Identification of a Skp1-like protein interacting with SFB, the pollen S determinant of the gametophytic self-incompatibility in Prunus

Plant Physiology

Volumn 159, Issue 3, 2012, Pages 1252-1262

  Matsumoto, Daiki ^a   Yamane, Hisayo ^a   Abe, Kazuyuki ^b   Tao, Ryutaro ^a  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIRRHINUM HISPANICUM; PETUNIA X HYBRIDA; PLANTAGINACEAE; PRUNUS; PRUNUS AVIUM; ROSACEAE; SACCHAROMYCES CEREVISIAE; SOLANACEAE;

EID: 84863643538     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.197343     Document Type: Article

References (71)

1. Adachi Y, Komori S, Hoshikawa Y, Tanaka N, Abe K, Bessho H, Watanabe M, Suzuki A (2009) Characteristics of fruiting and pollen tube growth of apple autotetraploid cultivars showing self-compatibility. J Jpn Soc Hortic Sci 78: 402-409
2. Dawson K, Toone WM, Jones N, Wilkinson CR (2008) Loss of regulators of vacuolar ATPase function and ceramide synthesis results in multi-drug sensitivity in Schizosaccharomyces pombe. Eukaryot Cell 7: 926-937
3. de Nettancourt D (2001) Incompatibility and Incongruity in Wild and Cultivated Plants. Springer, Berlin
4. Deshaies RJ, Joazeiro CAP (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78: 399-434
5. Dyson HJ, Wright PE (2005) Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol 6: 197-208
6. 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: 203-213
7. Entani T, Takayama S, Iwano M, Shiba H, Ches FS, Isogai A (1999) Relationship between polyploidy and pollen self-incompatibility phenotype in Petunia hybrida Vilm Bios. Biotech Biochem 63: 1882-1888
8. Francheschi P, Pierantoni L, Dondini L, Grandi M, Sansavini S, Sanzol J (2011) Evaluation of candidate F-box genes for the pollen S of gametophytic self-incompatibility in the Pyrinae (Rosaceae) on the basis of their phylogenomic context. Tree Genet Genomes 7: 663-683
9. Franklin-Tong VE (2008) Self-Incompatibility in Flowering Plants. Springer, Berlin
10. Frottin F, Martinez A, Peynot P, Mitra S, Holz RC, Giglione C, Meinnel T (2006) The proteomics of N-terminal methionine cleavage. Mol Cell Proteomics 5: 2336-2349
11. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure BA (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439: 805-810
12. Golz JF, Oh HY, Su V, Kusaba M, Newbigin E (2001) Genetic analysis of Nicotiana pollen-part mutants is consistent with the presence of an S-ribonuclease inhibitor at the S locus. Proc Natl Acad Sci USA 98: 15372-15376
13. Hauck NR, Yamane H, Tao R, Iezzoni AF (2006) Accumulation of nonfunctional S-haplotypes results in the breakdown of gametophytic self-incompatibility in tetraploid Prunus. Genetics 172: 1191-1198
14. Hermand D (2006) F-box proteins: more than baits for the SCF? Cell Div 1: 30
15. Hua Z, Kao TH (2006) Identification and characterization of components of a putative petunia S-locus F-box-containing E3 ligase complex involved in S-RNase-based self-incompatibility. Plant Cell 18: 2531-2553
16. Hua Z, Kao TH (2008) Identification of major lysine residues of S(3)-RNase of Petunia inflata involved in ubiquitin-26S proteasome-mediated degradation in vitro. Plant J 54: 1094-1104
17. Hua Z, Meng XY, Kao TH (2007) Comparison of Petunia inflata S-locus F-box protein (Pi SLF) with Pi SLF like proteins reveals its unique function in S-RNase based self-incompatibility. Plant Cell 19: 3593-3609
18. Huang J, Zhao L, Yang Q, Xue Y (2006) AhSSK1, a novel SKP1-like protein that interacts with the S-locus F-box protein SLF. Plant J 46: 780-793
19. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci USA 98: 13167-13171
20. 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: 235-243
21. Jourdain I, Spielewoy N, Thompson J, Dhut S, Yates JR, Toda T (2009) Identification of a conserved F-box protein 6 interactor essential for endocytosis and cytokinesis in fission yeast. Biochem J 420: 169-177
