Abstract
The two main objectives of this research were to identify new S-RNase alleles in Iranian almond cultivars and to characterize naturally occurring mutations in these alleles that may cause self-compatibility. We investigated S genotypes of 22 Iranian almond cultivars using stylar RNase electrophoresis, PCR and DNA sequencing. We report six previously unidentified P. dulcis S-RNase alleles (S 45 , S 46 , S 47 , S 48 , S 49 and S 50 ). Four of 12 tested S-RNases were found to be non-functional in vitro: S 49 , S 50 , S 24 /S na and S 25 /S 47 . Detected point mutations in the C3 coding region of S 49 - and S 50 -RNase, leading to the replacement of a highly conserved cysteine and histidine residues, are with the highest probability the reason of these S-RNases inactivity. Results also suggested that ten Iranian almond cultivars display unique S genotype. All presented data confirm Iranian cultivars as valuable almond sources which are of interest to almond breeding and conservation programs.
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Abbreviations
- CIG:
-
Cross incompatibility group
- IP:
-
Isoelectric point
- SI:
-
Self-incompatibility
- SC:
-
Self-compatibility
- SP:
-
Signal peptide
References
Alonso JM, Socías i Company R (2005a) Identification of the S 3 self-incompatibility allele in almond by specific primers. Span J Agric Res 3(3):286–303
Alonso JM, Socías i Company R (2005b) Physiological and genetic determination of self-compatibility in an almond breeding progeny. In: Oliveira MM, Cordeiro V (eds) XIII GREMPA Meeting on almonds and pistachios. CIHEAM-IAMZ, Zaragoza, pp 101–105
Ayfer M (1975) Varietal selection of almond for central and southern Anatolia, 2nd Colloque. GREMPA, CIHEAM, Montpellier
Babadaii R (2007) The study of mechanism and amount of self-incompatibility and determination of best pollinizer for Mamaei almond, Ph.D. diss. The Islamic Azad University, Tehran
Banović B, Šurbanovski N, Konstantinović M, Maksimović V (2009) Basic RNases of wild almond (Prunus webbii): cloning and characterization of six new S-RNase and one “non-S RNase” genes. J Plant Physiol 166(4):395–402
Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90(2):245–250
Bošković R, Tobutt KR, Batlle I, Duval H (1997) Correlation of ribonuclease stylar RNase electrophoresis and incompatibility genotypes in almond. Euphytica 97(2):167–176
Bošković R, Tobutt KR, Duval H, Rovira M, Romero M, Batlle I, Dicenta F (1998) Inheritance of stylar ribonucleases in two almond progenies and their correlation with self-compatibility. Acta Hortic 470:118–122
Bošković R, Tobutt KR, Duval H, Batlle I, Dicenta F, Vargas FJ (1999) A stylar ribonuclease assay to detect self-incompatible seedling in almond progenies. Theor Appl Genet 99(5):800–810
Bošković R, Tobutt KR, Batlle I, Duval H, Martinez-Gomez P, Gradziel TM (2003) Stylar ribonucleases in almond: correlation with and prediction of incompatibility genotypes. Plant Breed 122(1):70–76
Bošković RI, Tobutt KR, Ortega E, Sutherland BG, Godini A (2007) Self-(in)compatibility of the almonds P. dulcis and P. webbii: detection and cloning of wild-type S (f) and new self-compatibility alleles encoding inactive S-RNases. Mol Genet Genomics 278(6):665–676
Certal AC, Almeida RB, Bošković R, Oliveira MM, Feijό JA (2002) Structural and molecular analysis of self-incompatibility in almond (Prunus dulcis). Sex Plant Reprod 15(1):13–20
Channuntapipat C, Sedgley M, Collins G (2001) Sequences of the cDNAs and genomic DNAs encoding the S 1 , S 7 , S 8 , and S f alleles from almond (Prunus dulcis). Theor Appl Genet 103(6–7):1115–1122
