Capturing sequence variation among flowering-time regulatory gene homologs in the allopolyploid crop species Brassica napus

Frontiers in Plant Science

Volumn 5, Issue AUG, 2014, Pages

  Schiessl, Sarah ^a   Samans, Birgit ^a   Hüttel, Bruno ^b   Reinhard, Richard ^b   Snowdon, Rod J ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b MAX PLANCK INSTITUTE FOR PLANT BREEDING RESEARCH   (Germany)

Author keywords

CNV; Copy number variation; PAV; Presence absence variation; Rapeseed; Sequence capture

Indexed keywords

EID: 84907321608     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00404     Document Type: Article

References (59)

1. Allender, C. J., and King, G. J. (2010). Origins of the amphiploid species Brassica napu L. investigated by chloroplast and nuclear molecular markers. BMC Plant Biol. 10:54. doi: 10.1186/1471-2229-10-54
2. Andrés, F., and Coupland, G. (2012). The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13, 627-639. doi: 10.1038/nrg3291
3. Axelsson, T., Bowman, C. M., Sharpe, A. G., Lydiate, D. J., and Lagercrantz, U. (2000). Amphidiploid Brassica juncea contains conserved progenitor genomes. Genome 43, 679-688. doi: 10.1139/gen-43-4-679
4. Bancroft, I., Morgan, C., Fraser, F., Higgins, J., Wells, R., Clissold, L., et al. (2011). Dissecting the genome of the polyploid crop oilseed rape by transcriptome sequencing. Nat. Biotechnol. 29, 762-766. doi: 10.1038/nbt.1926
5. Basunanda, P., Radoev, M., Ecke, W., Friedt, W., Becker, H. C., and Snowdon, R. J. (2010). Comparative mapping of quantitative trait loci involved in heterosis for seedling and yield traits in oilseed rape (Brassica napus L.). Theor. Appl. Genet. 120, 271-281. doi: 10.1007/s00122-009-1133-z
6. Brenchley, R., Spannagl, M., Pfeifer, M., Barker, G. L. A., D'Amore, R., Allen, A. M., et al. (2012). Analysis of the bread wheat genome using whole-genome shotgun sequencing. Nature 491, 705-710. doi: 10.1038/nature11650
7. Bundock, P. C., Casu, R. E., and Henry, R. J. (2012). Enrichment of genomic DNA for polymorphism detection in a non-model highly polyploid crop plant. Plant Biotechnol. J. 10, 657-667. doi: 10.1111/j.1467-7652.2012.00707.x
8. Bus, A., Körber, N., Snowdon, R. J., and Stich, B. (2011). Patterns of molecular variation in a species-wide germplasm set of Brassica napus. Theor. Appl. Genet. 123, 1413-1423. doi: 10.1007/s00122-011-1676-7
9. Castillejo, C., and Pelaz, S. (2008). The Balance between CONSTANS and TEMPRANILLO activities determines FT expression to trigger flowering. Curr. Biol. 18, 1338-1343. doi: 10.1016/j.cub.2008.07.075
10. Chen, W., Zhang, Y., Liu, X., Chen, B., Tu, J., and Tingdong, F. (2007). Detection of QTL for six yield-related traits in oilseed rape (Brassica napus) using DH and immortalized F2 populations. Theor. Appl. Genet. 115, 849-858. doi: 10.1007/s00122-007-0613-2
11. Chen, Z. J. (2010). Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci. 15, 57-71. doi: 10.1016/j.tplants.2009.12.003
12. Chianga, G. C. K., Baruaa, D., Kramera, E. M., Amasinob, R. M., and Donohuea, K. (2009). Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 106, 11661-11666. doi: 10.1073/pnas.0901367106
13. Choi, K., Kim, J., Hwang, H. J., Kim, S., Park, C., Kim, S. Y., et al. (2011). The FRIGIDA complex activates transcription of flc, a strong flowering repressor in arabidopsis, by recruiting chromatin modification factors. Plant Cell 23, 289-303. doi: 10.1105/tpc.110.075911
14. de Montaigu, A., Toth, R., and Coupland, G. (2010). Plant development goes like clockwork. Trends Genet. 26, 296-306. doi: 10.1016/j.tig.2010.04.003
15. Deng, W., Ying, H., Helliwell, C. A., Taylor, J. M., Peacock, W. J., and Dennis, E. S. (2011). FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 108, 6680-6685. doi: 10.1073/pnas.1103175108
16. Doyle, J. J., and Doyle, J. L. (1990). Isolation of plant DNA from fresh tissues. Focus 12, 13-15.
17. Edwards, D., Batley, J., and Snowdon, R. J. (2013). Accessing complex crop genomes with next-generation sequencing. Theor. Appl. Genet. 126, 1-11. doi: 10.1007/s00122-012-1964-x
18. Friedt, W., and Snowdon, R. J. (2010). "Oilseed rape, " in Handbook of Plant Breeding, Vol. 4: Oil Crops Breeding, ed J. I. R. Vollmann (Berlin: Heidelberg), 91-126.
