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Genome-wide analysis of Gro/Tup1 family corepressors and their responses to hormones and abiotic stresses in maize

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Abstract

Gro/Tup1 proteins act as negative transcriptional regulators and play crucial roles in many growth and developmental processes in a wide range of organisms. However, our understanding of Gro/Tup1 protein functions in plants is confined to the model plant Arabidopsis. Here, 11 Gro/Tup1 genes, which were characterized by the typical LisH and WD40 repeat domains, were identified in maize through a genome-wide survey. A phylogenetic analysis revealed that maize Gro/Tup1 proteins could be divided into three subfamilies, in which members shared similar protein and gene structures. The predicted maize Gro/Tup1 genes were distributed on seven chromosomes and segmental duplication contributed to their expansion. Many predicted cis-elements associated with hormones, biotic- or abioticstress responses, meristem and seed development, and circadian rhythms, were found in their putative promoter regions. A potential associated protein analysis identified a large number of candidates, including transcription factors, chromatin-modifying enzymes, protein kinases, and ubiquitinconjugating enzymes. An expression profile derived from the RNA-seq data indicated that Gro/Tup1 genes in maize were widely expressed in various organs and tissues. Quantitative real-time PCR revealed that these genes responded to at least one hormone or abiotic stress, either in roots or in shoots. Our study provides useful information on the Gro/Tup1 genes in maize and will facilitate the further functional validation of these genes in growth and development, hormone responses, and biotic- or abiotic-stress resistance.

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References

  • Abed M, Barry KC, Kenyagin D, Koltun B, Phippen TM, Delrow JJ, Parkhurst SM, Orian A (2011) Degringolade, a SUMO-targeted ubiquitin ligase, inhibits Hairy/Groucho-mediated repression. EMBO J 30:1289–1301

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bui M, Lim N, Sijacic P, Liu Z (2011) LEUNIG_HOMOLOG and LEUNIG regulate seed mucilage extrusion in Arabidopsis. J Integr Plant Biol 53:399–408

    Article  CAS  PubMed  Google Scholar 

  • Buscarlet M, Hermann R, Lo R, Tang Y, Joachim K, Stifani S (2009) Cofactor-activated phosphorylation is required for inhibition of cortical neuron differentiation by Groucho/TLE1. PLoS ONE 4:e8107

    Article  Google Scholar 

  • Causier B, Ashworth M, Guo W, Davies B (2012) The TOP LESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Courey AJ (2000) Groucho/TLE family proteins and transcriptional repression. Gene 249:1–16

    Article  CAS  PubMed  Google Scholar 

  • Chen G, Fernandez J, Mische S, Courey AJ (1999) A functional interaction between the histone deacetylase Rpd3 and the corepressor groucho in Drosophila development. Genes Dev 13:2218–2230

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cinnamon E, Paroush Z (2008) Context-dependent regulation of Groucho/TLE-mediated repression. Curr Opin Genet Dev 18:435–440

    Article  CAS  PubMed  Google Scholar 

  • Courey AJ, Jia S (2001) Transcriptional repression: the long and the short of it. Genes Dev 15:2786–2796.

    CAS  PubMed  Google Scholar 

  • Davidson RM, Hansey CN, Gowda M, Childs KL, Lin H, Vaillancourt B, Sekhon RS, de Leon N, Kaeppler SM, Jiang N, Buell CR (2011) Utility of RNA Sequencing for Analysis of Maize Reproductive Transcriptomes. Plant Genome 4:191–203

    Article  CAS  Google Scholar 

  • Finn RD, Mistry J, Schuster-Böckler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucl Acids Res 34:D247–D251

    Article  CAS  PubMed  Google Scholar 

  • Gallavotti A, Long JA, Stanfield S, Yang X, Jackson D, Vollbrecht E, Schmidt RJ (2010) The control of axillary meristem fate in the maize ramosa pathway. Development 137:2849–2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaut BS, Morton BR, McCaig BC, Clegg MT (1996) Substitution rate comparisons between grasses and palms: synonymous rate differences at the nuclear gene Adh parallel rate differences at the plastid gene rbcL. Proc Natl Acad Sci USA 93:10274–10279