Channuntapipat C, Wirthensohn M, Ramesh SA, Batlle I, Arús P, Sedgley M, Collins G (2003) Identification of incompatibility genotypes in almond (Prunus dulcis Mill.) using specific primers based on the introns the S-alleles. Plant Breed 122(2):164–168
Crossa-Raynaud P, Grassely C (1985) Existence de groups d’interstérilité chez l`amandier. Options Méditerr 85:43–45
De Giorgio D, Polignano GB (2001) Evaluating the biodiversity of almond cultivars from a germplasm collection field in Southern Italy. In: Stott DE, Mohtar RH, Steinhardt GC (eds) Sustaining the global farm. Purdue University, West Lafayette, pp 305–311
Delplancke M, Alvarez N, Espíndola A, Joly H, Benoit L, Brouck E, Arrigo N (2012) Gene flow among wild and domesticated almond species: insights from chloroplast and nuclear markers. Evol Appl 5(4):317–329
Dicenta F, Gracia JE (1993) Inheritance of self-incompatibility in almond. Heredity 70(3):313–317
Dukuzoguz M (1975) A summary of almond selections studies in western Turkey, 2nd Colloque. GREMPA, CIHEAM, Montpellier
Duval A, Boutard A, Faurobert M (2001) Analysis of stylar ribonucleases (S-RNases) in an almond progeny of ‘Ferralise’ x ‘Tuono’. Options Méditerr 56:91–94
Felipe AJ, Socías i Company R (1987) ‘Aylés’, ‘Guara’ and ‘Moncayo’ almonds. Hort Sci 22(5):961–962
Fernández i Martí A (2010) La autocompatibilidad en el almendro (Prunus amygdalus Batsch): estructura genética del alelo S f y modificaciones de su expresión, Ph.D. diss. University Lleida, Spain
Fernández i Martí A, Hanada T, Alonso JM, Yamane H, Tao R, Socías i Company R (2009a) A modifier locus affecting the expression of the S-RNase gene could be the cause of breakdown of self-incompatibility in almond. Sex Plant Reprod 22(3):179–186
Fernández i Martí A, Alonso JM, Espiau MT, Rubio-Cabetas MJ, Socías i Company R (2009b) Genetic diversity in Spanish and foreign almond germplasm assessed by molecular characterization with simple sequence repeats. J Am Soc Hortic Sci 134(5):535–542
Gradziel TM (1997) Almond. In: Brooks RM, Olmo HP (eds) The brooks and Olmo register of fruit and nut varieties, 3rd edn. ASHS Press, Alexandria, pp 1–12
Green PJ (1994) The ribonucleases of higher plants. Annu Rev Plant Phys 45(1):421–445
Grigorian V (1976) Descriptión de la situation de l’ amandier en Iran. Options Méditerr 60:77–79
Halász J, Fodor A, Pedryc A, Hegedús A (2010) S-genotyping of Eastern European almond cultivars: identification and characterization of new (S36–S39) self-incompatibility ribonuclease alleles. Plant Breed 129(2):227–232
Hanada T, Kibe T, Watari A, Yamane H, Yaegaki H, Yamaguchi M, Sasabe Y, Dandekar A, Gradziel T, Tao R (2010) Self-compatible S-haplotypes in Peach and Peach-related species. Functional genomics of horticultural crops symposium, Lisbon, pp 318
Hauck N, Ikeda K, Tao R, Iezzoni AF (2006a) The mutated S 1 -haplotype in Sour Cherry has an altered S-haplotype–specific F-box protein gene. J Hered 97(5):514–520
Hauck NR, Yamane H, Tao R, Iezzoni AF (2006b) Accumulation of nonfunctional S- haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172(2):1191–1198
Imani A, Talaei AR (2006) Stigmatoidy in almond. Acta Hort 726:85–88
Kester DE, Gradziel TM (1996) Almonds (Prunus). In: Moore JN, Janick J (eds) Fruit breeding. Wiley, New York, pp 1–97
Kester DE, Gradzeil TM, Grasselly C (1991) Almond in genetic resources of temperate fruit and crops. Acta Hort 209:701–758
Kester DE, Gradziel TM, Micke WC (1994) Identifying pollen incompatibility groups in California almond cultivars. J Am Soc Hortic Sci 119(1):106–109
