De novo and comparative transcriptome analysis of genetic male sterile and fertile lines in radish (Raphanus sativus)

References

• Adamczyk, B.J., Lehti‐Shiu, M.D., & Fernandez, D.E. (2007). The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. The Plant Journal, 50, 1007–1019. doi:10.1111/j.1365-313X.2007.03105.x
   PubMed Web of Science ®Google Scholar
• Altschul, S.F., Gish, W., Miller, W., Myers, E.W., & Lipman, D.J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. doi:10.1016/S0022-2836(05)80360-2
   PubMed Web of Science ®Google Scholar
• An, H., Yang, Z., Yi, B., Wen, J., Shen, J., Tu, J., … Fu, T. (2014). Comparative transcript profiling of the fertile and sterile flower buds of pol CMS in B. napus. BMC Genomics, 15, 258. doi:10.1186/1471-2164-15-258
   PubMed Web of Science ®Google Scholar
• Becker, A., & Theißen, G. (2003). The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution, 29, 464–489.
   PubMed Web of Science ®Google Scholar
• Belyayev, A. (2014). Bursts of transposable elements as an evolutionary driving force. Journal of Evolutionary Biology, 27, 2573–2584. doi:10.1111/jeb.12513
   PubMed Web of Science ®Google Scholar
• Bolger, A.M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30, 2114–2120. doi:10.1093/bioinformatics/btu170
   PubMed Web of Science ®Google Scholar
• Chase, C.D. (2007). Cytoplasmic male sterility: A window to the world of plant mitochondrial–Nuclear interactions. TRENDS in Genetics, 23, 81–90. doi:10.1016/j.tig.2006.12.004
   PubMed Web of Science ®Google Scholar
• Conesa, A., Götz, S., García-Gómez, J.M., Terol, J., Talón, M., & Robles, M. (2005). Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674–3676. doi:10.1093/bioinformatics/bti610
   PubMed Web of Science ®Google Scholar
• Covington, M.F., Maloof, J.N., Straume, M., Kay, S.A., & Harmer, S.L. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biology, 9, R130. doi:10.1186/gb-2008-9-8-r130
   PubMed Web of Science ®Google Scholar
• De Bodt, S., Raes, J., Van de Peer, Y., & Theißen, G. (2003). And then there were many: MADS goes genomic. Trends in Plant Science, 8, 475–483. doi:10.1016/j.tplants.2003.09.006
   PubMed Web of Science ®Google Scholar
• Dong, X., Feng, H., Xu, M., Lee, J., Kim, Y.K., Lim, Y.P., … Hur, Y. (2013). Comprehensive analysis of genic male sterility-related genes in Brassica rapa using a newly developed Br300K oligomeric chip. PloS One, 8, e72178. doi:10.1371/journal.pone.0072178
   PubMed Web of Science ®Google Scholar
• Goldberg, R.B., Beals, T.P., & Sanders, P.M. (1993). Anther development: Basic principles and practical applications. The Plant Cell, 5, 1217.
   PubMed Web of Science ®Google Scholar
• Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., … Zeng, Q. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology, 29, 644–652. doi:10.1038/nbt.1883
   PubMed Web of Science ®Google Scholar
• Gramzow, L., & Theissen, G. (2010). A hitchhiker’s guide to the MADS world of plants. Genome Biology, 11, 214. doi:10.1186/gb-2010-11-11-r110
   PubMed Web of Science ®Google Scholar
• Huilian, S., & Qiwei, H. (1987). STUDIES ON THE BREEDING AND INHERITANCE OF MALE STERILE LINE OF CHINESE RADISH (in Chinese). Scientia Agricultura Sinica, 2, 4–8.
