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Plant Molecular Biology Reporter

, Volume 37, Issue 1–2, pp 50–62 | Cite as

Two Genes (ClS1 and ClF-box) Involved the Self-Incompatibility of ”Xiangshui” Lemon (Citrus limon (L.) Burm. f.)

  • Wei Lin
  • Shuwei Zhang
  • Feng Ding
  • Xinhua HeEmail author
  • Cong Luo
  • Guixiang Huang
  • Minhphu Do
  • Qing Wang
  • Zaiyun Yang
  • Ling Su
  • Guibing Hu
Original Paper
  • 552 Downloads

Abstract

Gametophytic self-incompatibility (GSI) is an important factor affecting fruit development and is one of the important mechanisms of seedlessness in citrus. Although many studies have investigated the mechanisms of SI, this process remains unclear in “Xiangshui” lemon (C. limon). In this study, we cloned one S-RNase homologous gene and one SLF homologous gene from the “Xiangshui” lemon, designated as ClS1 (pistil-specific expression) and ClF-box (pollen-specific expression), which contain open reading frames (ORFs) of 534 and 810 bp, respectively. The expression pattern of these two genes was analyzed by quantitative real-time polymerase chain reaction, and the results showed that the expression pattern of these two genes was significantly upregulated after self-pollination compared to that after cross-pollination. Through pollination in transgenic tobacco, we found that the pollen tubes grew slowly and became twisted after cross-pollination of ClS1♀ and ClF-box ♂ transgenic tobaccos, but the pollen tubes of control, self-pollination ClS1 and cross-pollination ClS1♂, and ClF-box ♀ grew normally. Furthermore, significantly fewer pollen tubes of ClS1♀ and ClF-box ♂ entered the ovules than that in other combinations, and the seed number of cross-pollination ClS1♀ and ClF-box ♂ transgenic tobaccos was significantly reduced. These results indicated that the ClS1 and ClF-box genes contribute to the self-incompatibility of the “Xiangshui” lemon.

Keywords

Lemon Self-incompatibility S-RNase SLF Genetic transformation 

Notes

Financial Support

This research was supported by the National Natural Science Foundation of China (31460508), Guangxi Natural Science Foundation under Grant No. 2018GXNSFAA294004 and the Innovation Team of the Guangxi Citrus Industry Project.

Supplementary material

11105_2019_1135_MOESM1_ESM.docx (332 kb)
Supplementary Figure 1 (DOCX 331 kb)
11105_2019_1135_MOESM2_ESM.docx (27 kb)
Supplementary Figure 2 (DOCX 26 kb)
11105_2019_1135_MOESM3_ESM.docx (14 kb)
Supplementary Table 1 (DOCX 13 kb)

