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Transcriptome comparative analysis between the cytoplasmic male sterile line and fertile line in soybean (Glycine max (L.) Merr.)

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Abstract

To further elucidate the molecular mechanism and fertility restoration of cytoplasmic male sterility (CMS) in soybean, a comparative transcriptome analysis was conducted between the CMS line NJCMS1A, restorer line NJCMS1C and their hybrid F1 progeny (NJCMS1A × NJCMS1C) using RNA-Seq strategy. After pairwise comparative analysis of these soybean lines, 294, 222, and 288 differentially expressed genes (DEGs) were identified, respectively. Further bioinformatic analysis indicated that these DEGs were involved in diverse molecular functions and metabolic pathways. qRT-PCR analysis validated that the gene expression pattern in RNA-Seq was reliable. These results significantly showed that the male sterility and fertility restoration in NJCMS1A might be related to a series of the abnormal of growth development and metabolic processes, such as pollen development, DNA methylation process, pollen viability, cell wall development, programmed cell death, as well as carbohydrate and energy metabolism. This study could facilitate our understanding of the molecular mechanisms and fertility restoration behind CMS in soybean.

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References

  • An H, Yang ZH, Yi B, 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  Google Scholar 

  • Ansorge WJ (2009) Next-generation DNA sequencing techniques. New Biotechnol 25:195–203

    Article  CAS  Google Scholar 

  • Benjamini BY, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Benjamini BY, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188

    Article  Google Scholar 

  • Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676

    Article  CAS  PubMed  Google Scholar 

  • Ding DR, Gai JY, Cui ZL, Yang SP, Qiu JX (1999) Development and verification of the cytoplasmic-nuclear male sterile soybean line NJCMS1A and its maintainer NJCMS1B. Chin Sci Bull 44:191–192

    Article  Google Scholar 

  • Ding DR, Gai JY, Cui ZL, Qiu JX (2002) Development of a cytoplasmic-nuclear male-sterile line of soybean. Euphytica 124:85–91

    Article  CAS  Google Scholar 

  • Fan JM (2003) Studies on cyto-morphological and cyto-chemical features of cytoplasmic-nuclear male-sterile lines of soybeans (Glycine max (L.) Merr.). M. Sc. Thesis, Nanjing Agricultural University, Supervisor: S.P. Yang

  • Feldmann KA (2001) Cytochrome P450s as genes for crop improvement. Curr Opin Plant Biol 4:162–167

    Article  CAS  PubMed  Google Scholar 

  • Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge S, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282:821–828

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gai JY, Cui ZL, Ji DF, Ren ZJ, Ding DR (1995) A report on the nuclear cytoplasmic male sterility from a cross between two soybean cultivars. Soy Genet Newsl 22:55–58

    Google Scholar 

  • Ge X, Dietrich C, Matsuno M, Li G, Berg H, Xia Y (2005) An Arabidopsis aspartic protease functions as an anti-cell-death component in reproduction and embryogenesis. EMBO Rep 6:282–288

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Havey MJ (2004) The use of cytoplasmic male sterility for hybrid seed production. In: Daniell H, Chase CD (eds) Molecular biology and biotechnology of plant organelles. Springer, Dordrecht, pp 623–634

    Chapter  Google Scholar 

  • Huang F, Xu GL, Chi YJ, Liu HC, Xue Q, Zhao TJ, Gai JY, Yu DY (2014) A soybean MADS-box protein modulates floral organ numbers, petal identity and sterility. BMC Plant Biol 14:89

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kurasawa K, Matsui A, Yokoyama R, Kuriyama T, Yoshizumi T, Matsui M, Suwabe K, Watanabe M, Nishitani K (2009) The AtXTH28 gene, a xyloglucan endotransglucosylase/hydrolase, is involved in automatic self-pollination in Arabidopsis thaliana. Plant Cell Physiol 50:413–422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li JJ, Han SH, Ding XL, He TT, Dai JY, Yang SP, Gai JY (2015) Comparative transcriptome analysis between the cytoplasmic male sterile line NJCMS1A and its maintainer NJCMS1B in soybean (Glycine max (L.) Merr.). PLoS ONE 10:e0126771