   Google Scholar
• Ito, T., Nagata, N., Yoshiba, Y., Ohme-Takagi, M., Ma, H., & Shinozaki, K. (2007). Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. The Plant Cell, 19, 3549–3562. doi:10.1105/tpc.107.054536
   PubMed Web of Science ®Google Scholar
• Iwabuchi, M., Koizuka, N., Fujimoto, H., Sakai, T., & Imamura, J. (1999). Identification and expression of the kosena radish (Raphanus sativus cv. Kosena) homologue of the ogura radish CMS-associated gene, orf138. Plant Molecular Biology, 39, 183–188.
   PubMed Web of Science ®Google Scholar
• Jeong, H.-J., Kang, J.-H., Zhao, M., Kwon, J.-K., Choi, H.-S., Bae, J.H., … Kang, B.-C. (2014). Tomato Male sterile 10 35 is essential for pollen development and meiosis in anthers. Journal of Experimental Botany, 65, 6693–6709. doi:10.1093/jxb/eru389
   PubMed Web of Science ®Google Scholar
• Jing, B., Naibin, D., Kun, X., Junfeng, W., & Xiaomu, W. (2016). Breeding of radish recessive nuclear male sterile line 136A and its fertility study (in Chinese). Shandong Agricultural Sciences, 48, 26–31.
   Google Scholar
• Kanehisa, M. (2002). The KEGG database. Silico Simulation of Biological Processes, 247, 91–103.
   Google Scholar
• Kang, J., Guo, Y., Chen, Y., Li, H., Zhang, L., & Liu, H. (2014). Upregulation of the AT-hook DNA binding gene BoMF2 in OguCMS anthers of Brassica oleracea suggests that it encodes a transcriptional regulatory factor for anther development. Molecular Biology Reports, 41, 2005–2014. doi:10.1007/s11033-014-3048-2
   PubMed Web of Science ®Google Scholar
• Kitamura, S., Lee, Y.-P., Cho, Y., Kim, S., Iwabuchi, M., Koizuka, N., … Kim, S. (1958). Varieties of radish and their transition A high-resolution linkage map of the Rfd1, a restorer-of-fertility locus for cytoplasmic male sterility in radish (Raphanus sativus L.) produced by a combination of bulked segregant analysis and RNA-Seq Identification and expression of the kosena radish (Raphanus sativus cv. Kosena) homologue of the ogura radish CMS-associated gene, orf138. Japanese Radish, The Japan Science Society Press, Tokyo, 127, 1–19.
   Google Scholar
• Kofuji, R., Sumikawa, N., Yamasaki, M., Kondo, K., Ueda, K., Ito, M., & Hasebe, M. (2003). Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Molecular Biology and Evolution, 20, 1963–1977. doi:10.1093/molbev/msg216
   PubMed Web of Science ®Google Scholar
• Langmead, B., Trapnell, C., Pop, M., & Salzberg, S.L. (2009). Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology, 10, R25. doi:10.1186/gb-2009-10-3-r25
   PubMed Web of Science ®Google Scholar
• Lee, Y.-P., Cho, Y., & Kim, S. (2014). A high-resolution linkage map of the Rfd1, a restorer-of-fertility locus for cytoplasmic male sterility in radish (Raphanus sativus L.) produced by a combination of bulked segregant analysis and RNA-Seq. Theoretical and Applied Genetics, 127, 2243–2252. doi:10.1007/s00122-014-2376-x
   PubMed Web of Science ®Google Scholar
• Li, B., & Dewey, C.N. (2011). RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics, 12, 323. doi:10.1186/1471-2105-12-323
   PubMed Web of Science ®Google Scholar
• Liu, C., Ma, N., Wang, P.-Y., Fu, N., & Shen, H.-L. (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. doi:10.1371/journal.pone.0065209
   PubMed Web of Science ®Google Scholar
• Ma, Y., Kang, J., Wu, J., Zhu, Y., & Wang, X. (2015). Identification of tapetum-specific genes by comparing global gene expression of four different male sterile lines in Brassica oleracea. Plant Molecular Biology, 87, 541–554. doi:10.1007/s11103-015-0287-0
   PubMed Web of Science ®Google Scholar
• Martínez-Castilla, L.P., & Alvarez-Buylla, E.R. (2003). Adaptive evolution in the Arabidopsis MADS-box gene family inferred from its complete resolved phylogeny. Proceedings of the National Academy of Sciences, 100, 13407–13412. doi:10.1073/pnas.1835864100
   PubMed Web of Science ®Google Scholar
• Mehdi, M., & Anwar, A. (2009). Role of genetically engineered system of male sterility in hybrid production of vegetables. Journal of Phytology, 1.
