Skip to main content

Transcriptomic analysis of contrasting inbred lines and F2 segregant of Chinese cabbage provides valuable information on leaf morphology

Genes & Genomics volume 41, pages 811–829 (2019)Cite this article

Abstract

Background

Leaf morphology influences plant growth and productivity and is controlled by genetic and environmental cues. The various morphotypes of Brassica rapa provide an excellent resource for genetic and molecular studies of morphological traits.

Objective

This study aimed to identify genes regulating leaf morphology using segregating B. rapa p F2 population.

Methods

Phenotyping and transcriptomic analyses were performed on an F2 population derived from a cross between Rapid cycling B. rapa (RCBr) and B. rapa ssp. penkinensis, inbred line Kenshin. Analyses focused on four target traits: lamina (leaf) length (LL), lamina width (LW), petiole length (PL), and leaf margin (LM).

Results

All four traits were controlled by multiple QTLs, and expression of 466 and 602 genes showed positive and negative correlation with leaf phenotypes, respectively. From this microarray analysis, large numbers of genes were putatively identified as leaf morphology-related genes. The Gene Ontology (GO) category containing the highest number of differentially expressed genes (DEGs) was “phytohormones”. The sets of genes enriched in the four leaf phenotypes did not overlap, indicating that each phenotype was regulated by a different set of genes. The expression of BrAS2, BrAN3, BrCYCB1;2, BrCYCB2;1,4, BrCYCB3;1, CrCYCBD3;2, BrULT1, and BrANT seemed to be related to leaf size traits (LL and LW), whereas BrCUC1, BrCUC2, and BrCUC3 expression for LM trait.

Conclusion

An analysis integrating the results of the current study with previously published data revealed that Kenshin alleles largely determined LL and LW but LM resulted from RCBr alleles. Genes identified in this study could be used to develop molecular markers for use in Brassica breeding projects and for the dissection of gene function.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  • Albinsky D, Kusano M, Higuchi M, Hayashi N, Kobayashi M, Fukushima A, Mori M, Ichikawa T, Matsui K, Kuroda H, Horii Y, Tsumoto Y, Sakakibara H, Hirochika H, Matsui M, Saito K (2010) Metabolomic screening applied to rice FOX Arabidopsis lines leads to the identification of a gene-changing nitrogen metabolism. Mol Plant 3:125–142

    Article  CAS  PubMed  Google Scholar 

  • Arenas-M A, Zehrmann A, Moreno S, Takenaka M, Jordana X (2014) The pentatricopeptide repeat protein MEF26 participates in RNA editing in mitochondrial cox3 and nad4 transcripts. Mitochondrion 19(Pt B):126–134

    Article  CAS  PubMed  Google Scholar 

  • Ashburner M. Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bar M, Ori N (2014) Leaf development and morphogenesis. Development 141:4219–4230

    Article  CAS  PubMed  Google Scholar 

  • Barkoulas M, Galinha C, Grigg SP, Tsiantis M (2007) From genes to shape: regulatory interactions in leaf development. Curr Opin Plant Biol 10:660–666

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Bolstad BM, Irizarry RA, Ǻstrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19:185–193

    Article  CAS  Google Scholar 

  • Bonnema G, Carpio DPD, Zhao JJ (2011) Diversity analysis and molecular taxonomy of Brassica vegetable crops. In: Kole C, Sadowski J (eds) Genetics, genomics and breeding of crop plants. Science Publishers, pp 81–124

  • Brown DM, Zhang Z, Stephens E, Dupree P, Turner SR (2009) Characterization of IRX10 and IRX10-like reveals an essential role in glucuronoxylan biosynthesis in Arabidopsis. Plant J 57:732–746

    Article  CAS  PubMed  Google Scholar 

  • Cavalier DM, Lerouxel O, Neumetzler L, Yamauchi K, Reinecke A, Freshour G, Zabotina OA, Hahn MG, Burgert I, Pauly M, Raikhel NV, Keegstra K (2008) Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell 20:1519–1537

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cha YK, Liu L, Kim JY (2007) Signaling network for stem cell maintenance and functioning in Arabidopsis shoot apical meristem. J Plant Biol 50:274–281