19. Gaeta, R. T., and Pires, J. C. (2010). Homoeologous recombination in allopolyploids: the polyploid ratchet. New Phytol. 186, 18-28. doi: 10.1111/j.1469-8137.2009.03089.x
20. Gaeta, R. T., Pires, J. C., Iniguez-Luy, F., Leon, E., and Osborn, T. C. (2007). Genomic changes in resynthesizedBrassica napus and their effect on gene expression and phenotype. Plant Cell 19, 3403-3417. doi: 10.1105/tpc.107.054346
21. Harper, A. L., Trick, M., Higgins, J., Fraser, F., Clissold, L., Wells, R., et al. (2012). Associative transcriptomics of traits in the polyploid crop species Brassica napus. Nat. Biotechnol. 30, 798-802. doi: 10.1038/nbt.2302
22. Hou, J., Long, Y., Raman, H., Zou, X., Wang, J., Dai, S., et al. (2012). A tourist-like MITE insertion in the upstream region of the BnFLC. A10 gene is associated with vernalization requirement in rapeseed (Brassica napus L.). BMC Plant Biol. 12:238. doi: 10.1186/1471-2229-12-238
23. Jaeger, K. E. (2008). The Control of Flowering in Time and Space in Arabidopsis thaliana. Norwich: University of East Anglia.
24. Jaeger, K. E., Graf, A., and Wigge, P. A. (2006). The control of flowering in time and space. J. Exp. Bot. 57, 3415-3418. doi: 10.1093/jxb/erl159
25. Johnston, J. S. (2005). Evolution of genome size in brassicaceae. Ann. Bot. 95, 229-235. doi: 10.1093/aob/mci016
26. Jung, C., and Muller, A. E. (2009). Flowering time control and applications in plant breeding. Trends Plant Sci. 14, 563-573. doi: 10.1016/j.tplants.2009.07.005
27. Jupe, F., Witek, K., Verweij, W., Śliwka, J., Pritchard, L., Etherington, G. J., et al. (2013). Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 76, 530-544. doi: 10.1111/tpj.12307
28. Kaufmann, K., Wellmer, F., Muino, J. M., Ferrier, T., Wuest, S. E., Kumar, V., et al. (2010). Orchestration of floral initiation by APETALA1. Science 328, 85-89. doi: 10.1126/science.1185244
29. Körber, N., Wittkop, B., Bus, A., Friedt, W., Snowdon, R. J., and Stich, B. (2012). Seedling development in a Brassica napus diversity set and its relationship to agronomic performance. Theor. Appl. Genet. 125, 1275-1287. doi: 10.1007/s00122-012-1912-9
30. Lagercrantz, U., Putterill, J., Coupland, G., and Lydiate, D. (1996). Comparative mapping in Arabidopsis and Brassica, fine scale genome collinearity and congruence of genes controlling flowering time. Plant J. 9, 13-20. doi: 10.1046/j.1365-313X.1996.09010013.x
31. Lee, J., and Lee, I. (2010). Regulation and function of SOC1, a flowering pathway integrator. J. Exp. Bot. 61, 2247-2254. doi: 10.1093/jxb/erq098
32. Li, Y., Huang, Y., Bergelson, J., Nordborg, M., and Borevitz, J. O. (2010). Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107, 21199-21204. doi: 10.1073/pnas.1007431107
33. Lisch, D. (2012). How important are transposons for plant evolution? Nat. Rev. Genet. 14, 49-61. doi: 10.1038/nrg3374
34. Mamanova, L., Coffey, A. J., Scott, C. E., Kozarewa, I., Turner, E. H., Kumar, A., et al. (2010). Target-enrichment strategies for next-generation sequencing. Nat. Methods 7, 111-118. doi: 10.1038/nmeth.1419
35. Mascher, M., Richmond, T. A., Gerhardt, D. J., Himmelbach, A., Clissold, L., Sampath, D., et al. (2013). Barley whole exome capture: a tool for genomic research in the genus Hordeum and beyond. Plant J. 76, 494-505. doi: 10.1111/tpj.12294
36. Ni, Z., Kim, E. D., Ha, M., Lackey, E., Liu, J., Zhang, Y., et al. (2008). Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327-331. doi: 10.1038/nature07523
37. Niwa, Y., Ito, S., Nakamichi, N., Mizoguchi, T., Niinuma, K., Yamashino, T., et al. (2007). Genetic linkages of the circadian clock-associated genes, TOC1, CCA1 and LHY, in the photoperiodic control of flowering time inArabidopsis thaliana. Plant Cell Physiol. 48, 925-937. doi: 10.1093/pcp/pcm067
38. Osborn, T. C., Kole, C., Parkin, I. A. P., Sharpe, A. G., Kuiper, M., Lydiate, D. J., et al. (1997). Comparison of flowering time genes in Brassica rapa, B. napus and Arabidopsis thaliana. Genetics 146, 1123-1129.
39. Pak, H., Guo, Y., Chen, M., Chen, K., Li, Y., Hua, S., et al. (2009). The effect of exogenous methyl jasmonate on the flowering time, floral organ morphology, and transcript levels of a group of genes implicated in the development of oilseed rape flowers (Brassica napus L.). Planta 231, 79-91. doi: 10.1007/s00425-009-1029-9
