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Molecular Breeding

, 39:40 | Cite as

Fine-mapping of a gene for the lobed leaf, BoLl, in ornamental kale (Brassica oleracea L. var. acephala)

  • Jie Ren
  • Zhiyong Liu
  • Jiangtao Du
  • Wei Fu
  • Ailin Hou
  • Hui FengEmail author
Article
  • 132 Downloads

Abstract

Leaf shape is an important agronomic trait of ornamental kale (Brassica oleracea L. var. acephala). In this study, we isolated a lobed-leaf DH line by microspore culture of ornamental kale. The genetic analysis indicated that the lobed-leaf trait was quantitatively inherited. By QTL-seq analysis, the candidate region for BoLl (lobed-leaf) was mapped on chromosome 9 (BRAD, Brassica oleracea, chromosome v1.0). The mapping region was confirmed and narrowed by simple sequence repeat (SSR) and insertion–deletion (Indel) markers in the F2 population; BoLl was located between the markers LYIn39 (0.17 cM) and LYIn40 (0.11 cM). According to the B. oleracea genome database (chromosome v1.0), the mapped interval (75.3 kb) contained eight genes, and seven of which were annotated in BRAD and one was not. According to the other B. oleracea genome information on EnsemblPlant, the mapped interval (79.6 kb) contained 11 genes. Two orthologous genes of AtLMI1/ATHB5 related to lobed leaves in Arabidopsis, Bol010029/Bo9g181710 (BRAD/EnsemblPlant) and Bol010030/Bo9g1181720, were identified as possible genes for BoLl, but the sequence analysis revealed no variation in their promoter and coding regions. The expression of Bol010029/Bo9g181710 and Bol010030/Bo9g1181720 was significantly higher in young lobed leaves than in young entire leaves. Among the other genes in the interval, only Bol010025 and Bol010031/Bo9g181730 showed co-dominance in the recombinant individuals, and their expression level was similar in lobed and entire leaves. Three hypotheses were proposed for the formation of lobed leaf. These results lay a foundation for uncovering the molecular mechanism of the lobed-leaf trait in ornamental kale.

Keywords

Kale. Fine-mapping BoLl Ornamental kale Lobed leaf 

Notes

Funding

This work was supported by the National Natural Science Foundation of China (grant number 31672144).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

