Skip to main content
Log in

Investigation of the genes associated with a male sterility mutant (msm) in Chinese cabbage (Brassica campestris ssp. pekinensis) using RNA-Seq

  • Original Article
  • Published:
Molecular Genetics and Genomics Aims and scope Submit manuscript

Abstract

In Chinese cabbage, hybrid seed production is performed using male sterility lines, an important approach to heterosis utilization. In this study, a stably inherited male sterile mutant msm was obtained from the ‘FT’-doubled haploid line of Chinese cabbage using isolated microspore culture combined with 60Co γ-ray mutagenesis. The genetic backgrounds of ‘FT’ and msm were highly consistent; however, compared with wild-type ‘FT’, msm exhibited completely degenerated stamens and no pollen phenotype. Other characters showed no significant differences. Cytological observations revealed that stamen abortion in msm begins during the tetrad period and that tapetum cells were abnormally expanded and highly vacuolated, leading to microspore abortion. Genetic analysis indicated that the msm mutant phenotype is controlled by a single recessive nuclear gene. Comparative transcriptome analysis of ‘FT’ and msm flower buds using RNA-Seq technology revealed 1653 differentially expressed genes, among which, a large number associated with male sterility were detected, including 64 pollen development- and pollen tube growth-related genes, 94 pollen wall development-related genes, 11 phytohormone-related genes, and 16 transcription factor-related genes. An overwhelming majority of these genes were down-regulated in msm compared with ‘FT’. Furthermore, KEGG pathway analysis indicated that a variety of carbohydrate metabolic and lipid metabolic pathways were significantly enriched, which may be related to pollen abortion. The expression patterns of 24 male sterility-related genes were analyzed using qRT-PCR. In addition, 24,476 single-nucleotide polymorphisms and 413,073 insertion–deletion events were specifically detected in msm. These results will facilitate elucidation of the regulatory mechanisms underlying male sterility in Chinese cabbage.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abdi H (2007) Bonferroni and Šidák corrections for multiple comparisons. In: Salkind N (ed) Encyclopedia of measurement and statistics. SAGE, Thousand Oaks, pp 103–107

    Google Scholar 

  • Adamczyk BJ, Fernandez DE (2009) MIKC* MADS domain heterodimers are required for pollen maturation and tube growth in Arabidopsis. Plant Physiol 149:1713–1723

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An H, Yang ZH, YiB Wen J, Shen JX, Tu JX, Ma CZ, Fu TD (2014) Comparative transcript profiling of the fertile and sterile flower buds of pol CMS in B. napus. BMC Genomics 15:258

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106

    Article  CAS  PubMed  PubMed Central  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. Gene Ontol Consortium Nat Genet 25:25–29

    CAS  Google Scholar 

  • Bou DF, van Oostende C, Geitmann A (2011) Spatial and temporal expression of actin depolymerizing factors ADF7 and ADF10 during male gametophyte development in Arabidopsis thaliana. Plant Cell Physiol 52:1177–1192

    Article  CAS  Google Scholar 

  • Cao MJ, Cheng J, Wang J, Zhang CB, Pan GT, Rong TZ (2010) Relationship between phytohormones and genic male sterility induced by space flight in maize. J Nucl Agric Sci 24:447–452

    CAS  Google Scholar 

  • Chen LT, Liu YG (2014) Male sterility and fertility restoration in crops. Annu Rev Plant Biol 65:579–606

    Article  CAS  PubMed  Google Scholar 

  • Chen JJ, Pang WX, Chen B, Zhang CY, Piao ZY (2016) Transcriptome analysis of Brassica rapa near-isogenic lines carrying clubroot-resistant and –susceptible alleles in response to Plasmodiophora brassicae during early infection. Front Plant Sci 6:1183

    PubMed  PubMed Central  Google Scholar 

  • Chong YT, Gidda SK, Sanford C, Parkinson J, Mullen RT, Goring DR (2010) Characterization of the Arabidopsis thaliana exocyst complex gene families by phylogenetic, expression profiling, and subcellular localization studies. New Phytol 185:401–419

    Article  CAS  PubMed  Google Scholar 

  • Czemmel S, Heppel CS, Bogs J (2012) R2R3MYB transcription factors: key regulators of the flavonoid biosynthetic pathway in grapevine. Protoplasma 249:109–118

