Abstract
Chinese cabbage (Brassica rapa L. var. pekinensis) is an economically important vegetable providing nutrients such as fiber, calcium and vitamins. Most cultivars of Chinese cabbage are F1 hybrids with vegetative heterosis, and harvesting of commercial F1 hybrid seeds makes use of self-incompatibility or cytoplasmic male sterility. Production of Chinese cabbage is always threatened by abiotic and biotic stress; climate change and increasing numbers of races and varieties of pathogens are also serious problems. The demand for abiotic or biotic resistant cultivars is growing year by year. An effective breeding method is desired, and marker-assisted selection (MAS) is a leading candidate. To apply MAS, identification of the causative gene or the locus linked to the causative gene controlling a trait for breeding is required. We review the recent research using molecular biology approaches and discuss how this information can apply to Chinese cabbage breeding.
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References
Akter A, Nishida N, Takada T et al (2018) Genetic and epigenetic regulation of vernalization in Brassicaceae. In: El-Esawi MA (ed) Brassica germplasm – characterization, breeding and utilization. IntechOpen, London, pp 75–94
Baird NA, Etter PD, Atwood TS et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3:e3376
Bao A, Burritt DJ, Chen H et al (2019) The CRISPR/Cas9 system and its applications in crop genome editing. Crit Rev Biotechnol 39:321–336
Barth S, Busimi AK, Friedrich Utz H, Melchinger AE (2003) Heterosis for biomass yield and related traits in five hybrids of Arabidopsis thaliana L. Heynh. Heredity 91:36–42
Baskar V, Gangadhar BH, Park SW, Nile SH (2016) A simple and efficient Agrobacterium tumefaciens-mediated plant transformation of Brassica rapa ssp. pekinensis. 3 Biotech 6:88
Bateman AJ (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9:53–68
Bayer PE, Golicz AA, Tirnaz S et al (2018) Variation in abundance of predicted resistance genes in the Brassica oleracea pangenome. Plant Biotechnol J 17:789–800
Berry S, Dean C (2015) Environmental perception and epigenetic memory: mechanistic insight through FLC. Plant J 83:133–148
Blümel M, Dally N, Jung C (2015) Flowering time regulation in crops—what did we learn from Arabidopsis? Curr Opin Biotechnol 32:121–129
Boggs NA, Dwyer KG, Nasrallah ME, Nasrallah JB (2009) In vivo detection of residues required for ligand-selective activation of the S-locus receptor in Arabidopsis. Curr Biol 19:786–791
Braselton JP, Miller CE, Pechak DG (1975) The ultrastructure of cruciform nuclear division in Sorosphaera veronicae (Plasmodiophoromycete). Am J Bot 62:349–358
Buczacki ST, Toxopeus H, Mattusch P et al (1975) Study of physiologic specialization in Plasmodiophora brassicae: proposals for attempted rationalization through an international approach. Trans Br Mycol Soc 65:295–303
Burki F, Kudryavtsev A, Matz MV et al (2010) Evolution of Rhizaria: new insights from phylogenomic analysis of uncultivated protists. BMC Evol Biol 10:377
Cheng F, Wu J, Fang L et al (2012) Biased gene fractionation and dominant gene expression among the subgenomes of Brassica rapa. PLoS One 7:e36442
Cheng F, Wu J, Wang X (2014) Genome triplication drove the diversification of Brassica plants. Hortic Res 1:14024
Cheng F, Sun R, Hou X et al (2016) Subgenome parallel selection is associated with morphotype diversification and convergent crop domestication in Brassica rapa and Brassica oleracea. Nat Genet 48:1218–1224
Cho YN, Park SY, Noh TK et al (2003a) Transformation of Chinese cabbage with L-gulono-γ-lactone oxidase (GLOase)-encoding gene using Agrobacterium tumefaciens. Korean J Hortic Sci 21:9–13
Cho WD, Kim WG, Takahashi K (2003b) Occurrence of clubroot in cruciferous vegetable crops and races of the pathogen in Korea. Plant Pathol J 19:64–68
Chookajorn T, Kachroo A, Ripoll DR et al (2004) Specificity determinants and diversification of the Brassica self-incompatibility pollen ligand. Proc Natl Acad Sci U S A 101:911–917
Chu M, Song T, Falk KC et al (2014) Fine mapping of Rcr1 and analyses of its effect on transcriptome patterns during infection by Plasmodiophora brassicae. BMC Genomics 15:1166
Crisp P, Crute IR, Sutherland RA et al (1989) The exploitation of genetic resources of Brassica oleracea in breeding for resistance to clubroot (Plasmodiophora brassicae). Euphytica 42:215–226
Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928
Cui J, Li M, Qiu L et al (2017) Stable expression of exogenous imported sporamin in transgenic Chinese cabbage enhances resistance against insects. Plant Growth Regul 81:543–552
De Nettancourt D (2001) Incompatibility and incongruity in wild and cultivated plants. Springer, Berlin
Diederichsen E, Frauen M, Linders EGA et al (2009) Status and perspectives of clubroot resistance breeding in crucifer crops. J Plant Growth Regul 28:265–281
Dixon GR (2009) The occurrence and economic impact of Plasmodiophora brassicae and clubroot disease. J Plant Growth Regul 28:194–202
