The
lifetime of G.
biloba is
very long, and its growth is relatively slow. However, little is known about
growth-related genes in this species. We combined mRNA sequencing (RNA-Seq)
with bulked segregant analysis (BSA) to fine map significant agronomic trait
genes by developing polymorphism molecular markers at the transcriptome level.
In this study, transcriptome sequencing of high growth (GD) and low growth (BD)
samples of G.
biloba half-sib families was performed. After assembling the clean reads, 601
differential expression genes were detected and 513 of them were assigned
functional annotations. Single nucleotide polymorphism (SNP) analysis
identified SNPs associated with 119 genes in the GD and BD groups; 58 of these
genes were annotated. Two Homeobox-leucine zipper protein genes were
up-regulated in the GD group compared with the BD group; therefore, these are
very likely related to high growth of G.
biloba.
References
[1]
Jacobs, B.P. and Browner, W.S. (2000) Ginkgo Biloba: A Living Fossil. The American Journal of Medicine, 3, 341-342. https://doi.org/10.1016/S0002-9343(00)00290-4
[2]
Kato-Noguchi, H., Takeshita, S., Kimura, F., Ohno, O. and Suenaga, K. (2013) A Novel Substance with Allelopathic Activity in Ginkgo biloba. Journal of Plant Physiology, 170, 1595-1599. https://doi.org/10.1016/j.jplph.2013.07.003
[3]
Xing, S.Y. (2014) Ginkgo Germplasm Resources in China. Chinese Forestry Press, Beijing.
[4]
Yuan, J., Li, Q., Xiao, G.L. and Zhu, S.H. (2002) Discussion on the Utilization and Development of Ginkgo Wood. China Forestry Science and Technology, 16, 6-8, 23.
[5]
Cao, F.L. (2007) Chinese Ginkgo Records. Chinese Forestry Press, Beijing.
[6]
Xing, S.Y., Huangpu, G.Y., Hou, J.H. and Guo, C.T. (1993) Study on the Quality of the Fine Single Plant of Ginkgo biloba. Deciduous Fruits, 4, 15-18.
[7]
Newcomer, E.H. (1954) The Karyotype and Possible Sex Chromosomes of Ginkgo biloba. American Journal of Botany, 41, 542-545. https://doi.org/10.1002/j.1537-2197.1954.tb14375.x
[8]
Echenard, V., Lefort, F., Calmin, G., Perroulaz, R. and Belhahri, L. (2008) A New and Improved Automated Technology for Early Sex Determination of Ginkgo biloba. Arboriculture & Urban Forestry, 34, 300-307.
[9]
Zhang, Q., Li, J.H., Sang, Y.L., Xing, S.Y., Wu, Q.K. and Liu, X.J. (2015) Identification and Characterization of Micro-RNAs in Ginkgo biloba var. epiphylla Mak. PLoS ONE, 10, e0127184. https://doi.org/10.1371/journal.pone.0127184
[10]
Guo, C.L., Chen, L.G., He, X.H., Dai, Z. and Yuan, H.Y. (2005) Expressions of Leafy Homologous Genes in Different Organs and Stages of Ginkgo biloba. Hereditas, 27, 241-244.