    Article  CAS  Google Scholar 

  • Dong MY, Zhang LG, Deng YL (2008) The cytomorphology of the fertility restoration in thermo-sensitive male sterile Chinese cabbage TsCMS7311. Acta Agri Boreali-Occidentalis Sin 17:104–108

    Google Scholar 

  • Dong XS, Feng H, Xu M, Lee J, Kim YK, Lim YP, Piao ZY, Park YD, Ma H, Hur Y (2013) Comprehensive analysis of genic male sterility-related genes in Brassica rapa using a newly developed Br 300 K oligomeric chip. PLoS ONE 8:e72178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dou JS, Wang LL, Yan JP, Fu MY, Zhang X, Xu F (2017) Molecular cloning and expression analysis of a AGAMOUS-like 66 gene (GbAGL66) in Ginkgo biloba. Biotechnology 16:100–107

    Article  CAS  Google Scholar 

  • Dukowic-Schulze S, Harris A, Li JH, Sundararajan A, Mudge J, Retzel EF, Pawlowski WP, Chen CB (2014) Comparative transcriptomics of early meiosis in Arabidopsis and maize. J Genet Genomics 41:139–152

    Article  PubMed  Google Scholar 

  • Feng ZM, Zhang FL, Zhang DS, Yu XC (2005) Study on changes of hormones in anther at different development stage in cytoplasmic male sterility line and its maintainer of Chinese cabbage. Acta Agri Boreali-Sin 20:40–43

    Google Scholar 

  • Feng B, Lu D, Ma X, Peng Y, Sun Y, Ning G, Ma H (2012) Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J 72:612–624

    Article  CAS  PubMed  Google Scholar 

  • Gu JN, Zhu J, Yu Y, Teng XD, Lou Y, Xu XF, Liu JL, Yang ZN (2014) DYT1 directly regulates the expression of TDF1 for tapetum development and pollen wall formation in Arabidopsis. Plant J 80:1005–1013

    Article  CAS  PubMed  Google Scholar 

  • Guan YF, Meng XZ, Khanna R, LaMontagne E, Liu YD, Zhang SQ (2014) Phosphorylation of a WRKY transcription factor by MAPKs is required for pollen development and function in Arabidopsis. PLoS Genet 10:e1004384

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo JX, Liu YG (2012) Molecular control of male reproductive development and pollen fertility in rice. J Integr Plant Biol 54:967–978

    Article  CAS  PubMed  Google Scholar 

  • Guo JX, Sun RF, Song JX, Zhang SJ (2001) Microsporogenesis of several male-sterile lines in Brassica rapa L. ssp. Pekinensis. Acta Hortic Sin 28:409–414

    Google Scholar 

  • Guo RX, Sun DF, Tan ZB, Rong DF, Li CD (2006) Two recessive genes controlling thermophotoperiod-sensitive male sterility in wheat. Theor Appl Genet 112:1271–1276

    Article  CAS  PubMed  Google Scholar 

  • Guo YH, Zhang LS, Lin TR, Jiang KX, Qu MN (2010) Comparative study on anther cytology of different sterile lines in rice. Jiangsu Agric Sci 1:91–94

    Google Scholar 

  • Hu Y, Wu Q, Liu S, Wei L, Chen X (2005) Study of rice pollen grains by multispectral imaging microscopy. Microsc Res Tech 68:335–346

    Article  PubMed  Google Scholar 

  • Huang L, Ye YQ, Zhang YC, Zhang AH, Liu TT, Cao JS (2009) BcMF9, a novel polygalacturonase gene, is required for both Brassica campestris intine and exine formation. Ann Bot 104:1339–1351

    Article  CAS  PubMed  PubMed Central  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 Breeding 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 

  • Huang SN, Liu ZY, Li CY, Yao RP, Li DY, Hou L, Li X, Liu WJ, Feng H (2017) Transcriptome analysis of a female-sterile mutant (fsm) in Chinese cabbage (Brassica campestris ssp. pekinensis). Front Plant Sci 8:546

    PubMed  PubMed Central  Google Scholar 

  • Ji JL, Yang LM, Fang ZY, Zhuang M, Zhang YY, Lv HH, Liu YM, Li ZS (2017) Recessive male sterility in cabbage (Brassica oleracea var. capitata) caused by loss of function of BoCYP704B1due to the insertion of a LTR-retrotransposon. Theor Appl Genet 130:1441–1451

