Transcriptome Analysis of Ten-DPA Fiber in an Upland Cotton (<i>Gossypium hirsutum</i>) Line with Improved Fiber Traits from Phytochrome A1 RNAi Plants — Oak Academic Publishing
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Transcriptome Analysis of Ten-DPA Fiber in an Upland Cotton (<i>Gossypium hirsutum</i>) Line with Improved Fiber Traits from Phytochrome A1 RNAi Plants
Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, USA
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Department of Pharmacology, Weill Cornell Medical College, New York, NY, USA
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USDA-ARS, Crop Science Research Laboratory, Mississippi State, MS, USA
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USDA-ARS, Crop Science Research Laboratory, Mississippi State, MS, USA
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Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS, USA
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Center of Genomics and Bioinformatics, Academy of Sciences of Uzbekistan, Tashkent, Uzbekistan
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Center of Genomics and Bioinformatics, Academy of Sciences of Uzbekistan, Tashkent, Uzbekistan
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Department of Biology, Texas A & M University, College Station, TX, USA
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Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, USA
1 Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, USA
2 Department of Pharmacology, Weill Cornell Medical College, New York, NY, USA
3 USDA-ARS, Crop Science Research Laboratory, Mississippi State, MS, USA
4 USDA-ARS, Crop Science Research Laboratory, Mississippi State, MS, USA
5 Institute for Genomics, Biocomputing and Biotechnology, Mississippi State University, Mississippi State, MS, USA
6 Center of Genomics and Bioinformatics, Academy of Sciences of Uzbekistan, Tashkent, Uzbekistan
7 Center of Genomics and Bioinformatics, Academy of Sciences of Uzbekistan, Tashkent, Uzbekistan
8 Department of Biology, Texas A & M University, College Station, TX, USA
9 Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS, USA
Silencing phytochrome A1 gene ( PHYA 1) by RNA interference in Upland cotton ( Gossypium hirsutum L. cv. Coker 312) had generated PHYA 1 RNAi lines with improved fiber quality (longer, stronger and finer fiber). To reveal molecular mechanisms that govern fiber development with positive fiber traits, a study of global gene expression profiling of 10-DPA fibers in a PHYA 1 RNAi line and its parent Coker 312 was conducted by high-throughput RNA se quencing. A comparative analysis of transcriptomes between the two lines had identified 142 genes that were differentially expressed in the 10-DPA fiber of the RNAi line. Gene Ontology analysis showed that these differentially expressed genes were mainly involved in metabolic pathways, heterocyclic/organic cyclic compound binding and multiple enzyme activities, and cell structures which were reported to play important roles in fiber development. Twenty-eight KEGG pathways were mapped for the 142 genes, and the pathways related to glycolysis/gluconeogenesis and pyruvate metabolism were the most abundant and followed by cytochrome P450-involved pathways, suggesting that fiber improvement could be through the regulation of proteins involved in cytochrome P450 pathways. Genes encoding WRKY transcription factors, su crose synthase, xyloglucan endotransglucosylase hydrolase, udp-glucuronate: xylan alpha-glucuronosyltransferase, and genes involved in lipid metabolism and ABA/brassinosteroid signal transduction pathways were found differentially expressed in the RNAi line. These genes have direct impacts on cotton fiber quality. The results of this study elucidate molecular signatures and possible mechanisms of fiber improvement in the background of PHYA 1 RNAi in cotton and should help for future fine-tuning and programming of cotton fiber development.
Abdellatif, K.F., Khidr, Y., El-Mansy, Y.M., El-Lawendey, M.M. and Soliman, Y.A. (2012) Molecular Diversity of Egyptian Cotton (Gossypium barbadense L.) and Its Relation to Varietal Development. Journal of Crop Science and Biotechnology, 15, 93-99. https://doi.org/10.1007/s12892-011-0120-5
Smith, C.W. and Coyle, G.G. (1997) Association of Fiber Quality Parameters and Within-Boll Yield Components in Upland Cotton. Crop Science, 37, 1775-1779. https://doi.org/10.2135/cropsci1997.0011183X003700060019x
Basra, A.S. and Malik, C. (1984) Development of the Cotton Fiber. International Review of Cytology, 89, 65-113. https://doi.org/10.1016/S0074-7696(08)61300-5
Seagull, R.W., Oliveri, V., Murphy, K., Binder, A. and Kothari, S. (2000) Cotton Fiber Growth and Development 2. Changes in Cell Diameter and Wall Birefringence. Journal of Cotton Science, 4, 97-104.