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References

  1. Andres RJ, Bowman DT, Kaur B, Kuraparthy V (2014) Mapping and genomic targeting of the major leaf shape gene (L) in Upland cotton (Gossypium hirsutum L.). Theor Appl Genet 127:167–177CrossRefGoogle Scholar
  2. Andres RJ, Coneva V, Frank MH, Tuttle JR, Samayoa LF, Han SW, Kaur B, Zhu L, Fang H, Bowman DT, Rojas-Pierce M, Haigler CH, Jones DC, Holland JB, Chitwood DH, Kuraparthy V (2017) Modifications to a LATE MERISTEM IDENTITY1 gene are responsible for the major leaf shapes of Upland cotton (Gossypium hirsutum L.). Proc Natl Acad Sci U S A 114:E57–E66CrossRefGoogle Scholar
  3. Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40:1136–1141CrossRefGoogle Scholar
  4. Bell EM, Lin WC, Husbands AY, Yu L, Jaganatha V, Jablonska B, Mangeon A, Neff MM, Girke T, Springer PS (2012) Arabidopsis lateral organ boundaries negatively regulates brassinosteroid accumulation to limit growth in organ boundaries. Proc Natl Acad Sci U S A 109:21146–21151CrossRefGoogle Scholar
  5. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120CrossRefGoogle Scholar
  6. Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808CrossRefGoogle Scholar
  7. Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965PubMedGoogle Scholar
  8. Deng J, Wang H, Cheng F, Wu J, Wang XW (2012) QTL mapping of a leaf-lobed trait in Brassica campestris. Acta Horticulturae Sinica 39(4):661–668Google Scholar
  9. Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131:1101–1110CrossRefGoogle Scholar
  10. Feng X (2016) Genetic analysis and molecular markers of frathered leaved trait in ornamental kale. Dissertation, Shenyang Agriculture University, ChinaGoogle Scholar
  11. Gu WH, Zheng HJ, Zhang Y, Liu ZY (2002) A preliminary study on selection and breeding of new lines and main genetic characteristics of omamental kale. Journal of Shanghai Jiaotong University (Agricultural science) 20(2):129–132Google Scholar
  12. Guo M, Thomas J, Collins G, Timmermans MCP (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58CrossRefGoogle Scholar
  13. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG (2003) The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130:161–172CrossRefGoogle Scholar
  14. Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947CrossRefGoogle Scholar
  15. Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUP-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18:2946–2957CrossRefGoogle Scholar
  16. Hui MX (2011) Fine mapping of lobed-leafed gene and cloning and functional analysis of boundary-specific BsCUC1 and BcCUC3 gene from non-heading Vhinese cabbage (Brassica campeatris ssp. chinensis). Dissertation, Northwest A&F University, ChinaGoogle Scholar
  17. Ikezaki M, Kojima M, Sakakibara H, Kojima S, Ueno Y, Machida C, Machida Y (2010) Genetic networks regulated by ASYMMETRIC LEAVES1 (AS1) and AS2 in leaf development in Arabidopsis thaliana: KNOX genes control five morphological events. Plant J 61:70–82CrossRefGoogle Scholar
  18. Ishibashi N, Kanamaru K, Ueno Y, Kojima S, Kobayashi T, Machida C, Machida Y (2012) ASYMMETRIC-LEAVES2 and an ortholog of eukaryotic NudC domain proteins repress expression of AUXIN-RESPONSE-FACTOR and class 1 KNOX homeobox genes for development of flat symmetric leaves in Arabidopsis. Biol Open 1:197–207CrossRefGoogle Scholar
  19. Kamiuchi Y, Yamamoto K, Furutani M, Tasaka M, Aida M (2014) The CUC1 and CUC2 genes promote carpel margin meristem formation during Arabidopsis gynoecium development. Front Plant Sci 5:165CrossRefGoogle Scholar
  20. Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360CrossRefGoogle Scholar
  21. Kosambi DD (1943) THE ESTIMATION OF MAP DISTANCES FROM RECOMBINATION VALUES. Ann Hum Genet 12:172–175Google Scholar
  22. Koyama T, Mitsuda N, Seki M, Shinozaki K, Ohmetakagi M (2010) TCP transcription factors regulate the activities of ASYMMETRIC LEAVES1 and miR164, as well as the auxin response, during differentiation of leaves in Arabidopsis. Plant Cell 22:3574–3588CrossRefGoogle Scholar
  23. Kumar R, Kushalappa K, Godt D, Pidkowich MS, Pastorelli S, Hepworth SR, Haughn GW (2007) The Arabidopsis BEL1-LIKE HOMEODOMAIN proteins SAW1 and SAW2 act redundantly to regulate KNOX expression spatially in leaf margins. Plant Cell 19:2719–2735CrossRefGoogle Scholar
  24. Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359CrossRefGoogle Scholar
  25. Li C, Guan Z, Liu D, Raetz CR (2011) Pathway for lipid a biosynthesis in Arabidopsis thaliana resembling that of Escherichia coli. Proc Natl Acad Sci U S A 108:11387–11392CrossRefGoogle Scholar
  26. Liu S, Liu Y, Yang X, Tong C, Edwards D, Parkin IA, Zhao M, Ma J, Yu J, Huang S (2014) The Brassica oleracea genome reveals the asymmetrical evolution of polyploid genomes. Nat Commun 5:3930CrossRefGoogle Scholar
  27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  28. Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325CrossRefGoogle Scholar