    Article  Google Scholar 

  • Choi SR, Yu X, Dhandapani V, Li X, Wang Z, Lee SY, Oh SH, Pang W, Ramchiary N, Hong CP, Park S, Piao Z, Kim H, Lim YP (2017) Integrated analysis of leaf morphological and color traits in different populations of Chinese cabbage (Brassica rapa ssp. pekinensis). Theor Appl Genet 130:1617–1634

    Article  PubMed  Google Scholar 

  • Cosgrove DJ (2005) Growth of the plant cell wall. Nat Rev Mol Cell Biol 6:850–861

    Article  CAS  Google Scholar 

  • Du Z, Zhou X, Ling Y, Zhang Z, Su Z (2010) agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res 38:W64–W70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, Bodt SD, Bossche RV, Milde LD, Yoshizumi T, Matsui M, Inzé D (2013) ETHYLENE RESPONSE FACTOR6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol 162:319–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2005) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103:236–241

    Article  CAS  PubMed  Google Scholar 

  • Fambrini M, Pugliesi C (2013) Usual and unusual development of the dicot leaf: involvement of transcription factors and hormones. Plant Cell Rep 32:899–922

    Article  CAS  PubMed  Google Scholar 

  • Fisher K, Southall SM, Wilson JR, Poulin GB (2010) Methylation and demethylation activities of a C. elegans MLL-like complex attenuate RAS signalling. Dev Biol 341:142–153

    Article  CAS  PubMed  Google Scholar 

  • Geldermann H (1975) Investigations on inheritance of quantitative characters in animals by gene markers. Theor Appl Genet 46:319–330

    Article  CAS  PubMed  Google Scholar 

  • Goldman IL (1999) Teaching recurrent selection in the classroom with Wisconsin fast plants. Hort Technol 9:579–584

    Article  Google Scholar 

  • Gonzalez N, De Bodt S, Sulpice R, Jikumaru Y, Chae E, Dhondt S, Van Daele T, De Milde L, Weigel D, Kamiya Y, Stitt M, Beemster GT, Inzé D (2010) Increased leaf size: Different means to an end. Plant Physiol 153:1261–1279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gonzalez N, Vanhaeren H, Inzé D (2012) Leaf size control: complex coordination of cell division and expansion. Trends Plant Sci 17:332–340

    Article  CAS  PubMed  Google Scholar 

  • Hare PD, Moller SG, Huang LF, Chua NH (2003) LAF3, a novel factor required for normal phytochrome A signaling. Plant Physiol 133:1592–1604

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hay A, Tsiantis M (2010) KNOX genes: Versatile regulators of plant development and diversity. Development 137:3153–3165

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Huang L, Yang Y, Zhang F, Cao J (2017) A genome-wide SNP-based genetic map and QTL mapping for agronomic traits in Chinese cabbage. Sci Rep 7:46305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichihashi Y, Kawade K, Usami T, Horiguchi G, Takahashi T, Tsukaya H (2011) Key proliferative activity in the junction between the leaf blade and leaf petiole of Arabidopsis. Plant Physiol 157:1151–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Irizarry TA, Bolstad BM, Collin F, Cope RM, Hobbs B, Speed TP (2003) Summaries of Affymetrix GeneChip prove level data. Nucleic Acids Res 31:e15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iwakawa H, Iwasaki M, Kojima S, Ueno Y, Soma T, Tanaka H, Semiarti E, Machida Y, Machida C (2007) Expression of the ASYMMETRIC LEAVES2 gene in the adaxial domain of Arabidopsis leaves represses cell proliferation in this domain and is critical for the development of properly expanded leaves. Plant J 51:173–184

    Article  CAS  PubMed  Google Scholar 

  • Jung HJ, Dong X, Park JI, Thamilarasan SK, Lee SS, Kim YK, Lim YP, Nou IS, Hur Y (2014) Genome-wide transcriptome analysis of two contrasting Brassica rapa doubled haploid lines under cold-stresses using Br135K oligomeric chip. PLoS One 9:e106069

    Article  PubMed  PubMed Central  Google Scholar 

  • Kalve S, De Vos D, Beemster GT (2014) Leaf development: a cellular perspective. Front Plant Sci 5:1–25