References

  1. Anderson MA, Cornish EC, Mau S-L, Williams EG, Hoggart R, Atkinson A, Bonig I, Grego B, Simpson R, Roche PJ, Haley JD, Penschow JD, Niall HD, Tregear GW, Coghlan JP, Crawford RJ, Clarke AE (1986) Cloning of cDNA for a stylar glycoprotein associated with expression of self-incompatibility in Nicotiana alata. Nature 321:38–44CrossRefGoogle Scholar
  2. 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 166:395–402CrossRefPubMedGoogle Scholar
  3. Bošković R, Tobutt KR (1996) Correlation of stylar ribonuclease zymograms with incompatibility alleles in sweet cherry. Euphytica 90:245–250CrossRefGoogle Scholar
  4. Bošković R, Russell K, Tobutt KR (1997) Inheritance of stylar ribonucleases in cherry progenies and reassignment of incompatibility alleles to incompatibility groups. Euphytica 95:221–228CrossRefGoogle Scholar
  5. 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 106:703–714CrossRefPubMedGoogle Scholar
  6. Choi C, Tao R, Andersen RL (2002) Identification of self-incompatibility alleles and pollen incompatibility groups in sweet cherry by PCR based s-allele typing and controlled pollination. Euphytica 123:9–20CrossRefGoogle Scholar
  7. De Nettancourt D (1997) Incompatibility in angiosperms. Sex Plant Reprod 10:185–199CrossRefGoogle Scholar
  8. Dodds PN, Ferguson C, Clarke AE, Newbigin E (1999) Pollen-expressed S-RNases are not involved in self-incompatibility in Lycopersicon peruvianum. Sex Plant Reprod 12:76–87CrossRefGoogle Scholar
  9. Entani T, Iwano M, Shiba H, Che FS, Isogai A, Takayama S (2003) Comparative analysis of the self-incompatibility (S-) locus region of Prunus mume: identification of a pollen-expressed F-box gene with allelic diversity. Genes Cells 8:203–213CrossRefPubMedGoogle Scholar
  10. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible nicotiana. Nature 439:805–810CrossRefPubMedGoogle Scholar
  11. Gu C, Zhang S, Huang S, Heng W, Liu Q, Wu H, Wu J (2010) Identification of S-genotypes in Chinese cherry cultivars (Prunus pseudocerasus Lindl.). Tree Genet Genome 6:579–590CrossRefGoogle Scholar
  12. Haring V, Gray JE, McClure BA, Anderson MA, Clarke AE (1990) Self-incompatibility: a self-recognition system in plants. Science 250:937–941CrossRefPubMedGoogle Scholar
  13. Hiratsuka S, Nakashima M, Kamasaki K, Kubo T, Kawai Y (1999) Comparison of an S-protein expression between self-compatible and -incompatible Japanese pear cultivars. Sex Plant Reprod 12:88–93CrossRefGoogle Scholar
  14. Huang S, Lee HS, Karunanandaa B, Kao TH (1994) Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell 6:1021–1028CrossRefPubMedPubMedCentralGoogle Scholar
  15. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci U S A 98:13167–13171CrossRefPubMedPubMedCentralGoogle Scholar
  16. Ikeda K, Igic B, Ushijima K, Yamane H, Hauck NR, Nakano R, Sassa H, Iezzoni AF, Kohn JR, Tao R (2004) Primary structural features of the S haplotype-specific F-box protein, SFB, in Prunus. Sex Plant Reprod 16:235–243CrossRefGoogle Scholar
  17. Janssens GA, Goderis IJ, Broekaert WF, Broothaerts W (1995) A molecular method for S-allele identification in apple based on allele-specific PCR. Theor Appl Genet 91:691–698CrossRefPubMedGoogle Scholar
  18. Kao TH, McCubbin AG (1997) Molecular and biochemical bases of gametophytic self-incompatibility in Solanaceae. Plant Physiol Biochem 35:171–176Google Scholar
  19. Kao TH, Tsukamoto T (2004) The molecular and genetic bases of S-RNase-based self-incompatibility. Plant Cell 16:S72–S83CrossRefPubMedPubMedCentralGoogle Scholar
