Abstract
Gametophytic self-incompatibility, one of the key characters for production of seedless citrus, is known in pummelo [Citrus maxima (Burm.) Merr.], mandarin (C. reticulata Blanco) and their hybrid cultivars. The allelic variation in Citrus was reported for the self-incompatibility gene (S). However, S allele frequencies and S genotypes of self-incompatible and semi-self-incompatible Citrus cultivars were known only in a few S alleles. In the present study, S3 and S11 alleles were examined with homozygous S1 seedlings (S3S3 and S11S11) of self-incompatible Clementine mandarin (C. clementina hort. ex Tanaka; S3S11) a putative hybrid between self-compatible ‘Mediterranean’ mandarin (C. deliciosa Ten.) and self-compatible sweet orange [C. sinensis (L.) Osbeck]. One-hundred-forty-six Citrus accessions, including 43 pummelo accessions, were pollinated with each of the homozygous S1 seedlings (S3S3 and S11S11). Pollen tube arrest in the styles of their pollinated pistils indicated that 25 accessions, including Clementine, have an S3 allele each and 18 accessions, including Clementine, have an S11 allele each. Frequency of accessions with S3 allele was 17.7% (25 of 141 accessions examined) and S3 allele frequency was 11.8% (25 of 212 alleles excluding Sf self-compatible allele). Frequency of accessions with S11 allele was 13.2% (18 of 136 accessions examined) and S11 allele frequency was 8.8% (18 of 205 alleles excluding Sf allele). Pummelo accessions have S3 and S11 alleles with the frequencies of 12.2% and 33.3% respectively, suggesting that the two alleles originated from pummelo. Clementine shared S3 allele with two navel oranges, ten common oranges and two tangors, but not with three blood oranges. In the three blood oranges, it was suggested that stylar part mutation (S3sm) resulting in cross compatibility with S3 pollen occurred in their common ancestor. Clementine shared S11 allele with two tangors but did not share it with ‘Mediterranean’ mandarin. The present result for S3 and S11 alleles in Citrus accessions suggests that the two S alleles expanded their distribution in Citrus plants including sweet orange along with stylar part mutation for S3 allele during long history of cultivation.
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References
Barkley NA, Roose ML, Krueger RR, Federici CT (2006) Assessing genetic diversity and population structure in a citrus germplasm collection utilizing simple sequence repeat markers (SSRs). Theor Appl Genet 112:1519–1531
Butelli E, Licciardello C, Zhang Y, Liu J, Mackay S, Bailey P, Reforgiato-Recupero G, Martin C (2012) Retrotransposons control fruit-specific, cold-dependent accumulation of anthocyanins in blood oranges. Plant Cell 24:1242–1255
Caruso M, Merelo P, Distefano G, Malfa SL, Piero ARL, Tadeo FR, Talon M, Gentile A (2012) Comparative transcriptome analysis of stylar canal cells identifies novel candidate genes implicated in the self-incompatibility response of Citrus clementina. BMC Plant Biol 12:20. https://doi.org/10.1186/1471-2229-12-20
Chao C-CT (2005) Pollination study of mandarins and the effect on seediness and fruit size: implications for seedless mandarin production. HortScience 40:362–365
de Nettancourt D (1977) Incompatibility in angiosperms. Springer, New York
de Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin
Distefano G, Caruso M, La Malfa S, Gentile A, Tribulato E (2009) Histological and molecular analysis of pollen-pistil interaction in clementine. Plant Cell Rep 28:1439–1451
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