  29. Ni X, Huang J, Ali B, Zhou W, Zhao J (2015) Genetic analysis and fine mapping of the LOBED - LEAF 1 (BnLL1) gene in rapeseed (Brassica napus L.). Euphytica 204:29–38CrossRefGoogle Scholar
  30. Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132:2203–2213CrossRefGoogle Scholar
  31. Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122CrossRefGoogle Scholar
  32. Peppe DJ, Royer DL, Cariglino B, Oliver SY, Newman S, Leight E, Enikolopov G, Fernandez-Burgos M, Herrera F, Adams JM, Correa E, Currano ED, Erickson JM, Hinojosa LF, Hoganson JW, Iglesias A, Jaramillo CA, Johnson KR, Jordan GJ, Kraft NJ, Lovelock EC, Lusk CH, Niinemets U, Penuelas J, Rapson G, Wing SL, Wright IJ (2011) Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytol 190:724–739CrossRefGoogle Scholar
  33. Piazza P, Bailey CD, Cartolano M, Krieger J, Cao J, Ossowski S, Schneeberger K, He F, De MJ, Hall N (2010) Arabidopsis thaliana leaf form evolved via loss of KNOX expression in leaves in association with a selective sweep. Curr Biol 20:2223–2228CrossRefGoogle Scholar
  34. Saddic LA, Huvermann B, Bezhani S, Su Y, Winter CM, Kwon CS, Collum RP, Wagner D (2006) The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development 133:1673–1682CrossRefGoogle Scholar
  35. Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001) KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev 15:581–590CrossRefGoogle Scholar
  36. Sanguinetti CJ, Dias NE, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914–921PubMedGoogle Scholar
  37. Semchenko M, Zobel K (2007) The role of leaf lobation in elongation responses to shade in the rosette-forming forb Serratula tinctoria (Asteraceae). Ann Bot 100:83–90CrossRefGoogle Scholar
  38. Seveno M, Seveno-Carpentier E, Voxeur A, Menu-Bouaouiche L, Rihouey C, Delmas F, Chevalier C, Driouich A, Lerouge P (2010) Characterization of a putative 3-deoxy-D-manno-2-octulosonic acid (Kdo) transferase gene from Arabidopsis thaliana. Glycobiology 20:617–628CrossRefGoogle Scholar
  39. Sicard A, Thamm A, Marona C, Lee YW, Wahl V, Stinchcombe JR, Wright SI, Kappel C, Lenhard M (2014) Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene. Curr Biol 24:1880–1886CrossRefGoogle Scholar
  40. Sinha N (2004) Shaping up: the genetic control of leaf shape. Curr Opin Plant Biol 7:65–72CrossRefGoogle Scholar
  41. Streubel S, Fritz MA, Teltow M, Kappel C, Sicard A (2018) Successive duplication-divergence mechanisms at the RCO locus contributed to leaf shape diversity in the Brassicaceae. Development 145:dev164301CrossRefGoogle Scholar
  42. Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183CrossRefGoogle Scholar
  43. Takahashi H, Iwakawa H, Ishibashi N, Kojima S, Matsumura Y, Prananingrum P, Iwasaki M, Takahashi A, Ikezaki M, Luo L (2013) Meta-analyses of microarrays of Arabidopsis asymmetric leaves1 (as1), as2 and their modifying mutants reveal a critical role for the ETT pathway in stabilization of adaxial-abaxial patterning and cell division during leaf development. Plant Cell Physiol 54:418–431CrossRefGoogle Scholar
  44. Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49:547–555CrossRefGoogle Scholar
  45. Tu YQ, Sun J, Dai XL, Tang J, Tu WF, Shao HQ (2013) Character and genetic analysis of lobed-leaf traits in Brassica napus. Chin J Oil Crop Sci 35:93–96Google Scholar
  46. Vlad D, Kierzkowski D, Rast MI, Vuolo F, Dello Ioio R, Galinha C, Gan X, Hajheidari M, Hay A, Smith RS, Huijser P, Bailey CD, Tsiantis M (2014) Leaf shape evolution through duplication, regulatory diversification, and loss of a homeobox gene. Science 343:780–783CrossRefGoogle Scholar
  47. Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytol 183:13–26CrossRefGoogle Scholar
  48. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78CrossRefGoogle Scholar
  49. Vuolo F, Mentink RA, Hajheidari M, Bailey CD, Filatov DA, Tsiantis M (2016) Coupled enhancer and coding sequence evolution of a homeobox gene shaped leaf diversity. Genes Dev 30:2370–2375CrossRefGoogle Scholar
  50. Xie LN (2003) Studies on the inheritance of leaf color and leaf type and the mechanism of self incompatibility in Kale. Dissertation, Northeast Forestry University, ChinaGoogle Scholar
  51. Yan ZY (2011) Inheritance of mosaic-leaf trait in Brassica napus and its gene mapping. Dissertation, Huazhong Agricultural University, ChinaGoogle Scholar
  52. Zhang LN, Shen XQ (2007) A preliminary study on the inheritance of leaf shape of kale. Northern Horticulture:108–109Google Scholar
  53. Zhu P, Feng X, Cheng M, Pan Z, University SA (2016a) Genetic analysis of feathered-leaved related traits in Brassica oleracea var. acephala. Acta Botan Boreali-Occident Sin 36(2):0288–0295Google Scholar
  54. Zhu QH, Zhang J, Liu D, Stiller W, Liu D, Zhang Z, Llewellyn D, Wilson I (2016b) Integrated mapping and characterization of the gene underlying the okra leaf trait in Gossypium hirsutum L. J Exp Bot 67(3):763–774CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of HorticultureShenyang Agricultural UniversityShenyangChina

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