  20. Kapila J, De Rycke R, Van Montagu M, Angenon G (1997) An agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci 122:101–108CrossRefGoogle Scholar
  21. Karunanandaa B, Huang S, Kao T (1994) Carbohydrate moiety of the Petunia inflata S3 protein is not required for self-incompatibility interactions between pollen and pistil. Plant Cell 6:1933–1940PubMedPubMedCentralGoogle Scholar
  22. Kitahara K, Matsumoto S (2002) Sequence of the S10 cDNA from ‘McIntosh’ apple and a PCR-digestion identification method. Hortscience 37:187–190CrossRefGoogle Scholar
  23. Kirch H-H, Li Y-Q, Seul U, Thompson RD (1995) The expression of a potato (Solanum tuberosum) S-RNase gene in Nicotiana tabacum pollen. Sex Plant Reprod 8(2):77–84CrossRefGoogle Scholar
  24. Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y (2002) An F-box gene linked to the self-incompatibility (S) locus of antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol 50:29–42CrossRefPubMedGoogle Scholar
  25. Lee HS, Singh A, Kao T (1992) RNase X2, a pistil-specific ribonuclease from Petunia inflata, shares sequence similarity with solanaceous S proteins. Plant Mol Biol 20:1131–1141CrossRefPubMedGoogle Scholar
  26. Lee HS, Huang S, Kao T (1994) S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367:560–563CrossRefPubMedGoogle Scholar
  27. Li TZ, Long SS, Li MF, Bai SL, Meng D (2011) Advances in research of the self-incompatibility genotypes (S-genotypes) in apple. Sci Agric Sin 44:1173–1183Google Scholar
  28. Liang M, Yang W, Su SY, Fu LL, Yi HL, Chen CW, Deng XX, Chai LJ (2017) Genome-wide identification and functional analysis of S-RNase involved in the self-incompatibility of citrus. Mol Gen Genomics 292:325–341CrossRefGoogle Scholar
  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 (−Delta Delta C (T)) method. Methods 25:402–408CrossRefGoogle Scholar
  30. Luo W, Yang L (2006) Study on the optimization of transformation conditions for Agrohacterium tumefaciens. Biotechnology 16:41–43Google Scholar
  31. Luu DT, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407:649–651CrossRefPubMedGoogle Scholar
  32. Matsumoto S, Furusawa Y, Kitahara K, Soejima J (2003) Partial genomic sequences of S 6 -, S 12 -, S 13 -, S 14 -, S 17 -, S 19 -, and S 21-RNase of apple and their allele designations. Plant Biotechnol 20:323–329CrossRefGoogle Scholar
  33. McClure BA, Franklin-Tong V (2006) Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224:233–245CrossRefPubMedGoogle Scholar
  34. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotiana alata are ribonucleases. Nature 342:955–957CrossRefPubMedGoogle Scholar
  35. Mesejo C, Yuste R, Martínez-Fuentes A, Reig C, Iglesias DJ, Primo-Millo E, Agustí M (2013) Self-pollination and parthenocarpic ability in developing ovaries of self-incompatible Clementine mandarins (Citrus clementina). Physiol Plant 148:87–96CrossRefPubMedGoogle Scholar
  36. Murase K, Shiba H, Iwano M, Che FS, Watanabe M, Isogai A, Takayama S (2004) A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303:1516–1519CrossRefPubMedGoogle Scholar
  37. Murfett J, Atherton TL, Mou B, Gasser CS, McClure BA (1994) S-RNase expressed in transgenic nicotiana causes S-allele-specific pollen rejection. Nature 367:563–566CrossRefPubMedGoogle Scholar
  38. Ngo BX, Wakana A, Kim JH, Mori T, Sakai K (2010) Estimation of self-incompatibility Sgenotypes of citrus cultivars and plants based on controlled pollination with restricted number of pollen grains. J Fac Agric Kyushu Univ 55:67–72Google Scholar