Fang DQ, Roose ML (1997) Identification of closely related citrus cultivars with inter-simple sequence repeat markers. Theor Appl Genet 95:408–417
Froelicher Y, Mouhaya W, Bassene J-B, Gilles C, 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
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
Herrero R, Asíns MJ, Carbonell EA, Navarro L (1996) Genetic diversity in the orange subfamily Aurantioideae. I. Intraspecies and intragenus genetic variability. Theor Appl Genet 92:599–609
Hiratsuka S, Takahasi E, Hirata N (1987) Crossability of self-compatible mutant ‘Osa-Nijisseiki’ (Pyrus serotina Rehd.). Japan Soc Hort Sci 56(2):166–172
Hodgson RW (1967) Horticultural varieties of citrus. In: Reuther W, Webber HJ, Batchelor LD (eds) Citrus industry, vol 1. University of California Press, Berkeley, pp 431–591
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)
Kim JH, Mori T, Wakana A, Ngo BX, Masuda J, 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 (S9 and S10) by pollination with the S1 seedlings to Citrus cultivars. J Fac Agr Kyushu Univ 55(2):239–245
Kim JH, Mori T, Wakana A, Ngo BX, Sakai K, Kajiwara K (2011) Determination of self-incompatible Citrus cultivars with S1 and/or S2 alleles by pollination with homozygous S1 seedlings (S1S1 or S2S2) of ‘Banpeiyu’ pummelo. J Japan Soc Hort Sci 80(4):404–413
Li X, Xie R, Lu Z, Zhou Z (2010) The origin of cultivated Citrus as inferred from internal transcribed spacer and chloroplast DNA sequence and amplified fragment length polymorphism fingerprints. J Am Soc Hortic Sci 135:341–350
Mabberley DJ (1997) A classification of edible Citrus (Rutaceae). Telopea (Syd) 7:167–172
Madhumathi C, Purushotham K, Chandhrasekhar R, Gopal K, Sekhar MR, Shankar GT (2015) Assessment of molecular diversity in elite sweet orange (Citrus sinensis L. Osbeck) accessions using RAPD markers. Electron J Plant Breed. https://doi.org/10.5958/0975-928X.2016.00041.7
Malik SK, Rohni MR, Kumar S, Choudhary R, Pal D, Choudhury R (2012) Assessment of genetic diversity in sweet orange [Citrus sinensis (L.) Osbeck] cultivars of India using morphological and RAPD markers. Agric Res 1:317. https://doi.org/10.1007/s40003-012-0045-3
Miao H, Ye Z, Silva JATD, Qin Y, Hu G (2013) Identifying differentially expressed genes in pollen from self-Incompatible ‘Wuzishatangju’ and self-compatible ‘Shatangju’ mandarins. Int J Mol Sci 14:8538–8555
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)
Nagai K, Tanikawa O (1928) On citrus pollination. Proc Third Pan-Pacific Sci Cong 2:2023–2029
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 Uni 55(1):67–72
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
Ngo BX, Chu TD, Wakana A, Bui TT, Nguyen TD, Nguyen TT, Nguyen TH, Kim JH, Sakai K (2019) Patterns and strength of pollen tube arrest in self-incompatible Citrus accessions (Rutaceae). J Fac Agr Kyushu Univ 64(2):225–236
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
Novelli VM, Cristofani M, Souza AA, Machado MA (2006) Development and characterization of polymorphic microsatellite markers for the sweet orange (Citrus sinensis L. Osbeck). Genet Mol Biol 29:90–96
Nuriyal JP (1952) Self-incompatibility in pummelo (Citrus maxima Merr.). Curr Sci 21:347
Orford SJ, Steele SN, Timmis JN (1995) A hypervariable middle repetitive DNA sequence from citrus. Theor Appl Genet 91:1248–1252
Sankar TG, Gopi V, Deepa B, Gopal K (2014) Genetic diversity analysis of sweet orange (Citrus sinensis Osbeck) varieties/clones through RAPD markers. Int J Curr Microbiol App Sci 3:75–84
Sawamura Y, Mase N, Takada N, Sato A, Nishitani C, Abe K, Masuda T, Yamamoto T, Saito T, Kotobuki K (2013) A self-compatible pollen-part mutant of Japanese pear produced by crossing ‘Kosui’ with pollen from gamma-irradiated ‘Kosui’. J Japan Soc Hort Sci 82:222–226
