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Theoretical and Applied Genetics

, Volume 130, Issue 4, pp 727–741 | Cite as

Brassica napus DS-3, encoding a DELLA protein, negatively regulates stem elongation through gibberellin signaling pathway

  • Bo Zhao
  • Haitao Li
  • Juanjuan Li
  • Bo Wang
  • Cheng Dai
  • Jing Wang
  • Kede LiuEmail author
Original Article

Abstract

Key message

Identification and characterization of a semi-dwarfing gene ds-3 encoding a mutant DELLA protein regulating plant height through gibberellin signaling pathway.

Abstract

Lodging is one of the most important factors causing severe yield loss in oilseed rape. Utilization of semi-dwarf varieties has been proved the most effective way to increase lodging resistance and yield in many crops. To develop semi-dwarf germplasm in oilseed rape, we identified a semi-dwarf mutant ds-3 which showed a reduced response to phytohormones gibberellins (GAs). Genetic analysis indicated the dwarfism was controlled by a single semi-dominant gene, ds-3. The DS-3 gene was mapped to a genomic region on chromosome C07, which is syntenic to the region of a previously identified semi-dwarf gene ds-1 (BnaA06.RGA). In this region, DS-3 (BnaC07.RGA) gene was identified to encode a DELLA protein that functions as a repressor in GA signaling pathway. A substitution of proline to leucine was identified in ds-3 in the conserved VHYNP motif, which is essential for GA-dependent interaction between gibberellin receptor GID1 and DELLA proteins. Segregation analysis in the F2 population derived from the cross between ds-1 and ds-3 demonstrated that BnaA06.RGA displayed a stronger effect on plant height than BnaC07.RGA, indicating that different RGA genes may play different roles in stem elongation. In addition to BnaA06.RGA and BnaC07.RGA, two more RGA genes (BnaA09.RGA and BnaC09.RGA) were identified in the Brassica napus (B. napus) genome. Reverse-transcription polymerase chain reaction (RT-PCR) and yeast two-hybrid (Y2H) assays suggest that both BnaA09.RGA and BnaC09.RGA are transcribed in leaves and stems and can mediate GA signaling in vivo. These genes represent potential targets for screening ideal semi-dwarfing alleles for oilseed rape breeding.

Keywords

Plant Height Simple Sequence Repeat Marker Oilseed Rape DELLA Protein Dwarf Phenotype 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgements

The research was supported by the National Hi-Tech R&D Program (2013AA102602) and the National Key Basic Research Program (2015CB150200).

Compliance with ethical standards

Conflict of interest

The authors declare that there are no conflicts of interest.

Ethical standards

The authors declare that the experiments comply with the current laws of the country in which they were performed.

Supplementary material

122_2016_2846_MOESM1_ESM.pptx (1.2 mb)
Supplementary material 1 (PPTX 1188 KB)
122_2016_2846_MOESM2_ESM.xlsx (13 kb)
Supplementary material 2 (XLSX 13 KB)
122_2016_2846_MOESM3_ESM.xlsx (11 kb)
Supplementary material 3 (XLSX 11 KB)