   Google Scholar
• Mei, S., Liu, T., & Wang, Z. (2016). Comparative transcriptome profile of the cytoplasmic male sterile and fertile floral buds of radish (Raphanus sativus L.). International Journal of Molecular Sciences, 17, 42. doi:10.3390/ijms17010042
   Web of Science ®Google Scholar
• Nahm, S.-H., Lee, H.-J., Lee, S.-W., Joo, G.-Y., Harn, C.-H., Yang, S.-G., & Min, B.-W. (2005). Development of a molecular marker specific to a novel CMS line in radish (Raphanus sativus L.). Theoretical and Applied Genetics, 111, 1191–1200. doi:10.1007/s00122-005-0052-x
   PubMed Web of Science ®Google Scholar
• Ogura, H. (1968). Studies on the new male-sterility in Japanese radish, with special reference to the utilization of this sterility towards the practical raising of hybrid seeds. Memoirs of the Faculty of Agriculture, Kagoshima University, 6, 39–78.
   Google Scholar
• Par̆enicová, L., de Folter, S., Kieffer, M., Horner, D.S., Favalli, C., Busscher, J., … Davies, B. (2003). Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis. The Plant Cell Online, 15, 1538–1551. doi:10.1105/tpc.011544
   PubMed Web of Science ®Google Scholar
• Park, J.Y., Lee, Y.-P., Lee, J., Choi, B.-S., Kim, S., & Yang, T.-J. (2013). Complete mitochondrial genome sequence and identification of a candidate gene responsible for cytoplasmic male sterility in radish (Raphanus sativus L.) containing DCGMS cytoplasm. Theoretical and Applied Genetics, 126, 1763–1774. doi:10.1007/s00122-013-2090-0
   PubMed Web of Science ®Google Scholar
• Pasquier, C., Promponas, V., Palaios, G., Hamodrakas, J., & Hamodrakas, S. (1999). A novel method for predicting transmembrane segments in proteins based on a statistical analysis of the SwissProt database: The PRED-TMR algorithm. Protein Engineering, 12, 381–385.
   PubMedGoogle Scholar
• Pertea, G., Huang, X., Liang, F., Antonescu, V., Sultana, R., Karamycheva, S., … Parvizi, B. (2003). TIGR Gene Indices clustering tools (TGICL): A software system for fast clustering of large EST datasets. Bioinformatics, 19, 651–652. doi:10.1093/bioinformatics/btg034
   PubMed Web of Science ®Google Scholar
• Pruitt, K.D., Tatusova, T., & Maglott, D.R. (2005). NCBI reference sequence (RefSeq): A curated non-redundant sequence database of genomes, transcripts and proteins. Nucleic Acids Research, 33, D501–D504. doi:10.1093/nar/gki025
   PubMed Web of Science ®Google Scholar
• Quast, C., Pruesse, E., Yilmaz, P., Gerken, J., Schweer, T., Yarza, P., … Glöckner, F.O. (2012). The SILVA ribosomal RNA gene database project: Improved data processing and web-based tools. Nucleic Acids Research, 41, D590–D596. doi:10.1093/nar/gks1219
   PubMed Web of Science ®Google Scholar
• Sanders, P.M., Bui, A.Q., Weterings, K., McIntire, K., Hsu, Y.-C., Lee, P.Y., … Goldberg, R. (1999). Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sexual Plant Reproduction, 11, 297–322. doi:10.1007/s004970050158
   Web of Science ®Google Scholar
• Staiger, D., Kappeler, S., Müller, M., & Apel, K. (1994). The proteins encoded by two tapetum-specific transcripts, Satap35 and Satap44, from Sinapis alba L. are localized in the exine cell wall layer of developing microspores. Planta, 192, 221–231.