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu C, Ma N, Wang PY, Fu N, Shen HL (2013) Transcriptome sequencing and de novo analysis of a cytoplasmic male sterile line and its near-isogenic restorer line in chili pepper (Capsicum annuum L.). PLoS ONE 8:e65209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mamun EA, Alfred S, Cantrill LC, Overall RL, Sutton BG (2006) Effects of chilling on male gametophyte development in rice. Cell Biol Int 30:583–591

    Article  CAS  PubMed  Google Scholar 

  • Ng HH, Adrian B (1999) DNA methylation and chromatin modification. Curr Opin Genet Dev 9:158–163

    Article  CAS  PubMed  Google Scholar 

  • Nishitani K, Tominaga R (1992) Endo-xyloglucan transferase, a novel class of glycosyltransferase that catalyzes transfer of a segment of xyloglucan molecule to another xyloglucan molecule. J Biol Chem 267:21058–21064

    CAS  PubMed  Google Scholar 

  • O’Keefe DP, Tepperman JM, Dean C, Leto KJ, Erbes DL, Odell JT (1994) Plant expression of a bacterial cytochrome P450 that catalyses activation of a sulfonylurea pro-herbicide. Plant Physiol 105:473–482

    Article  PubMed  PubMed Central  Google Scholar 

  • Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  CAS  PubMed  Google Scholar 

  • Schuster SC (2008) Next-generation sequencing transforms today’s biology. Nat Methods 5:16–18

    Article  CAS  PubMed  Google Scholar 

  • Sheoran IS, Sawhney VK (2010) Proteome analysis of the normal and Ogura (ogu) CMS anthers of Brassica napus to identify proteins associated with male sterility. Botany 88:217–230

    Article  CAS  Google Scholar 

  • Stefan M, Anja P, Ulrich M (2010) Multifunctional flavonoid dioxygenases: flavonol and anthocyanin biosynthesis in Arabidopsis thaliana L. Phytochemistry 71:1040–1049

    Article  Google Scholar 

  • Tang HB, Wang XY, Bowers JE, Ming R, Alam M, Paterson AH (2008) Unraveling ancient hexaploidy through multiply-aligned angiosperm gene maps. Genome Res 18:1944–1954

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-SEq. Bioinformatics 25:1105–1111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-Seq experiments with TopHat and Cufflinks. Nat Protoc 7:562–578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapnell C, Hendrickson DG, Sauvageau M, Goff L, Rinn JL, Pachter L (2013) Differential analysis of gene regulation at transcript resolution with RNA-SEq. Nat Biotechnol 31:46–53

    Article  CAS  PubMed  Google Scholar 

  • Van der Meer IM, Stam ME, Tunen AJ, Mol JN, Suitje AR (1992) Antisense inhibition of flavonoid biosynthesis in petunia anthers results in male sterility. Plant Cell 4:253–262

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang LG, Wang SQ, Li W (2012) RSeQC: quality control of RNA-Seq experiments. Bioinformatics 28:2184–2185

    Article  CAS  PubMed  Google Scholar 

  • Wei MM, Song MZ, Fan SL, Yu SX (2013) Transcriptomic analysis of differentially expressed genes during anther development in genetic male sterile and wild type cotton by digital gene-expression profiling. BMC Genomics 14:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Werck-Reichhart D, Hehn A, Didierjean L (2000) Cytochromes P450 for engineering herbicide tolerance. Trends Plant Sci 5:116–123

    Article  CAS  PubMed  Google Scholar 

  • Wu ZM, Cheng JW, Qin C, Hu ZQ, Yin CX, Hu KL (2013) Differential proteomic analysis of anthers between cytoplasmic male sterile and maintainer lines in Capsicum annuum L. Int J Mol Sci 14:22982–22996

    Article  PubMed  PubMed Central  Google Scholar 

  • Xie C, Mao XZ, Huang JJ, Ding Y, Wu JM, Dong S, Kong L, Gao G, Li CY, Wei L (2011) KOBAS 2.0: a web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Res 39:W316–W322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu PZ, Yan WG, He J, Li Y, Zhang HY, Peng H, Wu XJ (2013) DNA methylation affected by male sterile cytoplasm in rice (Oryza sativa L.). Mol Breed 31:719–727