Doucet J, Lee HK, Goring DR (2016) Pollen acceptance or rejection: a tale of two pathways. Trends Plant Sci 21:1058–1067
Enya J, Togawa M, Takeuchi T et al (2008) Biological and phylogenetic characterization of Fusarium oxysporum complex, which causes yellows on Brassica spp., and proposal of F. oxysporum f. sp. rapae, a novel forma specialis pathogenic on B. rapa in Japan. Phytopathology 98:475–483
Farnham MW, Keinath AP, Smith JP (2001) Characterization of Fusarium yellows resistance in collard. Plant Dis 85:890–894
Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:550–550.e2
Fuchs J, Demidov D, Houben A, Schubert I (2006) Chromosomal histone modification patterns -from conservation to diversity. Trends Plant Sci 11:199–208
Fujimoto R, Nishio T (2003) Identification of S haplotypes in Brassica by dot-blot analysis of SP11 alleles. Theor Appl Genet 106:1433–1437
Fujimoto R, Nishio T (2007) Self-incompatibility. Adv Bot Res 45:139–154
Fujimoto R, Okazaki K, Fukai E et al (2006a) Comparison of the genome structure of the self-incompatibility (S) locus in interspecific pairs of S haplotypes. Genetics 173:1157–1167
Fujimoto R, Sugimura T, Fukai E, Nishio T (2006b) Suppression of gene expression of a recessive SP11/SCR allele by an untranscribed SP11/SCR allele in Brassica self-incompatibility. Plant Mol Biol 61:577–587
Fujimoto R, Sugimura T, Nishio T (2006c) Gene conversion from SLG to SRK resulting in self-compatibility in Brassica rapa. FEBS Lett 580:425–430
Fujimoto R, Sasaki T, Ishikawa R et al (2012a) Molecular mechanisms of epigenetic variation in plants. Int J Mol Sci 13:9900–9922
Fujimoto R, Taylor JM, Shirasawa S et al (2012b) Heterosis of Arabidopsis hybrids between C24 and Col is associated with increased photosynthesis capacity. Proc Natl Acad Sci U S A 109:7109–7114
Fujimoto R, Uezono K, Ishikura S et al (2018) Recent research on the mechanism of heterosis is important for crop and vegetable breeding systems. Breed Sci 68:145–158
Garber RC, Aist JR (1979) The ultrastructure of mitosis in Plasmodiophora brassicae (Plasmodiophorales). J Cell Sci 40:89–110
Girke A, Schierholt A, Becker HC (2012) Extending the rapeseed gene pool with resynthesized Brassica napus II: Heterosis. Theor Appl Genet 124:1017–1026
Golicz AA, Bayer PE, Barker GC et al (2016) The pangenome of an agronomically important crop plant Brassica oleracea. Nat Commun 7:13390
Gu T, Mazzurco M, Sulaman W et al (1998) Binding of an arm repeat protein to the kinase domain of the S-locus receptor kinase. Proc Natl Acad Sci U S A 95:382–387
Guo Y, Chen S, Li Z, Cowling WA (2014) Center of origin and centers of diversity in an ancient crop, Brassica rapa (turnip rape). J Hered 105:555–565
Hasan MJ, Strelkov SE, Howard RJ, Rahman H (2012) Screening of Brassica germplasm for resistance to Plasmodiophora brassicae pathotypes prevalent in Canada for broadening diversity in clubroot resistance. Can J Plant Sci 92:501–515
Hatakeyama K, Watanabe M, Takasaki T et al (1998) Dominance relationships between S-alleles in self-incompatible Brassica campestris L. Heredity 80:241–247
Hatakeyama K, Takasaki T, Suzuki G et al (2001) The S receptor kinase gene determines dominance relationships in stigma expression of self-incompatibility in Brassica. Plant J 26:69–76
Hatakeyama K, Fujimura M, Ishida M, Suzuki T (2004) New classification method for Plasmodiophora brassicae field isolates in Japan based on resistance of F1 cultivars of Chinese cabbage (Brassica rapa L.) to clubroot. Breed Sci 54:197–201
Hatakeyama K, Horisaki A, Niikura S et al (2010) Mapping of quantitative trait loci for high level of self-incompatibility in Brassica rapa L. Genome 53:257–265
Hatakeyama K, Suwabe K, Tomita RN et al (2013) Identification and characterization of Crr1a, a gene for resistance to clubroot disease (Plasmodiophora brassicae Woronin) in Brassica rapa L. PLoS One 8:e54745
Hatakeyama K, Niwa T, Kato T et al (2017) The tandem repeated organization of NB-LRR genes in the clubroot-resistant CRb locus in Brassica rapa L. Mol Genet Genomics 292:397–405
He G, Elling AA, Deng XW (2011) The epigenome and plant development. Annu Rev Plant Biol 62:411–435
Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79
Hirai M, Harada T, Kubo N et al (2004) A novel locus for clubroot resistance in Brassica rapa and its linkage markers. Theor Appl Genet 108:639–643
Hirani AH, Li G (2015) Understanding the genetics of clubroot resistance for effectively controlling this disease in Brassica species. Plants for the Future:1
Hirani AH, Gao F, Liu J et al (2018) Combinations of independent dominant loci conferring clubroot resistance in all four turnip accessions (Brassica rapa) from the European clubroot differential set. Front Plant Sci 9:1628
Holtz MD, Hwang SF, Strelkov SE (2018) Genotyping of Plasmodiophora brassicae reveals the presence of distinct populations. BMC Genomics 19:254