   PubMed Web of Science ®Google Scholar
• Suzuki, H., Rodriguez-Uribe, L., Xu, J., & Zhang, J. (2013). Transcriptome analysis of cytoplasmic male sterility and restoration in CMS-D8 cotton. Plant Cell Reports, 32, 1531–1542. doi:10.1007/s00299-013-1465-7
   PubMed Web of Science ®Google Scholar
• Tarazona, S., García, F., Ferrer, A., Dopazo, J., & Conesa, A. (2012). NOIseq: A RNA-seq differential expression method robust for sequencing depth biases. EMBnet Journal, 17, 18–19. doi:10.14806/ej.17.B.265
   Google Scholar
• Tatusov, R.L., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Kiryutin, B., Koonin, E.V., … Nikolskaya, A.N. (2003). The COG database: An updated version includes eukaryotes. BMC Bioinformatics, 4, 41.
   PubMed Web of Science ®Google Scholar
• Tian, Z., Li, J., Han, S., Ding, X., He, T., Dai, J., … Gai, J. (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. doi:10.1371/journal.pone.0126771
   PubMed Web of Science ®Google Scholar
• Vedel, F., Pla, M., Vitart, V., Gutierres, S., Chetrit, P., & De Paepe, R. (1994). Molecular basis of nuclear and cytoplasmic male sterility in higher plants. Plant Physiology and Biochemistry, 32, 601–608.
   Web of Science ®Google Scholar
• Wei, M., Song, M., Fan, S., & Yu, S. (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. doi:10.1186/1471-2164-14-181
   PubMed Web of Science ®Google Scholar
• Xie, Y., Zhang, W., Wang, Y., Xu, L., Zhu, X., Muleke, E.M., & Liu, L. (2016). Comprehensive transcriptome-based characterization of differentially expressed genes involved in microsporogenesis of radish CMS line and its maintainer. Functional & Integrative Genomics, 16, 529–543. doi:10.1007/s10142-016-0504-1
   PubMed Web of Science ®Google Scholar
• Yamagishi, H., & Terachi, T. (2001). Intra-and inter-specific variations in the mitochondrial gene orf138 of Ogura-type male-sterile cytoplasm from Raphanus sativus and Raphanus raphanistrum. TAG Theoretical and Applied Genetics, 103, 725–732. doi:10.1007/s001220100614
   Web of Science ®Google Scholar
• Yan, X., Dong, C., Yu, J., Liu, W., Jiang, C., Liu, J., … Wei, W. (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. doi:10.1186/1471-2164-14-181
   PubMed Web of Science ®Google Scholar
• Yang, C., Vizcay-Barrena, G., Conner, K., & Wilson, Z.A. (2007). MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. The Plant Cell, 19, 3530–3548. doi:10.1105/tpc.107.054981
   PubMed Web of Science ®Google Scholar
• Ye, J., Fang, L., Zheng, H., Zhang, Y., Chen, J., Zhang, Z., … Bolund, L. (2006). WEGO: A web tool for plotting GO annotations. Nucleic Acids Research, 34, W293–W297. doi:10.1093/nar/gkl031
   PubMed Web of Science ®Google Scholar
• Zhang, L., Yasumoto, K., & Yamagishi, H. (2012). Identification of cytoplasmic male sterility in Chinese radish following PCR analysis of mitochondrial DNA. Plant Molecular Biology Reporter, 30, 817–826. doi:10.1007/s11105-011-0391-5
   Web of Science ®Google Scholar