    Article  CAS  Google Scholar 

  • Yan XH, Dong CH, Yu JY, Liu WH, Jiang CH, Liu J, Hu Q, Fang XP, Wei WH (2013) Transcriptome profile analysis of young floral buds of fertile and sterile plants from the self-pollinated offspring of the hybrid between novel restorer line NR1 and Nsa CMS line in Brassica napus. BMC Genomics 14:26

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang SP, Duan MP, Meng QC, Qiu JX, Fan JM, Zhao TJ, Yu DY, Gai JY (2007) Inheritance and gene tagging of male fertility restoration of cytoplasmic-nuclear male-sterile line NJCMS1A in soybean. Plant Breed 126:302–305

    Article  CAS  Google Scholar 

  • Zenoni S, Ferrarini A, Giacomelli E, Xumerle L, Fasoli M, Malerba G, Bellin D, Pezzotti M, Delledonne M (2010) Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-SEq. Plant Physiol 152:1787–1795

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng R, Yue SY, Xu XY, Liu JY, Xu Q, Wang XL, Han L, Yu DY (2012) Proteome analysis of the wild and YX-1 male sterile mutant anthers of wolfberry (Lycium barbarum L.). PLoS ONE 7:e41861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu J, Yang ZN (2013) The research progress of pollen wall development. Chin J Nat 35:112–117 (in Chinese)

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key Research and Development Program of China (2016YFD0101500, 2016YFD0101504), the National Hightech R & D Program of China (2011AA10A105), and the Program for Changjiang Scholars and Innovative Research Team in University (PCSIRT13073).

Author contributions

SPY and JYG conceived this study. JJL and SPY designed the experimental plan and drafted and revised the manuscript. JJL analyzed and interpreted the sequence data. All authors read and approved the final manuscript.

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Authors and Affiliations

  1. Soybean Research Institute, National Center for Soybean Improvement, Key Laboratory of Biology and Genetic Improvement of Soybean (General, Ministry of Agriculture), State Key Laboratory of Crop Genetics and Germplasm Enhancement, Jiangsu Collaborative Innovation Center for Modern Crop Production, Nanjing Agricultural University, Nanjing, 210095, China

    Jiajia Li, Shouping Yang & Junyi Gai

  2. College of Agronomy, Anhui Agricultural University, Hefei, 230036, China

    Jiajia Li

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  1. Jiajia Li
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  2. Shouping Yang
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  3. Junyi Gai
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Corresponding authors

Correspondence to Shouping Yang or Junyi Gai.

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All the authors declare that they have no conflict of interest.

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

Additional information

The transcriptome sequence data in this article were deposited in NCBI Sequence Read Archive database (http://www.ncbi.nlm.nih.gov/traces/sra/), accession number SRP052011 and PRJNA308269.

Electronic supplementary material

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13258_2017_578_MOESM1_ESM.xls

Table S1: Number of differentially expressed genes (DEGs) between different comparison groups. Table S1-1: Number of DEGs between NJCMS1A and NJCMS1C. Table S1-2: Number of DEGs between NJCMS1A and F1. Table S1-3: Number of DEGs between NJCMS1C and F1. (XLS 233 KB)

13258_2017_578_MOESM2_ESM.xls

Table S2: KEGG pathways enriched of differentially expressed gene (DEGs) between different compared groups. Table S2-1: KEGG pathways enriched of DEGs between NJCMS1A and NJCMS1C. Table S2-2: KEGG pathways enriched of DEGs between NJCMS1A and F1. Table S2-3: KEGG pathways enriched of DEGs between NJCMS1C and F1. (XLS 36 KB)

13258_2017_578_MOESM3_ESM.xls

Table S3: Comparison of expression patterns between RNA-Seq and qRT-PCR. Table S3-1: DEGs confirmed by qRT-PCR using the same sample as that in RNA-Seq. Table S3-2: DEGs confirmed by qRT-PCR using different sample from that in RNA-Seq. Table S3-3: The compare results between qRT-PCR and RNA-Seq of DEG (Glyma.16G045100) shared in three different compared groups. (XLS 32 KB)

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Li, J., Yang, S. & Gai, J. Transcriptome comparative analysis between the cytoplasmic male sterile line and fertile line in soybean (Glycine max (L.) Merr.). Genes Genom 39, 1117–1127 (2017). https://doi.org/10.1007/s13258-017-0578-8

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