Generic placeholder image

Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

General Research Article

Phylogenomic Analysis of R2R3 MYB Transcription Factors in Sorghum and their Role in Conditioning Biofuel Syndrome

Author(s): Vinay Singh, Neeraj Kumar, Anuj K. Dwivedi, Rita Sharma and Manoj K. Sharma*

Volume 21, Issue 2, 2020

Page: [138 - 154] Pages: 17

DOI: 10.2174/1389202921666200326152119

Price: $65

Abstract

Background: Large scale cultivation of sorghum for food, feed, and biofuel requires concerted efforts for engineering multipurpose cultivars with optimised agronomic traits. Due to their vital role in regulating the biosynthesis of phenylpropanoid-derived compounds, biomass composition, biotic, and abiotic stress response, R2R3-MYB family transcription factors are ideal targets for improving environmental resilience and economic value of sorghum.

Methods: We used diverse computational biology tools to survey the sorghum genome to identify R2R3-MYB transcription factors followed by their structural and phylogenomic analysis. We used inhouse generated as well as publicly available high throughput expression data to analyse the R2R3 expression patterns in various sorghum tissue types.

Results: We have identified a total of 134 R2R3-MYB genes from sorghum and developed a framework to predict gene functions. Collating information from the physical location, duplication, structural analysis, orthologous sequences, phylogeny, and expression patterns revealed the role of duplications in clade-wise expansion of the R2R3-MYB family as well as intra-clade functional diversification. Using publicly available and in-house generated RNA sequencing data, we provide MYB candidates for conditioning biofuel syndrome by engineering phenylpropanoid biosynthesis and sugar signalling pathways in sorghum.

Conclusion: The results presented here are pivotal to prioritize MYB genes for functional validation and optimize agronomic traits in sorghum.

Keywords: Biofuel, phenylpropanoids, R2R3-MYB, transcription factors, sorghum, stress.