Kodad O, Socías i Company R (2009) Review and update of self-incompatibility alleles in almond. XΙΙth Eucarpia symp on fruit breeding and genetics, pp 421–424
Kodad O, Alonso JM, Sánchez A, Oliveira M, Socías i Company R (2008) Evaluation of genetic diversity of S-alleles in an almond germplasm collection. J Hortic Sci Biotech 83(5):603–608
Kodad O, Socías i Company R, Sánchez A, Oliveira MM (2009) The expression of self-compatibility in almond may not only be due to the presence of the S f allele. J Am Soc Hortic Sci 134(2):221–227
Kodad O, Sánchez A, Saibo N, Oliveira MM, Socías i Company R (2010a) Molecular characterization of five new S alleles associated with self-incompatibility in local Spanish almond cultivars. Options Méditerr 94:105–109
Kodad O, Alonso JM, Fernández i Martí A, Oliveira MM, Socías R (2010b) Molecular and physiological identification of new S-alleles associated with self-(in) compatibility in local Spanish almond cultivars. Sci Hortic 123(3):308–311
Ledbetter CA (2009) Using central asian germplasm to improve fruit quality and enhance diversity in California adapted apricots. Acta Hort 814:77–80
López M, Mnejja M, Rovira M, Collins G, Vargas FJ, Arus P (2004) Self-incompatibility genotypes in almond re-evaluated by PCR, stylar ribonucleases, sequencing analysis and controlled pollinations. Theor Appl Genet 109(5):954–964
López M, Vargas FJ, Batlle I (2006) Self-(in) compatibility almond genotypes: a review. Euphytica 150(1–2):1–16
Ma RC, Oliverira MM (2001) Molecular cloning of the self-incompatibility genes S1 and S3 from almond (Prunus dulcis cv. Ferragnés). Sex Plant Reprod 14(3):163–167
Marchese A, Bošković RI, Martínez-García PJ, Tobutt KR (2008) The origin of the self-compatible almond ‘Supernova’. Plant Breed 127(1):105–107
Martínez-García P, Mañas F, López P, Dicenta F, Ortega E (2011) Molecular and phenotypic characterization of the S-locus and determination of flowering time in new `Marcona’ and `Desmayo Largueta’-type almond (Prunus dulcis) selections. Euphytica 177(1):67–78
Martínez-Gómez P, Ortega E, Sánchez-Pérez R, Dicenta F, Dandekar AM, Alonso JM, Socías i Company R, López M, Batlle I, Gradziel TM (2003) Identification of self-incompatibility alleles in almond and related Prunus species using PCR. Acta Hort 622:397–401
McClure B, Mou B, Canevacini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci USA 96(23):13548–13553
Momenpour A, Ebadi A, Imani A (2011) Discrimination of almond self compatible genotypes by different methods in a breeding program in Iran. Afr J Agric Res 6(23):5251–5260
Mousavi A, Fatahi R, Zamani Z, Imani A, Dicenta F, Ortega E (2011) Identification of self-incompatibility genotypes in Iranian almond cultivars. Acta Hort 912:303–311
Murray HC, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8(19):4321–4325
Nikoumanesh K, Ebadi A, Zeinalabedini M, Gogorcena Y (2011) Morphological and molecular variability in some Iranian almond genotypes and related Prunus species and their potentials for rootstock breeding. Sci Hort 129(1):108–118
Ortega E, Sutherland BG, Dicenta F, Bošković R, Tobutt KR (2005) Determination of incompatibility genotypes in almond using first and second intron consensus primers: detection of new S alleles and correction of reported S genotypes. Plant Breed 124(2):188–196
Ortega E, Boskovic R, Sargent DJ, Tobutt KR (2006) Analysis of S-RNase alleles of almond (Prunus dulcis): characterization of new sequences, resolution of synonyms and evidence of intragenic recombination. Mol Genet Genomics 276(5):413–426
