high-performance liquid chromatography. J Chromatogr A 910:265–273
Silfverberg-Dilworth E, Matasci CL, Van de Weg WE, Van Kaauwen MPW, Walser M, Kodde LP, Soglio V, Gianfranceschi L, Durel CE, Costa F, Yamamoto T, Koller B, Gessler C, Patocchi A (2006) Microsatellite markers spanning the apple (Malus × domestica Borkh.) genome. Tree Genet Genomes 2:202–224
Takasaki T, Moriya Y, Okada K, Yamamoto K, Iwanami H, Bessho H, Nakanishi T (2006) cDNA cloning of nine S alleles and establishment of a PCR-RFLP system for genotyping European pear cultivars. Theor Appl Genet 112:1543–1552
Tatum T, Stepanovic S, Biradar DP, Lane Rayburn A, Korban S (2005) Variation in nuclear DNA content in Malus species and cultivated apples. Genome 48:924–930
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar SK, Troggio M, Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, Komjanc M, Longhi S, Magnago P, Malacarne G, Malnoy M et al (2010) The genome of the domesticated apple (Malus × domestica Borkh.). Nat Genet 42:833–839
Vrhovsek U, Masuero D, Gasperotti M, Franceschi P, Caputi L, Viola R, Mattivi F (2012) A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages. J Agric Food Chem 60:8831–8840
Williams AH (1955) Phenolic substances of pear-apple hybrids. Nature 175:213
Wright S (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution 19:395–420
Wu J, Wang Z, Shi Z, Zhang S, Ming R, Zhu S, Khan MA, Tao S, Korban SS, Wang H, Chen NJ, Nishio T, Xu X, Cong L, Qi K, Huang X, Wang Y, Zhao X, Wu J, Deng C, Gou C, Zhou W, Yin H, Qin G, Sha Y, Tao Y, Chen H, Yang Y, Song Y, Zhan D, Wang J, Li L, Dai M, Gu C, Wang Y, Shi D, Wang X, Zhang H, Zeng L, Zheng D, Wang C, Chen M, Wang G, Xie L, Sovero V, Sha S, Huang W, Zhang S, Zhang M, Sun J, Xu L, Li Y, Liu X, Li Q, Shen J, Wang J, Paull RE, Bennetzen JL, Wang J, Zhang S (2013) The genome of pear (Pyrus bretschneideri Rehd.). Genome Res 23:396–408
Yamamoto T, Kimura T, Sawamura Y, Kotobuki K, Ban Y, Hayashi T, Matsuta N (2001) SSRs isolated from apple can identify polymorphism and genetic diversity in pear. Theor Appl Genet 102:865–870
Yamamoto T, Kimura T, Shoda M, Imai T, Saito T, Sawamura Y, Kotobuki K, Hayashi T, Matsuta N (2002) Genetic linkage maps constructed by using an interspecific cross between Japanese and European pears. Theor Appl Genet 106:9–18
Yamamoto T, Kimura T, Terakami S, Nishitani C, Sawamura Y, Saito T, Kotobuki K, Hayashi T (2007) Integrated reference genetic linkage maps of pear based on SSR and AFLP markers. Breed Sci 57:321–329
Acknowledgments
This work is based on the hybrid produced by the breeder Max Zwintzscher (now deceased) from the former Institut für gärtnerische Pflanzenzüchtung in Köln-Vogelsang (Germany) whose fundamental contribution is gratefully acknowledged. Breeder Hanna Schmidt (Ahrensburg) later took care of the material and hence helped to preserve it. The authors also gratefully acknowledge the contribution of Domenico Masuero (FEM IASMA, Italy) assistance for performing UPLC-MS and Raksha Ravi for performing work on the rDNA analysis. Chris Carrie (LMU) is acknowledged for proof reading the manuscript as a native speaker. This research was supported by the ADP 2011-13 project funded by the Autonomous Province of Trento.
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Fischer, T.C., Malnoy, M., Hofmann, T. et al. F1 hybrid of cultivated apple (Malus × domestica) and European pear (Pyrus communis) with fertile F2 offspring. Mol Breeding 34, 817–828 (2014). https://doi.org/10.1007/s11032-014-0077-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11032-014-0077-4