Graphical Abstract
[1]
Mathur, S.; Umakanth, A.V.; Tonapi, V.A.; Sharma, R.; Sharma, M.K. Sweet sorghum as biofuel feedstock: recent advances and available resources. Biotechnol. Biofuels, 2017, 10, 146.
[http://dx.doi.org/10.1186/s13068-017-0834-9] [PMID: 28603553]
[2]
Somerville, C.; Youngs, H.; Taylor, C.; Davis, S.C.; Long, S.P. Feedstocks for lignocellulosic biofuels. Science, 2010, 329(5993), 790-792.
[http://dx.doi.org/10.1126/science.1189268] [PMID: 20705851]
[3]
Rabara, R.C.; Tripathi, P.; Rushton, P.J. The potential of transcription factor-based genetic engineering in improving crop tolerance to drought. OMICS, 2014, 18(10), 601-614.
[http://dx.doi.org/10.1089/omi.2013.0177] [PMID: 25118806]
[4]
Wang, H.; Wang, H.; Shao, H.; Tang, X. Recent advances in utilizing transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front. Plant Sci., 2016, 7, 67.
[http://dx.doi.org/10.3389/fpls.2016.00067] [PMID: 26904044]
[5]
Gaponenko, A.K.; Shulga, O.A.; Mishutkina, Y.B.; Tsarkova, E.A.; Timoshenko, A.A.; Spechenkova, N.A. Perspectives of use of transcription factors for improving resistance of wheat productive varieties to abiotic stresses by transgenic technologies. Russ. J. Genet., 2018, 54, 27-35.
[http://dx.doi.org/10.1134/S1022795418010039]
[6]
Du, H.; Wang, Y.B.; Xie, Y.; Liang, Z.; Jiang, S.J.; Zhang, S.S.; Huang, Y.B.; Tang, Y.X. Genome-wide identification and evolutionary and expression analyses of MYB-related genes in land plants. DNA Res., 2013, 20(5), 437-448.
[http://dx.doi.org/10.1093/dnares/dst021]
[7]
Dubos, C.; Stracke, R.; Grotewold, E.; Weisshaar, B.; Martin, C.; Lepiniec, L. MYB transcription factors in Arabidopsis. Trends Plant Sci., 2010, 15(10), 573-581.
[http://dx.doi.org/10.1016/j.tplants.2010.06.005] [PMID: 20674465]
[8]
Ogata, K.; Morikawa, S.; Nakamura, H.; Sekikawa, A.; Inoue, T.; Kanai, H.; Sarai, A.; Ishii, S.; Nishimura, Y. Solution structure of a specific DNA complex of the Myb DNA-binding domain with cooperative recognition helices. Cell, 1994, 79(4), 639-648.
[http://dx.doi.org/10.1016/0092-8674(94)90549-5] [PMID: 7954830]
[9]
Ogata, K.; Kanei-Ishii, C.; Sasaki, M.; Hatanaka, H.; Nagadoi, A.; Enari, M.; Nakamura, H.; Nishimura, Y.; Ishii, S.; Sarai, A. The cavity in the hydrophobic core of Myb DNA-binding domain is reserved for DNA recognition and trans-activation. Nat. Struct. Biol., 1996, 3(2), 178-187.
[http://dx.doi.org/10.1038/nsb0296-178] [PMID: 8564545]
[10]
Jia, L.; Clegg, M.T.; Jiang, T. Evolutionary dynamics of the DNA-binding domains in putative R2R3-MYB genes identified from rice subspecies indica and japonica genomes. Plant Physiol., 2004, 134(2), 575-585.
[http://dx.doi.org/10.1104/pp.103.027201] [PMID: 14966247]
[11]
Ogata, K.; Morikawa, S.; Nakamura, H.; Hojo, H.; Yoshimura, S.; Zhang, R.; Aimoto, S.; Ametani, Y.; Hirata, Z.; Sarai, A. Comparison of the free and DNA-complexed forms of the DNA-binding domain from c-Myb. Nat. Struct. Biol., 1995, 2(4), 309-320.
[http://dx.doi.org/10.1038/nsb0495-309] [PMID: 7796266]
[12]
Braun, E.L.; Grotewold, E. Newly discovered plant c-myb-like genes rewrite the evolution of the plant myb gene family. Plant Physiol., 1999, 121(1), 21-24.
[http://dx.doi.org/10.1104/pp.121.1.21] [PMID: 10482656]
[13]
Dias, A.P.; Braun, E.L.; McMullen, M.D.; Grotewold, E. Recently duplicated maize R2R3 Myb genes provide evidence for distinct mechanisms of evolutionary divergence after duplication. Plant Physiol., 2003, 131(2), 610-620.
[http://dx.doi.org/10.1104/pp.012047] [PMID: 12586885]
[14]
Ito, M. Conservation and diversification of three-repeat Myb transcription factors in plants. J. Plant Res., 2005, 118(1), 61-69.
[http://dx.doi.org/10.1007/s10265-005-0192-8] [PMID: 15703854]
[15]
Feng, G.; Burleigh, J.G.; Braun, E.L.; Mei, W.; Barbazuk, W.B. Evolution of the 3R-MYB gene family in plants. Genome Biol. Evol., 2017, 9(4), 1013-1029.