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han YC, Kuang JF, Chen JY, Liu XC, Xiao YY, Fu CC, Wang JN, Wu KQ, Lu WJ (2016) Banana transcription factor MaERF11 recruits histone deacetylase MaHDA1 and represses the expression of MaACO1 and expansins during fruit ripening. Plant Physiol 171:1070–1084

    PubMed  PubMed Central  Google Scholar 

  • Hao Y, Wang X, Li X, Bassa C, Mila I, Audran C, Maza E, Li Z, Bouzayen M, van der Rest B, Zouine M (2014) Genome-wide identification, phylogenetic analysis, expression profiling, and protein-protein interaction properties of TOPLESS gene family members in tomato. J Exp Bot 65:1013–1023

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higo K, Ugawa Y, Iwamoto M, Korenaga T (1999) Plant cis-acting regulatory DNA elements (PLACE) database. Nucleic Acids Res 27:297–300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang J, De Bowles D, Esfandiari E, Dean G, Carpita NC, Haughn GW (2011) The Arabidopsis transcription factor LUH/MUM1 is required for extrusion of seed coat mucilage. Plant Physiol 156:491–502

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kang WH, Park YH, Park HM (2010) The LAMMER kinase homolog, Lkh1, regulates Tup transcriptional repressors through phosphorylation in Schizosaccharomyces pombe. J Biol Chem 285:13797–13806

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kagale S, Rozwadowski K (2011) EAR motif-mediated transcriptional repression in plants: an underlying mechanism for epigenetic regulation of gene expression. Epigenetics 6:141–146

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18:560–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kong H, Landherr LL, Frohlich MW, Leebens-Mack J, Ma H, de Pamphilis CW (2007) Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant J 50:873–885

    Article  CAS  PubMed  Google Scholar 

  • Krogan NT, Long JA (2009) Why so repressed? Turning off transcription during plant growth and development. Curr Opin Plant Biol 12:628–636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krogan NT, Hogan K, Long JA (2012) APETALA2 negatively regulates multiple floral organ identity genes in Arabidopsis by recruiting the co-repressor TOPLESS and the histone deacetylase HDA19. Development 139:4180–4190

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JE, Golz JF (2012) Diverse roles of Groucho/Tup1-like corepressors in plant growth and development. Plant Signaling & Behavior 7:1–7

    Article  CAS  Google Scholar 

  • Lee N, Park J, Kim K, Choi G (2015) The transcriptional coregulator LEUNIG_HOMOLOG inhibits light-dependent seed germination in Arabidopsis. Plant Cell 27:2301–2313

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Copley RR, Schmidt S, Ciccarelli FD, Doerks T, Schultz J, Ponting CP, Bork P (2004) SMART 4.0: towards genomic data integration. Nucl Acids Res 32:D142–D144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li P, Ponnala L, Gandotra N, Wang L, Si Y, Tausta SL, Kebrom TH, Provart N, Patel R, Myers CR, Reidel EJ, Turgeon R, Liu P, Sun Q, Nelson T, Brutnell TP (2010) The developmental dynamics of the maize leaf transcriptome. Nat Genet 42:1060–1067

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lin Y, Zhang C, Lan H, Gao S, Liu H, Liu J, Cao M, Pan G, Rong T, Zhang S (2014) Validation of potential reference genes for qPCR in maize across abiotic stresses, hormone treatments, and tissue types. PLoS ONE 9:e95445

    Article  Google Scholar 

  • Liu Z, Franks RG, Klink VP (2000) Regulation of gynoecium marginal tissue formation by LEUNIG and AINTEGUMENTA. Plant Cell 12:1879–1892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu Z, Karmarkar V (2008) Groucho/Tup1 family co-repressors in plant development. Trends Plant Sci 13:137–144