Meinert, M.C. and Delmer, D.P. (1977) Changes in Biochemical Composition of the Cell Wall of the Cotton Fiber during Development. Plant Physiology, 59, 1088-1097. https://doi.org/10.1104/pp.59.6.1088
Abdurakhmonov, I.Y., Buriev, Z.T., Saha, S., Jenkins, J.N., Abdukarimov, A. and Pepper, A.E. (2014) Phytochrome RNAi Enhances Major Fibre Quality and Agronomic Traits of the Cotton Gossypium hirsutum L. Nature Communications, 5, 3062. https://doi.org/10.1038/ncomms4062
Abdurakhmonov, I.Y., Ayubov, M.S., Ubaydullaeva, K.A., Buriev, Z.T., Shermatov, S.E., Ruziboev, H.S., Shapulatov, U.M., Saha, S., Ulloa, M., Yu, J.Z., Percy, R.G., Devor, E.J., Sharma, G.C., Sripathi, V.R., Kumpatla, S.P., van der Krol, A., Kater, H.D., Khamidov, K., Salikhov, S.I., Jenkins, J.N., Abdukarimov, A. and Pepper, A.E. (2016) RNA Interference for Functional Genomics and Improvement of Cotton (Gossypium sp.). Frontiers in Plant Science, 7, PMC4762190. https://doi.org/10.3389/fpls.2016.00202
Kasperbauer, M.J. (2000) Cotton Fibre Length Is Affected by Far-Red Light Impinging on Developing Bolls. Crop Science, 40, 1673-1678. https://doi.org/10.2135/cropsci2000.4061673x
Wang, Z., Zhang, D., Wang, X., Tan, X., Guo, H. and Paterson, A.H. (2013b) A Whole-Genome DNA Marker Map for Cotton Based on the D-Genome Sequence of Gossypium raimondii L. G3: Genes, Genomes, Genetics, 3,1759-1767.
Kosmidou-Dimitropoulou, K. (1986) Hormonal Influences on Fiber Development. Cotton Physiology, The Cotton Foundation, Memphis, TN, 361-373.
Lee, J.J., Woodward, A.W. and Chen, Z.J. (2007) Gene Expression Changes and Early Events in Cotton Fibre Development. Annals of Botany, 100, 1391-1401. https://doi.org/10.1093/aob/mcm232
Guan, X., Song, Q. and Chen, Z.J. (2014) Polyploidy and Small RNA Regulation of Cotton Fiber Development. Trends in Plant Science, 19, 516-528. https://doi.org/10.1016/j.tplants.2014.04.007
Wang, Q.Q., Liu, F., Chen, X.S., Ma, X.J., Zeng, H.Q. and Yang, Z.M. (2010) Transcriptome Profiling of Early Developing Cotton Fiber by Deep-Sequencing Reveals Significantly Differential Expression of Genes in a Fuzzless/Lintless Mutant. Genomics, 96, 369-376. https://doi.org/10.1016/j.ygeno.2010.08.009
Wang, Q., Zhu, Z., Ozkardesh, K. and Lin, C. (2013a) Phytochromes and Phytohormones: The Shrinking Degree of Separation. Molecular Plant, 6, 5-7. https://doi.org/10.1093/mp/sss102
Abdurakhmonov, I.Y. (2001) Molecular Cloning and Characterization of Genomic Sequence Tags (GSTS) from the PHYA, PHYB, and HY5 Gene Families of Cotton (Gossypium Species). Thesis, Texas A&M University, Texas.