[http://dx.doi.org/10.1093/gbe/evx056] [PMID: 28444194]
[16]
Du, H.; Liang, Z.; Zhao, S.; Nan, M.G.; Tran, L.S.P.; Lu, K.; Huang, Y.B.; Li, J.N. The evolutionary history of R2R3-MYB proteins across 50 eukaryotes: new insights into subfamily classification and expansion. Sci. Rep., 2015, 5, 11037.
[http://dx.doi.org/10.1038/srep11037] [PMID: 26047035]
[17]
Jiang, C.; Gu, J.; Chopra, S.; Gu, X.; Peterson, T. Ordered origin of the typical two- and three-repeat Myb genes. Gene, 2004, 326, 13-22.
[http://dx.doi.org/10.1016/j.gene.2003.09.049] [PMID: 14729259]
[18]
Meneses, E.; Cárdenas, H.; Zárate, S.; Brieba, L.G.; Orozco, E.; López-Camarillo, C.; Azuara-Liceaga, E. The R2R3 Myb protein family in Entamoeba histolytica. Gene, 2010, 455(1-2), 32-42.
[http://dx.doi.org/10.1016/j.gene.2010.02.004] [PMID: 20156532]
[19]
Yang, T.; Perasso, R.; Baroin-Tourancheau, A. Myb genes in ciliates: a common origin with the myb protooncogene? Protist, 2003, 154(2), 229-238.
[http://dx.doi.org/10.1078/143446103322166527] [PMID: 13677450]
[20]
Ambawat, S.; Sharma, P.; Yadav, N.R.; Yadav, R.C. MYB transcription factor genes as regulators for plant responses: an overview. Physiol. Mol. Biol. Plants, 2013, 19, 307-321.
[http://dx.doi.org/10.1007/s12298-013-0179-1]
[21]
Liu, J.; Osbourn, A.; Ma, P. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant, 2015, 8(5), 689-708.
[http://dx.doi.org/10.1016/j.molp.2015.03.012] [PMID: 25840349]
[22]
Roy, S. Function of MYB domain transcription factors in abiotic stress and epigenetic control of stress response in plant genome. Plant Signal. Behav., 2016, 11(1) e1117723
[http://dx.doi.org/10.1080/15592324.2015.1117723] [PMID: 26636625]
[23]
Poovaiah, C.R.; Bewg, W.P.; Lan, W.; Ralph, J.; Coleman, H.D. Sugarcane transgenics expressing MYB transcription factors show improved glucose release. Biotechnol. Biofuels, 2016, 9, 143.
[http://dx.doi.org/10.1186/s13068-016-0559-1] [PMID: 27429646]
[24]
Xu, C.; Fu, X.; Liu, R.; Guo, L.; Ran, L.; Li, C.; Tian, Q.; Jiao, B.; Wang, B.; Luo, K. PtoMYB170 positively regulates lignin deposition during wood formation in poplar and confers drought tolerance in transgenic Arabidopsis. Tree Physiol., 2017, 37(12), 1713-1726.
[http://dx.doi.org/10.1093/treephys/tpx093] [PMID: 28985414]
[25]
Fornale, S.; Shi, X.; Chai, C.; Encina, A.; Irar, S.; Capellades, M.; Fuguet, E.; Torres, J.L.; Rovira, P.; Puigdomenech, P.; Rigau, J.; Grotewold, E.; Gray, J.; Caparros-Ruiz, D. ZmMYB31 directly represses maize lignin genes and redirects the phenylpropanoid metabolic flux. Plant J., 2010, 64(4), 633-644.
[26]
Shen, H.; He, X.; Poovaiah, C.R.; Wuddineh, W.A.; Ma, J.; Mann, D.G.J.; Wang, H.; Jackson, L.; Tang, Y.; Stewart, C.N., Jr; Chen, F.; Dixon, R.A. Functional characterization of the switchgrass (Panicum virgatum) R2R3-MYB transcription factor PvMYB4 for improvement of lignocellulosic feedstocks. New Phytol., 2012, 193(1), 121-136.
[http://dx.doi.org/10.1111/j.1469-8137.2011.03922.x] [PMID: 21988539]
[27]
Paterson, A.H.; Bowers, J.E.; Bruggmann, R.; Dubchak, I.; Grimwood, J.; Gundlach, H.; Haberer, G.; Hellsten, U.; Mitros, T.; Poliakov, A.; Schmutz, J.; Spannagl, M.; Tang, H.; Wang, X.; Wicker, T.; Bharti, A.K.X.; Chapman, J.; Feltus, F.A.; Gowik, U.; Grigoriev, I.V.; Lyons, E.; Maher, C.A.; Martis, M.; Narechania, A.; Otillar, R.P.; Penning, B.W.; Salamov, A.A.; Wang, Y.; Zhang, L.; Carpita, N.C.; Freeling, M.; Gingle, A.R.; Hash, C.T.; Keller, B.; Klein, P.; Kresovich, S.; McCann, M.C.; Ming, R.; Peterson, D.G.; Mehboob-ur-Rahman, ; Ware, D.; Westhoff, P.; Mayer, K.F.; Messing, J.; Rokhsar, D.S. The Sorghum bicolor genome and the diversification of grasses. Nature, 2009, 457(7229), 551-556.
[http://dx.doi.org/10.1038/nature07723] [PMID: 19189423]
[28]