    Article  CAS  PubMed  Google Scholar 

  • Jiang CM, Li CP, Chang JC, Chang HM (2002) Characterization of pectinesterase inhibitor in jelly fig (Ficus awkeotsang Makino) achenes. J Agric Food Chem 50:4890–4894

    Article  CAS  PubMed  Google Scholar 

  • Jiang Y, Zeng B, Zhao HN, Zhang M, Xie SJ, Lai JS (2012) Genome-wide transcription factor gene prediction and their expressional tissue-specificities in maize. J Integr Plant Biol 54:616–630

    Article  CAS  PubMed  Google Scholar 

  • Jiang JX, Lv ML, Liang Y, Ma ZM, Cao JS (2014) Identification of novel and conserved miRNAs involved in pollen development in Brassica campestris ssp. chinensis by high-throughput sequencing and degradome analysis. BMC Genomics 15:146

    Article  PubMed  PubMed Central  CAS  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 

  • Lai KS (2016) Analysis of EXO70C2 expression revealed its specific association with late stages of pollen development. Plant Cell Tiss Org 124:209–215

    Article  CAS  Google Scholar 

  • Lamport DTA, Varnai P (2013) Periplasmic arabinogalactan glycoproteins acts as a calcium capacitor that regulates plant growth and development. New Phytol 197:58–64

    Article  CAS  PubMed  Google Scholar 

  • Laser KD, Lersten NR (1972) Anatomy and cytology of microsporogenesis in cytoplasmic male sterile Angiosperms. Bot Rev 38:425–454

    Article  Google Scholar 

  • Lee DH, Lee IC, Kim KJ, Kim DS, Na HJ, Lee IJ, Kang SM, Jeon HW, Le PY, Ko JH (2014) Expression of gibberellin 2-oxidase 4 from Arabidopsis under the control of a senescence-associated promoter results in a dominant semi-dwarf plant with normal flowering. J Plant Biol 57:106–116

    Article  CAS  Google Scholar 

  • Li LL, Zhang SL (2006) Regulative effects of plant growth substances on male fertility. Chinese Agri Sci Bull 22:211–215

    CAS  Google Scholar 

  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R (2009a) The sequence alignment-map format and SAMtools. Bioinformatics 25:2078–2079

    Article  PubMed  PubMed Central  Google Scholar 

  • Li W, Ma LJ, He BR (2009b) Change of some physiological characters in the fertility sensitive period of two types of temperature sensitive male sterile wheat lines. J Triticeae Crops 29:89–92

    Google Scholar 

  • Li RQ, Yu C, Li YR, Lam TW, Yiu SM, Kristiansen K, Wang J (2009c) SOAP2: an improved ultrafast tool for short read alignment. Bioinformatics 25:1966–1967

    Article  CAS  PubMed  Google Scholar 

  • Li SP, van Os GMA, Ren SC, Yu DL, Ketelaar T, Emons AMC, Liu CM (2010) Expression and functional analyses of EXO70 genes in Arabidopsis implicate roles in regulating cell type-specific exocytosis. Plant Physiol 154:1819–1830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu QY, Liu FH, He KY, Zhu XW, Li LX (2006) Preliminary study on the relationship between cytoplasmic male sterility and the contents of flower bud endogenous hormone in tobacco. Acta Agri Boreali-Sin 21:79–82

    CAS  Google Scholar 

  • Liu TK, Li Y, Zhang CW, Duan WK, Huang FY, Hou XL (2014) Basic helix-loop-helix transcription factor BcbHLHpol functions as a positive regulator of pollen development in non-heading Chinese cabbage. Funct Integr Genomics 14:731–739

    Article  CAS  PubMed  Google Scholar 

  • Liu YM, Zhang L, Zhou JY, Cao MJ (2015) Research progress of the bHLH transcription factors involved in genic male sterility in plants. Hereditas (Beijing) 37:1194–1203

    CAS  Google Scholar 

  • Liu C, Liu ZY, Li CY, Zhang Y, Feng H (2016) Comparative transcriptome analysis of fertile and sterile buds from a genetically male sterile line of Chinese cabbage. Vitro Cell Dev-Pl 52:130–139