22. 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). Plant J 68: 1028-1038
23. Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, dePamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50: 873-885
24. Kong H, Leebens-Mack J, Ni W, dePamphilis CW, Ma H (2004) Highly heterogeneous rates of evolution in the SKP1 gene family in plants and animals: functional and evolutionary implications. Mol Biol Evol 21: 117-128
25. Kubo K, Entani T, Takara A, Wang N, Fields AM, Hua Z, Toyoda M, Kawashima S, Ando T, Isogai A, et al (2010) Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330: 796-799
26. 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: 29-42
27. Luu DT, Qin X, Laublin G, Yang Q, Morse D, Cappadocia M (2001) Rejection of S-heteroallelic pollen by a dual-specific s-RNase in Solanum chacoense predicts a multimeric SI pollen component. Genetics 159: 329-335
28. Luu DT, Qin X, Morse D, Cappadocia M (2000) S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407: 649-651
29. Marín I (2009) Diversification of the cullin family. BMC Evol Biol 9: 267
30. Martinez A, Traverso JA, Valot B, Ferro M, Espagne C, Ephritikhine G, Zivy M, Giglione C, Meinnel T (2008) Extent of N-terminal modifications in cytosolic proteins from eukaryotes. Proteomics 8: 2809-2831
31. Matsumoto D, Yamane H, Tao R (2008) Characterization of SLFL1, a pollenexpressed F-box gene located in the Prunus S locus. Sex Plant Reprod 21: 113-121
32. McClure BA (2009) Darwin's foundation for investigating self-incompatibility and the progress toward a physiological model for S-RNase-based SI. J Exp Bot 60: 1069-1081
33. Meng X, Sun P, Kao TH (2011) S-RNase-based self-incompatibility in Petunia inflata. Ann Bot (Lond) 108: 637-646
34. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
35. Minamikawa M, Kakui H, Wang S, Kotoda N, Kikuchi S, Koba T, Sassa H (2010) Apple S locus region represents a large cluster of related, polymorphic and pollen-specific F-box genes. Plant Mol Biol 74: 143-154
36. Newbigin E, Paape T, Kohn JR (2008) RNase-based self-incompatibility: puzzled by pollen S. Plant Cell 20: 2286-2292
37. Nowak MD, Davis AP, Anthony F, Yoder AD (2011) Expression and trans-specific polymorphism of self-incompatibility RNases in coffea (Rubiaceae). PLoS ONE 6: e21019
38. Nunes MDS, Santos RAM, Ferreira SM, Vieira J, Vieira CP (2006) Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild self-incompatible Prunus spinosa (Rosaceae) population. New Phytol 172: 577-587
39. Okada K, Tonaka N, Moriya Y, Norioka N, Sawamura Y, Matsumoto T, Nakanishi T, Takasaki-Yasuda T (2008) Deletion of a 236 kb region around S4-RNase in a stylar-part mutant S 4 sm-haplotype of Japanese pear. Plant Mol Biol 66: 389-400
40. Okada K, Tonaka N, Taguchi T, Ichikawa T, Sawamura Y, Nakanishi T, Takasaki-Yasuda T (2011) Related polymorphic F-box protein genes between haplotypes clustering in the BAC contig sequences around the S-RNase of Japanese pear. J Exp Bot 62: 1887-1902
41. 2 controls the pollen function of S-RNase-based self-incompatibility. Plant Cell 16: 2307-2322
42. Qiao H, Wang H, Zhao L, Zhou J, Huang J, Zhang Y, Xue Y (2004b) 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: 582-595
43. Risseeuw EP, Daskalchuk TE, Banks TW, Liu E, Cotelesage J, Hellmann H, Estelle M, Somers DE, Crosby WL (2003) Protein interaction analysis of SCF ubiquitin E3 ligase subunits from Arabidopsis. Plant J 34: 753-767
44. Saito T, Sato Y, Sawamura Y, Shoda M, Takasaki-Yasuda T, Kotobuki K (December 9, 2011) Dual recognition of S1 and S4 pistils by S4sm pollen in self-incompatibility of Japanese pear (Pyrus pyrifolia Nakai). Tree Genet Genomes http://dx.doi.org/10.1007/s11295-011-0456-5