    Article  CAS  PubMed  Google Scholar 

  • Liu Z, Meyerowitz EM (1995) LEUNIG regulates AGAMOUS expression in Arabidopsis flowers. Development 121:975–991

    CAS  PubMed  Google Scholar 

  • Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523

    Article  CAS  PubMed  Google Scholar 

  • Long JA, Woody S, Poethig S, Meyerowitz EM, Barton MK (2002) Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 129:2797–2806

    CAS  PubMed  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mannervik M, Nibu Y, Zhang H, Levine M (1999) Transcriptional coregulators in development. Science 284:606–609

    Article  CAS  PubMed  Google Scholar 

  • Ng CH, Akhter A, Yurko N, Burgener JM, Rosonina E, Manley JL (2015) Sumoylation controls the timing of Tup1-mediated transcriptional deactivation. Nat Commun 6:6610

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuthall HN, Husain J, McLarren KW, Stifani S (2002) Role for Hes1-induced phosphorylation in Grouchomediated transcriptional repression. Mol Cell Biol 22:389–399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nuthall HN, Joachim K, Stifani S (2004) Phosphorylation of serine 239 of Groucho/ TLE1 by protein kinase CK2 is important for inhibition of neuronal differentiation. Mol Cell Biol 24:8395–8407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oh E, Zhu JY, Ryu H, Hwang I, Wang ZY (2014) TOPLESS mediates brassinosteroid-induced transcriptional repression through interaction with BZR1. Nat Commun 5:4140

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pauwels L, Barbero GF, Geerinck J, Tilleman S, Grunewald W, Pérez AC, Chico JM, Bossche RV, Sewell J, Gil E, García-Casado G, Witters E, Inzé D, Long JA, De Jaeger G, Solano R, Goossens A (2010) NINJA connects the co-repressor TOPLESS to jasmonate signalling. Nature 464:788–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pi L, Aichinger E, van der Graaff E, Llavata-Peris CI, Weijers D, Hennig L, Groot E, Laux T (2015) Organizer-derived WOX5 signal maintains root columella stem cells through chromatinmediated repression of CDF4 expression. Developmental Cell 33:576–588

    Article  CAS  PubMed  Google Scholar 

  • Sasai Y, Kageyama R, Tagawa Y, Shigemoto R, Nakanishi S (1992) Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes & Dev 6:2620–2634

    Article  CAS  Google Scholar 

  • Salse J, Abrouk M, Bolot S, Guilhot N, Courcelle E, Faraut T, Close TJ, Messing J, Feuillet (2009) Reconstruction of monocotelydoneous protochromosomes reveals faster evolution in plants than in animals. Proc Natl Acad Sci USA 106:14908–14913

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schneitz K, Hülskamp M, Kopczak SD, Pruitt RE (1997) Dissection of sexual organ ontogenesis: a genetic analysis of ovule development in Arabidopsis thaliana. Development 124:1367–1376

    CAS  PubMed  Google Scholar 

  • Shrestha B, Guragain B, Sridhar VV (2014) Involvement of corepressor LUH and the adapter proteins SLK1 and SLK2 in the regulation of abiotic stress response genes in Arabidopsis. BMC Plant Biol 14:54

    Article  PubMed  PubMed Central  Google Scholar 

  • Sitaraman J, Bui M, Liu Z (2008) LEUNIG_HOMOLOG and LEUNIG perform partially redundant functions during Arabidopsis embryo and floral development. Plant Physiol 147:672–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21:3105–3118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swigonova Z, Lai JS, Ma JX, Ramakrishna W, Llaca V, Bennetzen JL, Messing J (2004) Close split of sorghum and maize genome progenitors. Genome Res 14:1916–1923

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    Article  CAS  PubMed  Google Scholar 

  • Szklarczyk D, Franceschini A, Wyder S, Forslund K, Heller D, Huerta-Cepas J, Simonovic M, Roth A, Santos A, Tsafou KP, Kuhn M, Bork P, Jensen LJ, von Mering C (2015) STRING v10: protein-protein interaction networks, integrated over the tree of life. Nucleic Acids Res 43:D447–452