    Article  CAS  Google Scholar 

  • Lou P, Kang JG, Zhang GY, Bonnema G, Fang ZY, Wang XW (2007) Transcript profiling of a dominant male sterile mutant (Ms-cd1) in cabbage during flower bud development. Plant Sci 172:111–119

    Article  CAS  Google Scholar 

  • Luo DP, Xu H, Liu ZL, Guo JX, Li HY, Chen LT, Fang C, Zhang QY, Bai M, Yao N, Wu H, Wu H, Ji CH, Zheng HQ, Chen YL, Ye S, Li XY, Zhao XC, Li RQ, Liu YG (2013) A detrimental mitochondrial-nuclear interaction causes cytoplasmic male sterility in rice. Nat Genet 45:573–577

    Article  CAS  PubMed  Google Scholar 

  • Meuter-Gerhards A, Riegert S, Wiermann R (1999) Studies on sporopollenin biosynthesis in Cucurbita maxima (DUCH.)-II. The involvement of aliphatic metabolism. J Plant Physiol 154:431–436

    Article  CAS  Google Scholar 

  • Moon S, Kim SR, Zhao GC, Yi J, Yoo Y, Jin P, Lee SW, Jung KH, Zhang DB, An G (2013) Rice GLYCOSYLTRANSFERASE1 encodes a glycosyltransferase essential for pollen wall formation. Plant Physiol 161:663–675

    Article  CAS  PubMed  Google Scholar 

  • Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628

    Article  CAS  PubMed  Google Scholar 

  • Ni F, Qi J, Hao QQ, Lyu B, Luo MC, Wang Y, Chen FJ, Wang SY, Zhang CZ, Epstein Zhao XY, Wang HG, Zhang XS, Chen CX, Sun LZ, Fu DL (2017) Wheat Ms2 encodes for an orphan protein that confers male sterility in grass species. Nat Commun 8:15121

    Article  PubMed  PubMed Central  Google Scholar 

  • Parish RW, Li SF (2010) Death of a tapetum: a programme of developmental altruism. Plant Sci 178:73–89

    Article  CAS  Google Scholar 

  • Phan HA, Iacuone S, Li SF, Parish RW (2011) The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23:2209–2224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu CM, Fu FY, Liu M, Zhao HY, Liu C, Li JN, Tang ZL, Xu XF, Qiu X, Wang R, Lu K (2015) Comparative transcriptome analysis of recessive male sterility (RGMS) in sterile and fertile Brassica napus lines. PLoS ONE 10:e0144118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rao GS, Tyagi AK, Rao KV (2017) Development of an inducible male-sterility system in rice through pollen-specific expression of l-ornithinase (argE) gene of E. coli. Plant Sci 256:139–147

    Article  CAS  PubMed  Google Scholar 

  • Reimegård J, Kundu S, Pendle A, Irish V, Shaw P, Nakayama N, Sundström JF, Emanuelsson O (2017) Genome-wide identification of physically clustered genes suggests chromatin-level co-regulation in male reproductive development in Arabidopsis thaliana. Nucleic Acids Res 45:3253–3265

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Ruzicka DR, Kandasamy MK, McKinney EC, Burgos-Rivera B, Meagher RB (2007) The ancient subclasses of Arabidopsis Actin Depolymerizing Factor genes exhibit novel and differential expression. Plant J 52:460–472

    Article  CAS  PubMed  Google Scholar 

  • Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:S46–S60

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi GJ, Hou XL, Hu W (2004) Changes of endogenous hormones and polyamines in cytoplasmic male sterile non-heading Chinese cabbage during anther development. Acta Bot Boreali-Occidentalia Sin 24:2109–2112

    CAS  Google Scholar 

  • Shi J, Liang WQ, Zhang DB (2007) Pollen wall development in plant. Plant Physiol Commun 43:588–592

    Google Scholar 

  • Song XY, Hu YG, Ma LJ, Li HB, He BR (2009) Changes of material content in panicles and leaves of YS type thermo-sensitive male sterile wheat line A3314 during transfer from sterility to fertility. J Northwest A&F Univ (Nat Sci Ed) 37:81–91

    CAS  Google Scholar 

  • Song XY, Qian HH, Zhang LL (2014) Cytogenetic analysis of cytoplasmic male sterility in wheat line KTP116A and molecular mapping of two thermo-sensitive restoration genes. Euphytica 196:129–136

