A dominant point mutation in a RINGv E3 ubiquitin ligase homoeologous gene leads to cleistogamy in brassica napus

Plant Cell

Volumn 24, Issue 12, 2013, Pages 4875-4891

  Lu, Yun Hai ^a   Arnaud, Dominique ^a   Belcram, Harry ^a   Falentin, Cyril ^b   Rouault, Patricia ^b   Piel, Nathalie ^b   Lucas, Marie Odile ^b   Just, Jérémy ^a   Renard, Michel ^b   Delourme, Régine ^b   Chalhoub, Boulos ^a  

^a UNIVERSITÉ D EVRY VAL D ESSONNE   (France)

^b CEMAGREF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84873023268     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.112.104315     Document Type: Article

References (83)

1. Ammitzbøll, H., and Bagger Jørgensen, R. (2006). Hybridization between oilseed rape (Brassica napus) and different populations and species of Raphanus. Environ. Biosafety Res. 5: 3-13.
2. Beckie, H.J., Warwick, S.I., Nair, H., and Seguin-Swartz, G. (2003). Gene flow in commercial fields of herbicide-resistant canola (Brassica napus). Ecol. Appl. 13: 1276-1294.
3. Borden, K.L. (2000). RING domains: Master builders of molecular scaffolds? J. Mol. Biol. 295: 1103-1112.
4. Borden, K.L., and Freemont, P.S. (1996). The RING finger domain: A recent example of a sequence-structure family. Curr. Opin. Struct. Biol. 6: 395-401.
5. Carroll, S.B. (2001). Chance and necessity: The evolution of morphological complexity and diversity. Nature 409: 1102-1109.
6. Carvalho, P., Goder, V., and Rapoport, T.A. (2006). Distinct ubiquitin-ligase complexes define convergent pathways for the degradation of ER proteins. Cell 126: 361-373.
7. Chalhoub, B., Belcram, H., and Caboche, M. (2004). Efficient cloning of plant genomes into bacterial artificial chromosome (BAC) libraries with larger and more uniform insert size. Plant Biotechnol. J. 2: 181-188.
8. Chalhoub, B.A., Thibault, S., Laucou, V., Rameau, C., Höfte, H., and Cousin, R. (1997). Silver staining and recovery of AFLP amplification products on large denaturing polyacrylamide gels. Biotechniques 22: 216-218, 220.
9. Chantret, N., et al. (2005). Molecular basis of evolutionary events that shaped the hardness locus in diploid and polyploid wheat species (Triticum and Aegilops). Plant Cell 17: 1033-1045.
10. Chaudhary, B., Flagel, L., Stupar, R.M., Udall, J.A., Verma, N., Springer, N.M., and Wendel, J.F. (2009). Reciprocal silencing, transcriptional bias and functional divergence of homeologs in polyploid cotton (Gossypium). Genetics 182: 503-517.
11. Cheng, F., Wu, J., Fang, L., Sun, S., Liu, B., Lin, K., Bonnema, G., and Wang, X. (2012). Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS ONE 7: e36442.
12. Chhabra, A.K., and Sethi, S.K. (1991). Inheritance of cleistogamic flowering in durum wheat (Triticum aestivum L.). Euphytica 55: 147-150.
13. Clough, S.J., and Bent, A.F. (1998). Floral dip: A simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
14. Culley, T.M., and Klooster, M.R. (2007). The cleistogamous breeding system: A review of its frequency, evolution, and ecology in angiosperms. Bot. Rev. 73: 1-30.
15. Daniell, H. (2002). Molecular strategies for gene containment in transgenic crops. Nat. Biotechnol. 20: 581-586.
16. Darwin, C. (1877). The Different Forms of Flowers on Plants of the Same Species. (London: John Murray).
17. Fargue, A.N., Colbach, P.J., Picault, H., Renard M., and Meynard, J.M. (2006). Predictive study of the advantages of cleistogamy in oilseed rape in limiting unwanted gene flow. Euphytica 151: 1-13.
18. Felsenstein, J. (1985). Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791.
19. Ford, C.S., Allainguillaume, J., Grilli-Chantler, P., Cuccato, G., Allender, C.J., and Wilkinson, M.J. (2006). Spontaneous gene flow from rapeseed (Brassica napus) to wild Brassica oleracea. Proc. Biol. Sci. 273: 3111-3115.