    Article  PubMed  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tao Q, Guo D, Wei B, Zhang F, Pang C, Jiang H, Zhang J, Wei T, Gu H, Qu LJ, Qin G (2013) The TIE1 Transcriptional Repressor Links TCP Transcription Factors with TOPLESS/TOPLESSRELATED Corepressors and Modulates Leaf Development in Arabidopsis. Plant Cell 25:421–437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wahi M, Komachi K, Johnson AD (1998) Gene regulation by the yeast Ssn6-Tup1 corepressor. Cold Spring Harb Symp Quant Biol 63:447–57

    Article  CAS  PubMed  Google Scholar 

  • Walker M, Tehseen M, Doblin MS, Pettolino FA, Wilson SM, Bacic A, Golz JF (2011) The transcriptional regulator LEUNIG_ HOMOLOG regulates mucilage release from the Arabidopsis testa. Plant Physiol 56:46–60

    Article  Google Scholar 

  • Wang L, Kim J, Somers DE (2013) Transcriptional corepressor TOPLESS complexes with pseudoresponse regulator proteins and histone deacetylases to regulate circadian transcription. Proc Natl Acad Sci USA 110:761–766

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Shi XL, Hao BL, Ge S, Luo JC (2005) Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol 165:937–946

    Article  CAS  PubMed  Google Scholar 

  • Waters AJ, Makarevitch I, Eichten SR, Swanson-Wagner RA, Yeh CT, Xu W, Schnable PS, Vaughn MW, Gehring M, Springer NM (2011) Parent-of-Origin Effects on Gene Expression and DNA Methylation in the Maize Endosperm. Plant Cell 23:4221–4233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wei F, Coe E, Nelson W, Bharti AK, Engler F, Butler E, Kim H, Goicoechea JL, Chen M, Lee S, Fuks G, Sanchez-Villeda H, Schroeder S, Fang Z, McMullen M, Davis G, Bowers JE, Paterson AH, Schaeffer M, Gardiner J, Cone K, Messing J, Soderlund C, Wing RA (2007) Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet 3:1254–1263

    Article  CAS  Google Scholar 

  • Yoshida A, Ohmori Y, Kitano H, Taguchi-Shiobara F, Hirano HY (2012) Aberrant spikelet and panicle1, encoding a TOPLESSrelated transcriptional co-repressor, is involved in the regulation of meristem fate in rice. Plant J 70:327–339

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Jeong JC, Zhu Y, Sokolchik I, Miyazaki S, Zhu JK, Hasegawa PM, Bohnert HJ, Shi H, Yun DJ, Bressan RA (2008) Involvement of Arabidopsis HOS15 in histone deacetylation and cold tolerance. Proc Natl Acad Sci USA 105:4945–4950

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu Z, Xu F, Zhang Y, Cheng YT, Wiermer M, Li X, Zhang Y. (2010) Arabidopsis resistance protein SNC1 activates immune responses through association with a transcriptional corepressor. Proc Natl Acad Sci USA 107:13960–13965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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  1. Key Laboratory of Biology and Genetic Improvement of Maize in Southwest China of Agricultural Department, Ministry of Agriculture, Maize Research Institute, Sichuan Agricultural University, Chengdu, 611130, China

    Hongyou Li, Kaifeng Huang, Hanmei Du, Hongling Wang, Xin Chen, Shibin Gao, Hailan Liu, Moju Cao, Yanli Lu, Tingzhao Rong & Suzhi Zhang

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  1. Hongyou Li
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  2. Kaifeng Huang
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  3. Hanmei Du
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  4. Hongling Wang
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  9. Yanli Lu
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  10. Tingzhao Rong
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  11. Suzhi Zhang
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Correspondence to Suzhi Zhang.

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Li, H., Huang, K., Du, H. et al. Genome-wide analysis of Gro/Tup1 family corepressors and their responses to hormones and abiotic stresses in maize. J. Plant Biol. 59, 603–615 (2016). https://doi.org/10.1007/s12374-016-0333-8

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