References

  1. Ariizumi T, Lawrence PK, Steber CM (2011) The role of two F-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol 155:765–775CrossRefPubMedGoogle Scholar
  2. Asano K, Hirano K, Ueguchi-Tanaka M, Angeles-Shim RB, Komura T, Satoh H, Kitano H, Matsuoka M, Ashikari M (2009) Isolation and characterization of dominant dwarf mutants, Slr1-d, in rice. Mol Gen Genet 281:223–231CrossRefGoogle Scholar
  3. Chalhoub B, Denoeud F, Liu S, Parki IAP, Tang H, Wang X, Chique J, Belcram H, Tong C, Samans B, Corréa M, Silva CD, Just J, Falentin C, Koh CS, Clainche IL, Bernard M, Bento P, Noel B, Labadie K, Alberti A, Charles M, Arnaud D, Guo H, Daviaud C, Alamery S, Jabbari K, Zhao M, Edger PP, Chelaifa H, Tack D, Lassalle G, Mestiri I, Schnel N, Paslier M-CL, Fan G, Renault V, Bayer PE, Golicz AA, Manoli S, Lee T-H, Thi VHD, Chalabi S, Hu Q, Fan C, Tollenaere R, Lu Y, Battail C, Shen J, Sidebottom CHD, Wang X, Canaguier A, Chauveau A, Bérard A, Deniot G, Guan M, Liu Z, Sun F, Lim YP, Lyons E, Town CD, Bancroft I, Wang X, Meng J, Ma J, Pires JC, King GJ, Brunel D, Delourme R, Renard M, Aury J-M, Adams KL, Batley J, Snowdon RJ, Tost J, Edwards D, Zhou Y, Hua W, Sharpe AG, Paterson AH, Guan C, Wincker P (2014) Early allopolyploid evolution in the post-Neolithic Brassica napus oilseed genome. Science 345:950–953CrossRefPubMedGoogle Scholar
  4. Chandler PM, Marion-Poll A, Ellis M, Gubler F (2002) Mutants at the Slender1 locus of barley cv Himalaya. Molecular and physiological characterization. Plant Physiol 129:181–190CrossRefPubMedPubMedCentralGoogle Scholar
  5. Cheng H, Qin L, Lee S, Fu X, Richards D, Cao D, Luo D, Harberd N, Peng J (2004) Gibberellin regulates Arabidopsis floral development via suppression of DELLA protein function. Development 131:1055–1064CrossRefPubMedGoogle Scholar
  6. Cheng X, Xu J, Xia S, Gu J, Yang Y, Fu J, Qian X, Zhang S, Wu J, Liu K (2009) Development and genetic mapping of microsatellite markers from genome survey sequences in Brassica napus. Theor Appl Genet 118:1121–1131CrossRefPubMedGoogle Scholar
  7. Cheng F, Liu S, Wu J, Fang L, Sun S, Liu B, Li P, Hua W, Wang X (2011) BRAD, the genetics and genomics database for Brassica plants. BMC Plant Biol 11:136CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cheung F, Trick M, Drou N, Lim YP, Park JY, Kwon SJ, Kim JA, Scott R, Pires JC, Paterson AH, Town C, Bancroft I (2009) Comparative analysis between homoeologous genome segments of Brassica napus and its progenitor species reveals extensive sequence-level divergence. Plant Cell 21:1912–1928CrossRefPubMedPubMedCentralGoogle Scholar
  9. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743CrossRefPubMedGoogle Scholar
  10. Davière J-M, Achard P (2013) Gibberellin signaling in plants. Development 140:1147–1151Google Scholar
  11. Davière J-M, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9:10–20CrossRefPubMedGoogle Scholar
  12. Doyle JJ (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
  13. Foisset N, Delourme R, Barret P, Renard M (1995) Molecular tagging of the dwarf BREIZH (Bzh) gene in Brassica napus. Theor Appl Genet 91:756–761CrossRefPubMedGoogle Scholar