Horisaki A, Niikura S (2008) Developmental and environmental factors affecting level of self-incompatibility response in Brassica rapa L. Sex Plant Reprod 21:123–132
Huang Z, Peng G, Liu X et al (2017) Fine mapping of a clubroot resistance gene in Chinese cabbage using SNP markers identified from bulked segregant RNA sequencing. Front Plant Sci 8:1448
Hwang SF, Strelkov SE, Feng J et al (2012) Plasmodiophora brassicae: a review of an emerging pathogen of the Canadian canola (Brassica napus) crop. Mol Plant Pathol 13:105–113
Ingram DS, Tommerup IC (1972) The life history of Plasmodiophora brassicae Woron. Proc R Soc London Ser B 180:103–112
Isokawa S, Osaka M, Shirasawa A et al (2010) Novel self-compatible lines of Brassica rapa L. isolated from the Japanese bulk-populations. Genes Genet Syst 85:87–96
Itabashi E, Osabe K, Fujimoto R, Kakizaki T (2018) Epigenetic regulation of agronomical traits in Brassicaceae. Plant Cell Rep 37:87–101
Jang HY, Park MY, Lee JS et al (2019) Development of a molecular marker using GWAS to select the resistance resource for the Yeoncheon Strain causing kimchi cabbage clubroot disease. Hortic Sci Tech 37:92–107
Jiang J, Bai J, Li S et al (2018) HTT2 promotes plant thermotolerance in Brassica rapa. BMC Plant Biol 18:127
Kachroo A, Schopfer CR, Nasrallah ME, Nasrallah JB (2001) Allele-specific receptor-ligand interactions in Brassica self-incompatibility. Science 293:1824–1826
Kageyama K, Asano T (2009) Life cycle of Plasmodiophora brassicae. J Plant Growth Regul 28:203–211
Kakita M, Murase K, Iwano M et al (2007) Two distinct forms of M-locus protein kinase localize to the plasma membrane and interact directly with S-locus receptor kinase to transduce self-incompatibility signaling in Brassica rapa. Plant Cell 19:3961–3973
Kakizaki T, Takada Y, Ito A et al (2003) Linear dominance relationship among four class-II S haplotypes in pollen is determined by the expression of SP11 in Brassica self-incompatibility. Plant Cell Phys 44:70–75
Kakizaki T, Takada Y, Fujioka T et al (2006) Comparative analysis of the S-intergenic region in the class-II S haplotypes of self-incompatible Brassica rapa (syn. campestris). Genes Genet Syst 81:63–67
Kaneko Y, Bang SW (2014) Interspecific and intergeneric hybridization and chromosomal engineering of Brassicaceae crops. Breed Sci 64:14–22
Kawamura K, Kawanabe T, Shimizu M et al (2015) Genetic characterization of inbred lines of Chinese cabbage by DNA markers; towards the application of DNA markers to breeding of F1 hybrid cultivars. Data Brief 6:229–237
Kawamura K, Kawanabe T, Shimizu M et al (2016) Genetic distance of inbred lines of Chinese cabbage and its relationship to heterosis. Plant Gene 5:1–7
Kim DH, Sung S (2017) Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs. Dev Cell 40:302–312
Kim SY, Park BS, Kwon SJ et al (2007) Delayed flowering time in Arabidopsis and Brassica rapa by the overexpression of FLOWERING LOCUS C (FLC) homologs isolated from Chinese cabbage (Brassica rapa L. ssp. pekinensis). Plant Cell Rep 26:327–336
Kitamoto N, Yui S, Nishikawa K et al (2014) A naturally occurring long insertion in the first intron in the Brassica rapa FLC2 gene causes delayed bolting. Euphytica 196:213–223
Kitamoto N, Nishikawa K, Tanimura Y et al (2017) Development of late-bolting F1 hybrids of Chinese cabbage (Brassica rapa L.) allowing early spring cultivation without heating. Euphytica 213:292
Konagaya K, Tsuda M, Okuzaki A et al (2013) Application of the acetolactate synthase gene as a cisgenic selectable marker for Agrobacterium-mediated transformation in Chinese cabbage (Brassica rapa ssp. pekinensis). Plant Biotech 30:125–133
Kuginuki Y, Tsukazaki H (2001) Regeneration ability and Agrobacterium-mediated transformation of different cultivars in Brassica oleracea L. and B. rapa L. (syn. B. campestris L.). J Jpn Soc Hortic Sci 70:682–690
Kuginuki Y, Ajisaka H, Yui M et al (1997) RAPD markers linked to a clubroot-resistance locus in Brassica rapa L. Euphytica 98:149–154
Kuginuki Y, Yoshikawa H, Hirai M (1999) Variation in virulence of Plasmodiophora brassicae in Japan tested with clubroot-resistant cultivars of Chinese cabbage (Brassica rapa L. ssp. pekinensis). Eur J Plant Pathol 105:327–332
Kusaba M, Nishio T, Satta Y et al (1997) Striking sequence similarity in inter- and intra-specific comparisons of class I SLG alleles from Brassica oleracea and Brassica campestris: implications for the evolution and recognition mechanism. Proc Natl Acad Sci U S A 94:7673–7678
Laila R, Robin AHK, Yang K et al (2017) Detection of ribosomal DNA sequence polymorphisms in the protist Plasmodiophora brassicae for the identification of geographical isolates. Int J Mol Sci 18:84
Laila R, Park JI, Robin AHK et al (2019) Mapping of a novel clubroot resistance QTL using ddRAD-seq in Chinese cabbage (Brassica rapa L.). BMC Plant Biol 19:13
Lao X, Suwabe K, Niikura S et al (2014) Physiological and genetic analysis of CO2-induced breakdown of self-incompatibility in Brassica rapa. J Exp Bot 65:939–951