    Article  Google Scholar 

  • Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:D480–D484

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kim GT, Cho KH (2006) Recent advances in the genetic regulation of the shape of simple leaves. Physiol Plant 126:494–502

    CAS  Google Scholar 

  • Kim GT, Fujioka S, Kozuka T, Tax FE, Takatsuto S, Yoshida S, Tsukaya H (2005) CYP90C1 and CYP90D1 are involved in different steps in the brassinosteroid biosynthesis pathway in Arabidopsis thaliana. Plant J 41:710–721

    Article  CAS  PubMed  Google Scholar 

  • Kozuka T, Horiguchi G, Kim GT, Ohgishi M, Sakai T, Tsukaya H (2005) The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by photoreceptors and sugar. Plant Cell Physiol 46:213–223

    Article  CAS  PubMed  Google Scholar 

  • Kozuka T, Kobayashi J, Horiguchi G, Demura T, Sakakibara H, Tsukaya H, Nagatani A (2010) Involvement of auxin and brassinosteroid in the regulation of petiole elongation under the shade. Plant Physiol 153:1608–1618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kryvych S, Nikiforova V, Herzog M, Perazza D, Fisahn J (2008) Gene expression profiling of the different stages of Arabidopsis thaliana trichome development on the single cell level. Plant Physiol Biochem 46:160–173

    Article  CAS  PubMed  Google Scholar 

  • Li F, Kitashiba H, Inaba K, Nishio T (2009) A Brassica rapa linkage map of EST-based SNP markers for identification of candidate genes controlling flowering time and leaf morphological traits. DNA Res 16:311–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Ramchiary N, Dhandapani V, Choi SR, Hur Y, Nou IS, Yoon MK, Lim YP (2013) Quantitative trait loci mapping in Brassica rapa revealed the structural and functional conservation of genetic loci governing morphological and yield component traits in the A, B, and C subgenomes of Brassica species. DNA Res 20:1–16

    Article  CAS  PubMed  Google Scholar 

  • Li X, Wang W, Wang Z, Li K, Lim YP, Piao Z (2015) Construction of chromosome segment substitution lines enables QTL mapping for flowering and morphological traits in Brassica rapa. Front Plant Sci 6:432

    PubMed  PubMed Central  Google Scholar 

  • Li Z, Li B, Liu J, Guo Z, Liu Y, Li Y, Shen WH, Huang Y, Huang H, Zhang Y, Dong A (2016) Transcription factors AS1 and AS2 interact with LHP1 to repress KNOX genes in Arabidopsis. J Integr Plant Biol 58:959–970

    Article  CAS  PubMed  Google Scholar 

  • Lo SF, Yang SY, Chen KT, Hsing YI, Zeevaart JA, Chen LJ, Yub SM (2008) A Novel class of gibberellin 2-Oxidases control semidwarfism, tillering, and root development in rice. Plant Cell 20:2603–2618

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lou P, Zhao J, Kim JS, Shen S, Del Carpio DP, Song X, Jin M, Vreugdenhil D, Wang X, Koornneef M, Bonnema G (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 58:4005–4016

    Article  CAS  PubMed  Google Scholar 

  • Magyar Z, De Veylder L, Atanassova A, Bakó L, Inzé D, Bögre L (2005) The role of the Arabidopsis E2FB transcription factor in regulating auxin-dependent cell division. Plant Cell 17:2527–2541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menke FL, Champion A, Kijne JW, Memelink J (1999) A novel jasmonate- and elicitor-responsive element in the periwinkle secondary metabolite biosynthetic gene Str interacts with a jasmonate- and elicitor-inducible AP2-domain transcription. EMBO J 18:4455–4463

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Micol JL (2009) Leaf development: time to turn over a new leaf? Curr Opin Plant Biol 12:9–16

    Article  CAS  PubMed  Google Scholar 

  • Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103:16598–16603

    Article  CAS  PubMed  Google Scholar 

  • Nikovics K, Blein T, Peaucelle A, Ishida T, Morin H, Aida M, Laufs P (2006) The balance between the MIR164A and CUC2 genes controls leaf margin serration in Arabidopsis. Plant Cell 18:2929–2945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park YB, Cosgrove DJ (2012) Changes in cell wall biomechanical properties in the xyloglucan-deficient xxt1/xxt2 mutant of Arabidopsis. Plant Physiol 158:465–475