40. Parkin, I. A., Clarke, W. E., Sidebottom, C., Zhang, W., Robinson, S. J., Links, M. G., et al. (2010). Towards unambiguous transcript mapping in the allotetraploid Brassica napus. Genome 53, 929-938. doi: 10.1139/G10-053
41. Parkin, I. A. P., Sharpe, A. G., Keith, D. J., and Lydiate, D. J. (1995). Identification of the A and C genomes of amphidiploid Brassica napus (oilseed rape). Genome 38, 1122-1131. doi: 10.1139/g95-149
42. Pires, J. C., Zhao, J. W., Schranz, M. E., Leon, E. J., Quijada, P. A., Lukens, L. N., et al. (2004). Flowering time divergence and genomic rearrangements in resynthesized Brassica polyploids (Brassicaceae). Biol. J. Linn. Soc. 82, 675-688. doi: 10.1111/j.1095-8312.2004.00350.x
43. Preston, J. C., and Sandve, S. R. (2013). Adaptation to seasonality and the winter freeze. Front. Plant Sci. 4:167. doi: 10.3389/fpls.2013.00167
44. Quijada, P. A., Udall, J. A., Lambert, B., and Osborn, T. C. (2006). Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 1. Identification of genomic regions from winter germplasm. Theor. Appl. Genet. 113, 549-561. doi: 10.1007/s00122-006-0323-1
45. Razi, H., Howell, E. C., Newbury, H. J., and Kearsey, M. J. (2008). Does sequence polymorphism of FLC paralogues underlie flowering time QTL in Brassica oleracea? Theor. Appl. Genet. 116, 179-192. doi: 10.1007/s00122-007-0657-3
46. Samans, B. (2014). "Patterns of genome rearrangment after polyploidisation of Brassica napus, " in Plant and Animal Genome XXII: The International Conference on the Status of Plant and Animal Genome Research, ed S. R. Heller (San Diego, CA).
47. Schranz, M. E., Quijada, P., Sung, S. B., Lukens, L., Amasino, R., and Osborn, T. C. (2002). Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162, 1457-1468.
48. Snowdon, R., Lühs, W., and Friedt, W. (2006). "Oilseed rape, " in Genome Mapping and Molecular Breeding in Plants, ed C. Kole (Berlin; New York, NY: Springer), 55-114.
49. Song, Y. H., Ito, S., and Imaizumi, T. (2013). Flowering time regulation: photoperiod-and temperature-sensing in leaves. Trends Plant Sci. 18, 575-583. doi: 10.1016/j.tplants.2013.05.003
50. Srikanth, A., and Schmid, M. (2011). Regulation of flowering time: all roads lead to Rome. Cell. Mol. Life Sci. 68, 2013-2037. doi: 10.1007/s00018-011-0673-y
51. Town, C. D. (2006). Comparative genomics of Brassica oleracea and Arabidopsis thaliana reveal gene loss, fragmentation, and dispersal after polyploidy. Plant Cell 18, 1348-1359.
52. Udall, J. A., Quijada, P. A., Lambert, B., and Osborn, T. C. (2006). Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 2. Identification of alleles from unadapted germplasm. Theor. Appl. Genet. 113, 597-609. doi: 10.1007/s00122-006-0324-0
53. Vallender, E. J. (2011). Expanding whole exome resequencing into non-human primates. Genome Biol. 12:R87. doi: 10.1186/gb-2011-12-9-r87
54. Wang, J., Long, Y., Wu, B., Liu, J., Jiang, C., Shi, L., et al. (2009). The evolution of Brassica napus FLOWERING LOCUST paralogues in the context of inverted chromosomal duplication blocks. BMC Evol. Biol. 9:271. doi: 10.1186/1471-2148-9-271
55. Wang, N., Qian, W., Suppanz, I., Wei, L., Mao, B., Long, Y., et al. (2011a). Flowering time variation in oilseed rape (Brassica napus L.) is associated with allelic variation in the FRIGIDA homologue BnaA. FRI.a. J. Exp. Bot. 62, 5641-5658. doi: 10.1093/jxb/err249
56. Wang, X., Wang, H., Wang, J., Sun, R., Wu, J., Liu, S., et al. (2011b). The genome of the mesopolyploid crop speciesBrassica rapa. Nat. Genet. 43, 1035-1039. doi: 10.1038/ng.919
57. Wigge, P. A. (2013). Ambient temperature signalling in plants. Curr. Opin. Plant Biol. 16, 661-666. doi: 10.1016/j.pbi.2013.08.004
58. Żmieńko, A., Samelak, A., Kozłowski, P., and Figlerowicz, M. (2013). Copy number polymorphism in plant genomes. Theor. Appl. Genet. 127, 1-18. doi: 10.1007/s00122-013-2177-7
59. Zou, X., Suppanz, I., Raman, H., Hou, J., Wang, J., Long, Y., et al. (2012). Comparative analysis of flc homologues in brassicaceae provides insight into their role in the evolution of oilseed rape. PLoS ONE 7:e45751. doi: 10.1371/journal.pone.0045751