McCormick, R.F.; Truong, S.K.; Sreedasyam, A.; Jenkins, J.; Shu, S.; Sims, D.; Kennedy, M.; Amirebrahimi, M.; Weers, B.D.; McKinley, B.; Mattison, A.; Morishige, D.T.; Grimwood, J.; Schmutz, J.; Mullet, J.E. The Sorghum bicolor reference genome: improved assembly, gene annotations, a transcriptome atlas, and signatures of genome organization. Plant J., 2018, 93(2), 338-354.
[http://dx.doi.org/10.1111/tpj.13781] [PMID: 29161754]
[29]
Finn, R.D.; Bateman, A.; Clements, J.; Coggill, P.; Eberhardt, R.Y.; Eddy, S.R.; Heger, A.; Hetherington, K.; Holm, L.; Mistry, J.; Sonnhammer, E.L.L.; Tate, J.; Punta, M. Pfam: the protein families database. Nucleic Acids Res., 2014, 42(Database issue), D222-D230.
[http://dx.doi.org/10.1093/nar/gkt1223] [PMID: 24288371]
[30]
Goodstein, D.M.; Shu, S.; Howson, R.; Neupane, R.; Hayes, R.D.; Fazo, J.; Mitros, T.; Dirks, W.; Hellsten, U.; Putnam, N.; Rokhsar, D.S. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res., 2012, 40(Database issue), D1178-D1186.
[http://dx.doi.org/10.1093/nar/gkr944] [PMID: 22110026]
[31]
Gonzales, N.R.; Chitsaz, F.; Derbyshire, M.K.; Geer, L.; Gwadz, M.; Han, L.; He, J.; Hurwitz, D.I.; Lanczycki, C.J.; Lu, F.; Marchler, G.H.; Song, J.S.; Thanki, N.; Wang, Z.; Yamashita, R.A.; Zheng, C.; Bryant, S.H.; Marchler-Bauer, A. Manual curation in the conserved domain database. Protein Sci., 2016, 25, 20.
[32]
Letunic, I.; Bork, P. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res., 2018, 46(D1), D493-D496.
[http://dx.doi.org/10.1093/nar/gkx922] [PMID: 29040681]
[33]
Voorrips, R.E. MapChart: software for the graphical presentation of linkage maps and QTLs. J. Hered., 2002, 93(1), 77-78.
[http://dx.doi.org/10.1093/jhered/93.1.77] [PMID: 12011185]
[34]
Yu, J.; Ke, T.; Tehrim, S.; Sun, F.; Liao, B.; Hua, W. PTGBase: an integrated database to study tandem duplicated genes in plants. Database (Oxford), 2015, 2015 pii: bav017
[http://dx.doi.org/10.1093/database/bav017]
[35]
Lee, T.H.; Tang, H.; Wang, X.; Paterson, A.H. PGDD: a database of gene and genome duplication in plants. Nucleic Acids Res., 2013, 41(Database issue), D1152-D1158.
[PMID: 23180799]
[36]
Krzywinski, M.; Schein, J.; Birol, I.; Connors, J.; Gascoyne, R.; Horsman, D.; Jones, S.J.; Marra, M.A. Circos: an information aesthetic for comparative genomics. Genome Res., 2009, 19(9), 1639-1645.
[http://dx.doi.org/10.1101/gr.092759.109] [PMID: 19541911]
[37]
Chou, K.C.; Shen, H.B. Plant-mPLoc: a top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS One, 2010, 5(6) e11335
[http://dx.doi.org/10.1371/journal.pone.0011335] [PMID: 20596258]
[38]
Blum, T.; Briesemeister, S.; Kohlbacher, O. MultiLoc2: integrating phylogeny and Gene Ontology terms improves subcellular protein localization prediction. BMC Bioinformatics, 2009, 10, 274.
[http://dx.doi.org/10.1186/1471-2105-10-274] [PMID: 19723330]
[39]
Yu, C.S.; Chen, Y.C.; Lu, C.H.; Hwang, J.K. Prediction of protein subcellular localization. Proteins, 2006, 64(3), 643-651.
[http://dx.doi.org/10.1002/prot.21018] [PMID: 16752418]
[40]
Almagro Armenteros, J.J.; Sønderby, C.K.; Sønderby, S.K.; Nielsen, H.; Winther, O. DeepLoc: prediction of protein subcellular localization using deep learning. Bioinformatics, 2017, 33(21), 3387-3395.
[http://dx.doi.org/10.1093/bioinformatics/btx431] [PMID: 29036616]
[41]
Horton, P.; Park, K.J.; Obayashi, T.; Fujita, N.; Harada, H.; Adams-Collier, C.J.; Nakai, K. WoLF PSORT: protein localization predictor. Nucleic Acids Res., 2007, 35(Web Server issue), W585-W587.
[PMID: 17517783]
[42]
O’Brien, K.P.; Remm, M.; Sonnhammer, E.L.L. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic Acids Res., 2005, 33(Database issue), D476-D480.
[http://dx.doi.org/10.1093/nar/gki107] [PMID: 15608241]
[43]
Katoh, K.; Standley, D.M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol., 2013, 30(4), 772-780.
[http://dx.doi.org/10.1093/molbev/mst010] [PMID: 23329690]
[44]
Crooks, G.E.; Hon, G.; Chandonia, J.M.; Brenner, S.E. WebLogo: a sequence logo generator. Genome Res., 2004, 14(6), 1188-1190.
