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Candidate gene prediction for a petal degeneration mutant, pdm, of the Chinese cabbage (Brassica campestris ssp. pekinensis) by using fine map** and transcriptome analysis

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Abstract

A stably inherited petal degeneration mutant pdm of the Chinese cabbage was obtained from its wild-type ‘FT’ by radiation treatment (60Co γ-rays) and isolated microspore culture. Petals of the pdm mutant were observed to be shriveled, degenerated, not fully expanded, and darker at the flowering stage than those of ‘FT.’ The pdm mutant phenotype was found to be controlled by a single recessive nuclear gene. For linkage analysis and gene map**, 1419 recessive homozygous individuals with the pdm phenotype of the F2 generation were investigated as the map** population. Results showed that the pdm was located between markers Indelhsn26 and SSRhsn123 at a genetic distance of 0.04 and 0.04 cM, respectively, on linkage group A01. Physical distance between Indelhsn26 and SSRhsn123, the two most closely linked markers, was estimated to be approximately 285.2 kb. Twenty-eight genes were predicted in the target region. Using RNA-seq, Bra040093 was predicted to be the most likely candidate gene for pdm. Based on gene annotation, Bra040093 encodes a peroxisomal acyl-coenzyme A oxidase 1 (ACX1). Comparison of the sequences in pdm and ‘FT’ revealed two single-nucleotide polymorphisms in pdm. Expression patterns of Bra040093 between pdm and ‘FT’ were analyzed using quantitative real-time PCR, and the expression level was dramatically higher in ‘FT’ than in pdm. These findings provide a solid foundation and valuable resources for map-based cloning, identification, and functional analysis of pdm and facilitate the understanding of floral development processes in the Chinese cabbage.

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References

  • Andersson S (2012) Does inbreeding promote evolutionary reduction of flower size? Experimental evidence from Crepis tectorum (Asteraceae). Am J Bot 99:1388–1398

    Article  PubMed  Google Scholar 

  • Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  CAS  PubMed  Google Scholar 

  • Battaglia R, Brambilla V, Colombo L, Stuitje AR, Kater MM (2006) Functional analysis of MADS-box genes controlling ovule development in Arabidopsis using the ethanol-inducible alc gene-expression system. Mech Dev 123:267–276

    Article  CAS  PubMed  Google Scholar 

  • Baurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125:655–664

    Article  CAS  PubMed  Google Scholar 

  • Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boss PK, Bastow RM, Mylne JS, Dean C (2004) Multiple pathways in the decision to flower: enabling, promoting, and resetting. Plant Cell 16:18–31

    Article  Google Scholar 

  • Bowman JL, Smyth DR, Meyerowitz EM (1989) Genes directing flower development in Arabidopsis. Plant Cell 1:37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brioudes F, Joly C, Szécsi J, Varaud E, Leroux J, Bellvert F, Bertrand C, Bendahmane M (2009) Jasmonate controls late development stages of petal growth in Arabidopsis thaliana. Plant J 60:1070–1080

    Article  CAS  PubMed  Google Scholar 

  • Chandler J, Dean C (1994) Factors influencing the vernalization response and flowering time of late flowering mutants of Arabidopsis thaliana. J Exp Bot 45:1279–1288

    Article  CAS  Google Scholar 

  • Cnops G, Jover-Gil S, Peters JL, Neyt P, De Block S, Robles P, Ponce MR, Gerats T, Micol JL, Van Lijsebettens M (2004) The rotund a2 mutants identify a role for the LEUNIG gene in vegetative leaf morphogenesis. J Exp Bot 55:1529–1539

    Article  CAS  PubMed  Google Scholar 

  • Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37

    Article  CAS  PubMed  Google Scholar 

  • Corbesier L, Coupland G (2005) Photoperiodic flowering of Arabidopsis: integrating genetic and physiological approaches to characterization of the floral stimulus. Plant Cell Environ 28:54–66

    Article  CAS  Google Scholar 

  • Delker C, Stenzel I, Hause B, Miersch O, Feussner I, Wasternack C (2006) Jasmonate biosynthesis in Arabidopsis thaliana—enzymes, products, regulation. Plant Biol 8:297–306

    Article  CAS  PubMed  Google Scholar 

  • Delph LF, Arntz AM, Scotti-Saintagne C, Scotti I (2010) The genomic architecture of sexual dimorphism in the dioecious plant Silene latifolia. Evolution 64:2873–2886

    PubMed  Google Scholar 

  • Feng H, Wei P, Piao ZY, Liu ZY, Li CY, Wang YG, Ji RQ, Ji SJ, Zou T, Choi SR, Lim YP (2009) SSR and SCAR map** of a multiple-allele male-sterile gene in Chinese cabbage (Brassica rapa L.). Theor Appl Genet 119:333–339