20. Halfhill, M.D., Millwood, R.J., Raymer, P.L., and Stewart, C.N. Jr. (2002). Bt-transgenic oilseed rape hybridization with its weedy relative, Brassica rapa. Environ. Biosafety Res. 1: 19-28.
21. Hampton, R.Y. (2002). ER-associated degradation in protein quality control and cellular regulation. Curr. Opin. Cell Biol. 14: 476-482.
22. Hassink, G., Kikkert, M., van Voorden, S., Lee, S.J., Spaapen, R., van Laar, T., Coleman, C.S., Bartee, E., Früh, K., Chau, V., and Wiertz, E. (2005). TEB4 is a C4HC3 RING finger-containing ubiquitin ligase of the endoplasmic reticulum. Biochem. J. 388: 647-655.
23. Hovav, R., Udall, J.A., Chaudhary, B., Rapp, R., Flagel, L., and Wendel, J.F. (2008). Partitioned expression of duplicated genes during development and evolution of a single cell in a polyploid plant. Proc. Natl. Acad. Sci. USA 105: 6191-6195.
24. Hwang, C.S., Shemorry, A., and Varshavsky, A. (2010). N-terminal acetylation of cellular proteins creates specific degradation signals. Science 327: 973-977.
25. Isidore, E., Scherrer, B., Bellec, A., Budin, K., Faivre-Rampant, P., Waugh, R., Keller, B., Caboche, M., Feuillet, C., and Chalhoub, B. (2005). Direct targeting and rapid isolation of BAC clones spanning a defined chromosome region. Funct. Integr. Genomics 5: 97-103.
26. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: b-Glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
27. Jørgensen, R.B., and Andersen, B. (1994). Spontaneous hybridization between oilseed rape (Brassica napus) and weedy B. campestris (Brassicaceae): A risk of genetically modified oilseed rape. Am. J. Bot. 81: 1520-1526.
28. Koornneef, M., Hanhart, C.J., and Thiel, F. (1989). A genetic and phenotypic description of Eceriferum (cer) mutants in Arabidopsis thaliana. J. Hered. 80: 118-122.
29. Kraft, E., Stone, S.L., Ma, L., Su, N., Gao, Y., Lau, O.S., Deng, X.W., and Callis, J. (2005). Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiol. 139: 1597-1611.
30. Kreft, S.G., Wang, L., and Hochstrasser, M. (2006). Membrane topology of the yeast endoplasmic reticulum-localized ubiquitin ligase Doa10 and comparison with its human ortholog TEB4 (MARCH-VI). J. Biol. Chem. 281: 4646-4653.
31. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001). Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305: 567-580.
32. Kumar, N., Srivastava, G.C., and Dixit, K. (2008). Flower bud opening and senescence in roses (Rosa hybrida L.). Plant Growth Regul. 55: 81-99.
33. Kurauchi, N., Makino, T., and Hirose, S. (1993). Inheritance of cleistogamy-chasmogamy in barley. Barley Genet. Newsl. 23: 19.
34. Kwon, Y.W., Kim, D.S., and Yim, K.O. (2001). Herbicide-resistant genetically modified crop: assessment and management of gene flow. Weed Biol. Manage. 1: 42-51.
35. Li-Beisson, Y., Pollard, M., Sauveplane, V., Pinot, F., Ohlrogge, J., and Beisson, F. (2009). Nanoridges that characterize the surfacemorphology of flowers require the synthesis of cutin polyester. Proc. Natl. Acad. Sci. USA 106: 22008-22013.
36. Lord, E.M. (1981). Cleistogamy: A tool for the study of floral morphogenesis, function and evolution. Bot. Rev. 47: 421-449.
37. Lorick, K.L., Jensen, J.P., Fang, S., Ong, A.M., Hatakeyama, S., and Weissman, A.M. (1999). RING fingers mediate ubiquitinconjugating enzyme (E2)-dependent ubiquitination. Proc. Natl. Acad. Sci. USA 96: 11364-11369.
38. Lovering, R., Hanson, I.M., Borden, K.L., Martin, S., O'Reilly, N.J., Evan, G.I., Rahman, D., Pappin, D.J., Trowsdale, J., and Freemont, P.S. (1993). Identification and preliminary characterization of a protein motif related to the zinc finger. Proc. Natl. Acad. Sci. USA 90: 2112-2116.
39. Lu, B.R. (2003). Transgene containment by molecular means-Is it possible and cost effective? Environ. Biosafety Res. 2: 3-8.