[http://dx.doi.org/10.1101/gr.849004] [PMID: 15173120]
[45]
Gasteiger, E.; Hoogland, C.; Gattiker, A.; Duvaud, S.; Wilkins, M.R.; Appel, R.D.; Bairoch, A. In: The Proteomics Protocols Handbook; Humana Press: Totowa, NJ, 2005; pp. 571-607.
[http://dx.doi.org/10.1385/1-59259-890-0:571]
[46]
Hu, B.; Jin, J.; Guo, A.Y.; Zhang, H.; Luo, J.; Gao, G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics, 2015, 31(8), 1296-1297.
[http://dx.doi.org/10.1093/bioinformatics/btu817] [PMID: 25504850]
[47]
Bailey, T.L.; Boden, M.; Buske, F.A.; Frith, M.; Grant, C.E.; Clementi, L.; Ren, J.; Li, W.W.; Noble, W.S. MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res., 2009, 37(Web Server issue), W202-W208.
[http://dx.doi.org/10.1093/nar/gkp335 ] [PMID: 19458158]
[48]
Bastian, M.; Heymann, S.; Jacomy, M. Third international AAAI conference on weblogs and social media 2009.
[49]
Waterhouse, A.M.; Procter, J.B.; Martin, D.M.A.; Clamp, M.; Barton, G.J. Jalview Version 2--a multiple sequence alignment editor and analysis workbench. Bioinformatics, 2009, 25(9), 1189-1191.
[http://dx.doi.org/10.1093/bioinformatics/btp033] [PMID: 19151095]
[50]
Kumar, S.; Stecher, G.; Tamura, K. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 2016, 33(7), 1870-1874.
[http://dx.doi.org/10.1093/molbev/msw054] [PMID: 27004904]
[51]
Letunic, I.; Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res., 2019, 47(W1), W256-W259.
[http://dx.doi.org/10.1093/nar/gkz239] [PMID: 30931475]
[52]
Davidson, R.M.; Gowda, M.; Moghe, G.; Lin, H.; Vaillancourt, B.; Shiu, S.H.; Jiang, N.; Robin Buell, C. Comparative transcriptomics of three Poaceae species reveals patterns of gene expression evolution. Plant J., 2012, 71(3), 492-502.
[http://dx.doi.org/10.1111/j.1365-313X.2012.05005.x]
[53]
Kebrom, T.H.; McKinley, B.; Mullet, J.E. Dynamics of gene expression during development and expansion of vegetative stem internodes of bioenergy sorghum. Biotechnol. Biofuels, 2017, 10, 159.
[http://dx.doi.org/10.1186/s13068-017-0848-3] [PMID: 28649278]
[54]
Rao, S.S.; Patil, J.V.; Prasad, P.V.V.; Reddy, D.C.S.; Mishra, J.S.; Umakanth, A.V.; Reddy, B.V.S.; Kumar, A.A. Sweet sorghum planting effects on stalk yield and sugar quality in semi-arid tropical environment. Agron. J., 2013, 105, 1458.
[http://dx.doi.org/10.2134/agronj2013.0156]
[55]
Zhang, J.; Jiang, F.; Shen, Y.; Zhan, Q.; Bai, B.; Chen, W.; Chi, Y. Transcriptome analysis reveals candidate genes related to phosphorus starvation tolerance in sorghum. BMC Plant Biol., 2019, 19(1), 306.
[http://dx.doi.org/10.1186/s12870-019-1914-8] [PMID: 31296169]
[56]
Pertea, M.; Kim, D.; Pertea, G.M.; Leek, J.T.; Salzberg, S.L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc., 2016, 11(9), 1650-1667.
[http://dx.doi.org/10.1038/nprot.2016.095] [PMID: 27560171]
[57]
Stelpflug, S.C.; Sekhon, R.S.; Vaillancourt, B.; Hirsch, C.N.; Buell, C.R. An expanded maize gene expression atlas based on RNA sequencing and its use to explore root development. Plant Genome, 2016, 9(1)
[http://dx.doi.org/10.3835/plantgenome2015.04.0025]
[58]
Heine, G.F.; Hernandez, J.M.; Grotewold, E. Two cysteines in plant R2R3 MYB domains participate in REDOX-dependent DNA binding. J. Biol. Chem., 2004, 279(36), 37878-37885.
[http://dx.doi.org/10.1074/jbc.M405166200] [PMID: 15237103]
[59]
Du, H.; Feng, B.R.; Yang, S.S.; Huang, Y.B.; Tang, Y.X. The R2R3-MYB transcription factor gene family in maize. PLoS One, 2012, 7(6) e37463
[http://dx.doi.org/10.1371/journal.pone.0037463] [PMID: 22719841]
[60]
Chen, S.; Niu, X.; Guan, Y.; Li, H. Genome-wide analysis and expression profiles of the MYB genes in Brachypodium distachyon. Plant Cell Physiol., 2017, 58(10), 1777-1788.
[http://dx.doi.org/10.1093/pcp/pcx115] [PMID: 29016897]
[61]
Wang, Z.; Tang, J.; Hu, R.; Wu, P.; Hou, X.L.; Song, X.M.; Xiong, A.S. Genome-wide analysis of the R2R3-MYB transcription factor genes in Chinese cabbage (Brassica rapa ssp. pekinensis) reveals their stress and hormone responsive patterns. BMC Genomics, 2015, 16, 17.