Lawrenson T, Shorinola O, Stacey N et al (2015) Induction of targeted, heritable mutations in barley and Brassica oleracea using RNA-guided Cas9 nuclease. Genome Biol 16:258
Li E, Wang G, Yang Y et al (2015) Microscopic analysis of the compatible and incompatible interactions between Fusarium oxysporum f. sp. conglutinans and cabbage. Eur J Plant Pathol 141:597–609
Li X, Zhang S, Bai J, He Y (2016) Tuning growth cycles of Brassica crops via natural antisense transcripts of BrFLC. Plant Biotechnol J 14:905–914
Liu Y, Xu A, Liang F et al (2018) Screening of clubroot-resistant varieties and transfer of clubroot resistance genes to Brassica napus using distant hybridization. Breed Sci 68:258–267
Lou P, Zhao J, Kim JS et al (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 58:4005–4016
Lu Y, Dai S, Gu A et al (2016) Microspore induced doubled haploids production from ethyl methanesulfonate (EMS) soaked flower buds is an efficient strategy for mutagenesis in Chinese cabbage. Front Plant Sci 7:1780
Lv H, Fang Z, Yang L et al (2014) Mapping and analysis of a novel candidate Fusarium wilt resistance gene FOC1 in Brassica oleracea. BMC Genomics 15:1094
Ma R, Han Z, Hu Z et al (2016) Structural basis for specific self-incompatibility response in Brassica. Cell Res 26:1320–1329
Ma C, Zhu C, Zheng M et al (2019) CRISPR/Cas9-mediated multiple gene editing in Brassica oleracea var. capitata using the endogenous tRNA-processing system. Hortic Res 6:20
Mao Y, Wu F, Yu X et al (2014) microRNA319a-targeted Brassica rapa ssp. pekinensis TCP genes modulate head shape in Chinese cabbage by differential cell division arrest in leaf regions. Plant Physiol 164:710–720
Matsubara S (1980) Overcoming self-incompatibility in Raphanus sativus L. with high temperature. J Am Soc Hortic Sci 105:842–846
Matsumoto E, Yasui C, Ohi M, Tsukada M (1998) Linkage analysis of RFLP markers for clubroot resistance and pigmentation in Chinese cabbage (Brassica rapa ssp. pekinensis). Euphytica 104:79–86
Matsumoto E, Hayashida N, Sakamoto K, Ohi M (2005) Behavior of DNA markers linked to a clubroot resistance gene in segregating populations of Chinese cabbage (Brassica rapa ssp. pekinensis). J Jpn Soc Hortic Sci 74:367–373
Matsumoto E, Ueno H, Aruga D et al (2012) Accumulation of three clubroot resistance genes through marker-assisted selection in Chinese cabbage (Brassica rapa ssp. pekinensis). J Jpn Soc Hortic Sci 81:184–190
Min BW, Cho YN, Song MJ et al (2007) Successful genetic transformation of Chinese cabbage using phosphomannose isomerase as a selection marker. Plant Cell Rep 26:337–344
Mishima M, Takayama S, Sasaki K et al (2003) Structure of the male determinant factor for Brassica self-incompatibility. J Biol Chem 278:36389–36395
Mizushima U, Tsunoda S (1969) Aburana-zoku saibai-shu no kigen ni tuite. Agric Hortic 44:1347–1352. (in Japanese)
Moll RH, Lonnquist JH, Vélez Fortuno J, Johnson EC (1965) The relationship of heterosis and genetic divergence in maize. Genetics 52:139–144
Murase K, Shiba H, Iwano M et al (2004) A membrane-anchored protein kinase involved in Brassica self-incompatibility signaling. Science 303:1516–1519
Nakanishi T, Esashi Y, Hinata K (1969) Control of self-incompatibility by CO2 gas in Brassica. Plant Cell Phys 10:925–927
Nasrallah JB, Nasrallah ME (1993) Pollen-stigma signaling in the sporophytic self-incompatibility response. Plant Cell 5:1325–1335
Nasrallah JB, Nishio T, Nasrallah ME (1991) The self-incompatibility genes of Brassica: expression and use in genetic ablation of floral tissues. Annu Rev Plant Phys Plant Mol Biol 42:393–422
Nguyen ML, Monakhos GF, Komakhin RA, Monakhos SG (2018) The new clubroot resistance locus is located on chromosome A05 in Chinese cabbage (Brassica rapa L.). Russ J Genet 54:296–304
Niemann J, Kaczmarek J, Książczyk T et al (2017) Chinese cabbage (Brassica rapa ssp. pekinensis) – a valuable source of resistance to clubroot (Plasmodiophora brassicae). Eur J Plant Pathol 147:181–198
Niikura S, Matsuura S (2000) Genetic analysis of the reaction level of self-incompatibility to a 4% CO2 gas treatment in the radish (Raphanus sativus L.). Theor Appl Genet 101:1189–1193
Nishio T, Sakamoto K, Yamaguchi J (1994) PCR-RFLP of S locus for identification of breeding lines in cruciferous vegetables. Plant Cell Rep 13:546–550
Nishio T, Kusaba M, Watanabe M, Hinata K (1996) Registration of S alleles in Brassica campestris L by the restriction fragment sizes of SLGs. Theor Appl Genet 92:388–394
Nou IS, Watanabe M, Isogai A et al (1991) Variation of S-alleles and S-glycoproteins in a naturalized population of self-incompatible Brassica campestris L. Jpn J Genet 66:227–239
Nou IS, Watanabe M, Isuzugawa K et al (1993a) Isolation of S-allele from a wild population of Brassica campestris L. at Balcesme, Turkey and their characterization by S-glycoprotein. Sex Plant Reprod 6:71–78
Nou IS, Watanabe M, Isogai A, Hinata K (1993b) Comparison of S-alleles and S-glycoproteins between two wild populations of Brassica campestris in Turkey and Japan. Sex Plant Reprod 6:79–86
