Skip to main content
Log in

Distribution and evolution of citrus with S 4 and/or S 5 gene alleles for self-incompatibility with special focus on the origin of satsuma mandarin (Citrus unshiu Marc.; S f S 4 )

  • Research Article
  • Published:
Genetic Resources and Crop Evolution Aims and scope Submit manuscript

Abstract

Gametophytic self-incompatibility, one of the key characters for seedless citrus production, is controlled by single codominant gene S known in pummelo, mandarin and their hybrid cultivars. However, little is known about S genotypes and S allele frequencies in Citrus cultivars. First, S genotypes and S allele frequencies of Citrus accessions were studied with S 4 and S 5 gene alleles of ‘Hassaku’ (C. hassaku hort. ex Tanaka) a putative hybrid between self-incompatible pummelo [C. maxima (Burm.) Merrill; syn. C. grandis Osbeck] and ‘Kunenbo’ (C. nobilis Lour. var. kunep Tanaka). About 200 Citrus accessions were pollinated with each of the homozygous S1 seedlings (S 4 S 4 and S 5 S 5 ) of ‘Hassaku’. Pollen tube arrest in the styles indicated that 19 of 202 (9.4%) accessions have an S 4 allele and 12 of 191 (6.3%) accessions have an S 5 allele. In pummelo, the rate of accessions with S 4 allele was 1.4% (1/72), while that with S 5 allele was 5.9% (9/76). This suggests that the two alleles are originated from pummelo and the allele frequency is 0.7% (1/144) for S 4 and 5.9% (9/152) for S 5 . Except ‘Kunenbo’, all accessions with S 4 alleles have their origin in Japan. These results suggest that self-incompatible ‘Kunenbo’ (S 4 S ? ) introduced from Southeast Asia to Japan about 600 years ago firstly generated satsuma mandarin (S f S 4 ) and ‘Kabuchii’ (S 4 S ? ) about 400–500 years ago, followed by 16 S 4 -carrying cultivars including ‘Hassaku’ (S 4 S 5 ) appearing as a chance seedling in Hiroshima in the nineteenth century.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • de Nettancourt D (1977) Incompatibility in angiosperms. Springer, New York

    Book  Google Scholar 

  • de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin

    Book  Google Scholar 

  • Durham RE, Liou PC, Gmitter JFG, Moore GA (1992) Linkage of restriction fragment length polymorphisms and isozymes in Citrus. Theor Appl Genet 84(1):39–48

    CAS  PubMed  Google Scholar 

  • Froelicher Y, Mouhaya W, Bassene J-B, Gilles Costantino, Kamiri M, Luro F, Morillon R, Ollitrault P (2011) New universal mitochondrial PCR markers reveal new information on maternal citrus phylogeny. Tree Genet Genome 7(1):49–61

    Article  Google Scholar 

  • Fukane S (918) Honzowamyo (Japanese Name of Medical Herbs). 2017.01.06 http://dl.ndl.go.jp/info:ndljp/pid/2555536(in Japanese)

  • Garcia-Lor A, Curkl F, Snoussi-Trifa H, Morillon R, Ancillo G, Luro F, Navarro L, Ollitrault P (2013) A nuclear phylogenetic analysis: SNPs, indels and SSRs deliver new insights into the relationships in the ‘true citrus fruit trees’ group (Citrinae, Rutaceae) and the origin of cultivated species. Annals Bot 111(1):1–19

    Article  CAS  Google Scholar 

  • Hodgson RW (1967) Horticultural varieties of citrus. In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus industry, vol I. University of California Press, Berkley, pp 431–591

    Google Scholar 

  • Isobe A (2006) Higo Pummelo. In. Maotani T, Ono Y, Kihara T, Sendaya M, Udagawa M (eds) Tokusan Kajyu (Speciality Fruit Trees). Nihon Syubyoukyokai, Tokyo, pp 490-492 (in Japanese)