[http://dx.doi.org/10.1186/s12864-015-1216-y] [PMID: 25613160]
[62]
Zargarian, L.; Le Tilly, V.; Jamin, N.; Chaffotte, A.; Gabrielsen, O.S.; Toma, F.; Alpert, B. Myb-DNA recognition: role of tryptophan residues and structural changes of the minimal DNA binding domain of c-Myb. Biochemistry, 1999, 38(6), 1921-1929.
[http://dx.doi.org/10.1021/bi981199j] [PMID: 10026273]
[63]
Jin, H.; Martin, C. Multifunctionality and diversity within the plant MYB-gene family. Plant Mol. Biol., 1999, 41(5), 577-585.
[http://dx.doi.org/10.1023/A:1006319732410] [PMID: 10645718]
[64]
Kranz, H.; Scholz, K.; Weisshaar, B. c-MYB oncogene-like genes encoding three MYB repeats occur in all major plant lineages. Plant J., 2000, 21, 231-235.
[65]
Millard, P.S.; Kragelund, B.B.; Burow, M. R2R3 MYB transcription factors - functions outside the DNA-binding domain. Trends Plant Sci., 2019, 24(10), 934-946.
[http://dx.doi.org/10.1016/j.tplants.2019.07.003]
[66]
Fernández-Calvo, P.; Chini, A.; Fernández-Barbero, G.; Chico, J.M.; Gimenez-Ibanez, S.; Geerinck, J.; Eeckhout, D.; Schweizer, F.; Godoy, M.; Franco-Zorrilla, J.M.; Pauwels, L.; Witters, E.; Puga, M.I.; Paz-Ares, J.; Goossens, A.; Reymond, P.; De Jaeger, G.; Solano, R. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell, 2011, 23(2), 701-715.
[http://dx.doi.org/10.1105/tpc.110.080788] [PMID: 21335373]
[67]
Liu, Y.; Chakrabortee, S.; Li, R.; Zheng, Y.; Tunnacliffe, A. Both plant and animal LEA proteins act as kinetic stabilisers of polyglutamine-dependent protein aggregation. FEBS Lett., 2011, 585(4), 630-634.
[http://dx.doi.org/10.1016/j.febslet.2011.01.020] [PMID: 21251910]
[68]
Schaefer, M.H.; Wanker, E.E.; Andrade-Navarro, M.A. Evolution and function of CAG/polyglutamine repeats in protein-protein interaction networks. Nucleic Acids Res., 2012, 40(10), 4273-4287.
[http://dx.doi.org/10.1093/nar/gks011] [PMID: 22287626]
[69]
Pelassa, I.; Corà, D.; Cesano, F.; Monje, F.J.; Montarolo, P.G.; Fiumara, F. Association of polyalanine and polyglutamine coiled coils mediates expansion disease-related protein aggregation and dysfunction. Hum. Mol. Genet., 2014, 23(13), 3402-3420.
[http://dx.doi.org/10.1093/hmg/ddu049] [PMID: 24497578]
[70]
Briggs, G.S.; Mahdi, A.A.; Wen, Q.; Lloyd, R.G. DNA binding by the substrate specificity (wedge) domain of RecG helicase suggests a role in processivity. J. Biol. Chem., 2005, 280(14), 13921-13927.
[http://dx.doi.org/10.1074/jbc.M412054200] [PMID: 15695524]
[71]
Alvarez, M.; Estivill, X.; de la Luna, S. DYRK1A accumulates in splicing speckles through a novel targeting signal and induces speckle disassembly. J. Cell Sci., 2003, 116(Pt 15), 3099-3107.
[http://dx.doi.org/10.1242/jcs.00618] [PMID: 12799418]
[72]
Hoque, M.; Young, T.M.; Lee, C.G.; Serrero, G.; Mathews, M.B.; Pe’ery, T. The growth factor granulin interacts with cyclin T1 and modulates P-TEFb-dependent transcription. Mol. Cell. Biol., 2003, 23(5), 1688-1702.
[http://dx.doi.org/10.1128/MCB.23.5.1688-1702.2003] [PMID: 12588988]
[73]
Gamsjaeger, R.; Liew, C.K.; Loughlin, F.E.; Crossley, M.; Mackay, J.P. Sticky fingers: zinc-fingers as protein-recognition motifs. Trends Biochem. Sci., 2007, 32(2), 63-70.
[http://dx.doi.org/10.1016/j.tibs.2006.12.007] [PMID: 17210253]
[74]
Gall, A.R.; Datsenko, K.A.; Figueroa-Bossi, N.; Bossi, L.; Masuda, I.; Hou, Y.M.; Csonka, L.N. Mg2+ regulates transcription of mgtA in Salmonella Typhimurium via translation of proline codons during synthesis of the MgtL peptide. Proc. Natl. Acad. Sci. USA, 2016, 113(52), 15096-15101.
[http://dx.doi.org/10.1073/pnas.1612268113] [PMID: 27849575]
[75]
Peil, L.; Starosta, A.L.; Lassak, J.; Atkinson, G.C.; Virumäe, K.; Spitzer, M.; Tenson, T.; Jung, K.; Remme, J.; Wilson, D.N. Distinct XPPX sequence motifs induce ribosome stalling, which is rescued by the translation elongation factor EF-P. Proc. Natl. Acad. Sci. USA, 2013, 110(38), 15265-15270.