Wan, C.Y. and Wilkins, T.A. (1994) A Modified Hot Borate Method Significantly Enhances the Yield of High-Quality RNA from Cotton (Gossypium hirsutum L.). Analytical Biochemistry, 223, 7-12. https://doi.org/10.1006/abio.1994.1538
Bolger, A.M., Lohse, M. and Usadel, B. (2014) Trimmomatic: A Flexible Trimmer for Illumina Sequence Data. Bioinformatics, 30, 2114-2120. https://doi.org/10.1093/bioinformatics/btu170
Zhang, T., Hu, Y., Jiang, W., Fang, L., Guan, X., Chen, J., et al. (2015) Sequencing of Allotetraploid Cotton (Gossypium hirsutum L. acc. TM-1) Provides a Resource for Fiber Improvement. Nature Biotechnology, 33, 531-537. https://doi.org/10.1038/nbt.3207
Mortazavi, A., Williams, B.A., McCue, K., Schaeffer, L. and Wold, B. (2008) Mapping and Quantifying Mammalian Transcriptomes by RNA-Seq. Nature Methods, 5, 621-628. https://doi.org/10.1038/nmeth.1226
Conesa, A., Götz, S., García-Gómez, J.M., Terol, J. and Talón, M. (2005) Blast2GO: a Universal Tool for Annotation, Visualization and Analysis in Functional Genomics Research. Bioinformatics, 21, 3674-3676. https://doi.org/10.1093/bioinformatics/bti610
Quevillon, E., Silventoinen, V., Pillai, S., Harte, N., Mulder, N., Apweiler, R. and Lopez, R. (2005) InterProScan: Protein Domains Identifier. Nucleic Acids Research, 33, W116-W120.
Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H., Cherry, J.M., Davis, A.P., Dolinski, K., Dwight, S.S., Eppig, J.T., Harris, M.A., Hill, D.P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J.C., Richardson, J.E., Ringwald, M., Rubin, G.M. and Sherlock, G. (2000) Gene Ontology: Tool for the Unification of Biology. Nature Genetics, 25, 25-29. https://doi.org/10.1038/75556
Fisher, R.A. (1925) Statistical Methods for Research Workers. Genesis Publishing Pvt Ltd., Delhi.
Auer, P.L. and Doerge, R.W. (2010) Statistical Design and Analysis of RNA Sequencing Data. Genetics, 185, 405-416. https://doi.org/10.1534/genetics.110.114983
Subramanian, A., Tamayo, P., Mootha, V.K., Mukherjee, S., Ebert. B.L., Gillette, M.A., Paulovich, A., Pomeroy, S.L., Golub, T.R., Landet, E.S. and Mesirov, J.P. (2005) Gene Set Enrichment Analysis: A Knowledge-Based Approach for Interpreting Genome-Wide Expression Profiles. Proceedings of the National Academy of Sciences of the United States of America, 102, 15545-15550. https://doi.org/10.1073/pnas.0506580102
Kanehisa, M. and Goto, S. (2000) KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Research, 28, 27-30. https://doi.org/10.1093/nar/28.1.27
Fu, W., Shen, Y., Hao, J., Wu, J., Ke, L., Wu, C., Huang, K., Luo, B., Xu, M., Cheng, X., Zhou, X., Sun, J., Xing, C. and Sun, Y. (2015) Acyl-CoA N-Acyltransferase Influences Fertility by Regulating Lipid Metabolism and Jasmonic Acid Biogenesis in Cotton. Scientific Reports, 5, 11790. https://doi.org/10.1038/srep11790
Livak, K.J. and Schmittgen, T.D. (2001) Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2¯ΔΔCT Method. Methods, 25, 402-408. https://doi.org/10.1006/meth.2001.1262
Ding, M., Chen, J., Jiang, Y., Lin, L., Cao, Y., Wang, M., Zhang, Y., Rong, J. and Ye, W. (2015) Genome-Wide Investigation and Transcriptome Analysis of the WRKY Gene Family in Gossypium. Molecular Genetics and Genomics, 290, 151-171. https://doi.org/10.1007/s00438-014-0904-7
Krochko, J.E., Abrams, G.D., Loewen, M.K., Abrams, S.R. and Cutler, A.J. (1998) (+)-Abscisic Acid 8-Hydroxylase Is a Cytochrome P450 Monooxygenase. Plant Physiology, 118, 849-860. https://doi.org/10.1104/pp.118.3.849
Saito, S., Hirai, N., Matsumoto, C., Ohigashi, H., Ohta, D., Sakata, K. and Mizutani, M. (2004) Arabidopsis CYP707As Encode (+)-Abscisic Acid 8'-Hydroxylase, a Key Enzyme in the Oxidative Catabolism of Abscisic Acid. Plant Physiology, 134, 1439-1449. https://doi.org/10.1104/pp.103.037614
Lodish, H., Berk, A., Zipursky, S.L., Matsudaira, P., Baltimore, D. and Darnell, J. (2000) The Dynamic Plant Cell Wall, Molecular Cell Biology. 4th Edition, W. H. Freeman and Company, New York.
