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Identification, classification and transcriptional profiles of dirigent domain-containing proteins in sugarcane

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Abstract

Dirigent (DIR) proteins, encoded by DIR genes, are referred to as “dirigent” because they direct the outcome of the coupling of the monolignol coniferyl alcohol into (+) or (−) pinoresinol, the first intermediates in the enantiocomplementary pathways for lignan biosynthesis. DIR domain-containing or DIR-like proteins are, thus, termed for not having a clear characterization. A transcriptome- and genome-wide survey of DIR domain-containing proteins in sugarcane was carried out, in addition to phylogenetic, physicochemical and transcriptional analyses. A total of 120 non-redundant sequences containing the DIR domain were identified and classified into 64 groups according to phylogenetic and sequence alignment analyses. In silico analysis of transcript abundance showed that these sequences are expressed at low levels in leaves and genes in the same phylogenetic clade have similar expression patterns. Expression analysis of ShDIR1-like transcripts in the culm internodes of sugarcane demonstrates their abundance in mature internodes, their induction by nitrogen fertilization and their predominant expression in cells that have a lignified secondary cell wall, such as vascular bundles of young internodes and parenchymal cells of the pith of mature internodes. Due to the lack of information about the functional role of DIR in plants, a possible relationship is discussed between the ShDIR1-like transcriptional profile and cell wall development in parenchyma cells of sugarcane culm, which typically accumulates large amounts of sucrose. The number of genes encoding the DIR domain-containing proteins in sugarcane is intriguing and is an indication per se that these proteins may have an important metabolic role and thus deserve to be better studied.

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References

  • Abraha TG (2005) Isolation and characterisation of a culm-specific promoter element from sugarcane. Stellenbosch University, Stellenbosch

    Google Scholar 

  • Arasan SKT, Park JI, Ahmed NU, Jung HJ, Hur Y, Kang KK, Lim YP, Nou IS (2013) Characterization and expression analysis of dirigent family genes related to stresses in Brassica. Plant Physiol Biochem 67:144–153. doi:10.1016/j.plaphy.2013.02.030

    Article  Google Scholar 

  • Asano J, Chiba K, Tada M, Yoshii T (1996) Antiviral activity of lignans and their glycosides from Justicia procumbens. Phytochemistry 42(3):713–717

    Article  CAS  PubMed  Google Scholar 

  • Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, Ren J, Li WW, Noble WS (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37(web server issue):W202–W208. doi:10.1093/nar/gkp335

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucleic Acids Res 42(web server issue):W252–W258. doi:10.1093/nar/gku340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bottcher A, Cesarino I, Santos AB, Vicentini R, Mayer JL, Vanholme R, Morreel K, Goeminne G, Moura JC, Nobile PM, Carmello-Guerreiro SM, Anjos IA, Creste S, Boerjan W, Landell MG, Mazzafera P (2013) Lignification in sugarcane: biochemical characterization, gene discovery, and expression analysis in two genotypes contrasting for lignin content. Plant Physiol 163(4):1539–1557. doi:10.1104/pp.113.225250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burlat V, Kwon M, Davin LB, Lewis NG (2001) Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry 57(6):883–897

    Article  CAS  PubMed  Google Scholar 

  • Casu RE, Dimmock CM, Chapman SC, Grof CP, McIntyre CL, Bonnett GD, Manners JM (2004) Identification of differentially expressed transcripts from maturing stem of sugarcane by in silico analysis of stem expressed sequence tags and gene expression profiling. Plant Mol Biol 54(4):503–517. doi:10.1023/B:PLAN.0000038255.96128.41

    Article  PubMed  Google Scholar 

  • Casu RE, Jarmey JM, Bonnett GD, Manners JM (2007) Identification of transcripts associated with cell wall metabolism and development in the stem of sugarcane by Affymetrix GeneChip Sugarcane Genome Array expression profiling. Funct Integr Genom 7(2):153–167. doi:10.1007/s10142-006-0038-z

    Article  CAS  Google Scholar 

  • Cesarino I, Araújo P, Sampaio Mayer JL, Paes Leme AF, Mazzafera P (2012) Enzymatic activity and proteomic profile of class III peroxidases during sugarcane stem development. Plant Physiol Biochem 55:66–76. doi:10.1016/j.plaphy.2012.03.014

    Article  CAS  PubMed  Google Scholar 

  • Cesarino I, Araújo P, Sampaio Mayer JL, Vicentini R, Berthet S, Demedts B, Vanholme B, Boerjan W, Mazzafera P (2013) Expression of SofLAC, a new laccase in sugarcane, restores lignin content but not S:G ratio of Arabidopsis lac17 mutant. J Exp Bot 64(6):1769–1781. doi:10.1093/jxb/ert045

