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

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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.

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References

  • 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 127:167–177

    Article  CAS  Google Scholar 

  • 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–E66

    Article  CAS  Google Scholar 

  • Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nat Genet 40:1136–1141

    Article  CAS  Google Scholar 

  • 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 109:21146–21151

    Article  CAS  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  Google Scholar 

  • Borghi L, Bureau M, Simon R (2007) Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. Plant Cell 19:1795–1808

    Article  CAS  Google Scholar 

  • Byrne ME, Simorowski J, Martienssen RA (2002) ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development 129:1957–1965

    CAS  PubMed  Google Scholar 

  • 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):661–668

    CAS  Google Scholar 

  • Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131:1101–1110

    Article  CAS  Google Scholar 

  • Feng X (2016) Genetic analysis and molecular markers of frathered leaved trait in ornamental kale. Dissertation, Shenyang Agriculture University, China

  • 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):129–132

    Google Scholar 

  • Guo M, Thomas J, Collins G, Timmermans MCP (2008) Direct repression of KNOX loci by the ASYMMETRIC LEAVES1 complex of Arabidopsis. Plant Cell 20:48–58

    Article  CAS  Google Scholar 

  • 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 130:161–172

    Article  CAS  Google Scholar 

  • Hay A, Tsiantis M (2006) The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nat Genet 38:942–947

    Article  CAS  Google Scholar 

  • 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 18:2946–2957

    Article  CAS  Google Scholar 

  • 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, China

  • 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 61:70–82

    Article  CAS  Google Scholar 

  • 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 1:197–207

    Article  CAS  Google Scholar 

  • 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 5:165

    Article  Google Scholar 

  • Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360

    Article  CAS  Google Scholar 

  • Kosambi DD (1943) THE ESTIMATION OF MAP DISTANCES FROM RECOMBINATION VALUES. Ann Hum Genet 12:172–175

    Google Scholar 

  • 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 22:3574–3588

    Article  CAS  Google Scholar 

  • 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 19:2719–2735

    Article  CAS  Google Scholar 

  • Langmead B, Salzberg SL (2012) Fast gapped-read alignment with bowtie 2. Nat Methods 9:357–359

    Article  CAS  Google Scholar 

  • 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 108:11387–11392

    Article  CAS  Google Scholar 

  • 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 5:3930

    Article  CAS  Google Scholar 

  • 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 25:402–408

    Article  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  Google Scholar 

  • 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 204:29–38

    Article  CAS  Google Scholar 

  • Norberg M, Holmlund M, Nilsson O (2005) The BLADE ON PETIOLE genes act redundantly to control the growth and development of lateral organs. Development 132:2203–2213

    Article  CAS  Google Scholar 

  • Ohno CK, Reddy GV, Heisler MG, Meyerowitz EM (2004) The Arabidopsis JAGGED gene encodes a zinc finger protein that promotes leaf tissue development. Development 131:1111–1122

    Article  CAS  Google Scholar 

  • 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 190:724–739

    Article  Google Scholar 

  • 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 20:2223–2228

    Article  CAS  Google Scholar 

  • 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 133:1673–1682

    Article  CAS  Google Scholar 

  • 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 15:581–590

    Article  CAS  Google Scholar 

  • Sanguinetti CJ, Dias NE, Simpson AJ (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Biotechniques 17:914–921

    CAS  PubMed  Google Scholar 

  • 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 100:83–90

    Article  Google Scholar 

  • 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 20:617–628

    Article  CAS  Google Scholar 

  • 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 24:1880–1886

    Article  CAS  Google Scholar 

  • Sinha N (2004) Shaping up: the genetic control of leaf shape. Curr Opin Plant Biol 7:65–72

    Article  Google Scholar 

  • 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:dev164301

    Article  Google Scholar 

  • 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 74:174–183

    Article  CAS  Google Scholar 

  • 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 54:418–431

    Article  CAS  Google Scholar 

  • Tsukaya H (2005) Leaf shape: genetic controls and environmental factors. Int J Dev Biol 49:547–555

    Article  Google Scholar 

  • 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 35:93–96

    Google Scholar 

  • 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 343:780–783

    Article  CAS  Google Scholar 

  • Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytol 183:13–26

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  Google Scholar 

  • 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 30:2370–2375

    Article  CAS  Google Scholar 

  • 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, China

  • Yan ZY (2011) Inheritance of mosaic-leaf trait in Brassica napus and its gene mapping. Dissertation, Huazhong Agricultural University, China

  • Zhang LN, Shen XQ (2007) A preliminary study on the inheritance of leaf shape of kale. Northern Horticulture:108–109

  • 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):0288–0295

    Google Scholar 

  • 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):763–774

    Article  CAS  Google Scholar 

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

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Correspondence to Hui Feng.

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Ren, J., Liu, Z., Du, J. et al. Fine-mapping of a gene for the lobed leaf, BoLl, in ornamental kale (Brassica oleracea L. var. acephala). Mol Breeding 39, 40 (2019). https://doi.org/10.1007/s11032-019-0944-0

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