  14. Foisset N, Delourme R, Barret P, Hubert N, Landry B, Renard M (1996) Molecular-mapping analysis in Brassica napus using isozyme, RAPD and RFLP markers on a doubled-haploid progeny. Theor Appl Genet 93:1017–1025CrossRefPubMedGoogle Scholar
  15. Gallego-Bartolomé J, Minguet EG, Marín JA, Prat S, Blázquez MA, Alabadí D (2010) Transcriptional diversification and functional conservation between DELLA proteins in Arabidopsis. Mol Biol Evol 27:1247–1256CrossRefPubMedGoogle Scholar
  16. Griffiths J, Murase K, Rieu I, Zentella R, Zhang Z-L, Powers SJ, Gong F, Phillips AL, Hedden P, Sun TP, Thomas SG (2006) Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18:3399–3414CrossRefPubMedPubMedCentralGoogle Scholar
  17. Harberd NP, Freeling M (1989) Genetics of dominant gibberellin-insensitive dwarfism in maize. Genetics 121:827–838PubMedPubMedCentralGoogle Scholar
  18. Hedden P (2003) The genes of the Green Revolution. Trends Genet 19:5–9CrossRefPubMedGoogle Scholar
  19. Hirano K, Asano K, Tsuji H, Kawamura M, Mori H, Kitano H, Ueguchi-Tanaka M, Matsuoka M (2010) Characterization of the molecular mechanism underlying gibberellin perception complex formation in rice. Plant Cell 22:2680–2696CrossRefPubMedPubMedCentralGoogle Scholar
  20. King KE, Moritz T, Harberd NP (2001) Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159:767–776PubMedPubMedCentralGoogle Scholar
  21. Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugen 12:172–175CrossRefGoogle Scholar
  22. Li H, Chen X, Yang Y, Xu J, Gu J, Fu J, Qian X, Zhang S, Wu J, Liu K (2011a) Development and genetic mapping of microsatellite markers from whole genome shotgun sequences in Brassica oleracea. Mol Breed 28:585–596Google Scholar
  23. Li H, Wang Y, Li X, Gao Y, Wang Z, Zhao Y, Wang M (2011b) A GA-insensitive dwarf mutant of Brassica napus L. correlated with mutation in pyrimidine box in the promoter of GID1. Mol Biol Rep 38:191–197Google Scholar
  24. Li H, Younas M, Wang X, Li X, Chen L, Zhao B, Chen X, Xu J, Hou F, Hong B (2013) Development of a core set of single-locus SSR markers for allotetraploid rapeseed (Brassica napus L.). Theor Appl Genet 126:937–947CrossRefPubMedGoogle Scholar
  25. Liu C, Wang J, Huang T, Wang F, Yuan F, Cheng X, Zhang Y, Shi S, Wu J, Liu K (2010) A missense mutation in the VHYNP motif of a DELLA protein causes a semi-dwarf mutant phenotype in Brassica napus. Theor Appl Genet 121:249–258CrossRefPubMedGoogle Scholar
  26. Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IAP, Zhao M, Ma J, Yu J, Huang S, Wang X, Wang J, Lu K, Fang Z, Bancroft I, Yang T-J, Hu Q, Wang X, Yue Z, Li H, Yang L, Wu J, Zhou Q, Wang W, King GJ, Pires JC, Lu C, Wu Z, Sampath P, Wang Z, Guo H, Pan S, Yang L, Min J, Zhang D, Jin D, Li W, Belcram H, Tu i, Guan M, Qi C, Du D, Li J, Jiang L, Batley J, Sharpe AG, Park B-S, Ruperao P, Cheng F, Waminal NE, Huang Y, Dong C, Wang L, Li J, Hu Z, Zhuang M, Huang Y, Huang J, Shi J, Mei D, Liu J, Lee T-H, Wang J, Jin H, Li Z, Li X, Zhang J, Xiao L, Zhou Y, Liu Z, Liu X, Qin R, Tang X, Liu W, Wang Y, Zhang Y, Lee J, Kim HH, Denoeud F, Xu X, Liang X, Hua W, Wang X, Wang J, Chalhoub B, Paterson AH (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930PubMedPubMedCentralGoogle Scholar
  27. Michelmore RW, Paran I, Kesseli R (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. Proc Natl Acad Sci USA 88:9828–9832CrossRefPubMedPubMedCentralGoogle Scholar