    Article  CAS  PubMed  Google Scholar 

  • Choi YW, Takamatsu S, Khan SI, Srinivas PV, Ferreira D, Zhao J, Khan IA (2006) Schisandrene, a dibenzocyclooctadiene lignan from Schisandra chinensis: structure-antioxidant activity relationships of dibenzocyclooctadiene lignans. J Nat Prod 69(3):356–359

    Article  CAS  PubMed  Google Scholar 

  • Chung YM, Wang HC, El-Shazly M, Leu YL, Cheng MC, Lee CL, Chang FR, Wu YC (2011) Antioxidant and tyrosinase inhibitory constituents from a desugared sugar cane extract, a byproduct of sugar production. J Agric Food Chem 59(17):9219–9225. doi:10.1021/jf202119m

    Article  CAS  PubMed  Google Scholar 

  • Corrêa LG, Riaño-Pachón DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS One 3(8):e2944. doi:10.1371/journal.pone.0002944

    Article  PubMed  PubMed Central  Google Scholar 

  • Damaj MB, Kumpatla SP, Emani C, Beremand PD, Reddy AS, Rathore KS, Buenrostro-Nava MT, Curtis IS, Thomas TL, Mirkov TE (2010) Sugarcane DIRIGENT and O-methyltransferase promoters confer stem-regulated gene expression in diverse monocots. Planta 231(6):1439–1458. doi:10.1007/s00425-010-1138-5

    Article  CAS  PubMed  Google Scholar 

  • Davin LB, Lewis NG (2005) Lignin primary structures and dirigent sites. Curr Opin Biotechnol 16(4):407–415

    Article  CAS  PubMed  Google Scholar 

  • Davin LB, Wang HB, Crowell AL, Bedgar DL, Martin DM, Sarkanen S, Lewis NG (1997) Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science 275(5298):362–366

    Article  CAS  PubMed  Google Scholar 

  • de Setta N, Monteiro-Vitorello CB, Metcalfe CJ, Cruz GM, Del Bem LE, Vicentini R, Nogueira FT, Campos RA, Nunes SL, Turrini PC, Vieira AP, Ochoa Cruz EA, Corrêa TC, Hotta CT, de Mello Varani A, Vautrin S, da Trindade AS, de Mendonça Vilela M, Lembke CG, Sato PM, de Andrade RF, Nishiyama MY, Cardoso-Silva CB, Scortecci KC, Garcia AA, Carneiro MS, Kim C, Paterson AH, Bergès H, D’Hont A, de Souza AP, Souza GM, Vincentz M, Kitajima JP, Van Sluys MA (2014) Building the sugarcane genome for biotechnology and identifying evolutionary trends. BMC Genom 15:540. doi:10.1186/1471-2164-15-540

    Article  Google Scholar 

  • Dias MO, Junqueira TL, Cavalett O, Cunha MP, Jesus CD, Rossell CE, Maciel Filho R, Bonomi A (2012) Integrated versus stand-alone second generation ethanol production from sugarcane bagasse and trash. Bioresour Technol 103(1):152–161. doi:10.1016/j.biortech.2011.09.120

    Article  CAS  PubMed  Google Scholar 

  • Effenberger I, Zhang B, Li L, Wang Q, Liu Y, Klaiber I, Pfannstiel J, Schaller A (2015) Dirigent proteins from cotton (Gossypium sp.) for the atropselective synthesis of gossypol. Angew Chem Int Ed Engl 54(49):14660–14663. doi:10.1002/anie.201507543

    Article  CAS  PubMed  Google Scholar 

  • Emanuelsson O, Nielsen H, Brunak S, von Heijne G (2000) Predicting subcellular localization of proteins based on their N-terminal amino acid sequence. J Mol Biol 300(4):1005–1016. doi:10.1006/jmbi.2000.3903

    Article  CAS  PubMed  Google Scholar 

  • Fauré M, Lissi E, Torres R, Videla LA (1990) Antioxidant activities of lignans and flavonoids. Phytochemistry 29(12):3773–3775. doi:10.1016/0031-9422(90)85329-E

    Article  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014) Pfam: the protein families database. Nucleic Acids Res 42(database issue):D222–D230. doi:10.1093/nar/gkt1223