    Article  CAS  Google Scholar 

  • Sousa E, Kost B, Malhό R (2008) Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. Plant Cell 20:3050–3064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang RS, Zheng JC, Jin ZQ, Zhang D, Huang H, Chen LG (2008) Possible correlation between high temperature-induced floret sterility and endogenous levels of IAA, GAs and ABA in rice (Oryza sativa L.). Plant Growth Regul 54:37–43

    Article  CAS  Google Scholar 

  • Thorstensen T, Grini PE, Mercy IS, Alm V, Erdal S, Aasland R, Aalen RB (2008) The Arabidopsis SET-domain protein ASHR3 is involved in stamen development and interacts with the bHLH transcription factor Aborted Microspores (AMS). Plant Mol Biol 66:47–59

    Article  CAS  PubMed  Google Scholar 

  • Twell D (2010) Male gametophyte development. In: Pua EC, Davey MR (eds) Plant developmental biology-biotechnological perspectives, vol 1. Springer, Berlin, pp 225–244

    Chapter  Google Scholar 

  • Verelst W, Saedler H, Munster T (2007a) MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters. Plant Physiol 143:447–460

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verelst W, Twell D, de Folter S, Immink R, Saedler H, Münster T (2007b) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8:R249

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wang Y, Zhang WZ, Song LF, Zou JJ, Su Z, Wu WH (2008) Transcriptome analyses show changes in gene expression to accompany pollen germination and tube growth in Arabidopsis. Plant Physiol 148:1201–1211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei MM, Wei HL, Wu M, Song MZ, Zhang JF, Yu JW, Fan SL, Yu SX (2013) Comparative expression profiling of miRNA during anther development in genetic male sterile and wild type cotton. BMC Plant Biol 13:1–14

    Article  CAS  Google Scholar 

  • Wu YL, Min L, Wu ZC, Yang L, Zhu LF, Yang XY, Yuan DJ, Guo XP, Zhang XL (2015) Defective pollen wall contributes to male sterility in the male sterile line 1355A of cotton. Sci Rep 5:9608

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xia C, Zhang LC, Zou C, Gu YQ, Duan JL, Zhao GY, Wu JJ, Liu Y, Fang XH, Gao LF, Jiao YN, Sun JQ, Pan YH, Liu X, Jia JZ, Kong XY (2017) A TRIM insertion in the promoter of Ms2 causes male sterility in wheat. Nat Commun 8:15407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xie HY, Jiang PD, Wang XL, Zhang ZW, Zhu W, Wang XD (2006) Changes of phytohormone contents in anther abortion of cytoplasmic male sterile cotton. Acta Agron Sin 32:1094–1096

    CAS  Google Scholar 

  • Xu J, Ding Z, Vizcay-Barrena G, Shi J, Liang W, Yuan Z, Werck-Reichhart D, Schreiber L, Wilson ZA, Zhang D (2014a) Aborted Microspores acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26:1544–1556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu XY, Zhang J, Sun XL, Li ML, Lei M, Zhang LG (2014b) The relationship between male sterile occurrence and dynamics of endogenous hormone contents during flower bud development in CMS7311 of heading Chinese cabbage. Acta Agri Boreali-Sin 29:177–182

    Google Scholar 

  • Xun ZL, Li XP, Zhang DD, Lu H, Liu D (2014) Functional analysis of transcription factor WRKY18 in pollen development of Arabidopsis thaliana (L.) Heynh. J Chin Electron Microsc Soc 33:156–162

    CAS  Google Scholar 

  • Yang LF, Diao XM (2013) Progress in identification of plant male sterility related nuclear genes. J Plant Genet Resour 14:1108–1117

    CAS  Google Scholar 

  • Yang K, Chen Y, Shi M, Converse R, Chen X, Zhao BM, Zhang Y, Lv J (2017) A novel dominant rice male sterility mutant, OsDMS-1, simultaneously controlled by independent loci on chromosomes 1, 2, and 3. Mol Breeding 37:25

    Article  CAS  Google Scholar 

  • Yu YC, Qiao M, Liu ZH, Xiang FN (2010) Diversification function of WRKY transcription factor. Chin Bull Life Sci 22:345–351