Lamport, D.T., Kieliszewski, M.J., Chen, Y. and Cannon, M.C. (2011) Role of the Extensin Superfamily in Primary Cell Wall Architecture. Plant Physiology, 156, 11-19. https://doi.org/10.1104/pp.110.169011
Jiménez-López, J.C., de Dios Alche, J. and Rodríguez-García, M.I. (2011) Systematic and Phylogenetic Analysis of the Ole e 1 Pollen Protein Family Members in Plants: INTECH Open Access Publisher.
Jiang, S.-Y., Jasmin, P.X.H., Ting, Y.Y. and Ramachandran, S. (2005) Genome-Wide Identification and Molecular Characterization of Ole_e_I, Allerg_1 and Allerg_2 Domain-Containing Pollen-Allergen-Like Genes in Oryza sativa. DNA Research, 12, 167-179. https://doi.org/10.1093/dnares/dsi005
Bruex, A., Kainkaryam, R.M., Wieckowski, Y., Kang, Y.H., Bernhardt, C., Xia, Y., Zheng, X., Wang, J.Y., Lee, M.M., Benfey, P., Woolf, P.J. and Schiefelbein, J. (2012) A Gene Regulatory Network for Root Epidermis Cell Differentiation in Arabidopsis. PLOS Genetics, 8, e1002446. https://doi.org/10.1371/journal.pgen.1002446
Van Hengel, A.J. and Roberts, K. (2003) AtAGP30, an Arabinogalactan-Protein in the Cell Walls of the Primary Root, Plays a Role in Root Regeneration and Seed Germination. The Plant Journal, 36, 256-270. https://doi.org/10.1046/j.1365-313X.2003.01874.x
Rao, A.Q., Irfan, M., Saleem, Z., Nasir, I.A., Riazuddin, S. and Husnain, T. (2011) Overexpression of the Phytochrome B Gene from Arabidopsis thaliana Increases Plant Growth and Yield of Cotton (Gossypium hirsutum). Journal of Zhejiang University—Science B, 12, 326-334. https://doi.org/10.1631/jzus.B1000168
Wang, H. and Deng, X.W. (2004) Phytochrome Signaling Mechanism in the Arabidopsis Book 3, 1-28.
Kushanov, F.N., Pepper, A.E., Yu, J.Z., Buriev, Z.T., Shermatov, S.E., Saha, S., Ulloa, M., Jenkins, J.N., Abdukarimov, A. and Abdurakhmonov, I.Y. (2016) Development, Genetic Mapping and QTL Association of Cotton PHYA, PHYB, and HY5-Specific CAPS and dCAPS Markers. BMC Genetics, 17, 141. https://doi.org/10.1186/s12863-016-0448-4
Yu, J., Yu, S., Gore, M., Wu, M., Zhai, H., Li, X., Fan, S., Song, M. and Zhang, J. (2013) Identification of Quantitative Trait Loci across Interspecific F2, F2:3 and Testcross Populations for Agronomic and Fiber Traits in Tetraploid Cotton. Euphytica, 191, 375-389. https://doi.org/10.1007/s10681-013-0875-5
Brill, E., Van Thournout, M., White, R.G., Llewellyn, D., Campbell, P.M., Engelen, S., Ruan, Y.L., Arioli, T. and Furbank, R.T. (2011) A Novel Isoform of Sucrose Synthase Is Targeted to the Cell Wall during Secondary Cell Wall Synthesis in Cotton Fiber. Plant Physiology, 157, 40-54. https://doi.org/10.1104/pp.111.178574
Chen, A., He, S., Li, F., Li, Z., Ding, M., Liu, Q. and Rong, J. (2012) Analyses of the Sucrose Synthase Gene Family in Cotton: Structure, Phylogeny and Expression Patterns. BMC Plant Biology, 12, 85. https://doi.org/10.1186/1471-2229-12-85
Bai, W.-Q., Xiao, Y.-H., Zhao, J., Song, S.-Q., Hu, L., Zeng, J.-Y., Li, X.-B., Hou, L., Luo, M., Li, D.-M. and Pei, Y. (2014) Gibberellin Overproduction Promotes Sucrose Synthase Expression and Secondary Cell Wall Deposition in Cotton Fibers. PLoS ONE, 9, e96537. https://doi.org/10.1371/journal.pone.0096537