[11]
Liao, L., Liu, J., Dai, Y., Li, Q., Xie, M., Chen, Q., et al. (2009) Development and Application of Scar Markers for Sex Identification in the Dioecious Species Ginkgo biloba L. Euphytica, 169, 49-55. https://doi.org/10.1007/s10681-009-9913-8
Fu, X., Fu, N., Guo, S., Yan, Z., Xu, Y., Hu, H., et al. (2009) Estimating Accuracy of RNA-Seq and Microarrays with Proteomics. BMC Genomics, 10, 161-160. https://doi.org/10.1186/1471-2164-10-161
[14]
Tang, F., Barbacioru, C., Wang, Y., Nordman, E. and Lee, C. (2009) MRNA-Seq Whole-Transcriptome Analysis of a Single Cell. Nature Methods, 6, 377-382. https://doi.org/10.1038/nmeth.1315
[15]
Wilhelm, B.T. and Landry, J.R. (2009) RNA-Seq-Quantitative Measurement of Expression through Massively Parallel RNA-Sequencing. Methods, 48, 249-257. https://doi.org/10.1016/j.ymeth.2009.03.016
[16]
Liu, S., Chen, H.D., Makarevitch, I., Shirmer, R., Emrich, S.J., et al. (2010) High Throughput Genetic Mapping of Mutants via Quantitative Single Nucleotide Polymorphism Typing. Genetics, 184, 19-26. https://doi.org/10.1534/genetics.109.107557
[17]
Maher, C.A., Kumar-Sinha, C., Cao, X., Kalyana-Sundaram, S., Han, B., et al. (2009) Transcriptome Sequencing to Detect Gene Fusions in Cancer. Nature, 458, 97-101. https://doi.org/10.1038/nature07638
[18]
Han, S.M., Wu, Z.J., Jin, Y., Yang, W.N. and Shi, H.Z. (2015) RNA-Seq Analysis for Transcriptome Assembly, Gene Identification, and SSR Mining in Ginkgo (Ginkgo biloba L.). The Tree Genetics & Genomes, 11, 37. https://doi.org/10.1007/s11295-015-0868-8
[19]
He, B., Gu, Y., Xu, M., Wang, J., Cao, F. and Xu, L. (2015) Transcriptome Analysis of Ginkgo biloba Kernels. Frontiers in Plant Science, 6, 819. https://doi.org/10.3389/fpls.2015.00819
[20]
Nan, Z. (2013) Sequencing and Analysis of the Transcriptome of Ginkgo biloba L. cells. China Biotechnology, 33, 112-119.
[21]
Ge, Y.Q., Qiu, Y.X., Ding, B.Y. and Fu, C.X. (2003) An ISSR Analysis on Population Genetic Diversity of the Relict Plant Ginkgo biloba. Chinese Biodiversity, 11, 276-287.
[22]
Zhang, Y.Y., Ma, C.G., Lin, M.J. and Li, B.H. (2001) Study on One of Genetic Variations for Ginkgo biloba in China: The Variation of Breeding Fruit-Stone Characters among and within Population. Scientia Silvae Sinicae, 37, 35-40.
[23]
Michelmore, R.W., Paran, I. and Kesseli, R.V. (1991) Identification of Markers Linked to Disease-Resistance Genes by Bulked Segregant Analysis: A Rapid Method to Detect Markers in Specific Genomic Regions by Using Segregating Populations. Proceedings of the National Academy of Sciences of the United States of America, 88, 9828-9832. https://doi.org/10.1073/pnas.88.21.9828
[24]
Livaja, M., Wang, Y., Wieckhorst, S., Haseneyer, G., Seidel, M., Hahn, V., et al. (2013) BSTA: A Targeted Approach Combines Bulked Segregant Analysis with Next-Generation Sequencing and de Novo Transcriptome Assembly for SNP Discovery in Sunflower. BMC Genomics, 14, 628. https://doi.org/10.1186/1471-2164-14-628
[25]
Bauer, E., Weyen, J., Schiemann, A., Graner, A. and Ordon, F. (1997) Molecular Mapping of Novel Resistance Genes against Barley Mild Mosaic Virus (BaMMV). Theoretical and Applied Genetics, 95, 1263-1269. https://doi.org/10.1007/s001220050691
[26]
Steuernagel, B., Taudien, S., Gundlach, H., Seidel, M., Ariyadasa, R., Schulte, D., et al. (2009) De Novo 454 Sequencing of Barcoded BAC Pools for Comprehensive Gene Survey and Genome Analysis in the Complex Genome of Barley. BMC Genomics, 10, 547. https://doi.org/10.1186/1471-2164-10-547
[27]
Mackay, I.J. and Caligari, P.D.S. (2000) Efficiencies of F and Backcross Generations for Bulked Segregant Analysis Using Dominant Markers. Crop Science, 40, 626-630. https://doi.org/10.2135/cropsci2000.403626x
[28]
Wolyn, D.J., Borevitz, J.O., Loudet, O., Schwartz, C., Maloof, J., Ecker, J.R., et al. (2004) Light-Response Quantitative Trait Loci Identified with Composite Interval and Extreme Array Mapping in Arabidopsis Thaliana. Genetics, 167, 907-917. https://doi.org/10.1534/genetics.103.024810
[29]
Duan, Y., Li, W., Wu, W., Pan, R., Zhou, Y., Qi, J., et al. (2003) Genetic Analysis and Mapping of Genefzp(t) Controlling Spikelet Differentiation in Rice. Science in china, 46, 328-334.