Ockendon DJ (1978) Effect of hexane and humidity on self-incompatibility in Brassica oleracea. Theor Appl Genet 52:113–117
Okazaki K, Hinata K (1987) Repressing the expression of self-incompatibility in crucifers by short-term high temperature treatment. Theor Appl Genet 73:496–500
Okuzaki A, Ogawa T, Koizuka C et al (2018) CRISPR/Cas9-mediated genome editing of the fatty acid desaturase 2 gene in Brassica napus. Plant Physiol Biochem 131:63–69
Olszak M, Truman W, Stefanowicz K et al (2019) Transcriptional profiling identifies critical steps of cell cycle reprogramming necessary for Plasmodiophora brassicae-driven gall formation in Arabidopsis. Plant J 97:715–729
Osabe K, Kawanabe T, Sasaki T et al (2012) Multiple mechanisms and challenges for the application of allopolyploidy in plants. Int J Mol Sci 13:8696–8721
Park JI, Nou IS, Lee SS et al (2001) Identification of S-genotypes by PCR-RFLP in breeding lines of Brassica. Mol Cells 12:227–232
Park JI, Lee SS, Watanabe M et al (2002) Identification of S-alleles using polymerase chain reaction-cleaved amplified polymorphic sequence of the S-locus receptor kinase in breeding lines of Brassica oleracea. Plant Breed 121:192–197
Piao ZY, Deng YQ, Choi SR et al (2004) SCAR and CAPS mapping of CRb, a gene conferring resistance to Plasmodiophora brassicae in Chinese cabbage (Brassica rapa ssp. pekinensis). Theor Appl Genet 108:1458–1465
Piao Z, Ramchiary N, Lim YP (2009) Genetics of clubroot resistance in Brassica species. J Plant Growth Regul 28:252–264
Pino Del Carpio D, Basnet RK, De Vos RCH et al (2011) The patterns of population differentiation in a Brassica rapa core collection. Theor Appl Genet 122:1105–1118
Pu Z, Shimizu M, Zhang Y et al (2012) Genetic mapping of a fusarium wilt resistance gene in Brassica oleracea. Mol Breed 30:809–818
Pu Z, Ino Y, Kimura Y et al (2016) Changes in the proteome of xylem sap in Brassica oleracea in response to Fusarium oxysporum stress. Front Plant Sci 7:31
Qiu L, Wu T, Dong H et al (2013) High-level expression of Sporamin in transgenic Chinese cabbage enhances resistance against diamondback moth. Plant Mol Biol Rep 31:657–664
Rahman H, Shakir A, Hasan MJ (2011) Breeding for clubroot resistant spring canola (Brassica napus L.) for the Canadian prairies: can the European winter canola cv. Mendel be used as a source of resistance? Can J Plant Sci 91:447–458
Ramchiary N, Nguyen VD, Li X et al (2011) Genic microsatellite markers in Brassica rapa: development, characterization, mapping, and their utility in other cultivated and wild Brassica relatives. DNA Res 18:305–320
Rolfe SA, Strelkov SE, Links MG et al (2016) The compact genome of the plant pathogen Plasmodiophora brassicae is adapted to intracellular interactions with host Brassica spp. BMC Genomics 17:272
Saeki N, Kawanabe T, Ying H et al (2016) Molecular and cellular characteristics of hybrid vigour in a commercial hybrid of Chinese cabbage. BMC Plant Biol 16:45
Sakamoto K, Nishio T (2001) Distribution of S haplotypes in commercial cultivars of Brassica rapa. Plant Breed 120:155–161
Sakamoto K, Saito A, Hayashida N et al (2008) Mapping of isolate-specific QTLs for clubroot resistance in Chinese cabbage (Brassica rapa L. ssp. pekinensis). Theor Appl Genet 117:759–767
Samuel MA, Chong YT, Haasen KE et al (2009) Cellular pathways regulating responses to compatible and self-incompatible pollen in Brassica and Arabidopsis stigmas intersect at Exo70A1, a putative component of the exocyst complex. Plant Cell 21:2655–2671
Sankaranarayanan S, Jamshed M, Samuel MA (2015) Degradation of glyoxalase I in Brassica napus stigma leads to self-incompatibility response. Nat Plants 1:15185
Sato K, Nishio T, Kimura R et al (2002) Coevolution of the S-locus genes SRK, SLG and SP11/SCR in Brassica oleracea and B. rapa. Genetics 162:931–940
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700
Schranz ME, Quijada P, Sung SB et al (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468
Schwelm A, Fogelqvist J, Knaust A et al (2015) The Plasmodiophora brassicae genome reveals insights in its life cycle and ancestry of chitin synthases. Sci Rep 5:11153
Shea DJ, Shimizu M, Nishida N et al (2017) IntroMap: a signal analysis based method for the detection of genomic introgressions. BMC Genet 18:101
Shea DJ, Itabashi E, Takada S et al (2018a) The role of FLOWERING LOCUS C in vernalization of Brassica: the importance of vernalization research in the face of climate change. Crop Past Sci 69:30–39
Shea DJ, Shimizu M, Itabashi E et al (2018b) Genome re-sequencing, SNP analysis, and genetic mapping of the parental lines of a commercial F1 hybrid cultivar of Chinese cabbage. Breed Sci 68:375–380
Shea DJ, Tomaru Y, Itabashi E et al (2018c) The production and characterization of a BoFLC2 introgressed Brassica rapa by repeated backcrossing to an F1. Breed Sci 68:316–325