45. Sassa H, Kakui H, Minamikawa M (2010) Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae. Sex Plant Reprod 23: 39-43
46. 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
47. Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS, Elledge SJ, Harper JW, Pagano M, Pavletich NP (2000) Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 408: 381-386
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-RNasemediated self-incompatibility. Nature 429: 302-305
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: 37-51
50. Steinbachs JE, Holsinger KE (2002) S-RNase-mediated gametophytic self-incompatibility is ancestral in eudicots. Mol Biol Evol 19: 825-829
51. Takahashi N, Kuroda H, Kuromori T, Hirayama T, Seki M, Shinozaki K, Shimada H, Matsui M (2004) Expression and interaction analysis of Arabidopsis Skp1-related genes. Plant Cell Physiol 45: 83-91
52. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599
53. Tao R, Iezzoni AF (2010) The S-RNase-based gametophytic self-incompatibility system in Prunus exhibits distinct genetic and molecular feature. Sci Hortic (Amsterdam) 124: 423-433
54. Tao R, Matsumoto D (2012) S locus mutation and self-compatibility in stone fruits. Acta Hortic (in press)
55. Tao R, Yamane H, Sugiura A, Murayama H, Sassa H, Mori H (1999) Molecular typing of S-alleles through identification, characterization and cDNA cloning for S-RNases in sweet cherry. J Am Soc Hortic Sci 124: 224-233
56. Tsukamoto T, Hauck NR, Tao R, Jiang N, Iezzoni AF (2010) Molecular and genetic analyses of four nonfunctional S haplotype variants derived from a common ancestral S haplotype identified in sour cherry (Prunus cerasus L.). Genetics 184: 411-427
57. 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: 771-781
58. 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: 573-586
59. Vieira J, Fonseca NA, Vieira CP (2008a) An S-RNase-based gametophytic self-incompatibility system evolved only once in eudicots. J Mol Evol 67: 179-190
60. Vieira J, Fonseca NA, Vieira CP (2009) RNase-based gametophytic self-incompatibility evolution: questioning the hypothesis of multiple independent recruitments of the S-pollen gene. J Mol Evol 69: 32-41
61. Vieira J, Teles E, Santos RAM, Vieira CP (2008b) Recombination at Prunus S-locus region SLFL1 gene. Genetics 180: 483-491
62. 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: 629-641
63. Wang Y, Wang X, McCubbin AG, Kao TH (2003) Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol Biol 53: 565-580
64. Ward JJ, Sodhi JS, McGuffin LJ, Buxton BF, Jones DT (2004) Prediction and functional analysis of native disorder in proteins from the three kingdoms of life. J Mol Biol 337: 635-645
65. Xu G, Ma H, Nei M, Kong H (2009) Evolution of F-box genes in plants: different modes of sequence divergence and their relationships with functional diversification. Proc Natl Acad Sci USA 106: 835-840
66. Xue Y, Zhang Y, Yang Q, Li Q, Cheng Z, Dickinson HG (2009) Genetic features of a pollen-part mutation suggest an inhibitory role for the Antirrhinum pollen self-incompatibility determinant. Plant Mol Biol 70: 499-509
67. 6-haplotype of sour cherry (Prunus cerasus) contains a functional pollen S allele and a non-functional pistil S allele. J Exp Bot 54: 2431-2437
68. Yamane H, Ikeda K, Ushijima K, Sassa H, Tao R (2003b) A pollenexpressed gene for a novel protein with an F-box motif that is very tightly linked to a gene for S-RNase in two species of cherry, Prunus cerasus and P. avium. Plant Cell Physiol 44: 764-769
69. Zhang Y, Zhao Z, Xue Y (2009) Roles of proteolysis in plant self-incompatibility. Annu Rev Plant Biol 60: 21-42
70. Zhao L, Huang J, Zhao Z, Li Q, Sims TL, Xue Y (2010) The Skp1-like protein SSK1 is required for cross-pollen compatibility in S-RNase-based self-incompatibility. Plant J 62: 52-63
71. Skp2 SCF ubiquitin ligase complex. Science 416: 703-709