  39. Okada K, Moriya S, Haji T, Abe K (2013) Isolation and characterization of multiple F-box genes linked to the S9- and S10-RNase in apple (Malus × domestica Borkh.). Plant Reprod. 26:101–111CrossRefPubMedGoogle Scholar
  40. Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004a) The F-box protein AhSLF-S2 physically interacts with S-RNases that may be inhibited by the ubiquitin/26S proteasome pathway of protein degradation during compatible pollination in Antirrhinum. Plant Cell 16:582–595CrossRefPubMedPubMedCentralGoogle Scholar
  41. Qiao H, Wang F, Zhao L, Zhou J, Lai Z, Zhang Y, Robbins TP, Xue Y (2004b) The F-box protein AhSLF-S2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16:2307–2322CrossRefPubMedPubMedCentralGoogle Scholar
  42. Roalson EH, McCubbin AG (2003) S-RNases and sexual incompatibility: structure, functions, and evolutionary perspectives. Mol Phylogenet Evol 29:490–506CrossRefPubMedGoogle Scholar
  43. Sakurai K, Brown SK, Weeden N (2000) Self-incompatibility alleles of apple cultivars and advanced selections. Hort Sci 35:116–119CrossRefGoogle Scholar
  44. Sassa H, Hirano H, Ikehashi H (1993) Identification and characterization of stylar glycoproteins associated with self-incompatibility genes of Japanese pear, Pyrus serotina Rehd. Mol Gen Genet 241:17–25CrossRefPubMedGoogle Scholar
  45. Sassa H, Nishio T, Kowyama Y, Hirano H, Koba T, Ikehashi H (1996) Self-incompatibility (S) alleles of the rosaceae encode members of a distinct class of the T2/S ribonuclease superfamily. Mol Gen Genet 250(5):547–557PubMedGoogle Scholar
  46. Schuster M (2012) Incompatible (S-) genotypes of sweet cherry cultivars (Prunus avium L.). Sci Hortic 148:59–73CrossRefGoogle Scholar
  47. Shi GJ, Hou XL (2004) Measurement of self-incompatible by fluoroscope observation in non-heading Chinese cabbage. J Wuhan Bot Res 22:197–200Google Scholar
  48. Sijacic P, Wang X, Skirpan AL, Wang Y, Dowd PE, McCubbin AG, Huang S, Kao TH (2004) Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429:302–305CrossRefPubMedGoogle Scholar
  49. 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 17:37–51CrossRefPubMedPubMedCentralGoogle Scholar
  50. Stone JL (2002) Molecular mechanisms underlying the breakdown of gametophytic self-incompatibility. Q Rev Biol 77:17–32CrossRefPubMedGoogle Scholar
  51. Tanksley SD, Loaiza-Figueroa F (1985) Gametophytic self-incompatibility is controlled by a single major locus on chromosome 1 in Lycopersicon peruvianum. Proc Natl Acad Sci U S A 82:5093–5096CrossRefPubMedPubMedCentralGoogle Scholar
  52. Tao R, Yamane H, Sassa H, Mori H, Gradziel TM, Dandekar AM, Sugiura A (1997) Identification of stylar RNases associated with gametophytic self-incompatibility in almond (Prunus dulcis). Plant Cell Physiol 38:304–311CrossRefPubMedGoogle Scholar
  53. Tao ST, Zhang SL, Chen DX, Wei BY (2004) Study on characteristics of in situ pollen germination and tube growth of Prunus mume. J Fruit Sci 21:338–340Google Scholar
  54. Ushijima K, Sassa H, Dandekar AM, Gradziel TM, Tao R, Hirano 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 15:771–781CrossRefPubMedPubMedCentralGoogle Scholar
  55. Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck NR, Iezzoni AF, Tao R (2004) The S haplotype- specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J 39:573–586CrossRefPubMedGoogle Scholar
  56. Wang HY, Xue YB (2005) Sub cellular localization of the S locus F-box protein AhSLF-S2 in pollen and pollen tubes of self-incompatible Antirrhinua. Plant Biol 47:76–83Google Scholar