[http://dx.doi.org/10.1073/pnas.1310642110] [PMID: 24003132]
[76]
Qi, F.; Motz, M.; Jung, K.; Lassak, J.; Frishman, D. Evolutionary analysis of polyproline motifs in Escherichia coli reveals their regulatory role in translation. PLOS Comput. Biol., 2018, 14(2) e1005987
[http://dx.doi.org/10.1371/journal.pcbi.1005987] [PMID: 29389943]
[77]
Liu, C.; Xie, T.; Chen, C.; Luan, A.; Long, J.; Li, C.; Ding, Y.; He, Y. Genome-wide organization and expression profiling of the R2R3-MYB transcription factor family in pineapple (Ananas comosus). BMC Genomics, 2017, 18(1), 503.
[http://dx.doi.org/10.1186/s12864-017-3896-y] [PMID: 28668094]
[78]
Weng, J.K.; Li, X.; Bonawitz, N.D.; Chapple, C. Emerging strategies of lignin engineering and degradation for cellulosic biofuel production. Curr. Opin. Biotechnol., 2008, 19(2), 166-172.
[http://dx.doi.org/10.1016/j.copbio.2008.02.014] [PMID: 18403196]
[79]
Zhong, R.; Lee, C.; Zhou, J.; McCarthy, R.L.; Ye, Z.H. A battery of transcription factors involved in the regulation of secondary cell wall biosynthesis in Arabidopsis. Plant Cell, 2008, 20(10), 2763-2782.
[http://dx.doi.org/10.1105/tpc.108.061325] [PMID: 18952777]
[80]
Zhong, R.; Ye, Z.H. Transcriptional regulation of lignin biosynthesis. Plant Signal. Behav., 2009, 4(11), 1028-1034.
[http://dx.doi.org/10.4161/psb.4.11.9875] [PMID: 19838072]
[81]
Zhou, J.; Lee, C.; Zhong, R.; Ye, Z.H. MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell, 2009, 21(1), 248-266.
[http://dx.doi.org/10.1105/tpc.108.063321] [PMID: 19122102]
[82]
Wang, H.Z.; Dixon, R.A. On-off switches for secondary cell wall biosynthesis. Mol. Plant, 2012, 5(2), 297-303.
[http://dx.doi.org/10.1093/mp/ssr098] [PMID: 22138968]
[83]
Yang, K.; Li, Y.; Wang, S.; Xu, X.; Sun, H.; Zhao, H.; Li, X.; Gao, Z. Genome-wide identification and expression analysis of the MYB transcription factor in moso bamboo (Phyllostachys edulis). PeerJ, 2019, 6 e6242
[http://dx.doi.org/10.7717/peerj.6242] [PMID: 30648007]
[84]
Zhao, K.; Bartley, L.E. Comparative genomic analysis of the R2R3 MYB secondary cell wall regulators of Arabidopsis, poplar, rice, maize, and switchgrass. BMC Plant Biol., 2014, 14, 135.
[http://dx.doi.org/10.1186/1471-2229-14-135] [PMID: 24885077]
[85]
Fornalé, S.; Sonbol, F.M.; Maes, T.; Capellades, M.; Puigdomènech, P.; Rigau, J.; Caparrós-Ruiz, D. Down-regulation of the maize and Arabidopsis thaliana caffeic acid O-methyl-transferase genes by two new maize R2R3-MYB transcription factors. Plant Mol. Biol., 2006, 62(6), 809-823.
[http://dx.doi.org/10.1007/s11103-006-9058-2] [PMID: 16941210]
[86]
Patzlaff, A.; Newman, L.J.; Dubos, C.; Whetten, R.W.; Smith, C.; McInnis, S.; Bevan, M.W.; Sederoff, R.R.; Campbell, M.M. Characterisation of Pt MYB1, an R2R3-MYB from pine xylem. Plant Mol. Biol., 2003, 53(4), 597-608.
[http://dx.doi.org/10.1023/B:PLAN.0000019066.07933.d6] [PMID: 15010621]
[87]
Scully, E.D.; Gries, T.; Palmer, N.A.; Sarath, G.; Funnell-Harris, D.L.; Baird, L.; Twigg, P.; Seravalli, J.; Clemente, T.E.; Sattler, S.E. Overexpression of SbMyb60 in Sorghum bicolor impacts both primary and secondary metabolism. New Phytol., 2018, 217(1), 82-104.
[http://dx.doi.org/10.1111/nph.14815] [PMID: 28944535]
[88]
Zhong, R.; Richardson, E.A.; Ye, Z.H. The MYB46 transcription factor is a direct target of SND1 and regulates secondary wall biosynthesis in Arabidopsis. Plant Cell, 2007, 19(9), 2776-2792.
[http://dx.doi.org/10.1105/tpc.107.053678] [PMID: 17890373]
[89]
Park, M.Y.; Kang, J.Y.; Kim, S.Y. Overexpression of AtMYB52 confers ABA hypersensitivity and drought tolerance. Mol. Cells, 2011, 31(5), 447-454.
[http://dx.doi.org/10.1007/s10059-011-0300-7] [PMID: 21399993]
[90]
Awika, J.M. Sorghum flavonoids: unusual compounds with promising implications for health. ACS Publications; Washigton: DC, 2011, pp. 171-200.
