Transcriptome analysis reveals the same 17 S-locus F-box genes in two haplotypes of the self-incompatibility locus of Petunia inflata

Plant Cell

Volumn 26, Issue 7, 2014, Pages 2873-2888

  Williams, Justin S ^a   Der, Joshua P ^a   dePamphilis, Claude W ^a   Kao, Teh Hui ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; PLANT PROTEIN; PRIMER DNA; RIBONUCLEASE; TRANSCRIPTOME;

ALLELE; ENZYMOLOGY; FLOWER; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LOCUS; GENETIC LINKAGE; GENETICS; HAPLOTYPE; METABOLISM; PETUNIA; PHYSIOLOGY; POLLEN; POLLINATION; PROTEIN DEGRADATION; SELF-INCOMPATIBILITY (PLANT); TRANSGENIC PLANT; UBIQUITINATION;

ALLELES; DNA PRIMERS; F-BOX PROTEINS; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENETIC LINKAGE; GENETIC LOCI; HAPLOTYPES; PETUNIA; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; POLLEN; POLLINATION; PROTEOLYSIS; RIBONUCLEASES; SELF-INCOMPATIBILITY IN FLOWERING PLANTS; TRANSCRIPTOME; UBIQUITINATION;

EID: 84907370919     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.114.126920     Document Type: Article

References (58)