Klein, M. and Papenbrock, J. (2004) The Multi-Protein Family of Arabidopsis Sulphotransferases and Their Relatives in Other Plant Species. Journal of Experimental Botany, 55, 1809-1820. https://doi.org/10.1093/jxb/erh183
Wang, M., Liu, X., Wang, R., Li, W., Rodermel, S. and Yu, F. (2012) Overexpression of a Putative Arabidopsis BAHD Acyltransferase Causes Dwarfism That Can Be Rescued by Brassinosteroid. Journal of Experimental Botany, 63, 5787-5801. https://doi.org/10.1093/jxb/ers227
Davis, L.A. and Addicott, F.T. (1972) Abscisic Acid: Correlations with Abscission and with Development in the Cotton Fruit. Plant Physiology, 49, 644-648. https://doi.org/10.1104/pp.49.4.644
Shi, Y.-H., Zhu, S.-W., Mao, X.-Z., Feng, J.-X., Qin, Y.-M., Zhang, L., Cheng, J., Wei, L.-P., Wang, Z.-Y. and Zhu, Y.-X. (2006) Transcriptome Profiling, Molecular Biological, and Physiological Studies Reveal a Major Role for Ethylene in Cotton fiber Cell Elongation. Plant Cell, 18, 651-664. https://doi.org/10.1105/tpc.105.040303
Binder, B.M., Walker, J.M., Gagne, J.M., Emborg, T.J., Hemmann, G., Bleecker, A.B. and Vierstra, R.D. (2007) The Arabidopsis EIN3 Binding F-Box Proteins EBF1 and EBF2 Have Distinct But Overlapping Roles in Ethylene Signaling. Plant Cell, 19, 509-523. https://doi.org/10.1105/tpc.106.048140
Yang, Z., Tian, L., Latoszek-Green, M., Brown, D. and Wu, K. (2005) Arabidopsis ERF4 Is a Transcriptional Repressor Capable of Modulating Ethylene and Abscisic Acid Responses. Plant Molecular Biology, 58, 585-596. https://doi.org/10.1007/s11103-005-7294-5
Wan, Q., Zhang, H., Ye, W., Wu, H. and Zhang, T. (2014) Genome-Wide Transcriptome Profiling Revealed Cotton Fuzz Fiber Development Having a Similar Molecular Model as Arabidopsis Trichome. PLoS ONE, 9, e97313. https://doi.org/10.1371/journal.pone.0097313
Narusaka, M., Seki, M., Umezawa, T., Ishida, J., Nakajima, M., Enju, A. and Shinozaki, K. (2004) Crosstalk in the Responses to Abiotic and Biotic Stresses in Arabidopsis: Analysis of Gene Expression in Cytochrome P450 Gene Superfamily by cDNA Microarray. Plant Molecular Biology, 55, 327-342. https://doi.org/10.1007/s11103-004-0685-1
Miao, Q., Deng, P., Saha, S., Jenkins, N.J, Hsu, C.-Y., Abdurakhmonov, I.Y., Buriev, Z.T., Pepper, A. and Ma, D.-P. (2017) Genome-Wide Identification and Characterization of microRNAs Differentially Expressed in Fibers in a Cotton Phytochrome A1 RNAi Line. PLoS ONE, 12, e0179381. https://doi.org/10.1371/journal.pone.0179381
Nelson, D.R., Ming, R., Alam, M. and Schuler, M.A. (2008) Comparison of Cytochrome P450 Genes from Six Plant Genomes. Tropical Plant Biology, 1, 216-235. https://doi.org/10.1007/s12042-008-9022-1
Jensen, K., Jensen, P.E. and Møller, B.L. (2011) Light-Driven Cytochrome p450 Hydroxylations. ACS Chemical Biology, 6, 533-539. https://doi.org/10.1021/cb100393j
Chinnusamy, V., Schumaker, K. and Zhu, J.K. (2004) Molecular Genetic Perspectives on Cross-Talk and Specificity in Abiotic Stress Signalling in Plants. Journal of Experimental Botany, 55, 225-236. https://doi.org/10.1093/jxb/erh005
Zhu, W., Miao, Q., Sun, D., Yang, G., Wu, C., Huang, J. and Zheng, C. (2012) The Mitochondrial Phosphate Transporters Modulate Plant Responses to Salt Stress via Affecting ATP and Gibberellin Metabolism in Arabidopsis thaliana. PloS ONE, 7, e43530. https://doi.org/10.1371/journal.pone.0043530