[http://dx.doi.org/10.1021/bk-2011-1089.ch009]
[91]
Boddu, J.; Svabek, C.; Ibraheem, F.; Jones, A.D.; Chopra, S. Characterization of a deletion allele of a sorghum Myb gene yellow seed1 showing loss of 3-deoxyflavonoids. Plant Sci., 2005, 169, 542-552.
[http://dx.doi.org/10.1016/j.plantsci.2005.05.007]
[92]
Makkena, S.; Lee, E.; Sack, F.D.; Lamb, R.S. The R2R3 MYB transcription factors FOUR LIPS and MYB88 regulate female reproductive development. J. Exp. Bot., 2012, 63(15), 5545-5558.
[http://dx.doi.org/10.1093/jxb/ers209] [PMID: 22915737]
[93]
Baumann, K.; Perez-Rodriguez, M.; Bradley, D.; Venail, J.; Bailey, P.; Jin, H.; Koes, R.; Roberts, K.; Martin, C. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development, 2007, 134(9), 1691-1701.
[http://dx.doi.org/10.1242/dev.02836] [PMID: 17376813]
[94]
Yang, H.; Xue, Q.; Zhang, Z.; Du, J.; Yu, D.; Huang, F. GmMYB181, a soybean R2R3-MYB protein, increases branch number in transgenic arabidopsis. Front. Plant Sci., 2018, 9, 1027.
[http://dx.doi.org/10.3389/fpls.2018.01027] [PMID: 30065741]
[95]
Borg, M.; Brownfield, L.; Khatab, H.; Sidorova, A.; Lingaya, M.; Twell, D. The R2R3 MYB transcription factor DUO1 activates a male germline-specific regulon essential for sperm cell differentiation in Arabidopsis. Plant Cell, 2011, 23(2), 534-549.
[http://dx.doi.org/10.1105/tpc.110.081059] [PMID: 21285328]
[96]
Zhang, Y.; Liang, W.; Shi, J.; Xu, J.; Zhang, D. MYB56 encoding a R2R3 MYB transcription factor regulates seed size in Arabidopsis thaliana. J. Integr. Plant Biol., 2013, 55(11), 1166-1178.
[http://dx.doi.org/10.1111/jipb.12094] [PMID: 23911125]
[97]
Chen, Y.S.; Chao, Y.C.; Tseng, T.W.; Huang, C.K.; Lo, P.C.; Lu, C.A. Two MYB-related transcription factors play opposite roles in sugar signaling in Arabidopsis. Plant Mol. Biol., 2017, 93(3), 299-311.
[http://dx.doi.org/10.1007/s11103-016-0562-8] [PMID: 27866313]
[98]
Kranz, H.; Denekamp, M.; Greco, R.; Jin, H.; Leyva, A.; Meissner, R.; Petroni, K.; Urzainqui, A.; Bevan, M.; Martin, C.; Smeekens, S.; Tonelli, C.; Paz-Ares, J.; Weisshaar, B. Towards functional characterisation of the members of the R2R3-MYB gene family from Arabidopsis thaliana. Plant J., 1998, 16(2), 263-276.
[http://dx.doi.org/10.1046/j.1365-313x.1998.00278.x]
[99]
Borevitz, J.O.; Xia, Y.; Blount, J.; Dixon, R.A.; Lamb, C. Activation tagging identifies a conserved MYB regulator of phenylpropanoid biosynthesis. Plant Cell, 2000, 12(12), 2383-2394.
[http://dx.doi.org/10.1105/tpc.12.12.2383] [PMID: 11148285]
[100]
Shukla, S.; Felderhoff, T.J.; Saballos, A.; Vermerris, W. The relationship between plant height and sugar accumulation in the stems of sweet sorghum (Sorghum bicolor (L.) Moench). Field Crops Res., 2017, 203, 181-191.
[http://dx.doi.org/10.1016/j.fcr.2016.12.004]
[101]
Bomal, C.; Duval, I.; Giguère, I.; Fortin, É.; Caron, S.; Stewart, D.; Boyle, B.; Séguin, A.; MacKay, J.J. Opposite action of R2R3-MYBs from different subgroups on key genes of the shikimate and monolignol pathways in spruce. J. Exp. Bot., 2014, 65(2), 495-508.
[http://dx.doi.org/10.1093/jxb/ert398] [PMID: 24336492]
[102]
Qian, M.; Kalbina, I.; Rosenqvist, E.; Jansen, M.A.K.; Teng, Y.; Strid, Å. UV regulates the expression of phenylpropanoid biosynthesis genes in cucumber (Cucumis sativus L.) in an organ and spectrum dependent manner. Photochem. Photobiol. Sci., 2019, 18(2), 424-433.
[http://dx.doi.org/10.1039/C8PP00480C] [PMID: 30628617]
[103]
Ibraheem, F.; Gaffoor, I.; Tan, Q.; Shyu, C.R.; Chopra, S.; Ibraheem, F.; Gaffoor, I.; Tan, Q.; Shyu, C.R.; Chopra, S. A sorghum MYB transcription factor induces 3-deoxyanthocyanidins and enhances resistance against leaf blights in maize. Molecules, 2015, 20(2), 2388-2404.
[http://dx.doi.org/10.3390/molecules20022388] [PMID: 25647576]

Rights & Permissions Print Export Cite as
© 2024 Bentham Science Publishers | Privacy Policy