    Article  CAS  PubMed  Google Scholar 

  • Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550

    Article  PubMed  Google Scholar 

  • Hermann K, Kuhlemeier C (2011) The genetic architecture of natural variation in flower morphology. Curr Opin Plant Biol 14:60–65

    Article  PubMed  Google Scholar 

  • Hu Y, **e Q, Chua NH (2003) The Arabidopsis auxin-inducible gene ARGOS controls lateral organ size. Plant Cell 15:1951–1961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu Y, Poh HM, Chua NH (2006) The Arabidopsis ARGOS-LIKE gene regulates cell expansion during organ growth. Plant J 47:1–9

    Article  CAS  PubMed  Google Scholar 

  • Huang SN, Liu ZY, Li DY, Yao RP, Meng Q, Feng H (2014) Screening of Chinese cabbage mutants produced by 60Co γ-ray mutagenesis of isolated microspore cultures. Plant Breed 133:480–488

    Article  CAS  Google Scholar 

  • Huang SN, Liu ZY, Yao RP, Li DY, Feng H (2015) Comparative transcriptome analysis of the petal degeneration mutant pdm in Chinese cabbage (Brassica campestris ssp. pekinensis) using RNA-Seq. Mol Genet Genomics 290:1833–1847

    Article  CAS  PubMed  Google Scholar 

  • Hwang J, Oh J, Kim Z, Staub JE, Chung SM, Park Y (2014) Fine genetic map** of a locus controlling short internode length in melon (Cucumis melo L.). Mol Breed 34:949–961

    Article  CAS  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCIENCE gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim JH, Choi D, Kende H (2003) The AtGRF family of putative transcription factors is involved in leaf and cotyledon growth in Arabidopsis. Plant J 36:94–104

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distance from recombination values. Ann Eugen 12:172–175

    Article  Google Scholar 

  • Koyama T, Furutani M, Tasaka M, Ohme-Takagi M (2007) TCP transcription factors control the morphology of shoot lateral organs via negative regulation of the expression of boundary specific genes in Arabidopsis. Plant Cell 19:473–484

    Article  CAS  PubMed  PubMed Central  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 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg I (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Li YF, Liu ZY, Wang YS, Yang N, **n XF, Yang S, Feng H (2012) Identification of quantitative trait loci for yellow inner leaves in Chinese cabbage (Brassica rapa L. ssp. pekinensis) based on SSR and SRAP markers. Sci Hortic 133:10–17

    Article  CAS  Google Scholar 

  • Liu Y, Zhang Y, ** quantitative trait loci for yield-related traits in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Euphytica 193:221–234

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lu YH, Arnaud D, Belcram H, Falentin C, Rouault P, Piel N, Lucas MO, Just J, Renard M, Delourme R, Chalhoub B (2012) A dominant point mutation in a RINGv E3 ubiquitin ligase homoeologous gene leads to cleistogamy in Brassica napus. Plant Cell 24:4875–4891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma H, dePamphilis C (2000) The ABCs of floral evolution. Cell 101:5–8

    Article  CAS  PubMed  Google Scholar 

  • Mojica JP, Kelly JK (2010) Viability selection prior to trait expression is an essential component of natural selection. Proc R Soc B 277:2945–2950

    Article  PubMed  PubMed Central  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nag A, King S, Jack T (2009) miR319a targeting of TCP4 is critical for petal growth and development in Arabidopsis. Proc Natl Acad Sci USA 106:22534–22539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nagpal P, Ellis CM, Weber H, Ploense SE, Barkawi LS, Guilfoyle TJ, Hagen G, Alonso JM, Cohen JD, Farmer EE, Ecker JR, Reed JW (2005) Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation. Development 132:4107–4118

    Article  CAS  PubMed  Google Scholar 

  • Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203

    Article  CAS  PubMed  Google Scholar 

  • Pelaz S, Gustafson-Brown C, Kohalmi SE, Crosby WL, Yanofsky MF (2001) APETALA1 and SEPALLATA3 interact to promote flower development. Plant J 26:385–394

    Article  CAS  PubMed  Google Scholar 

  • Sarvepalli K, Nat U (2011) Hyper-activation of the TCP4 transcription factor in Arabidopsis thaliana accelerates multiple aspects of plant maturation. Plant J 67:595–607

    Article  CAS  PubMed  Google Scholar 

  • Soltis DE, Chanderbali AS, Kim S, Buzgo M, Soltis PS (2007) The ABC model and its applicability to basal angiosperms. Ann Bot 100:155–163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suárez-López P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120

