Identification of S-Allele Based Self-incompatibility of Turkish Pear Gene Resources

Abstract

Self-incompatibility is considered to be a growth-limiting factor in fruit plants. In species with hermaphrodite flowers, S-locus (S-allele) has been accepted to control self-incompatibility, and the genetic control of this locus is provided by multiple genes (alleles). Pear (Pyrus communis L.) belongs to the Pomoideae from the Rosaceae family and is found to have great genetic potential in terms of ecological features in Turkey. To protect these cultivation features, national garden collections have been established across the country and Atatürk Horticultural Central Research Institute–Yalova collection is considered as genes bank. Identification of the different features of this collection (fruit quality, stress tolerance, self-incompatibility, grafting incompatibility, etc.) is of great importance for its utilization in pear breeding and cultivation. However, to our knowledge, this collection has not been characterized for self-incompatibility trait. In the current study, PCR (Polymerase Chain Reaction)-based amplification of the S-allele regions (S1, S6, S7, S8) causing the self-incompatibility in 180 pear genotypes obtained from the national pear germplasm was investigated by molecular biological methods based on the comparison of amplified products. In 180 pear genotypes, the S6 allele was the most prevalent one with 63% frequency, while the S8 allele was the least common allele with a rate of 4%. In allele combinations, the S1-S6 allele combination was the most common allele combination with a rate of 18%, and trilateral allele combinations (S1-S6-S7 and S1-S6-S8) were observed at a rate of 1%. Findings of the current research will enable the classification of the materials and the analysed material is likely to be used in breeding studies as well as pear cultivation.

Keywords

• Pear genotypes
• self -incompatibility
• S-allel
• PCR amplification

References

1. Akçay M E, Burak M, Kazan K, Yüksel Özmen C, Mutaf F, Bakir M, Ayanoğlu H & Ergül A (2014). Genetic analysis of Anatolian pear germplasm by simple sequence repeats. Annals of Applied Biology 164: 441–452.
2. Bagheri M & Ershadi A (2019). Self-Incompatibility Alleles in Iranian Pear Cultivars. CC-BY-NC 4.0 International license
3. Broothaerts W, Verdoodt L, Keulemans J, Janssens GA & Broekaert WF (1996). The self-incompatibility gene in apple and determination of the S-genotype of apple cultivars by PCR. Acta Horticulturae 423: 103-109.
4. Burke J M, Tang S, Knapp S & Rieseberg L H (2002).Genetic analysis of sunflower domestication. Genetics 162: 1257–1267
5. Claessen H, Keulemans W, Van de Poel B & De Storme N (2019). Finding a Compatible Partner: Self-Incompatibility in European Pear (Pyrus communis); Molecular Control, Genetic Determination, and Impact on Fertilization and Fruit Set. Frontiers in Plant Science 10: 407
6. De Nettancourt D (2001). Incompatibility and incongruity in wild and cultivated plants (Berlin Heidelberg: Springer-Verlag). De Franceschi, P, Dondini L & Sanzol J (2012). Molecular bases and evolutionary dynamics of self-incompatibility in the Pyrinae (Rosaceae). Journal of Experimental Botany 63: 4015–4032
7. Gandhi S D, Heesacker A F, Freeman C A, Argyris J, Bradford K & Knapp S J (2005). The self-incompatibility locus (S) and quantitative trait loci for self-pollination and seed dormancy in sunflower. Theoretical and Applied Genetics 111: 619–629
8. Gao C, Yuan D Y, Yang Y, Wang B F, Liu D M & Zou F (2015). Pollen tube growth and double fertilization in Camellia oleifera. Journal of the American Society for Horticultural Science 1401218