40. Lü, S., Zhao, H., Des Marais, D.L., Parsons, E.P., Wen, X., Xu, X., Bangarusamy, D.K., Wang, G., Rowland, O., Juenger, T., Bressan, R.A., and Jenks, M.A. (2012). Arabidopsis ECERIFERUM9 involvement in cuticle formation and maintenance of plant water status. Plant Physiol. 159: 930-944.
41. Lynch, M., and Force, A. (2000). The probability of duplicate gene preservation by subfunctionalization. Genetics 154: 459-473.
42. Lysak, M.A., Cheung, K., Kitschke, M., and Bures, P. (2007). Ancestral chromosomal blocks are triplicated in Brassiceae species with varying chromosome number and genome size. Plant Physiol. 145: 402-410.
43. Maeng, J.Y., Won, Y.J., Piao, R., Cho, Y.I., Jiang, W., Chin, J.H., and Koh, H.J. (2006). Molecular mapping of a gene 'ld(t)' controlling cleistogamy in rice. Theor. Appl. Genet. 112: 1429-1433.
44. Merwin, N.C., Glurey, L.M., and Blackwell, K.H. (1981). Inheritance of papery glume and cleistogamy in sorghum. Crop Sci. 21: 953-956.
45. Moloney, M.M., Walker, J.M., and Sharma, K.K. (1989). High efficiency transformation of Brassica napus using Agrobacterium vectors. Plant Cell Rep. 8: 238-242.
46. Nair, S.K., et al. (2010). Cleistogamous flowering in barley arises from the suppression of microRNA-guided HvAP2 mRNA cleavage. Proc. Natl. Acad. Sci. USA 107: 490-495.
47. Panikashvili, D., Shi, J.X., Schreiber, L., and Aharoni, A. (2009). The Arabidopsis DCR encoding a soluble BAHD acyltransferase is required for cutin polyester formation and seed hydration properties. Plant Physiol. 151: 1773-1789.
48. Panikashvili, D., Shi, J.X., Schreiber, L., and Aharoni, A. (2011). The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol. 190: 113-124.
49. Parkin, I.A., Gulden, S.M., Sharpe, A.G., Lukens, L., Trick, M., Osborn, T.C., and Lydiate, D.J. (2005). Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171: 765-781.
50. Polsoni, L., Kott, S., and Beversdorf, W.D. (1988). Large-scale microspore culture technique for mutation selection studies in Brassica napus. Can. J. Bot. 66: 1681-1685.
51. Prince, V.E., and Pickett, F.B. (2002). Splitting pairs: The diverging fates of duplicated genes. Nat. Rev. Genet. 3: 827-837.
52. Pyke, K.A., and Page, A.M. (1998). Plastid ontogeny during petal development in Arabidopsis. Plant Physiol. 116: 797-803.
53. Renard, M., and Tanguy, X. (1997). Obtention de mutants cléistogames de crucifères. Brevet FR 9715768.
54. Saitou, N., and Nei, M. (1987). The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
55. Saxena, K.B., Ariyanayagam, R.P., and Reddy, L.J. (1992). Genetics of a high-selfing trait in pigeonpea. Euphytica 59: 2-3.
56. Saxena, K.B., Singh, L., and Ariyanayagam, R.P. (1993). Role of partial cleistogamy in maintaining genetic purity of pigeonpea. Euphytica 66: 225-229.
57. Schemske, D.W. (1978). Evolution of reproductive characteristics in Impatiens (Balsaminaceae): The significance of cleistogamy and chasmogamy. Ecology 59: 596-613.
58. Shi, J.X., Malitsky, S., De Oliveira, S., Branigan, C., Franke, R.B., Schreiber, L., and Aharoni, A. (2011). SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet. 7: e1001388.
59. Schranz, M.E., and Mitchell-Olds, T. (2006). Independent ancient polyploidy events in the sister families Brassicaceae and Cleomaceae. Plant Cell 18: 1152-1165.
60. Silva, N.F., and Goring, D.R. (2001). Mechanisms of self-incompatibility in flowering plants. Cell. Mol. Life Sci. 58: 1988-2007.
61. Smalle, J., and Vierstra, R.D. (2004). The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 55: 555-590.
62. Song, X., Wang, Z., Zuo, J., Huangfu, C., and Qiang, S. (2010). Potential gene flow of two herbicide-tolerant transgenes from oilseed rape to wild B. juncea var. gracilis. Theor. Appl. Genet. 120: 1501-1510.