  28. Miersch S, Gertz A, Breuer F, Schierholt A, Becker HC (2016) Influence of the semi-dwarf growth type on seed yield and agronomic parameters at low and high nitrogen fertilization in winter oilseed rape. Crop Sci 56:1573–1585CrossRefGoogle Scholar
  29. Monna L, Kitazawa N, Yoshino R, Suzuki J, Masuda H, Maehara Y, Tanji M, Sato M, Nasu S, Minobe Y (2002) Positional cloning of rice semidwarfing gene, sd-1: rice “green revolution gene” encodes a mutant enzyme involved in gibberellin synthesis. DNA Res 9:11–17CrossRefPubMedGoogle Scholar
  30. Muangprom A, Thomas SG, Sun TP, Osborn TC (2005) A novel dwarfing mutation in a green revolution gene from Brassica rapa. Plant Physiol 137:931–938CrossRefPubMedPubMedCentralGoogle Scholar
  31. Muangprom A, Mauriera I, Osborn TC (2006) Transfer of a dwarf gene from Brassica rapa to oilseed B. napus, effects on agronomic traits, and development of a ‘perfect’marker for selection. Mol Breed 17:101–110CrossRefGoogle Scholar
  32. Murase K, Hirano Y, Sun TP, Hakoshima T (2008) Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456:459–463CrossRefPubMedGoogle Scholar
  33. Neff MM, Turk E, Kalishman M (2002) Web-based primer design for single nucleotide polymorphism analysis. Trends Genet 18:613–615CrossRefPubMedGoogle Scholar
  34. Østergaard L, King GJ (2008) Standardized gene nomenclature for the Brassica genus. Plant Methods 4:10CrossRefPubMedPubMedCentralGoogle Scholar
  35. Parkin IA, Gulden SM, Sharpe AG, Lukens L, Trick M, Osborn TC, Lydiate DJ (2005) Segmental structure of the Brassica napus genome based on comparative analysis with Arabidopsis thaliana. Genetics 171:765–781CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pearce S, Saville R, Vaughan SP, Chandler PM, Wilhelm EP, Sparks CA, Al-Kaff N, Korolev A, Boulton MI, Phillips AL, Hedden P, Nicholson P, Thomas SG (2011) Molecular characterization of Rht-1 dwarfing genes in hexaploid wheat. Plant Physiol 157:1820–1831CrossRefPubMedPubMedCentralGoogle Scholar
  37. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Gene Dev 11:3194–3205CrossRefPubMedPubMedCentralGoogle Scholar
  38. Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261CrossRefPubMedGoogle Scholar
  39. Raman H, Raman R, Kilian A, Detering F, Long Y, Edwards D, Parkin IA, Sharpe AG, Nelson MN, Larkan N, Zou J, Meng J, Aslam MN, Batley J, Cowling WA, Lydiate D (2013) A consensus map of rapeseed (Brassica napus L.) based on diversity array technology markers: applications in genetic dissection of qualitative and quantitative traits. BMC Genom 14:277CrossRefGoogle Scholar
  40. Rosa NM-dl, Pfeiffer A, Hill K, Locascio A, Bhalerao RP, Miskolczi P, Grønlund AL, Wanchoo-Kohli A, Thomas SG, Bennett MJ, Lohmann JU, Blázquez MA, Alabadí D (2015) Genome wide binding site analysis reveals transcriptional coactivation of cytokinin-responsive genes by DELLA proteins. PLoS Genet 11:e1005337CrossRefGoogle Scholar
  41. Sasaki A, Ashikari M, Ueguchi-Tanaka M, Itoh H, Nishimura A, Swapan D, Ishiyama K, Saito T, Kobayashi M, Khush GS, Kitano H, Matsuoka M (2002) Green revolution: a mutant gibberellin-synthesis gene in rice. Nature 416:701–702CrossRefPubMedGoogle Scholar