9. Goldraij A, Kondo K, Lee C B, Hancock C N, Sivaguru M, VazquezSantana S, Kım S, Philips T E, Cruz-Garcia F & McClure B (2006). Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439: 805–810
10. Goldway M, Stern R, Zisovich A, Raz A, Sapir G, Schnieder & Nyska R (2012). The self-incompatibility system in Rosaceae: agricultural and genetic aspects. Acta Horticulturae 967: 77–82
11. Goldway M, Takasaki T, Sanzol J, Mota M, Zisovich A H, Stern R A & Sansavini S (2009). Renumbering the S-RNase alleles of European pears (Pyrus communis L.) and cloning the S109 RNase allele. Scientia Horticulturae 119: 417–422
12. Goldway M, Zisovich A, Raz A & Stern R A (2008). Understanding the gametophytic self-incompatibility system and its impact on European pear (Pyrus communis L.) cultivation. Acta Horticulturae 800: 109–118
13. Herrera S, Rodrigo J, Hormaza J I & Lora J (2018). Identification of self-incompatibility alleles by specific PCR analysis and S-RNase sequencing in apricot. International Journal of Molecular Sciences 19
14. Hiscock S J & Tabah D A (2003). The different mechanisms of sporophytic self incompatibility. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 358: 1037–1045
15. Igic B, Lande R & Kohn J R (2008). Loss of self-incompatibility and its evolutionary consequences. International Journal of Plant Sciences 169: 93–104
16. Ishimizu T, Inoue K, Shimonaka M, Saito T, Terai O & Norioka S (1999). PCR-based method for identifying the S-genotypes of Japanese pear cultivars. Theoretical and Applied Genetics 98(6): 961-967
17. Ishimizu T, Sato Y, Saito T, Yoshimura Y, Norioka S, Nakanshi T & Sakiyama F (1996). Identification and partial aminoacid sequences of seven S-RNases associated with self-incompatibility of the Japanese pear, Pyrus pyriforia Nakai. Journal of Biochemistry 120: 326-334
18. Iwano M & Takayama S (2012). Self/non-self discrimination in angiosperm selfincompatibility. Current Opinion in Plant Biology 15: 78–83
19. Kakui H, Kato M, Ushijima K, Kitaguchi M, Kato S & Sassa H (2011). Sequence divergence and loss-of-function phenotypes of S locus F-box brothers genes are consistent with non-self recognition by multiple pollen determinants in self-incompatibility of Japanese pear (Pyrus pyrifolia). The Plant Journal 68: 1028–1038
20. Kim H T, Hirata Y & Nou I S (2002). Identification of self incompatibility alleles by S-RNases sequencing and PCR-RFLP analysis in Korean-bred pear (Pyrus pyrifolia) strains. Acta Horticulturae 587: 467–476
21. Kubo K, Entani T, Tanaka A, Wang N, Fields A M, Hua Z, Toyada M, Kawashima S, Ando T, Isogai A, Kao T & Takaya S (2010). Collaborative non-self recognition system in S-RNase-based selfincompatibility. Science 330: 796–799
22. Lefort F, Lally M, Thompson D & Douglas G C (1998). Morphological traits microsatellite fingerprinting and genetic relatedness of a stand of elite oaks (Q. RoburL.) at Tuallynally, Ireland. Silvae Genetica 47: 5–6
23. Martin M E & Lee T D (1993). Self pollination and resource availability affect ovule abortion in Cassia fasciculata (Caesalpiniaceae). Oecologia 94: 503–509
24. Mehlenbacher S A, Cociu V & Hough F L (1991). Apricots (Prunus). Acta Horticulturae 290: 65–110
25. Meng D, Gu Z, Li W, Wang A, Yuan H, Yang Q & Li T (2014a). Apple MdABCF assists in the transportation of S-RNase into pollen tubes. Plant Jornal 78: 990–1002
26. Meng D, Gu Z, Yuan H, Wang A, Li W, Yang Q, Zhu Y, Li T (2014b). The microtubule cytoskeleton and pollen tube golgi vesicle system are required for in vitro S-RNase internalization and gametic self-incompatibility in apple. Plant & Cell Physiology 55: 977–989
27. Muñoz-Sanz J V, Zuriaga E, Cruz-García F, McClure B & Romero C (2020) Self-(In)compatibility Systems: Target Traits for Crop-Production, Plant Breeding, and Biotechnology. Frontiers Plant Science 11:195
28. Muñoz-Sanz J V, Zuriaga E, López I, Badenes M L & Romero C (2017). Self-(in)compatibility in apricot germplasm is controlled by two major loci, S and M. BMC Plant Biology 17: 82