63. Sparrow, P.A.C., Townsend, T.M., Morgan, C.L., Dale, P.J., Arthur, A.E., and Irwin, J.A. (2004). Genetic analysis of in vitro shoot regeneration from cotyledonary petioles of Brassica oleracea. Theor. Appl. Genet. 108: 1249-1255.
64. Stone, S.L., Hauksdóttir, H., Troy, A., Herschleb, J., Kraft, E., and Callis, J. (2005). Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137: 13-30.
65. Swanson, R., Locher, M., and Hochstrasser, M. (2001). A conserved ubiquitin ligase of the nuclear envelope/endoplasmic reticulum that functions in both ER-associated and Matalpha2 repressor degradation. Genes Dev. 15: 2660-2674.
66. Takahashi, R., Kurosaki, H., Yumoto, S., Han, O.K., and Abe, J. (2001). Genetic and linkage analysis of cleistogamy in soybean. J. Hered. 92: 89-92.
67. Tamura, K., Dudley, J., Nei, M., and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
68. Tang, H., Woodhouse, M.R., Cheng, F., Schnable, J.C., Pedersen, B.S., Conant, G., Wang, X., Freeling, M., and Pires, J.C. (2012). Altered patterns of fractionation and exon deletions in Brassica rapa support a two-step model of paleohexaploidy. Genetics 190: 1563-1574.
69. Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F., and Higgins, D.G. (1997). The CLUSTAL_X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
70. Turuspekov, Y., Mano, Y., Honda, I., Kawada, N., Watanabe, Y., and Komatsuda, T. (2004). Identification and mapping of cleistogamy genes in barley. Theor. Appl. Genet. 109: 480-487.
71. Uphof, J.C.T. (1938). Cleistogamic flowers. Bot. Rev. 4: 21-49.
72. van Doorn, W.G., and Van Meeteren, U. (2003). Flower opening and closure: A review. J. Exp. Bot. 54: 1801-1812.
73. van Engelen, F.A., Molthoff, J.W., Conner, A.J., Nap, J.P., Pereira, A., and Stiekema, W.J. (1995). pBINPLUS: An improved plant transformation vector based on pBIN19. Transgenic Res. 4: 288-290.
74. Vierstra, R.D. (2009). The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10: 385-397.
75. von Heijne, G., Steppuhn, J., and Herrmann, R.G. (1989). Domain structure of mitochondrial and chloroplast targeting peptides. Eur. J. Biochem. 180: 535-545.
76. Vos, P., Hogers, R., Bleeker, M., Reijans, M., van de Lee, T., Hornes, M., Frijters, A., Pot, J., Peleman, J., Kuiper, M., and Zabeau, M. (1995). AFLP: A new technique for DNA fingerprinting. Nucleic Acids Res. 23: 4407-4414.
77. Waller, D.M. (1984). Differences in fitness between seedlings derived from cleistogamous and chasmogamous flowers in Impatiens capensis. Evolution 38: 427-440.
78. Wang, X., et al; Brassica rapa Genome Sequencing Project Consortium (2011). The genome of the mesopolyploid crop species Brassica rapa. Nat. Genet. 43: 1035-1039.
79. Warwick, S.I., Simard, M.J., Légère, A., Beckie, H.J., Braun, L., Zhu, B., Mason, P., Séguin-Swartz, G., and Stewart, C.N. Jr. (2003). Hybridization between transgenic Brassica napus L. and its wild relatives: Brassica rapa L., Raphanus raphanistrum L., Sinapis arvensis L., and Erucastrum gallicum (Willd.) O.E. Schulz. Theor. Appl. Genet. 107: 528-539.
80. Yoshida, H., Itoh, J.I., Ohmori, S., Miyoshi, K., Horigome, A., Uchida, E., Kimizu, M., Matsumura, Y., Kusaba, M., Satoh, H., and Nagato, Y. (2007). superwoman1-cleistogamy, a hopeful allele for gene containment in GM rice. Plant Biotechnol. J. 5: 835-846.
81. Zhang, Z., et al. (2011). Duplication and partitioning in evolution and function of homoeologous Q loci governing domestication characters in polyploid wheat. Proc. Natl. Acad. Sci. USA 108: 18737-18742.
82. Zuckerkandl, E., and Pauling, L. (1965). Evolutionary divergence and convergence in proteins. In Evolving Genes and Proteins, V. Bryson and H.J. Vogel, eds (New York: Academic Press), pp. 97-166.
83. Zybailov, B., Rutschow, H., Friso, G., Rudella, A., Emanuelsson, O., Sun, Q., and van Wijk, K.J. (2008). Sorting signals, N-terminal modifications and abundance of the chloroplast proteome. PLoS One 3: e1994.