[30]
Tang, H.M., Liu, S., Hillskinner, S., Wu, W., Reed, D., Yeh, C.T., et al. (2014) The Maize Brown midrib2 (bm2) Gene Encodes a Methylenetetrahydrofolate Reductase That Contributes to Lignin Accumulation. Plant Journal, 77, 380-392. https://doi.org/10.1111/tpj.12394
[31]
Yang, M., Zhu, L., Pan, C., Xu, L., Liu, Y., Ke, W. and Yang, P. (2015) Transcriptomic Analysis of the Regulation of Rhizome Formation in Temperate and Tropical Lotus (Nelumbo nucifera). Scientific Reports, 5, Article No. 13059. https://doi.org/10.1038/srep13059
[32]
Rong, L., Li, Q., Li, S., Tang, L. and Wen, J. (2016) De Novo Transcriptome Sequencing of Acer palmatum and Comprehensive Analysis of Differentially Expressed Genes under Salt Stress in Two Contrasting Genotypes. Molecular Genetics and Genomics, 291, 575-586. https://doi.org/10.1007/s00438-015-1127-2
[33]
Altschul, S.F., Madden, T.L., Shaffer, A., Zhang, J.H. and Zhang, Z. (1996) Gapped Blast and PSI-BLAST: A New Generation of Protein Database Search Programs. Nucleic Acids Research, 25, 3389-3402. https://doi.org/10.1093/nar/25.17.3389
[34]
https://www.broadinstitute.org/gatk/index.php
[35]
Hill, J.T., Demarest, B.L., Bisgrove, B.W., Gorsi, B., Su, Y.C. and Yost, H.J. (2013) MMAPPR, Mutation Mapping Analysis Pipeline for Pooled RNA-Seq. Genome Research, 23, 687-697. https://doi.org/10.1101/gr.146936.112
[36]
Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and Memory-Efficient Alignment of Short DNA Sequences to the Human Genome. Genome Biology, 10, R25. https://doi.org/10.1186/gb-2009-10-3-r25
[37]
Dewey, C.N. and Bo, L. (2011) RSEM, Accurate Transcript Quantification from RNA-Seq Data with or without a Reference Genome. BMC Bioinformatics, 12, 323. https://doi.org/10.1186/1471-2105-12-323
[38]
Anders, S. and Huber, W. (2010) Differential Expression Analysis for Sequence Count Data. Genome Biology, 11, R106. https://doi.org/10.1186/gb-2010-11-10-r106
[39]
Grabherr, M.G., Haas, B.J., Yassour, M., et al. (2011) Full Length Transcriptome Assembly from RNA-Seq Data without a Reference Genome. Nature Biotechnology, 29, 644-652. https://doi.org/10.1038/nbt.1883
[40]
Tatusov, R.L. (2000) The COG Database: A Tool for Genome-Scale Analysis of Protein Functions and Evolution. Nucleic Acids Research, 28, 33-36. https://doi.org/10.1093/nar/28.1.33
[41]
Koonin, E.V., Fedorova, N.D., Jackson, J.D., Jacobs, A.R., Krylov, D.M., Makarova, K.S., et al. (2004) A Comprehensive Evolutionary Classification of Proteins Encoded in Complete Eukaryotic Genomes. Genome Biology, 5, R7. https://doi.org/10.1186/gb-2004-5-2-r7
[42]
Finn, R.D., Bateman, A., Clements, J., Coggill, P., Eberhardt, R.Y.., Eddy, S.R., et al. (2014) Pfam: The Protein Families Database. Nucleic Acids Research, 42, 222-230. https://doi.org/10.1093/nar/gkt1223
[43]
Ashburner, M., Ball, C.A., Blake, J.A., et al. (2000) Gene Ontology, Tool for the Unification of Biology. Nature Genetics, 25, 25-29. https://doi.org/10.1038/75556
[44]
Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y. and Hattori, M. (2004) The KEGG Resource for Deciphering the Genome. Nucleic Acids Research, 32, D277-D280. https://doi.org/10.1093/nar/gkh063
[45]
Apweiler, R., Bairoch, A., Wu, C.H., et al. (2004) UniProt, the Universal Protein Knowledgebase. Nucleic Acids Research, 32, D115-D119. https://doi.org/10.1093/nar/gkh131
[46]
Deng, Y.Y., Li, J.Q., Wu, S.F., Zhu, Y.P., Cai, Y.W. and He, F.C. (2006) Integrated NR Database in Protein Annotation System and Its Localization. Computer Engineering, 32, 71-72.