Sheldon CC, Conn AB, Dennis ES, Peacock WJ (2002) Different regulatory regions are required for the vernalization-induced repression of FLOWERING LOCUS C and for the epigenetic maintenance of repression. Plant Cell 14:2527–2537
Shiba H, Takayama S, Iwano M et al (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol 125:2095–2103
Shiba H, Iwano M, Entani T et al (2002) The dominance of alleles controlling self-incompatibility in Brassica pollen is regulated at the RNA level. Plant Cell 14:491–504
Shiba H, Kakizaki T, Iwano M et al (2006) Dominance relationships between self-incompatibility alleles controlled by DNA methylation. Nat Genet 38:297–299
Shimizu M, Fujimoto R, Ying H et al (2014) Identification of candidate genes for fusarium yellows resistance in Chinese cabbage by differential expression analysis. Plant Mol Biol 85:247–257
Shimizu M, Pu Z, Kawanabe T et al (2015) Map-based cloning of a candidate gene conferring Fusarium yellows resistance in Brassica oleracea. Theor Appl Genet 128:119–130
Shimosato H, Yokota N, Shiba H et al (2007) Characterization of the SP11/SCR high-affinity binding site involved in self/nonself recognition in Brassica self-incompatibility. Plant Cell 19:107–117
Siemens J, Bulman S, Rehn F, Sundelin T (2009) Molecular biology of Plasmodiophora brassicae. J Plant Growth Regul 28:245–251
Some A, Manzanares MJ, Laurens F et al (1996) Variation for virulence on Brassica napus L. amongst Plasmodiophora brassicae collections from France and derived single-spore isolates. Plant Pathol 45:432–439
Song X, Liu G, Huang Z et al (2016) Temperature expression patterns of genes and their coexpression with LncRNAs revealed by RNA-Seq in non-heading Chinese cabbage. BMC Genomics 17:297
Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275
Stein JC, Howlett B, Boyes DC et al (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus of Brassica oleracea. Proc Natl Acad Sci U S A 88:8816–8820
Stephenson P, Baker D, Girin T et al (2010) A rich TILLING resource for studying gene function in Brassica rapa. BMC Plant Biol 10:62
Stone SL, Arnoldo M, Goring DR (1999) A breakdown of Brassica self-incompatibility in ARC1 antisense transgenic plants. Science 286:1729–1731
Stone SL, Anderson EM, Mullen RT, Goring DR (2003) ARC1 is an E3 ubiquitin ligase and promotes the ubiquitination of proteins during the rejection of self-incompatible Brassica pollen. Plant Cell 15:885–898
Strelkov SE, Hwang SF (2014) Clubroot in the Canadian canola crop: 10 years into the outbreak. Can J Plant Pathol 36:27–36
Strelkov SE, Tewari JP, Smith-Degenhardt E (2006) Characterization of Plasmodiophora brassicae populations from Alberta, Canada. Can J Plant Pathol 28:467–474
Su T, Wang W, Li P et al (2018) A genomic variation map provides insights into the genetic basis of spring Chinese cabbage (Brassica rapa ssp. pekinensis) selection. Mol Plant 11:1360–1376
Sun Q, Lin L, Liu D et al (2018a) CRISPR/Cas9-mediated multiplex genome editing of the BnWRKY11 and BnWRKY70 genes in Brassica napus L. Int J Mol Sci 19:2716
Sun X, Luo S, Luo L et al (2018b) Genetic analysis of Chinese cabbage reveals correlation between rosette leaf and leafy head variation. Front Plant Sci 9:1455
Suwabe K, Iketani H, Nunome T et al (2002) Isolation and characterization of microsatellites in Brassica rapa L. Theor Appl Genet 104:1092–1098
Suwabe K, Tsukazaki H, Iketani H et al (2003) Identification of two loci for resistance to clubroot (Plasmodiophora brassicae Woronin) in Brassica rapa L. Theor Appl Genet 107:997–1002
Suwabe K, Tsukazaki H, Iketani H et al (2006) Simple sequence repeat-based comparative genomics between Brassica rapa and Arabidopsis thaliana: the genetic origin of clubroot resistance. Genetics 173:309–319
Suwabe K, Suzuki G, Watanabe M (2010) Achievement of genetics in plant reproduction research: the past decade for the coming decade. Genes Genet Syst 85:297–310
Suzuki G, Kai N, Hirose T et al (1999) Genomic organization of the S locus: identification and characterization of genes in SLG/SRK region of S9 haplotype of Brassica campestris (syn. rapa). Genetics 153:391–400
Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462:799–802
Takada Y, Nakanowatari T, Sato J et al (2005) Genetic analysis of novel intra-species unilateral incompatibility in Brassica rapa (syn. campestris) L. Sex Plant Reprod 17:211–217
Takada Y, Sato T, Suzuki G et al (2013) Involvement of MLPK pathway in intraspecies unilateral incompatibility regulated by a single locus with stigma and pollen factors. G3: Genes Genom Genet 3:719–726
Takada Y, Murase K, Shimosato-Asano H et al (2017) Duplicated pollen–pistil recognition loci control intraspecific unilateral incompatibility in Brassica rapa. Nat Plants 3:17096
Takahashi S, Osabe K, Fukushima N et al (2018a) Genome-wide characterization of DNA methylation, small RNA expression, and histone H3 lysine nine di-methylation in Brassica rapa L. DNA Res 25:511–520
