Abstract
Key message
BoFL, a candidate gene conferring the feathered-leaved trait in ornamental kale, is located in a 374.532-kb region on chromosome C9.
Abstract
Leaf shape is an important economic trait in ornamental kale (Brassica oleracea var. acephala). Identifying the genes that influence leaf shape would provide insight into the mechanism underlying leaf development. In this study, we constructed F1, F2, BC1P1, BC1P2, and F2:3 populations from a cross between a feathered-leaved inbred line, F0819, and a smooth-leaved inbred line, S0835, of ornamental kale. Genetic analysis showed that the feathered-leaved trait was controlled by a semi-dominant gene, BoFL. Using bulked segregant analysis sequencing, we mapped the BoFL gene to a 4.17-Mb interval on chromosome C9. Next, we narrowed down the candidate region to 374.532-kb by fine-scale mapping between the two flanking markers INDEL940 and INDEL5443. We identified 38 genes in the candidate region, among which only Bo9g184610 showed significant variation in expression level between the two parental lines. Sequencing of the gene in the parental lines identified three single-nucleotide polymorphism (SNP) differences, containing two nonsynonymous and one synonymous SNPs, which resulted in coding variations of an aspartate and a phenylalanine residue in F0819, but an alanine and a leucine residue in S0835. A cleaved amplified polymorphic sequence (CAPS) marker, CAPS4610, corresponding to the first nonsynonymous SNP co-segregated with the leaf shape trait. We thus speculated that the gene conferring the feathered-leaved trait is BoALG10, a homolog of ALG10, which encodes an alpha-1,2-glucosyltransferase in Arabidopsis thaliana. This work will be useful for understanding the mechanism of leaf development and provides important information for the breeding of kale with novel leaf shapes.
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References
Abe A, Kosugi S, Yoshida K, Natsume S, Takagi H, Kanzaki H, Matsumura H, Yoshida K, Mitsuoka C, Tamiru M (2012) Genome sequencing reveals agronomically important loci in rice using MutMap. Nat Biotechnol 30:174–178
Aguilar-Martínez JA, Neelima S (2013) Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development. Front Plant Sci 4:406
Andres RJ, Coneva V, Frank MH, Tuttle JR, Samayoa LF, Hand SW, Kaur B, Zhu L, Fang H, Bowman DT, Rojas-Pierced M, Haigler CH, Jonese 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 USA 114:E57–E66
Bar M, Ori N (2015) Compound leaf development in model plant species. Curr Opin Plant Biol 23:61–69
Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR (2002) Homologies in leaf form inferred from KNOXI gene expression during development. Science 296:1858–1860
Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M (2011) Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci USA 108:3424–3429
Bresso EG, Chorostecki U, Rodriguez RE, Palatnik JF, Schommer C (2017) Spatial control of gene expression by miR319-regulated TCP transcription factors in leaf development. Plant Physiol 176:1694–1708
Burda P, Aebi M (1999) The dolichol pathway of N-linked glycosylation. Biochim Biophys Acta 1426:239–257
Champagne CEM, Goliber TE, Wojciechowski MF, Mei RW, Townsley BT, Wang K, Paz MM, Geeta R, Sinha NR (2007) Compound leaf development and evolution in the legumes. Plant Cell 19:3369–3378
Cheng F, Wu J, Fang L, Wang X (2012) Syntenic gene analysis between Brassica rapa and other Brassicaceae species. Front Plant Sci 3:198
Dkhar J, Pareek A (2014) What determines a leaf’s shape? Evodevo 5:47
Eshed Y, Izhaki A, Baum SF, Floyd S, Bowman J (2004) Asymmetric leaf development and blade expansion in Arabidopsisare mediated by KANADI and YABBY activities. Development 131:2997–3006
Farid A, Pabst M, Schoberer J, Altmann F, Josef G, Strasser R (2011) Arabidopsis thaliana alpha1,2-glucosyltransferase (ALG10) is required for efficient N-glycosylation and leaf growth. Plant J 68:314–325
Gao X, Ning X, Wang Y, Wang Y, Wang X, Yan W, Zhang Z, Li G (2014) Fine mapping of a gene that confers palmately lobed leaf (pll) in melon (Cucumis melo L.). Euphytica 200:337–347