    Article  CAS  PubMed  Google Scholar 

  • Fu L, Niu B, Zhu Z, Wu S, Li W (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28(23):3150–3152. doi:10.1093/bioinformatics/bts565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gang DR, Costa MA, Fujita M, Dinkova-Kostova AT, Wang HB, Burlat V, Martin W, Sarkanen S, Davin LB, Lewis NG (1999) Regiochemical control of monolignol radical coupling: a new paradigm for lignin and lignan biosynthesis. Chem Biol 6(3):143–151. doi:10.1016/S1074-5521(99)89006-1

    Article  CAS  PubMed  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appe RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, New York. doi:10.1385/1-59259-890-0:571

  • Goldemberg J (2007) Ethanol for a sustainable energy future. Science 315(5813):808–810. doi:10.1126/science.1137013

    Article  CAS  PubMed  Google Scholar 

  • Grativol C, Regulski M, Bertalan M, McCombie WR, da Silva FR, Zerlotini Neto A, Vicentini R, Farinelli L, Hemerly AS, Martienssen RA, Ferreira PC (2014) Sugarcane genome sequencing by methylation filtration provides tools for genomic research in the genus Saccharum. Plant J 79(1):162–172. doi:10.1111/tpj.12539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hakeem KR, Chandna R, Ahmad A, Qureshi MI, Iqbal M (2012) Proteomic analysis for low and high nitrogen-responsive proteins in the leaves of rice genotypes grown at three nitrogen levels. Appl Biochem Biotechnol 168(4):834–850. doi:10.1007/s12010-012-9823-4

    Article  CAS  PubMed  Google Scholar 

  • Harmatha J, Dinan L (2003) Biological activities of lignans and stilbenoids associated with plant-insect chemical interactions. Phytochem Rev 2(3):321–330. doi:10.1023/B:PHYT.0000045494.98645.a3

    Article  CAS  Google Scholar 

  • Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, Salt DE (2013) Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root. Proc Natl Acad Sci USA 110(35):14498–14503. doi:10.1073/pnas.1308412110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacobsen KR, Maretzki A, Moore PH (1992) Developmental changes in the anatomy of the sugarcane stem in relation to phloem unloading and sucrose storage. Bot Acta 105(1):70–80. doi:10.1111/j.1438-8677.1992.tb00269.x

    Article  Google Scholar 

  • Jin-Long G, Li-Ping X, Jing-Ping F, Ya-Chun S, Hua-Ying F, You-Xiong Q, Jing-Sheng X (2012) A novel dirigent protein gene with highly stem-specific expression from sugarcane, response to drought, salt and oxidative stresses. Plant Cell Rep 31(10):1801–1812. doi:10.1007/s00299-012-1293-1

    Article  PubMed  Google Scholar 

  • Kernan MR, Sendl A, Chen JL, Jolad SD, Blanc P, Murphy JT, Stoddart CA, Nanakorn W, Balick MJ, Rozhon EJ (1997) Two new lignans with activity against influenza virus from the medicinal plant Rhinacanthus nasutus. J Nat Prod 60(6):635–637. doi:10.1021/np960613i

    Article  CAS  PubMed  Google Scholar 

  • Kim MK, Jeon JH, Fujita M, Davin LB, Lewis NG (2002) The western red cedar (Thuja plicata) 8-8′ DIRIGENT family displays diverse expression patterns and conserved monolignol coupling specificity. Plant Mol Biol 49(2):199–214

    Article  CAS  PubMed  Google Scholar 

  • Kim KW, Moinuddin SG, Atwell KM, Costa MA, Davin LB, Lewis NG (2012) Opposite stereoselectivities of dirigent proteins in Arabidopsis and Schizandra species. J Biol Chem 287(41):33957–33972. doi:10.1074/jbc.M112.387423

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim KW, Smith CA, Daily MD, Cort JR, Davin LB, Lewis NG (2015) Trimeric structure of (+)-pinoresinol-forming dirigent protein at 1.95  Å resolution with three isolated active sites. J Biol Chem 290(3):1308–1318. doi:10.1074/jbc.M114.611780

    Article  PubMed  Google Scholar 

  • Kittur FS, Yu HY, Bevan DR, Esen A (2010) Deletion of the N-terminal dirigent domain in maize beta-glucosidase aggregating factor and its homolog sorghum lectin dramatically alters the sugar-specificities of their lectin domains. Plant Physiol Biochem 48(8):731–734. doi:10.1016/j.plaphy.2010.03.007

    Article  CAS  PubMed  Google Scholar 

  • Kiyota E, Mazzafera P, Sawaya AC (2012) Analysis of soluble lignin in sugarcane by ultrahigh performance liquid chromatography-tandem mass spectrometry with a do-it-yourself oligomer database. Anal Chem 84(16):7015–7020. doi:10.1021/ac301112y