1. Ai, Y., Singh, A., Coleman, C.E., Ioerger, T.R., Kheyr-Pour, A., and Kao, T.-h. (1990). Self-incompatibility in Petunia inflata: isolation and characterization of cDNAs encoding three S-allele-associated proteins. Sex. Plant Reprod. 3: 130-138.
2. Anderson, M.A., McFadden, G.I., Bernatzky, R., Atkinson, A., Orpin, T., Dedman, H., Tregear, G., Fernley, R., and Clarke, A.E. (1989). Sequence variability of three alleles of the self-incompatibility gene of Nicotiana alata. Plant Cell 1: 483-491.
3. Andrews, S. (2010). FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc/.
4. Bai, C., Sen, P., Hofmann, K., Ma, L., Goebl, M., Harper, J.W., and Elledge, S.J. (1996). SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box. Cell 86: 263-274.
5. Borodina, T., Adjaye, J., and Sultan, M. (2011). A strand-specific library preparation protocol for RNA sequencing. Methods Enzymol. 500: 79-98.
6. Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21: 3674-3676.
7. Cornish, E.C., Pettitt, J.M., Bonig, I., and Clarke, A.E. (1987). Developmentally controlled expression of a gene associated with self-incompatibility in Nicotiana alata. Nature 326: 99-102.
8. de Nettancourt, D. (2001). Incompatibility and Incongruity in Wild and Cultivated Plants. (Berlin: Springer).
9. Der, J.P., Barker, M.S., Wickett, N.J., dePamphilis, C.W., and Wolf, P.G. (2011). De novo characterization of the gametophyte transcriptome in bracken fern, Pteridium aquilinum. BMC Genomics 12: 99.
10. Eddy, S.R. (2011). Accelerated profile HMM searches. PLOS Comput. Biol. 7: e1002195.
11. Edgar, R.C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26: 2460-2461.
12. Fulton, T.M., Van der Hoeven, R., Eannetta, N.T., and Tanksley, S.D. (2002). Identification, analysis, and utilization of conserved ortholog set markers for comparative genomics in higher plants. Plant Cell 14: 1457-1467.
13. Goldraij, A., Kondo, K., Lee, C.B., Hancock, C.N., Sivaguru, M., Vazquez-Santana, S., Kim, S., Phillips, T.E., Cruz-Garcia, F., and McClure, B. (2006). Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439: 805-810.
14. Grabherr, M.G., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat. Biotechnol. 29: 644-652.
15. Haas, B.J., et al. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat. Protoc. 8: 1494-1512.
16. Hua, Z., and Kao, T.H. (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.
17. Hua, Z., and Kao, T.H. (2008). Identification of major lysine residues of S(3)-RNase of Petunia inflata involved in ubiquitin-26S proteasomemediated degradation in vitro. Plant J. 54: 1094-1104.
18. Hua, Z., Meng, X., and Kao, T.H. (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.
19. Huang, S., Lee, H.S., Karunanandaa, B., and Kao, T.H. (1994). Ribonuclease activity of Petunia inflata S proteins is essential for rejection of self-pollen. Plant Cell 6: 1021-1028.
20. Huson, D.H., Mitra, S., Ruscheweyh, H.-J., Weber, N., and Schuster, S.C. (2011). Integrative analysis of environmental sequences using MEGAN4. Genome Res. 21: 1552-1560.
21. Iseli, C., Jongeneel, C.V., and Bucher, P. (1999). ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 1999: 138-148.
22. Iwano, M., and Takayama, S. (2012). Self/non-self discrimination in angiosperm self-incompatibility. Curr. Opin. Plant Biol. 15: 78-83.
23. Kheyr-pour, A., Bintrim, S.B., Ioerger, T.R., Remy, R., Hammond, S., and Kao, T.-h. (1990). Sexual plant reproduction sequence diversity of pistil S-proteins associated with gametophytic selfincompatibility in Nicotiana alata. Sex. Plant Reprod. 3: 88-97.
24. Kozik, A., Matvienko, M., Kozik, I., van Leeuwen, H., Van Deynze, A., and Michelmore, R.M. (2008). Eukaryotic ultra conserved orthologs and estimation of gene capture in EST libraries [abstract]. Plant and Animal Genomes Conference 16: P6.
25. Kubo, K., Entani, T., Takara, A., Wang, N., Fields, A.M., Hua, Z., Toyoda, M., Kawashima, S., Ando, T., Isogai, A., Kao, T.H., and Takayama, S. (2010). Collaborative non-self recognition system in S-RNase-based self-incompatibility. Science 330: 796-799.
26. Kuroda, H., Takahashi, N., Shimada, H., Seki, M., Shinozaki, K., and Matsui, M. (2002). Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol. 43: 1073-1085.
27. Lamesch, P., et al. (2012). The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools. Nucleic Acids Res. 40: D1202-D1210.
28. Langmead, B., Trapnell, C., Pop, M., and Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10: R25.
29. Lechner, E., Achard, P., Vansiri, A., Potuschak, T., and Genschik, P. (2006). F-box proteins everywhere. Curr. Opin. Plant Biol. 9: 631-638.
30. Lee, H.S., Huang, S., and Kao, T. (1994). S proteins control rejection of incompatible pollen in Petunia inflata. Nature 367: 560-563.