    Google Scholar 

  • Zhang FL, Feng ZM, Zhang DS, Yu XC (2007) Studies on physiological and biochemical mechanisms for cytoplasmic male sterility in Chinese cabbage. Acta Agri Boreali-Sin 22:101–105

    Google Scholar 

  • Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610

    Article  CAS  PubMed  Google Scholar 

  • Zheng YY, Xie YR, Jiang YX, Qu XL, Huang SJ (2013) Arabidopsis actin depolymerizing factor 7 severs actin filaments and regulates actin cable turnover to promote normal pollen tube growth. Plant Cell 25:3405–3423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Liu ZY, Ji RQ, Feng H (2017) Comparative transcript profiling of fertile and sterile flower buds from multiple-allele-inherited male sterility in Chinese cabbage (Brassica campestris L. ssp. pekinensis). Mol Genet Genomics 292:967–990

    Article  CAS  PubMed  Google Scholar 

  • Zhu HF, Hou RX, Li XF, Zhu YY, Hou XL (2011a) Cytological observation of anther development between the male sterile line and its maintainer line in non-heading Chinese cabbage. Plant Sci J 29:183–187

    Article  CAS  Google Scholar 

  • Zhu J, Lou Y, Xu XF, Yang ZN (2011b) A genetic pathway for tapetum development and function in Arabidopsis. J Integr Plant Biol 53:892–900

    Article  CAS  PubMed  Google Scholar 

  • Zhu EG, You CJ, Wang SS, Cui J, Niu BX, Wang YX, Qi J, Ma H, Chang F (2015) The DYT1-interacting proteins bHLH010, bHLH089 and bHLH091 are redundantly required for Arabidopsis anther development and transcriptome. Plant J 83:976–990

    Article  CAS  PubMed  Google Scholar 

  • Zinkl GM, Zwiebel BI, Grier DG, Preuss D (1999) Pollen-stigma adhesion in Arabidopsis: a species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 126:5431–5440

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China (31801854) and the Doctoral Start-up Foundation of Liaoning Province (20170520096).

Author information

Authors and Affiliations

Authors

Contributions

HF, SNH, and ZYL conceived and designed the research; SLP, CYL, and TC performed the experiments; SNH, RPY, DYL, XL, and LH analyzed the data; SNH wrote the paper. All authors approved the manuscript.

Corresponding author

Correspondence to Hui Feng.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Database linking

The transcriptome sequencing data have been deposited in the NCBI Gene Expression Omnibus (GEO) Database under Accession Number GSE125485.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Communicated by Stefan Hohmann.

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Fig. S1

Distribution of gene coverage in ‘FT’ and msm. (TIFF 2060 kb)

Fig. S2

GO functional classification of DEGs in the msm versus ‘FT’ comparison. (TIFF 2226 kb)

Table S1

Primers sequences used for qRT-PCR analysis. (XLS 17 kb)

Table S2

Read statistics based on the RNA-Seq data of six libraries from ‘FT’ and msm. (XLSX 10 kb)

Table S3

List of all genes detected in the ‘FT’ and msm libraries. (XLS 14592 kb)

Table S4

List of DEGs identified in the msm versus ‘FT’ comparison. (XLS 473 kb)

Table S5

List of SEGs identified in the msm versus ‘FT’ comparison. (XLSX 69 kb)

Table S6

Significantly enriched GO terms identified in the msm versus ‘FT’ comparison. (XLS 38 kb)

Table S7

Summary of SNP types identified in ‘FT’ and msm. (XLS 26 kb)

Table S8

SNPs specifically detected in the ‘FT’ library. (XLSX 1054 kb)

Table S9

SNPs specifically detected in the msm library (XLSX 1063 kb)

Table S10

Insertions detected between ‘FT’ and msm libraries. (XLSX 11490 kb)

Table S11

Supplementary material 13 Deletions detected between ‘FT’ and msm libraries. (XLSX 21675 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, S., Peng, S., Liu, Z. et al. Investigation of the genes associated with a male sterility mutant (msm) in Chinese cabbage (Brassica campestris ssp. pekinensis) using RNA-Seq. Mol Genet Genomics 295, 233–249 (2020). https://doi.org/10.1007/s00438-019-01618-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00438-019-01618-z

Keywords

Navigation