  42. Silverstone AL, Mak PYA, Martinez EC, Sun TP (1997) The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146:1087–1099PubMedPubMedCentralGoogle Scholar
  43. Silverstone AL, Ciampaglio CN, Sun TP (1998) The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10:155–169CrossRefPubMedPubMedCentralGoogle Scholar
  44. Spielmeyer W, Ellis MH, Chandler PM (2002) Semidwarf (sd-1), “green revolution” rice, contains a defective gibberellin 20-oxidase gene. Proc Natl Acad Sci USA 99:9043–9048CrossRefPubMedPubMedCentralGoogle Scholar
  45. Sun TP (2010) Gibberellin-GID1-DELLA: a pivotal regulatory module for plant growth and development. Plant Physiol 154:567–570CrossRefPubMedPubMedCentralGoogle Scholar
  46. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  47. Tyler L, Thomas SG, Hu J, Dill A, Alonso JM, Ecker JR, Sun TP (2004) DELLA proteins and gibberellin-regulated seed germination and floral development in Arabidopsis. Plant Physiol 135:1008–1019CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ueguchi-Tanaka M, Nakajima M, Katoh E, Ohmiya H, Asano K, Saji S, Hongyu X, Ashikari M, Kitano H, Yamaguchi I, Matsuoka M (2007) Molecular interactions of a soluble gibberellin receptor, GID1, with a rice DELLA protein, SLR1, and gibberellin. Plant Cell 19:2140–2155CrossRefPubMedPubMedCentralGoogle Scholar
  49. Van Ooijen J (2006) JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen 33:10–1371Google Scholar
  50. Wang M, Zhao Y, Chen F, Yin X (2004) Inheritance and potentials of a mutated dwarfing gene ndf1 in Brassica napus. Plant Breed 123:449–453CrossRefGoogle Scholar
  51. Wang J, Lydiate DJ, Parkin IA, Falentin C, Delourme R, Carion PW, King GJ (2011a) Integration of linkage maps for the amphidiploid Brassica napus and comparative mapping with Arabidopsis and Brassica rapa. BMC Genom 12:101Google Scholar
  52. Wang X, Wang H, Wang J, Sun R, Wu J, Liu S, Bai Y, Mun J-H, Bancroft I, Cheng F, Huang S, Li X, Hua W, Wang J, Wang X, Freeling M, Pires JC, Paterson AH, Chalhoub B, Wang B, Hayward A, Sharpe AG, Park B-S, Weisshaar B, Liu B, Li B, Liu B, Tong C, Song C, Duran C, Peng C, Geng C, Koh C, Lin C, Edwards D, Mu D, Shen D, Soumpourou E, Li F, Fraser F, Conant G, Lassalle G, King GJ, Bonnema G, Tang H, Wang H, Belcram H, Zhou H, Hirakawa H, Abe H, Guo H, Wang H, Jin H, Parkin IAP, Batley J, Kim J-S, Just J, Li J, Xu J, Deng J, Kim JA, Li J, Yu J, Meng J, Wang J, Min J, Poulain J, Wang J, Hatakeyama K, Wu K, Wang L, Fang L, Trick M, Links MG, Zhao M, Jin M, Ramchiary N, Drou N, Berkman PJ, Cai Q, Huang Q, Li R, Tabata S, Cheng S, Zhang S, Zhang S, Huang S, Sato S, Sun S, Kwon S-J, Choi S-R, Lee T-H, Fan W, Zhao X, Tan X, Xu X, Wang Y, Qiu Y, Yin Y, Li Y, Du Y, Liao Y, Lim Y, Narusaka Y, Wang Y, Wang Z, Li Z, Wang Z, Xiong Z, Zhang Z (2011b) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039Google Scholar
  53. Wang Y, He J, Yang L, Wang Y, Chen W, Wan S, Chu P, Guan R (2016) Fine mapping of a major locus controlling plant height using a high-density single-nucleotide polymorphism map in Brassica napus. Theor Appl Genet 129:1479–1491CrossRefPubMedGoogle Scholar
  54. Wen C-K, Chang C (2002) Arabidopsis RGL1 encodes a negative regulator of gibberellin responses. Plant Cell 14:87–100CrossRefPubMedPubMedCentralGoogle Scholar