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Pérez JM, Esteve-Bruna D, Micol JL (2010) QTL analysis of leaf architecture. J Plant Res 123:15–23

    Article  PubMed  Google Scholar 

  • Pike S, Patel A, Stacey G, Gassmann W (2009) Arabidopsis OPT6 is an oligopeptide transporter with exceptionally broad substrate specificity. Plant Cell Physiol 50:1923–1932

    Article  CAS  PubMed  Google Scholar 

  • Plackett AR, Powers SJ, Fernandez-Garcia N, Urbanova T, Takebayashi Y, Seo M, Jikumaru Y, Benlloch R, Nilsson O, Ruiz-Rivero O, Phillips AL, Wilson ZA, Thomas SG, Hedden P (2012) Analysis of the developmental roles of the Arabidopsis gibberellin 20-oxidases demonstrates that GA20ox1, -2, and -3 are the dominant paralogs. Plant Cell 24:941–960

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rédei GP, Hirono Y (1964) Linkage studies. Arabidopsis Inf Serv 1:9–10

    Google Scholar 

  • Rubin G, Tohge T, Matsuda F, Saito K, Scheiblea WR (2009) Members of the LBD Family of transcription factors repress anthocyanin synthesis and affect additional nitrogen responses in Arabidopsis. Plant Cell 21:3567–3584

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sasidharan R, Keuskamp DH, Kooke R, Voesenek LA, Pierik R (2014) Interactions between auxin, microtubules and XTHs mediate green shade-induced petiole elongation in Arabidopsis. PLoS One 9:e90587

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scarpella E, Marcos D, Friml J, Berleth T (2006) Control of leaf vascular patterning by polar auxin transport. Genes Dev 20:1015–1027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Semiarti E, Ueno Y, Tsukaya H, Iwakawa H, Machida C, Machida Y (2001) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana regulates formation of a symmetric lamina, establishment of venation and repression of meristem-related homeobox genes in leaves. Development 128:1771–1783

    CAS  PubMed  Google Scholar 

  • Shani E, Ben-Gera H, Shleizer-Burko S, Burko Y, Weiss D, Ori N (2010) Cytokinin regulates compound leaf development in tomato. Plant Cell 22:3206–3217

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shikata M, Koyama T, Mitsuda N, Ohme-Takagi M (2009) Arabidopsis SBP-box genes SPL10, SPL11 and SPL2 control morphological change in association with shoot maturation in the reproductive phase. Plant Cell Physiol 50:2133–2145

    Article  CAS  PubMed  Google Scholar 

  • Slankster EE, Chase JM, Jones LA, Wendell DL (2012) DNA-based genetic markers for rapid cycling Brassica rapa (Fast Plants Type) designed for the teaching laboratory. Front Plant Sci 3:118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sluis A, Hake S (2015) Organogenesis in plants: initiation and elaboration of leaves. Trends Genet 31:300–306

    Article  CAS  PubMed  Google Scholar 

  • Song K, Slocum MK, Osborn TC (1995) Molecular marker analysis of genes controlling morphological variation in Brassica rapa (syn. campestris). Theor Appl Genet 90:1–10

    Article  CAS  PubMed  Google Scholar 

  • Song ZT, Sun L, Lu SJ, Tian Y, Ding Y, Liu JX (2015) Transcription factor interaction with COMPASS-like complex regulates histone H3K4 trimethylation for specific gene expression in plants. Proc Natl Acad Sci USA 112:2900–2905

    Article  CAS  PubMed  Google Scholar 

  • Sundin L, Vanholme R, Geerinck J, Goeminne G, Höfer R, Kim H, Ralph J, Boerjan W (2014) Mutation of the inducible ARABIDOPSIS THALIANA CYTOCHROME P450 REDUCTASE 2 alters lignin composition and improves saccharification. Plant Physiol 166:1956–1971

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    Article  CAS  PubMed  Google Scholar 