[47]
http://blast.ncbi.nlm.nih.gov/Blast.cgi
[48]
http://embossgui.sourceforge.net/demo/getorf.html
[49]
Qiu, Z.S. and Stern, B.R.I. (1985) Evidence for Electron Transport across the Plasma Membrane of Zea mays Root Cells. Planta, 165, 383-391. https://doi.org/10.1007/BF00392236
[50]
Cao, C.L., Li, N.Y., Lu, J.Y. and Lei, J.J. (1997) Roles of Plasma Membrane Redox System in Elongation Growth of Plants. The Journal of Northwest Agricultural University, No. 3.
[51]
Merrill Jr., A.H. (2002) De Novo Sphingolipid Biosynthesis: A Necessary, but Dangerous, Pathway. Journal of Biological Chemistry, 277, 25843-25846. https://doi.org/10.1074/jbc.R200009200
[52]
Liu, S.-H. and Gou, P. (2009) Progress in Sphingolipids Research. Biotechnology, No. 2.
[53]
Riebeling, C., Allegood, J.C., Wang, E., Merrill, A.H. and Futerman, A.H. (2003) Two Mammalian Longevity Assurance Gene (LAG1) Family Members, trh1 and trh4, Regulate Dihydroceramide Synthesis Using Different Fatty Acyl-CoA Donors. Journal of Biological Chemistry, 278, 43452-43459. https://doi.org/10.1074/jbc.M307104200
[54]
Hiller, M.M., Finger, A., Schweiger, M., et al. (1996) ER Degradation of a Misfolded Luminal Protein by the Cytosolic Ubiquitin-Proteasome Pathway. Science, 273, 1725-1728. https://doi.org/10.1126/science.273.5282.1725
[55]
Cai, H.W., Gao, Z.S., Yuyama, N. and Ogawa, N. (2003) Identification of AFLP Markers Closely Linked to the rhm Gene for Resistance to Southern Corn Leaf Blight in Maize by Using Bulked Segregant Analysis. Molecular Genetics and Genomics, 269, 299-303. https://doi.org/10.1007/s00438-003-0837-z
[56]
Molnar, S.J., James, L.E. and Kasha, K.J. (2000) Inheritance and RAPD Tagging of Multiple Genes for Resistance to Net Blotch in Barley. Genome, 43, 224-23l. https://doi.org/10.1139/g99-111
[57]
Li, X., Chen, G.H., Zhang, W.Y. and Zhang, X. (2010) Genome-Wide Transcriptional Analysis of Maize Endosperm in Response to ae wx Double Mutations. Journal of Genetics and Genomics, 37, 749-762. https://doi.org/10.1016/S1673-8527(09)60092-8
[58]
Shore, P. and Sharrocks, A.D. (1995) The MADS-Box Family of Transcription Factors. European Journal of Biochemistry, 229, 1-13.
[59]
Meirinho, S., Carvalho, M., Dominguez, A. and Choupina, A. (2010) Isolation and Characterization by Asymmetric PCR of the ENDO1 Gene for Glucan Endo-1,3-β-D-Glucosidase in Phytophthora cinnamomi Associated with the Ink Disease of Castanea sativa Mill. Brazilian Archives of Biology and Technology, 53, 513-518. https://doi.org/10.1590/S1516-89132010000300003
[60]
Lin, X., Zhang, J., Li, Y., Luo, H., Wu, Q., Sun, C., et al. (2011) Functional Genomics of a Living Fossil Tree, Ginkgo, Based on Next-Generation Sequencing Technology. Physiologia Plantarum, 143, 207-218. https://doi.org/10.1111/j.1399-3054.2011.01500.x