  55. Willige BC, Ghosh S, Nill C, Zourelidou M, Dohmann EM, Maier A, Schwechheimer C (2007) The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. Plant Cell 19:1209–1220CrossRefPubMedPubMedCentralGoogle Scholar
  56. Winkler RG, Freeling M (1994) Physiological genetics of the dominant gibberellin-nonresponsive maize dwarfs, Dwarf8 and Dwarf9. Planta 193:341–348CrossRefGoogle Scholar
  57. Wu J, Kong X, Wan J, Liu X, Zhang X, Guo X, Zhou R, Zhao G, Jing R, Fu X, Jia J (2011) Dominant and pleiotropic effects of a GAI gene in wheat results from a lack of interaction between DELLA and GID1. Plant Physiol 157:2120–2130CrossRefPubMedPubMedCentralGoogle Scholar
  58. Xu J, Qian X, Wang X, Li R, Cheng X, Yang Y, Fu J, Zhang S, King GJ, Wu J, Liu K (2010) Construction of an integrated genetic linkage map for the A genome of Brassica napus using SSR markers derived from sequenced BACs in B. rapa. BMC Genom 11:594CrossRefGoogle Scholar
  59. Yang T-J, Kim JS, Kwon S-J, Lim K-B, Choi B-S, Kim J-A, Jin M, Park JY, Lim M-H, Kim H-I, Lim YP, Kang JJ, Hong J-H, Kim C-B, Bhak J, Bancroft I, Park B-S (2006) Sequence-level analysis of the diploidization process in the triplicated FLOWERING LOCUS C region of Brassica rapa. Plant Cell 18:1339–1347CrossRefPubMedPubMedCentralGoogle Scholar
  60. Yang H, Liu J, Huang S, Guo T, Deng L, Hua W (2014) Selection and evaluation of novel reference genes for quantitative reverse transcription PCR (qRT-PCR) based on genome and transcriptome data in Brassica napus L. Gene 538:113–122CrossRefPubMedGoogle Scholar
  61. Yi B, Zeng F, Lei S, Chen Y, Yao X, Zhu Y, Wen J, Shen J, Ma C, Tu J, Fu T (2010) Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. Plant J 63:925–938CrossRefPubMedGoogle Scholar
  62. Yoshida H, Hirano K, Sato T, Mitsuda N, Nomoto M, Maeo K, Koketsu E, Mitani R, Kawamura M, Ishiguro S, Tada Y, Ohme-Takagi M, Matsuoka M, Ueguchi-Tanaka M (2014) DELLA protein functions as a transcriptional activator through the DNA binding of the indeterminate domain family proteins. Proc Natl Acad Sci USA 111:7861–7866CrossRefPubMedPubMedCentralGoogle Scholar
  63. Youssefian S, Kirby E, Gale M (1992) Pleiotropic effects of the GA-insensitive Rht dwarfing genes in wheat. 2. Effects on leaf, stem, ear and floret growth. Field Crop Res 28:191–210CrossRefGoogle Scholar
  64. Zeng X, Zhu L, Chen Y, Qi L, Pu Y, Wen J, Yi B, Shen J, Ma C, Tu J, Fu T (2011) Identification, fine mapping and characterisation of a dwarf mutant (bnaC.dwf) in Brassica napus. Theor Appl Genet 122:421–428CrossRefPubMedGoogle Scholar
  65. Zhang B, Liu C, Wang Y, Yao X, Wang F, Wu J, King GJ, Liu K (2015) Disruption of a CAROTENOID CLEAVAGE DIOXYGENASE 4 gene converts flower colour from white to yellow in Brassica species. New Phytol 206:1513–1526CrossRefPubMedGoogle Scholar
  66. Zhao F, Tian Z (2009) Research and utilization of dwarf or semi dwarf gene resources in rapeseed. Crop Res 23:157–160 (in Chinese)Google Scholar

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© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.National Key Laboratory of Crop Genetic ImprovementHuazhong Agricultural UniversityWuhanChina

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