29. Nashima K, Terakami S, Nishio S, Kunihisa M, Nishitani C, Saito T & Yamamoto T (2015). S-genotype identification based on allele-specific PCR in Japanese pear. Breeding science 65(3): 208-215
30. Okada, K, Tonaka N, Taguchi T, Ichikawa T, Sawamura Y, Nakanishi T & Takeshi T Y (2011). Related polymorphic F-box protein genes between haplotypes clustering in the BAC contig sequences around the S-RNase of Japanese pear. Journal of Experimental Botany 62: 1887–1902
31. Orcheski B & Brown S. (2012). A grower’s guide to self and crossincompatibility in apple. New York Fruit Quarterly 20: 25–28
32. Pannell J R & Labouche A M (2013). The incidence and selection of multiple mating in plants. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 368:20120051
33. Quinet M, Kelecom S, Raspe O & Jacquemart A L (2014). S-genotype characterization of 13 North Western European pear (Pyrus communis L.) cultivars. Scientia Horticulturae 165:1-4
34. Sanzol J (2009a). Pistil-function break down in a new S-allele of European pear, S21, confers self-compatibility. Plant Cell Reports 28: 457–467
35. Sanzol J (2009b). Genomic characterization of self-incompatibility ribonucleases in European pear cultivars and development of PCR detection for 20 alleles. Tree Genetics Genomes 5: 393–405
36. Sanzol J & Herrero M (2002). Identification of self-incompatibility alleles in pear cultivars (Pyrus communis L.). Euphytica 128: 325–331
37. Sanzol J & Robbins T P (2008). Combined analysis of S alleles in European pear by pollinations and PCR based S-genotyping: correlation between S phenotypes and S-RNase genotype. Journal of the American Society for Horticultural Science 133: 213–224
38. Sanzol J, Sutherland B G & Robbins T P (2006). Identification and characterization of genomic DNA sequences of the S-ribonuclease gene associated with self-incompatibility alleles S-1 to S-5 in European pear. Plant Breeding 125: 513–518
39. Sapir G, Stern R A, Shafir S & Goldway M (2008). S-RNase based Sgenotyping of Japanese plum (Prunus salicina Lindl.) and its implication on the assortment of cultivar couples in the orchard. Scientia Horticulturae 118: 8–13
40. Sassa H, Kakui H, Miyamoto M, Suzuki Y, Hanada T, Ushijima K, Kusaba M, Hirano H & Koba T (2007). S locus F-box brothers: multiple and pollen-specific F-box genes with S haplotype-specific polymorphisms in apple and Japanese pear. Genetics 175: 1869–1881
41. Schneider, D, Stern R A & Goldway M (2005). A comparison between semi and fully compatible apple pollinators grown under suboptimal conditions. HortScience 40: 1280–1282
42. 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. Theoretical and Applied Genetics 112: 1543–1552
43. Visser T & Marcucci M C (1984). The interaction between compatible and self-incompatible pollen of apple and pear as influcenced by their ratio in the pollen cloud. Euphytica 33: 699–704
44. Williams J S, Der J P, de Pamphilis C W & Kao, T-H (2014). Transcriptome analysis reveals the same 17 S-Locus F-box genes in two haplotypes of the self incompatibility locus of Petunia inflata. Plant cells 26: 2873–2888
45. Williams J S, Wu L, Li S, Sun P & Kao T-H (2015). Insight into S-RNase-based self-incompatibility in Petunia: recent findings and future directions. Frontiers in Plant Science 6:41
46. Zisovich A H, Raz A, Stern R A & Goldway M (2010) Syrian pear (Pyrus syriaca) as a pollinator for European pear (Pyrus communis) cultivars. Scientia Horticulturae 125(3):256-262
47. Zisovich A H, Stern R A, Shafir S & Goldway M (2004). Identification of seven S-alleles from the European pear (Pyrus communis L.) and the determination of compatibility among cultivars. The Journal of Horticultural Science and Biotechnology 79: 101–106
48. Zisovich A H, Stern R A, Shafir S & Goldway M (2005). Fertilisation efficiency of semi and fully-compatible European pear (Pyrus communis) cultivars. The Journal of Horticultural Science and Biotechnology 80: 143–146
49. Zuccherelli S, Tassinari P, Broothaerts W, Tartarini S, Dondini L & Sansavini S (2002). S-allele characterization in self-incompatible pear (Pyrus communis L.). Sexual Plant Reproduction 15(3):153-158