Gu W, Zheng J, Zhang Y, Liu Z (2002) A preliminary study on selection and breeding of new lines and main genetic characteristics of omamental kale. J Shanghai Jiao Tong Univ (Agric Sci) 20:129–132 (in Chinese)
Hasson A, Plessis A, Blein T, Adroher B, Grigg S, Tsiantis M, Boudaoud A, Damerval C, Laufs P (2011) Evolution and diverse roles of the cup-shaped cotyledon genes in Arabidopsis leaf development. Plant Cell 23:54–68
Hay A, Tsiantis M (2010) KNOX genes: versatile regulators of plant development and diversity. Development 137:3153–3165
Hay A, Barkoulas M, Tsiantis M (2006) ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis. Development 133:3955–3961
Hibara K, Karim MR, Takada S, Taoka K, Furutani M, Aida M, Tasaka M (2006) Arabidopsis CUC-SHAPED COTYLEDON3 regulates postembryonic shoot meristem and organ boundary formation. Plant Cell 18:2946–2957
Jiao K, Li X, Guo W, Yuan X, Cui X, Chen X (2016) Genome re-sequencing of two accessions and fine mapping the locus of lobed leaflet margins in mungbean. Mol Breed 36:128
Kierzkowski D, Runions A, Vuolo F, Strauss S, Lymbouridou R, Routier-Kierzkowska AL, Wilson-Sanchez D, Jenke H, Galinha C, Mosca G, Zhang Z, Canales C, Dello Ioio R, Huijser P, Smith RS, Tsiantis M (2019) A growth-based framework for leaf shape development and diversity. Cell 177:1–14
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760
Li Z, Li B, Shen W, Huang H, Dong A (2012) TCP transcription factors interact with AS2 in the repression of class-I KNOX genes in Arabidopsis thaliana. Plant J 71:99–107
Liebminger E, Grass J, Jez J, Neumann L, Altmann F, Strasser R (2012) Myrosinases TGG1 and TGG2 from Arabidopsis thaliana contain exclusively oligomannosidic N-glycans. Phytochemistry 84:24–30
Liu W, Kang J, Jeong H, Choi HJ, Yang H, Kim KT, Choi D, Choi GJ, Jahn M, Kang BC (2014) Combined use of bulked segregant analysis and microarrays reveals SNP markers pinpointing a major QTL for resistance to Phytophthora capsici in pepper. Theor Appl Genet 127:2503–2513
Liu X, Gao B, Han F, Fang Z, Yang L, Zhuang M, Lv H, Liu Y, Li Z, Cai C, Yu H, Li Z, Ya Zhang (2017) Genetics and fine mapping of a purple leaf gene, BoPr, in ornamental kale (Brassica oleracea L. var. acephala). BMC Genom 18:230
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−△△CT method. Methods 25:402–408
Matsumura Y, Iwakawa H, Machida Y, Machida C (2009) Characterization of genes in the ASYMMETRIC LEAVES2/LATERAL ORGAN BOUNDARIES (AS2/LOB) family in Arabidopsis thaliana, and functional and molecular comparisons between AS2 and other family members. Plant J 58:525–537
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
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
Ni X, Liu H, Huang J, Zhao J (2017) LMI1-like genes involved in leaf margin development of Brassica napus. Genetica 145:269–274
Nicotra AB, Leigh A, Boyce CK, Jones DC, Niklas EK, Royer FD, Tsukaya H (2011) The evolution and functional significance of leaf shape in the angiosperms. Funct Plant Biol 38:535–552
Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufsa P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2954
Ori N, Cohen AR, Etzioni A, Brand A, Yanai O, Shleizer S, Menda N, Amsellem Z, Efroni I, Pekker I, Alvarez J, Blum E, Zamir D, Eshed Y (2007) Regulation of LANCEOLATE by miR319 is required for compound-leaf development in tomato. Nat Genet 39:787–791
Parkin IAP, Koh C, Tang H, Robinson SJ, Kagale S, Clarke WE, Town CD, Nixon J, Krishnakumar V, Bidwell SL, Denoeud F, Belcram H, Links MG, Just J, Clarke C, Bender T, Huebert T, Mason AS, Pires JC, Barker G, Moore J, Walley PG, Manoli S, Batley J, Edwards D, Nelson MN, Wang X, Paterson AH, King G, Bancroft I, Chalhoub B, Sharpe AG (2014) Transcriptome and methylome profiling reveals relics of genome dominance in the mesopolyploid Brassica oleracea. Genome Biol 15:R77
Ren J, Liu Z, Niu R, Feng H (2015) Mapping of Re, a gene conferring the red leaf trait in ornamental kale (Brassica oleracea L. var. acephala). Plant Breed 134:494–500