  • Iwamasa M, Oba Y (1980) Seedlessness due to self-incompatibility in Egami-Buntan, a Japanese pummelo cultivar. Bull Fac Agr Saga Univ 49:39–45 (in Japanese with English abstract)

    Google Scholar 

  • Kahn TL, DeMason DA (1988) Citrus pollen tube development in cross-compatible gynoecia, self-incompatible gynoecia, and in vitro. Canad J Bot 66(12):2527–2532

    Article  Google Scholar 

  • Kajiura I (2008) A chronological table of fruit history in Japan. Yokendo, Tokyo (in Japanese)

    Google Scholar 

  • Kim JH, Mori T, Wakana A, Ngo BX, Masuda JI, Sakai K, Kajiwara K (2010) Production of homozygous S1 seedlings for S gene in ‘Hirado Buntan’ pummelo (Citrus grandis Osbeck) and determination of the S alleles (S 9 and S 10) by pollination with the S1 seedlings to Citrus cultivars. J Fac Agr Kyushu Univ 55(2):239–245

    Google Scholar 

  • Kim J-H, Mori T, Wakana A, Ngo BX, Sakai K, Kajiwara K (2011) Determination of self-incompatible Citrus cultivars with S 1 and/or S 2 alleles by pollination with homozygous S1 seedlings (S 1 S 1 or S 2 S 2) of ‘Banpeiyu’ pummelo. J Japan Soc Hort Sci 80(4):404–413

    Article  Google Scholar 

  • Mabberley DJ (1997) A classification for edible Citrus (Rutaceae). Telopea 7(2):167–172

    Article  Google Scholar 

  • Miwa T (1951) Pollination, fertilization, and fruit drop in Citrus tamurana. Hort Bull Miyazaki Univ (Nature Sci) 2:1–67 (in Japanese with English abstract)

    Google Scholar 

  • Nagai K, Tanikawa O (1928) On citrus pollination. Proc. Third Pan-Pacific Science Congress 2:2023–2029

    Google Scholar 

  • Ngo BX (2001) Study on the self-incompatibility in Citrus (Rutaceae) with special emphases on the pollen tube growth and allelic variation. Dissertation, Kyushu University

  • Ngo BX, Wakana A, Park SM, Nada Y, Fukudome I (2001) Pollen tube behaviors in self-incompatible and self-compatible Citrus cultivars. J Fac Agr, Kyushu Univ 45(2):443–457

    Google Scholar 

  • Ngo BX, Wakana A, Kim JH, Mori T, Sakai K (2010) Estimation of self-incompatibility S genotypes of Citrus cultivars and plants based on controlled pollination with restricted number of pollen grains. J Fac Agr, Kyushu Univ 55(1):67–72

    Google Scholar 

  • Ngo BX, Kim JH, Wakana A, Isshiki S, Mori T (2011) Estimation of self- incompatibility genotypes of Citrus cultivars with Got-3 allozyme markers. J Japan Soc Hort Sci 80(3):284–294

    Article  Google Scholar 

  • Nicolosi E, Deng ZN, Gentile A, La Malfa S, Continella G, Tribulato E (2000) Citrus phylogeny and genetic origin of important species as investigated by molecular markers. Theor Appl Genet 100(8):1155–1166

    Article  CAS  Google Scholar 

  • Nuriyal JP (1952) Self-incompatibility in pummelo (Citrus maxima Merr.). Curr Sci 21:347

    Google Scholar 

  • Okamoto H (2008) Several aspects of sea-going vessels of Ryukyu Kingdom in Old Ryukyu period. East Asian Cultural Interaction Stu 1:221–248 (in Japanese with English summary)

    Google Scholar 

  • Okamura S (1848) Keien Kippu. http://dl.ndl.go.jp/info:ndljp/pid/2536111. Accessed 6 Jan 2017