Ortega E, Mousavi DJ, Dicenta F (2009) Cloning and characterization of nine new S-RNases from Iranian almond cultivars. Acta Hort 912:593–599
Parry S, Newbigin E, Craik D, Nakamura KT, Bacic A, Oxley D (1998) Structural analysis and molecular model of a self-incompatibility RNase from wild Tomato. Plant Physiol 116(2):463–469
Rahemi A, Fatahi R, Ebadi A, Taghavi T, Hassani D, Gradziel T, Chaparro J (2010) Genetic variation of S-alleles in wild almonds and their related Prunus species. Aust J Crop Sci 4(8):648–659
Rahemi A, Fatahi R, Ebadi A, Taghavi T, Hassani D, Gradziel T, Folta K, Chaparro J (2012) Genetic diversity of some wild almonds and related Prunus species revealed by SSR and EST-SSR molecular markers. Plant Sys Evol 298:173–192
Sánchez-Pérez R, Dicenta F, Martínez-Gómez P (2004) Identification of S-alleles in almond using multiplex PCR. Euphytica 138(3):263–269
Shiran B, Amirbakhtiar N, Kiani S, Mohammadi Sh, Sayed-Tabatabaei BE, Moradi H (2007) Molecular characterization and genetic relationship among almond cultivars assessed by RAPD and SSR markers. Sci Hort 111(3):280–292
Socías i Company R, Alonso JM (2004) Cross-incompatibility of “Ferragness”and “Ferralise” and pollination efficiency for self-compatibility transmission in almond. Euphytica 135(3):333–338
Socías i Company R, Alonso JM, Espiau MT, Fernández i Martí A, Kodad O, Avanzato D, Bacchetta L, Botta R, Drogoudi P, Duval H, Metzidakis I, Rovira M, Silva AP, Solar A, Spera D (2011) The definition of the European almond core collection. Acta Hort 912:445–448
Socías i Company R, Alonso JM, Kodad O and Gradziel TM (2012) Fruit breeding. In: Badenes ML, Byrne DH (eds) Handbook of plant breeding, vol 8, 4th edn. springer, Berlin, pp 697–728
Socías i Company R, Fernández i Martí A, Kodad O, Alonso JM (2012) Self compatibility in Prunus species: Diversity of mutations. 19th Eucarpia General Congress, Budapest, Hungary, pp 196–199
Sonneveld T, Tobutt KR, Robbins TP (2003) Allele-specific PCR detection of sweet cherry self-incompatibility (S) alleles S1 to S16 using consensus and allele-specific primers. Theor Appl Genet 107(6):1059–1070
Sonneveld T, Tobutt KR, Vaughan SP, Robbins TP (2005) Loss of pollen-S function in two self-compatible selections of Prunus avium is associated with deletion/mutation of an S haplotype-specific F-box gene. Plant Cell 17(1):37–51
Sorkheh K, Shiran B, Gradziel TM, Epperson BK, Martínez-Gómez P, Asadi E (2007) Amplified fragment length polymorphism as a tool for molecular characterization of almond germplasm: genetic diversity among cultivated genotypes and related wild species of almond, and its relationships with agronomic traits. Euphytica 156(3):327–344
Sorkheh K, Shiran B, Kiani S, Amirbakhtiar N, Mousavi S, Rouhi V, Mohammady-D S, Gradziel TM, Malysheva-Otho LV, Martinez-Gomez P (2009) Discriminating ability of molecular markers and morphological characterization in the establishment of genetic relationships in cultivated genotypes of almond and related wild species. J Forest Res 20(3):183–194
Surbanovski N, Tobutt KR, Konstantinović M, Maksimović V, Sargent DJ, Stevanović V, Bošković RI (2007) Self-incompatibility of Prunus tenella and evidence that reproductively isolated species of Prunus have different SFB alleles coupled with an identical S-RNase allele. Plant J 50(4):723–734
Sutherland BG, Robbins TP, Tobutt KR (2004) Primers amplifying a range of Prunus S-alleles. Plant Breed 123(6):582–584
Sutherland BG, Tobutt KR, Robbins TP (2008) Trans-specific S-RNase and SFB alleles in Prunus self-incompatibility haplotypes. Mol Genet Genomics 279(1):95–106