Ren J, Fu W, Du J, Hou A, Liu Z, Feng H (2017) Identification of a candidate gene for Re, the factor determining the red leaf phenotype in ornamental kale using fine mapping and transcriptome analysis. Plant Breed 136:738–748
Ren J, Liu Z, Du J, Fu W, Hou A, Feng H (2019) Fine-mapping of a gene for the lobed leaf, BoLl, in ornamental kale (Brassica oleracea L. var. acephala). Mol Breed 39:40
Richard S (2016) Plant protein glycosylation. Glycobiology 26:926–939
Runions A, Tsiantis M, Prusinkiewicz P (2017) A common developmental programme can produce diverse leaf shapes. New Phytol 216:401–418
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
Saito F, Suyama A, Oka T, Yoko-o T, Matsuoka K, Jigami Y, Shimma Y (2014) Identification of novel Peptidyl Serine α-galactosyltransferase gene family in plants. J Biol Chem 289:20405–20420
Sarvepalli K, Nath U (2011) Interaction of TCP4-mediated growth module with phytohormones. Plant Signal Behav 6:1440–1443
Shleizerburko S, Burko Y, Benherzel O, Ori N (2011) Dynamic growth program regulated by LANCEOLATE enables flexible leaf patterning. Development 138:695–704
Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: JoinMap. Plant J 3:739–744
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
Tsukaya H (2006) Mechanism of leaf-shape determination. Annu Rev Plant Biol 57:477–496
Tsukaya H (2013) Leaf development. In: Arabidopsis Book 11:e0163
Vlad D, Kierzkowski D, Rast MI, Vuolo F, Ioio RD, 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
Vogel S (2009) Leaves in the lowest and highest winds: temperature, force and shape. New Phytol 183:13–26
Wang K, Li M, Hakonarson H (2010) ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res 38:e164
Wang W, Xu B, Wang H, Li J, Huang H, Xu L (2011) YUCCA genes are expressed in response to leaf adaxial-abaxial juxtaposition and are required for leaf margin development. Plant Physiol 157:1805–1819
Wang N, Liu Z, Zhang Y, Li C, Feng H (2017) Identification and fine mapping of a stay-green gene (Brnye1) in pakchoi (Brassica campestris L. ssp. chinensis). Theor Appl Genet 131:673–684
Wei C, Chen X, Wang Z, Liu Q, Li H, Zhang Y, Ma J, Yang J, Zhang X (2017) Genetic mapping of the LOBED LEAF 1 (ClLL1) gene to a 127.6-kb region in watermelon (Citrullus lanatus L.). Plos One 12:e0180741
Weiss D, Ori N (2007) Mechanisms of cross talk between gibberellin and other hormones. Plant Physiol 144:1240–1246
Win KT, Vegas J, Zhang C, Song K, Lee S (2017) QTL mapping for downy mildew resistance in cucumber via bulked segregant analysis using next-generation sequencing and conventional methods. Theor Appl Genet 130:199–211
Xie Q, Chen G, Chen X, Deng L, Liu Q, Zhang Y, Hu Z (2014) Jointly silencing BoDWARF, BoGA20ox and BoSP (SELF-PRUNING) produces a novel miniature ornamental Brassica oleracea var. acephala f. tricolor variety. Mol Breed 34:99–113
Zhang L, Shen X (2007) Preliminary study on genetic regularity of kale leaf shaped characters. Northern Horticul 2:108–109 (in Chinese)
Zhu P, Cheng M, Feng X, Xiong Y, Liu C, Kang Y (2016) Mapping of Pi, a gene conferring pink leaf in ornamental kale (Brassica oleracea L. var. acephala DC). Euphytica 207:377–385
Zhu P, Tian Z, Pan Z, Feng X (2017) Identification and quantification of anthocyanins in different coloured cultivars of ornamental kale (Brassica oleracea L. var. acephala DC). J Hortic Sci Biotechnol 93:466–473
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This research was supported by the National Natural Science Foundation of China (31770739).
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PZ designed the experiments. XF conducted the experiments and performed data analysis. XF and PZ wrote the manuscript. XL and XY participated in genetical population phenotypes investigation and PCR experiments. All authors have read and approved the manuscript.
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Feng, X., Li, X., Yang, X. et al. Fine mapping and identification of the leaf shape gene BoFL in ornamental kale. Theor Appl Genet 133, 1303–1312 (2020). https://doi.org/10.1007/s00122-020-03551-x
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DOI: https://doi.org/10.1007/s00122-020-03551-x