31. Lee, H.-s., Karunanandaa, B., Mccubbin, A., Gilroy, S., and Kao, T. (1996). PRK1, a receptor-like kinase of Petunia inflata, is essential for postmeiotic development of pollen. Plant J. 9: 613-624.
32. Li, B., and Dewey, C.N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12: 323.
33. Li, S., Sun, P., Williams, J.S., and Kao, T.H. (2014). Identification of the self-incompatibility locus F-box protein-containing complex in Petunia inflata. Plant Reprod 27: 31-45.
34. Lottaz, C., Iseli, C., Jongeneel, C.V., and Bucher, P. (2003). Modeling sequencing errors by combining Hidden Markov models. Bioinformatics 19 (suppl. 2): ii103-ii112.
35. Luu, D.T., Qin, X., Morse, D., and Cappadocia, M. (2000). S-RNase uptake by compatible pollen tubes in gametophytic self-incompatibility. Nature 407: 649-651.
36. McCubbin, A.G., Wang, X., and Kao, T.H. (2000). Identification of self-incompatibility (S-) locus linked pollen cDNA markers in Petunia inflata. Genome 43: 619-627.
37. Murfett, J., Atherton, T.L., Mou, B., Gasser, C.S., and McClure, B.A. (1994). S-RNase expressed in transgenic Nicotiana causes S-allele-specific pollen rejection. Nature 367: 563-566.
38. Nunes, M.D.S., Santos, R.A., Ferreira, S.M., Vieira, J., and Vieira, C.P. (2006). Variability patterns and positively selected sites at the gametophytic self-incompatibility pollen SFB gene in a wild selfincompatible Prunus spinosa (Rosaceae) population. New Phytol. 172: 577-587.
39. 2 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.
40. Rambaut, A. (2008). FigTree v1.1.1: Tree figure drawing tool. http:// tree.bio.ed.ac.uk/software/figtree/.
41. Roy, A., Kucukural, A., and Zhang, Y. (2010). I-TASSER: a unified platform for automated protein structure and function prediction. Nat. Protoc. 5: 725-738.
42. Schmidt, A., Wuest, S.E., Vijverberg, K., Baroux, C., Kleen, D., and Grossniklaus, U. (2011). Transcriptome analysis of the Arabidopsis megaspore mother cell uncovers the importance of RNA helicases for plant germline development. PLoS Biol. 9: e1001155.
43. Sijacic, P., Wang, X., Skirpan, A.L., Wang, Y., Dowd, P.E., McCubbin, A.G., Huang, S., and Kao, T.H. (2004). Identification of the pollen determinant of S-RNase-mediated self-incompatibility. Nature 429: 302-305.
44. Sims, T.L., and Robbins, T.P. (2009). Gametophytic self-incompatibility in Petunia. In Petunia: Evolutionary, Developmental and Physiological Genetics. T. Gerats and J. Strommer, eds (New York: Springer), pp. 85-106.
45. Spitzer, M., Fuellen, G., Cullen, P., and Lorkowski, S. (2004). VisCoSe: visualization and comparison of consensus sequences. Bioinformatics 20: 433-435.
46. Stamatakis, A. (2014). RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30: 1312-1313.
47. Stone, S.L., and Callis, J. (2007). Ubiquitin ligases mediate growth and development by promoting protein death. Curr. Opin. Plant Biol. 10: 624-632.
48. Sun, P., and Kao, T.H. (2013). Self-incompatibility in Petunia inflata: the relationship between a self-incompatibility locus F-box protein and its non-self S-RNases. Plant Cell 25: 470-485.
49. Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
50. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22: 4673-4680.
51. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10: 385-397.
52. Wang, L., Dong, L., Zhang, Y., Zhang, Y., Wu, W., Deng, X., and Xue, Y. (2004). Genome-wide analysis of S-Locus F-box-like genes in Arabidopsis thaliana. Plant Mol. Biol. 56: 929-945.
53. Wang, N., and Kao, T.H. (2012). Self-incompatibility in Petunia: a self/ nonself-recognition mechanism employing S-locus F-box proteins and S-RNase to prevent inbreeding. Wiley Interdiscip. Rev. Dev. Biol. 1: 267-275.
54. 2-RNase. Plant Mol. Biol. 54: 727-742.
55. Wang, Y., Wang, X., McCubbin, A.G., and Kao, T.H. (2003). Genetic mapping and molecular characterization of the self-incompatibility (S) locus in Petunia inflata. Plant Mol. Biol. 53: 565-580.
56. Wheeler, D., and Newbigin, E. (2007). Expression of 10 S-class SLF-like genes in Nicotiana alata pollen and its implications for understanding the pollen factor of the S locus. Genetics 177: 2171-2180.
57. Williams, J.S., Natale, C.A., Wang, N., Li, S., Brubaker, T.R., Sun, P., and Kao, T.-H. (2014). Four previously identified Petunia inflata S-locus F-box genes are involved in pollen specificity in selfincompatibility. Mol. Plant 7: 567-569.
58. Wu, F., Mueller, L.A., Crouzillat, D., Pétiard, V., and Tanksley, S.D. (2006). Combining bioinformatics and phylogenetics to identify large sets of single-copy orthologous genes (COSII) for comparative, evolutionary and systematic studies: a test case in the euasterid plant clade. Genetics 174: 1407-1420.