  • Pang XM, Hu CG, Deng XX (2007) Phylogenetic relationship within Citrus and its related genera as inferred from AFLP markers. Genet Resour Crop Evol 54(2):429–436

    Article  CAS  Google Scholar 

  • Shimizu T, Kitajima A, Nonaka K, Yoshioka T, Ohta S, Goto S, Toyoda A, Fujiyama A, Mochizuki T, Nagasaki H, Kaminuma E, Nakamura Y (2016) Hybrid origins of citrus varieties inferred from DNA marker analysis of nuclear and organelle genomes. PLoS ONE. https://doi.org/10.1371/journal.pone.0166969

    Google Scholar 

  • Soost RK (1965) Incompatibility allele in the genus Citrus. Pro Amer Soc Hort Sci 87:176–180

    Google Scholar 

  • Soost RK (1969) The incompatibility gene system in Citrus. In: Chapman H (ed) Proceedings of the first international citrus symposium, vol 1. University of California, Riverside, pp 189–190

    Google Scholar 

  • Swingle WT, Reece PC (1967) The botany of Citrus and its wild relatives of the orange subfamily. In: Reuther W, Webber HJ, Bachelor LD (eds) The citrus industry, vol I. Division of Agricultural Sciences. University of California, Berkeley, pp 190–430

    Google Scholar 

  • Tanaka T (1932) A monograph of the satsuma orange with special reference to the occurrence of new varieties through bud variation. Memory Faculty Science of Agriculture, Taihoku Imperial Univ. 4:1–626

    Google Scholar 

  • Tanaka Y (1948a) Iconograph of Japanese citrus fruits, vol 1. Yokendo, Tokyo (in Japanese)

    Google Scholar 

  • Tanaka Y (1948b) Iconograph of Japanese citrus fruits, vol 2. Yokendo, Tokyo (in Japanese)

    Google Scholar 

  • Tanaka T (1957) A revision of Ryukyu Rutaceae-Aurantioideae, Revisio Aurantiacearum X. Sci bull Agr Home Eco Division, University of the Ryukyus 4:91–116

    Google Scholar 

  • Tanaka T (1969) Misunderstanding with regards citrus classification and nomenclature. Bull Univ Osaka Prefecture, Series B 21:139–145

    Google Scholar 

  • Tanaka Y (1980) Iconograph of Japanese citrus fruits, vol 3. Yokendo, Tokyo (in Japanese)

    Google Scholar 

  • Ton LD, Krezdorn AH (1967) Growth of pollen tubes in three incompatible varieties of Citrus. Proc Amer Soc Hort Sci 89:211–215

    Google Scholar 

  • Ueno I (1978) Studies on cross-incompatibility in Citrus tachibana Tanaka. 1. Fruit set of tachibana after cross pollination with eight Citrus varieties. Bull Fruit Tree Res Station: Okitsu Series B 5:1–7

    Google Scholar 

  • Vardi A, Neumann H, Frydman-Shani A, Yaniv Y, Spiegel-Roy P (2000) Tentative model on the inheritance of juvenility, self-incompatibility and parthenocarpy. Acta Hort 535:199–205

    Article  Google Scholar 

  • Velasco R, Licciardello C (2014) A genealogy of the citrus family. Nature Biotechnol 32(7):640–642

    Article  CAS  Google Scholar 

  • Wakana A, Ngo BX, Isshiki S (1998) Self-incompatibility in Citrus: linkage between GOT isozyme loci and the incompatibility loci. In: Omura M, Hayashi H, Scott S (eds) Breed biotechnol fruit tees, proceedings of the second Japan–Australia internal workshop. NIFTS, Tsukuba, pp 90–93

    Google Scholar 

  • Wakana A, Ngo BX, Fukudome I, Kajiwara K (2004) Estimation of the degree of self-incompatibility reaction during flower bud development and production of self-fertilized seeds by bud pollination in self-incompatible Citrus cultivars. J Fac Agr Kyushu Univ 49(2):307–320