  57. Wang XQ, Shen X, He YM, Ren TN, Wu WT, Xi T (2011) An optimized freeze-thaw method for transformation of Agrobacterium tumefaciens EHA105 and LBA4404. Pharm Biotechnol 18:382–386Google Scholar
  58. Wang PP, Shi T, Zhuang WB, Zhang Z, Gao ZH (2012) Determination of S-RNase genotypes and isolation of four novel S-RNase genes in Japanese apricot ( Prunus mume Sieb. et Zucc.) native to China. J Hortic Sci Biotechnol 87:266–270CrossRefGoogle Scholar
  59. Watanabe M, Suwabe K, Suzuki G (2012) Molecular genetics, physiology and biology of self-incompatibility in Brassicaceae. Proc Jpn Acad, Ser B, Phys Biol Sci 88:519–535CrossRefPubMedPubMedCentralGoogle Scholar
  60. Wu J, Gu C, Khan MA, Wu J, Gao Y, Wang C, Korban SS, Zhang S (2013) Molecular determinants and mechanisms of gametophytic self-incompatibility in fruit trees of Rosaceae. Crit Rev Plant Sci 32:53–68CrossRefGoogle Scholar
  61. Xu C, Li MF, Wu JK, Guo H, Li Q, Zhang Y, Chai JJ, Li TZ, Xue YB (2013) Identification of a canonical SCF(SLF) complex involved in S-RNase-based self-incompatibility of Pyrus (Rosaceae). Plant Mol Biol 81:245–257CrossRefPubMedGoogle Scholar
  62. Ye WJ, Qin YH, Ye ZX, Silva JAT, Zhang LX, Wu XY, Lin SQ, Hu GB (2009) Seedless mechanism of a new mandarin cultivar “Wuzishatangju” (Citrus reticulata Blanco). Plant Sci 177:19–27CrossRefGoogle Scholar
  63. Zhang SJ, Huang SX, Heng W, Wu HQ, Wu J, Zhang SL (2008) Identification of S- genotypes in 17 Chinese cultivars of Japanese plum ( Prunus salicina Lindl.) and molecular characterisation of 13 novel S- alleles. J Hortic Sci Biotechnol 83:635–640CrossRefGoogle Scholar
  64. Zhang SW, Huang GX, Ding F, He XH, Pan JC (2012) Mechanism of seedlessness in a new lemon cultivar “Xiangshui” (citrus limon (L.) Burm. F.). Sex Plant Reprod 25:337–345CrossRefPubMedGoogle Scholar
  65. Zhang SW, Ding F, He XH, Luo C, Huang G, Hu Y (2015) Characterization of the ‘Xiangshui’ lemon transcriptome by de novo assembly to discover genes associated with self-incompatibility. Mol Gen Genomics 290:365–375CrossRefGoogle Scholar
  66. Zhang SQ, Liang M, Wang N, Xu Q, Deng XX, Chai LJ (2018) Reproduction in woody perennial Citrus: an update on nucellar embryony and self-incompatibility. Plant Reprod 31:43–57CrossRefPubMedGoogle Scholar
  67. Zheng N, Schulman BA, Song LZ, Miller JJ, Jeffrey PD, Wang P, Chu C, Koepp DM, Elledge SJ, Pagano M et al (2002) Structure of the Cul1-Rbx1-Skp1-F box Skp2 SCF ubiquitin ligase complex. Nature 416:703–709CrossRefPubMedGoogle Scholar
  68. Zisovich AH, Stern RA, Sapir G, Shafir S, Goldway M (2004) TheRHV region of S-RNase in the European pear (Pyrus communis) is not required for the determination of specific pollen rejection. Sex Plant Reprod 17:151–156CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Wei Lin
    • 1
  • Shuwei Zhang
    • 2
  • Feng Ding
    • 1
    • 2
  • Xinhua He
    • 1
    Email author
  • Cong Luo
    • 1
  • Guixiang Huang
    • 1
  • Minhphu Do
    • 1
  • Qing Wang
    • 1
  • Zaiyun Yang
    • 1
  • Ling Su
    • 1
  • Guibing Hu
    • 3
  1. 1.College of Agriculture, State Key Laboratory for Conservation and Utilization of Subtropical Agro-BioresourcesGuangxi UniversityNanningPeople’s Republic of China
  2. 2.Horticultural Research InstituteGuangxi Academy of Agricultural SciencesNanningPeople’s Republic of China
  3. 3.State Laboratory for Conservation and Utilization of Subtropical Agro-BioresourcesSouth China Agricultural UniversityGuangzhouChina

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