    Article  PubMed  Google Scholar 

  • Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508

    Article  CAS  PubMed  Google Scholar 

  • Szécsi J, Joly C, Bordji K, Varaud E, Cock JM, Dumas C, Bendahmane M (2006) BIGPETALp, a bHLH transcription factor is involved in the control of Arabidopsis petal size. EMBO J 25:3912–3920

    Article  PubMed  PubMed Central  Google Scholar 

  • Theissen G (2001) Development of floral organ identity stories from the MADS house. Curr Opin Plant Biol 4:75–85

    Article  CAS  PubMed  Google Scholar 

  • Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471

    Article  CAS  PubMed  Google Scholar 

  • Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:153–164

    Google Scholar 

  • Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006

    Article  CAS  PubMed  Google Scholar 

  • Wang XW, Wang HZ, Wang J, Sun RF, Wu J, Liu SY, Bai YQ, Mun JH, 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 BS, 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, ** H, Parkin IA, Batley J, Kim JS, 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, ** 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 SJ, Choi SR, Lee TH, 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 YP, Wang ZY, Li ZY, Wang ZW, **ong ZY, Zhang ZH (2011) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039

    Article  CAS  PubMed  Google Scholar 

  • Weigel D, Meyerowitz EM (1994) The ABCs of floral homeotic genes. Cell 78:203–209

    Article  CAS  PubMed  Google Scholar 

  • Wollenberg AC, Strasser B, Cerdán PD, Amasino RM (2008) Acceleration of flowering during shade avoidance in Arabidopsis alters the balance between FLOWERING LOCUS C-mediated repression and photoperiodic induction of flowering. Plant Physiol 148:1681–1694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu ZH (1999) Plant development and reproduction: advances and prospective. Acta Bot Sin 41:909–920

    CAS  Google Scholar 

  • Zhang JX, Li HX, Zhang MK, Hui MX, Wang Q, Zhang LG (2013a) Fine map** and identification of candidate Br-or gene controlling orange head of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Breed 32:799–805

    Article  CAS  Google Scholar 

  • Zhang X, Liu ZY, Wang P, Wang QS, Yang S, Feng H (2013b) Fine map** of Br Wax1, a gene controlling cuticular wax biosynthesis in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Mol Breed 32:867–874

    Article  Google Scholar 

  • Zhang T, Zhao Z, Zhang CY, Pang WX, Choi SR, Lim YP, Piao ZY (2014) Fine genetic and physical map** of the CRb gene conferring resistance to clubroot disease in Brassica rapa. Mol Breed 34:1173–1183

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the National Natural Science Foundation of China (31201625 and 31272157), the National Sci-Tech Support Plan (2012BAD02B01-9), and the Postgraduate Innovation Cultivation Project of Shenyang Agricultural University.

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    Authors and Affiliations

    1. Department of Horticulture, Shenyang Agricultural University, 120 Dongling Road, Shenhe District, Shenyang, 110866, People’s Republic of China

      Shengnan Huang, Zhiyong Liu, Runpeng Yao, Danyang Li, Teng Zhang, **ang Li, Li Hou, Yiheng Wang, **aoyan Tang & Hui Feng

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    1. Shengnan Huang
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    Shengnan Huang and Zhiyong Liu contributed equally to this work and share the first authorship.

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    Fig. S1

    Examples of makers tightly linked to pdm. (a) Polymorphism screened by part of the SSR primers between the two parents; (b) recombinant individuals with SSRhsn92 in the map** population; (c) recombinant individuals with SSRhsn87 in the map** population; (d) recombinant individuals with SSRhsn117 in the map** population; (e) recombinant individuals with SSRhsn123 in the map** population. M: Marker; P1: 11A150; P2: pdm; *: recombinant individuals (TIFF 40549 kb)

    Fig. S2

    Examination of PCR products by using agarose gel electrophoresis. M: Marker (TIFF 2948 kb)

    Fig. S3

    Sequence alignment analysis of Bra040093 in pdm and its wild-type ‘FT’ (TIFF 2730 kb)

    Table S1

    Primer sequences of SSR and Indel markers used in the gene map** of the pdm mutant (XLS 22 kb)

    Table S2

    Prediction of candidate genes within the gene-mapped region on linkage group A01 (XLS 23 kb)

    Table S3

    Differentially expressed genes of pdm and its wild-type ‘FT’ (XLS 51 kb)

    Table S4

    Sequencing results for BraA, BraB, BraC, and BraD in pdm and its wild-type ‘FT’ (DOC 33 kb)

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    Huang, S., Liu, Z., Yao, R. et al. Candidate gene prediction for a petal degeneration mutant, pdm, of the Chinese cabbage (Brassica campestris ssp. pekinensis) by using fine map** and transcriptome analysis. Mol Breeding 36, 26 (2016). https://doi.org/10.1007/s11032-016-0452-4

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