    Google Scholar 

  • Webber HJ (1967) History and development of the citrus industry. In: Reuther W, Webber HJ, Batchelor LD (eds) The citrus industry, vol I. Division of Agricultural Sciences, University of California, Berkeley, pp 1–39

    Google Scholar 

  • Wu GA, Prochnik S, Jenkins J, Salse J, Hellsten U, Murat F, Perrier X, Ruiz M, Scalabrin S, Terol J, Takita MA (2014) Sequencing of diverse mandarin, pummelo and orange genomes reveals complex history of admixture during citrus domestication. Nature Biotechnol 32(7):656–662

    Article  CAS  Google Scholar 

  • Yamaji H, Kondo K, Kuniga T, Nesumi H, Yoshida T, Hashimoto K, Takeda O (2013) Origin of cultivated Citrus (Rutaceae) documented by the contents of internal transcribed spacer sequences (ITS) in nuclear ribosomal DNA. J Japan Bot 88(4):232–238

    Google Scholar 

  • Yamamoto M, Kobayashi M (1996) Polymorphism of chloroplast DNA in Citrus. J Japan Soc Hort Sci 65(2):291–296

    Article  CAS  Google Scholar 

  • Yamamoto M, Kobayashi S, Nakamura Y, Yamada Y (1993) Phylogenic relationships of citrus revealed by RFLP analysis of mitochondrial and chloroplast DNA. Japan J Breed 43(3):355–365

    Article  CAS  Google Scholar 

  • Yamamoto M, Kubo T, Tominaga S (2006) Self- and cross-incompatibility of various Citrus accessions. J Japan Soc Hort Sci 75(5):372–378

    Article  Google Scholar 

  • Yamamoto M, Fukuda M, Koga T, Kubo T, Tominaga S (2010) Examination of the Origin of Keraji (Citrus keraji), Local Citrus of Kikaijima Island, Kagoshima Prefecture. Hort Res (Japan) 9(1):7–12 (in Japanese with English summary)

    Article  Google Scholar 

  • Yamamoto M, Kouno R, Nakagawa T, Usui T, Kubo T, Tominaga S (2011) Isozyme and DNA analyses of local citrus germplasm on Amami islands. Japan. J Japan Soc Hort Sci 80(3):268–275

    Article  Google Scholar 

  • Yamamoto M, Tsuchimochi Y, Ninomiya T, Koga T, Kitajima A, Yamasaki A, Inafuku-Teramoto S, Yang X, Yang X, Zhong G, Nasir N (2013) Diversity of chloroplast DNA in various mandarins (Citrus spp) and other citrus demonstrated by CAPS analysis. J Japan Soc Hort Sci 82(2):106–113

    Article  CAS  Google Scholar 

  • Yamane H, Tao R (2009) Molecular Basis of Self-(in)compatibility and Current Status of S-genotyping in Rosaceous Fruit Trees. J Jpn Soc Hortic Sci 78(2):137–157

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors are grateful to citrus breeding stuffs of the National Institute of Fruit Tree Science (NIFTS), Kumamoto Prefectural Fruit Tree Experiment Station (KMPFTS), and Kagoshima Prefectural Fruit Tree Experiment Station (KSPFTS) for kindly providing citrus scions from which a large number of the adult trees used in this experiment were raised.

Funding

This study was partially supported by JSPS KAKENHI Grant No. JP21380027.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Akira Wakana.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, XH., Kim, JH., Wakana, A. et al. Distribution and evolution of citrus with S 4 and/or S 5 gene alleles for self-incompatibility with special focus on the origin of satsuma mandarin (Citrus unshiu Marc.; S f S 4 ). Genet Resour Crop Evol 65, 1013–1033 (2018). https://doi.org/10.1007/s10722-017-0592-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10722-017-0592-3

Keywords

Navigation