Takahashi S, Fukushima N, Osabe K et al (2018b) Identification of DNA methylated regions by using methylated DNA immunoprecipitation sequencing in Brassica rapa. Crop Past Sci 69:107–120
Takasaki T, Hatakeyama K, Suzuki G et al (2000) The S receptor kinase determines self-incompatibility in Brassica stigma. Nature 403:913–916
Takayama S, Shiba H, Iwano M et al (2000a) The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci U S A 97:1920–1925
Takayama S, Shiba H, Iwano M et al (2000b) Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc Natl Acad Sci U S A 97:3765–3770
Takayama S, Shimosato H, Shiba H et al (2001) Direct ligand–receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538
Tanaka S, Fujiyama S, Shigemori S et al (1998) Pathogenesis of isolates of Plasmodiophora brassicae from Japan (1) Race and pathogenesis in clubroot resistant cultivars. Kyushu PI Prot Res 44:15–19
Tantikanjana T, Nasrallah JB (2015) Ligand-mediated cis-inhibition of receptor signaling in the self-incompatibility response of the Brassicaceae. Plant Physiol 169:1141–1154
Tarutani Y, Shiba H, Iwano M et al (2010) Trans-acting small RNA determines dominance relationships in Brassica self-incompatibility. Nature 466:983–986
Thompson KF, Taylor JP (1966) Non-linear dominance relationships between S alleles. Heredity 21:345–362
Tommerup IC, Ingram DS (1971) The life-cycle of Plasmodiophora brassicae Woron. In Brassica tissue cultures and in intact roots. New Phytol 70:327–332
Tonosaki K, Michiba K, Bang SW et al (2013) Genetic analysis of hybrid seed formation ability of Brassica rapa in intergeneric crossings with Raphanus sativus. Theor Appl Genet 126:837–846
Tonosaki K, Osabe K, Kawanabe T, Fujimoto R (2016) The importance of reproductive barriers and the effect of allopolyploidization on crop breeding. Breed Sci 66:333–349
Tsunoda S, Hinata K, Gomez-Campo C (1980) Brassica crops and wild allies - biology and breeding. Japan Scientific Societies Press, Tokyo
U N (1935) Genome analysis in Brassica with special reference to the experimental formation of B. napus and peculiar mode of fertilization. Jpn J Bot 7:389–452
Ueno H, Matsumoto E, Aruga D et al (2012) Molecular characterization of the CRa gene conferring clubroot resistance in Brassica rapa. Plant Mol Biol 80:621–629
Vanjildorj E, Song SY, Yang ZH et al (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
Voorrips RE (1995) Plasmodiophora brassicae: aspects of pathogenesis and resistance in Brassica oleracea. Euphytica 83:139–146
Walker JC (1930) Inheritance of fusarium resistance in cabbage. J Agric Res 40:721–745
Wallenhammar AC (1998) Observations on yield loss from Plasmodiophora brassicae infections in spring oilseed rape. J Plant Dis Protect 105:1–7
Wang L, Yu X, Wang H et al (2011a) A novel class of heat-responsive small RNAs derived from the chloroplast genome of Chinese cabbage (Brassica rapa). BMC Genomics 12:289
Wang X, Wang H, Wang J et al (2011b) The genome of the mesopolyploid crop species Brassica rapa. Nat Genet 43:1035–1039
Wang Y, Wu F, Bai J, He Y (2014) BrpSPL9 (Brassica rapa ssp. pekinensis SPL9) controls the earliness of heading time in Chinese cabbage. Plant Biotechnol J 12:312–321
Wang A, Hu J, Huang X et al (2016) Comparative transcriptome analysis reveals heat-responsive genes in Chinese cabbage (Brassica rapa ssp. chinensis). Front. Plant Sci 7:939
Wang A, Hu J, Gao C et al (2019) Genome-wide analysis of long non-coding RNAs unveils the regulatory roles in the heat tolerance of Chinese cabbage (Brassica rapa ssp. chinensis). Sci Rep 9:5002
Warwick SI, Francis A, Al-Shehbaz IA (2006) Brassicaceae: species checklist and database on CD-Rom. Plant Syst Evol 259:249–258
Watanabe M, Takasaki T, Toriyama K et al (1994) A high degree of homology exists between the protein encoded by SLG and the S receptor domain encoded by SRK in self-incompatible Brassica campestris L. Plant Cell Phys 35:1221–1229
Watanabe M, Ito A, Takada Y et al (2000) Highly divergent sequences of the pollen self-incompatibility (S) gene in class-I S haplotypes of Brassica campestris (syn. rapa) L. FEBS Lett 473:139–144
Watanabe M, Suwabe K, Suzuki G (2012) Molecular genetics, physiology and biology of self-incompatibility in Brassicaceae. Proc Jpn Acad Ser B 88:519–535
Whittaker C, Dean C (2017) The FLC locus: a platform for discoveries in epigenetics and adaptation. Annu Rev Cell Dev Biol 33:555–575
Williams PH (1966) A system for the determination of races of Plasmodiophora brassicae that infect cabbage and rutabaga. Phytopathology 56:624–626
Yamagishi H, Bhat SR (2014) Cytoplasmic male sterility in Brassicaceae crops. Breed Sci 64:38–47
Yang M, Wang X, Ren D et al (2017) Genomic architecture of biomass heterosis in Arabidopsis. Proc Natl Acad Sci U S A 114:8101–8106
Yasuda S, Wada Y, Kakizaki T et al (2016) A complex dominance hierarchy is controlled by polymorphism of small RNAs and their targets. Nat Plants 3:16206
Yoshikawa H (1983) Breeding for clubroot resistance of crucifer crop in Japan. Jpn Agric Res Q 17:6–11