Talaei A, Imani A (1995) Selection of the best pollinizer for late flowering almond varieties. Hort Sci 30(4):70–77
Tamura M, Ushijima K, Sassa H, Hirano H, Tao R, Gradziel TM, Dandekar AM (2000) Identification of self-incompatibility genotypes of almond by allele-specific PCR analysis. Theor Appl Genet 101(3):344–349
Tao R, Watari A, Hanada T, Habu T, Yaegaki H, Yamaguchi M, Yamane H (2007) Self compatible peach (Prunus persica) has mutant versions of the S haplotypes found in self-incompatible Prunus species. Plant Mol Biol 63(1):109–123
Tao R, Fernández À, Akagi T, Hanada T, Alonso J, Socías i Company R (2011) Characterization of self-compatible SF-haplotype in almond. Plant and Animal Genomes XIX Conference, San Diego
Thompson MM (1983) A survey of fruit genetic resources in Syria and recommendations for collection. FAO/IBPGR Consultant for Fruit Genetic Resources Report
Tsai DS, Lee HS, Post LC, Kreiling KM, Kao TH (1992) Sequence of an S-protein of Lycopersicon peruvianum and comparison with other solanaceous S-proteins. Sex Plant Reprod 5(4):256–263
Tsukamoto T, Hauck NR, Tao R, Jiang N, Iezzoni AF (2006) Molecular characterization of three non-functional S-haplotypes in Sour Cherry (Prunus cerasus). Plant Mol Biol 62(3):371–383
Ushijima K, Sassa H, Tao R, Yamane H, Dandekar AM, Gradziel TM, Hirano H (1998) Cloning and characterization of cDNAs encoding S-RNases from almond (Prunus dulcis): primary structural features sequence diversity and sequence diversity of the S-RNases in Rosaceae. Mol Gen Genet 260(2–3):261–268
Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hiranob H (2003) Structural and transcriptional analysis of the self-incompatibility locus of almond: identification of a pollen-expressed F-Box gene with haplotype-specific polymorphism. Plant Cell 15(3):771–781
Valizadeh B, Ershadi A, Gholami M (2009) Identification of self-incompatibility alleles in Iranian almond cultivars by PCR using consensus and allele-specific primers. J Hort Sci Biotech 84(3):285–290
Vargas F, Romero M, Clavé J, Vergés J, Santos J, Battle I (2008) ‘Vayro’, ‘Marinada’, ‘Constanti’, and ‘Tarraco’ almonds. Hort Sci 43(2):535–537
Vilanova S, Badenes ML, Burgos L, Martínez-Calvo J, Llácer G, Romero C (2006) Self compatibility of two apricot selections is associated with two pollen-part mutations of different nature. Plant Physiol 142(2):629–641
Yamane H, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2003) Self-incompatibility (S) locus region of the mutated S 6 -haplotype of Sour Cherry (Prunus cerasus) contains a functional pollen S allele and a non-functional pistil S allele. J Exp Bot 54(392):2431–2434
Acknowledgments
The authors are grateful to the Zanjan University, the Shahrekord University and Agriculture and Natural Resources Research Center of Karaj for financial assistance, and for providing plant material used in this work. We thank Dr. Ali Imani (Agriculture and Natural Resources Research Center of Karaj) for providing unpublished information about the field performance of the almond cultivars used in this study. We also thank Dr. Pedro Martínez-Gómez for his valuable comments and suggestions. We thank Ms Ivana Bosić for editing the manuscript.
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Hafizi, A., Shiran, B., Maleki, B. et al. Identification of new S-RNase self-incompatibility alleles and characterization of natural mutations in Iranian almond cultivars. Trees 27, 497–510 (2013). https://doi.org/10.1007/s00468-012-0803-7
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DOI: https://doi.org/10.1007/s00468-012-0803-7