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 11:e0166969. https://doi.org/10.1371/journal.pone.0166969
Siragusa M, De Pasquale F, Abbate L, Tusa N (2006) Identification of sour orange accessions and evaluation of their genetic variability by molecular marker analyses. HortSci 41(1):84–89
Soost RK (1965) Incompatibility alleles in the genus Citrus. Proc Amer Soc Hort Sci 87:176–180
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
Swingle WT (1946) The botany of Citrus and its wild relatives of the orange subfamily (family Rutaceae, subfamily Aurantioideae). In: Reuther W, Webber H, Batchelor L (eds) The Citrus Industry. University of California Press, Berkeley, pp 129–474
Swingle WT, Reece PC (1967) The botany of Citrus and its wild relatives. In: Reuther W, Webber H, Batchelor L (eds) The Citrus Industry, vol 1. University of California Press, Berkeley, pp 190–430
Tanaka Y (1948a) Iconograph of Japanese citrus fruits, vol 1. Yokendo, Tokyo (in Japanese)
Tanaka Y (1948b) Iconograph of Japanese citrus fruits, vol 2. Yokendo, Tokyo (in Japanese)
Tanaka T (1969) Misunderstanding with regards citrus classification and nomenclature. Bull Univ Osaka Prefect Ser B 21:139–145
Targon MLPN, Machado MA, Coletta Filho HD, Cristofani M (2000) Genetic polymorphism of sweet orange (Citrus sinensis L. Osbeck) varieties evaluated by random amplified polymorphic DNA. Acta Hort 535:51–53
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
Velasco R, Licciardello C (2014) A genealogy of the citrus family. Nature Biotechnol 32(7):640–642
Vithanage V (1991) Effect of different pollen parents on seediness and quality of ‘Ellendale’ tangor. Sci Hort 48:253–260
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
Webber HJ, Reuther W, Lawton HW (1967) History and development of the citrus industry. In: Reuther W, Webber HJ, Batchelor LD (eds) The Citrus industry, vol 1. University of California Press, Berkeley, pp 1–39
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
Xu Q, Chen LL, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W-B, Hao B-H, Lyon MP, Chen J, Gao S, Xing F, Lan H, Chang JW, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas MK, Zeng W, Guo F, Cao H, Yang X, Xu XW, Cheng YJ, Xu J, Liu JH, Luo OJ, Tang Z, Guo WW, Kuang H, Zhang HY, Roose ML, Nagarajan N, Deng XX, Ruan Y (2013) The draft genome of sweet orange (Citrus sinensis). Nat Genet 45:59–66
Yamamoto M, Kubo T, Tominaga S (2006) Self- and cross-incompatibility of various Citrus accessions. J Japan Soc Hort Sci 75(5):372–378
Zhou X-H, Kim J-H, Wakana A, Sakai K, Kajiwara K, Mizunoe Y (2018) Distribution and evolution of citrus with S4 and/or S5 gene alleles for self-incompatibility with special focus on the origin of satsuma mandarin (Citrus unshiu Marc.; SfS4). Genet Resour Crop Evol 65(3):1013–1033
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 most adult trees used in this experiment were raised.
Funding
This study was partially funded by KAKENHI (No. 21380027) of JSPS (Japan Society for the Promotion of Science), Kyushu University and Yamaguchi University.
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Kim, JH., Handayani, E., Wakana, A. et al. Distribution and evolution of Citrus accessions with S3 and/or S11 alleles for self-incompatibility with an emphasis on sweet orange [Citrus sinensis (L.) Osbeck; SfS3 or SfS3sm]. Genet Resour Crop Evol 67, 2101–2117 (2020). https://doi.org/10.1007/s10722-020-00964-x
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DOI: https://doi.org/10.1007/s10722-020-00964-x