Yoshikawa H, Buczacki ST (1978) Clubroot in Japan: research and problems. Rev Plant Pathol 57:253–257
Yu X, Wang H, Lu Y et al (2012) Identification of conserved and novel microRNAs that are responsive to heat stress in Brassica rapa. J Exp Bot 63:1025–1038
Yu F, Zhang X, Huang Z et al (2016) Identification of genome-wide variants and discovery of variants associated with Brassica rapa clubroot resistance gene Rcr1 through bulked segregant RNA sequencing. PLoS One 11:e0153218
Yu F, Zhang X, Peng G et al (2017) Genotyping-by-sequencing reveals three QTL for clubroot resistance to six pathotypes of Plasmodiophora brassicae in Brassica rapa. Sci Rep 7:4516
Zhang FL, Takahata Y, Xu JB (1998) Medium and genotype factors influencing shoot regeneration from cotyledonary explants of Chinese cabbage (Brassica campestris L. ssp. pekinensis). Plant Cell Rep 17:780–786
Zhang J, Liu F, Yao L et al (2012) Development and bioassay of transgenic Chinese cabbage expressing potato proteinase inhibitor II gene. Breed Sci 62:105–112
Zhao J, Kulkarni V, Liu N et al (2010) BrFLC2 (FLOWERING LOCUS C) as a candidate gene for a vernalization response QTL in Brassica rapa. J Exp Bot 61:1817–1825
Acknowledgements
This chapter includes results supported by grants from Project of the NARO Bio-oriented Technology Research Advancement Institution (Research program on development of innovation technology), JSPS Bilateral Joint Research Projects, and international cooperation program managed by the National Research Foundation of Korea (NRF-2018K2A9A2A08000113). We thank Dr. Elizabeth S. Dennis, Dr. Kenji Osabe, and Dr. Daniel J. Shea for their helpful comments and manuscript editing.
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Appendices
Appendices
1.1 Appendix I: Research Institutes Relevant to Chinese Cabbage
Institution | Specialization and research activities | Contact information and website |
|---|---|---|
Beijing Vegetable Research Center (BVRC), Beijing Academy of Agriculture and Forestry Science (BAAFS) | Genetic analysis on agronomical important traits | |
Chungnam National University | Genetics and molecular marker development in Chinese cabbage | |
Graduate School of Agricultural Science, Kobe University | Epigenetics, heterosis, vernalization | |
Graduate School of Life Sciences, Tohoku University | Self-incompatibility | |
Graduate School of Sciences and Technology, Niigata University | Disease resistance | |
Henan Academy of Agricultural Sciences | Creation of germplasm resources and QTL mapping for different traits in Chinese cabbage | |
Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences (IVF, CAAS) | Whole genome sequencing | |
John Innes Centre | Whole genome sequencing, germplasm resources | |
National Institute of Horticultural and Herbal Science | Germplasm collection, molecular marker and cultivar development in Brassicaceae | |
RIKEN BioResource Center | Germplasm resources | |
Shanghai Institutes for Biological Sciences, Chinese Academy of Sciences | Leafy heads of Chinese cabbage | |
State Key Laboratory of Crop Genetics and Germplasm Enhancement, Nanjing Agricultural University | Flowering | |
Sunchon National University | Genetic inheritance and molecular breeding of clubroot resistant Chinese cabbage | |
The National Agriculture and Food Research Organization in Japan | Development of parental lines for clubroot resistant Chinese cabbage using MAS | |
Tohoku university Brassica seed bank | Seed bank of Bressicaceae germplasm | http://www.agri.tohoku.ac.jp/pbreed/Seed_Stock_DB/Stock_English_top.html |
Wageningen UR Plant Breeding, Wageningen University and Research Centre | Genetic analysis on agronomical important traits |
1.2 Appendix II: Genetic Resources of Chinese Cabbage
Cultivar | Important traits | Cultivation location |
|---|---|---|
Akimeki | Clubroot (Crr1, Crr2, CRb) | Norin seed Co., Japan |
Bre | Inbred line of medium-cycling crop type | China |
Chihiri 70 | Transformable strain | Takii Seed Co., Japan |
Chiifu-401 | The first whole genome sequenced Chinese cabbage | Korea and Japan |
CR gangsan | Clubroot (Crr2, CRb, CRa) | Nonghyeob seed Co., Korea |
CR Shinki | Clubroot (CRb) | Takii Seed Co., Japan |
Gokurakuten | High regeneration rate, creation of transgenic Brassica rapa | Takii Seed Co., Japan |
R-o-18 | Reverse genetics (EMS-induced mutagenesis population) | UK |
RJKB lines | Inbred lines | Japan |
W39 | Biomass heterosis, early developmental heterosis | Watanabe seed Co., Japan |
Wantai | Inbred line of slow-cycling crop type | China |
Yellow sarson | Self-compatible, mutant for S-genes and MLPK gene | India |
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Okamoto, T. et al. (2021). Chinese Cabbage (Brassica rapa L. var. pekinensis) Breeding: Application of Molecular Technology. In: Al-Khayri, J.M., Jain, S.M., Johnson, D.V. (eds) Advances in Plant Breeding Strategies: Vegetable Crops. Springer, Cham. https://doi.org/10.1007/978-3-030-66969-0_2
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