  • Tanksley SD (1993) Mapping polygenes. Ann Rev Genet 27:205–233

    Article  CAS  PubMed  Google Scholar 

  • Thomas SG, Phillips AL, Hedden P (1999) Molecular cloning and functional expression of gibberellin 2-oxidases, multifunctional enzymes involved in gibberellin deactivation. Proc Natl Acad Sci USA 96:4698–4703

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Tsukaya H (2006) Mechanism of leaf-shape determination. Ann Rev Plant Biol 57:477–496

    Article  CAS  Google Scholar 

  • Tsukaya H, Kozuka T, Kim GT (2002) Genetic control of petiole length in Arabidopsis thaliana. Plant Cell Physiol 43:1221–1228

    Article  CAS  PubMed  Google Scholar 

  • Ueno Y, Springer P (2011) Molecular genetic studies on ASYMMETRIC LEAVES2 (AS2) of Arabidopsis: Insight into the function of the AS2 protein. Plant Morphol 23:71–80

    Article  Google Scholar 

  • Vanjildorj E, Song SY, Yang ZH, Choi JE, Noh YS, Park S, Lim WJ, Cho KM, Yun HD, Lim YP (2009) Enhancement of tolerance to soft rot disease in the transgenic Chinese cabbage (Brassica rapa L. ssp. pekinensis) inbred line, Kenshin. Plant Cell Rep 28:1581–1591

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Wilson-Sánchez D, Rubio-Díaz S, Muñoz-Viana R, Pérez-Pérez J, Jover-Gil S, Ponce M, Micol J (2014) Leaf phenomics: a systematic reverse genetic screen for Arabidopsis leaf mutants. Plant J 79:878–891

    Article  CAS  PubMed  Google Scholar 

  • Wolf S, Hematy K, Hofte H (2012) Growth control and cell wall signaling in plants. Annu Rev Plant Biol 63:381–407

    Article  CAS  PubMed  Google Scholar 

  • Xiao D, Wang H, Basnet RK, Zhao J, Lin K, Hou X, Bonnema G (2014) Genetic dissection of leaf development in Brassica rapa using a ‘genetical genomics’ approach. Plant Physiol 164:1309–1325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yin XJ, Volk S, Ljung K, Mehlmer N, Dolezal K, Ditengou F, Hanano S, Davis SJ, Schmelzer E, Sandberg G, Teige M, Palme K, Pickart C, Bachmair A (2007) Ubiquitin lysine 63 chain forming ligases regulate apical dominance in Arabidopsis. Plant Cell 19:1898–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao J, Wang X, Deng B, Lou P, Wu J, Sun R, Xu Z, Vromans J, Koornneef M, Bonnema G (2005) Genetic relationships within Brassica rapa as inferred from AFLP fingerprints. Theor Appl Genet 110:1301–1314

    Article  PubMed  Google Scholar 

  • Zhou X, Sun TH, Wang N, Ling HQ, Lu S, Li L (2011) The cauliflower Orange gene enhances petiole elongation by suppressing expression of eukaryotic release factor 1. New Phytol 190:89–100

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Technology Development Program for Agriculture and Forestry, Ministry for Food, Agriculture, Forestry, and Fisheries (Grant 213007-05-2-SB620), Republic of Korea.

Author information

Affiliations

  1. Department of Biological Sciences, College of Biological Science and Biotechnology, Chungnam National University, Daejeon, 34134, Republic of Korea

    Sang-Moo Lee, Hayoung Song, Hankuil Yi & Yoonkang Hur

  2. Korea Biosystems and Bioengineering Program, University of Science and Technology, Daejeon, 34141, Republic of Korea

    Sang-Moo Lee

Authors
  1. Sang-Moo Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hayoung Song
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hankuil Yi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yoonkang Hur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yoonkang Hur.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest, financial or otherwise.

Human and animal rights

No animals/humans were used for studies that are base of this research.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lee, SM., Song, H., Yi, H. et al. Transcriptomic analysis of contrasting inbred lines and F2 segregant of Chinese cabbage provides valuable information on leaf morphology. Genes Genom 41, 811–829 (2019). https://doi.org/10.1007/s13258-019-00809-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13258-019-00809-7

Keywords

  • Br135K microarray
  • DEGs
  • Leaf phenotype
  • Leaf size
  • Brassica rapa
  • Kenshin
  • Rapid cycling Brassica rapa.