    Article  CAS  PubMed  Google Scholar 

  • Liao Y, Liu S, Jiang Y, Hu C, Zhang X, Cao X, Xu Z, Gao X, Li L, Zhu J, Chen R (2017) Genome-wide analysis and environmental response profiling of dirigent family genes in rice (Oryza sativa). Genes Genom 39(1):47-62

    Article  CAS  Google Scholar 

  • Li Q, Chen J, Xiao Y, Di P, Zhang L, Chen W (2014) The dirigent multigene family in Isatis indigotica: gene discovery and differential transcript abundance. BMC Genom 15:388. doi:10.1186/1471-2164-15-388

    Article  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 25(4):402–408. doi:10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  • Ma QH (2014) Monocot chimeric jacalins: a novel subfamily of plant lectins. Crit Rev Biotechnol 34(4):300–306. doi:10.3109/07388551.2013.793650

    Article  CAS  PubMed  Google Scholar 

  • Ma QH, Zhen WB, Liu YC (2013) Jacalin domain in wheat jasmonate-regulated protein Ta-JA1 confers agglutinating activity and pathogen resistance. Biochimie 95(2):359–365. doi:10.1016/j.biochi.2012.10.014

    Article  CAS  PubMed  Google Scholar 

  • Mattiello L, Riaño-Pachón DM, Martins MC, da Cruz LP, Bassi D, Marchiori PE, Ribeiro RV, Labate MT, Labate CA, Menossi M (2015) Physiological and transcriptional analyses of developmental stages along sugarcane leaf. BMC Plant Biol 15:300. doi:10.1186/s12870-015-0694-z

    Article  PubMed  PubMed Central  Google Scholar 

  • Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the gateway computing environments workshop (GCE), New Orleans, pp 1–8

  • Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N (2012) Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proc Natl Acad Sci USA 109(25):10101–10106. doi:10.1073/pnas.1205726109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okura VK, de Souza RS, de Siqueira Tada SF, Arruda P (2016) BAC-pool sequencing and assembly of 19 Mb of the complex sugarcane genome. Front Plant Sci 7:342. doi:10.3389/fpls.2016.00342

    Article  PubMed  PubMed Central  Google Scholar 

  • Paniagua C, Bilkova A, Jackson P, Dabravolski S, Riber W, Didi V, Houser J, Gigli-Bisceglia N, Wimmerova M, Budinska E, Hamann T, Hejatko J (2017) Dirigent proteins in plants: modulating cell wall metabolism during abiotic and biotic stress exposure. J Exp Bot. doi:10.1093/jxb/erx141

    PubMed  Google Scholar 

  • Petersen B, Petersen TN, Andersen P, Nielsen M, Lundegaard C (2009) A generic method for assignment of reliability scores applied to solvent accessibility predictions. BMC Struct Biol 9:51. doi:10.1186/1472-6807-9-51

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30(9):e36

    Article  PubMed  PubMed Central  Google Scholar 

  • Pickel B, Constantin MA, Pfannstiel J, Conrad J, Beifuss U, Schaller A (2010) An enantiocomplementary dirigent protein for the enantioselective laccase-catalyzed oxidative coupling of phenols. Angew Chem Int Ed Engl 49(1):202–204. doi:10.1002/anie.200904622

    Article  CAS  PubMed  Google Scholar 

  • Pickel B, Pfannstiel J, Steudle A, Lehmann A, Gerken U, Pleiss J, Schaller A (2012) A model of dirigent proteins derived from structural and functional similarities with allene oxide cyclase and lipocalins. FEBS J 279(11):1980–1993. doi:10.1111/j.1742-4658.2012.08580.x

    Article  CAS  PubMed  Google Scholar 

  • Rabelo SC, Carrere H, Maciel Filho R, Costa AC (2011) Production of bioethanol, methane and heat from sugarcane bagasse in a biorefinery concept. Bioresour Technol 102(17):7887–7895. doi:10.1016/j.biortech.2011.05.081

    Article  CAS  PubMed  Google Scholar 

  • Ralph S, Park JY, Bohlmann J, Mansfield SD (2006) Dirigent proteins in conifer defense: gene discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Mol Biol 60(1):21–40. doi:10.1007/s11103-005-2226-y

    Article  CAS  PubMed  Google Scholar 

  • Ralph SG, Jancsik S, Bohlmann J (2007) Dirigent proteins in conifer defense II: extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry 68(14):1975–1991. doi:10.1016/j.phytochem.2007.04.042

    Article  CAS  PubMed  Google Scholar 

  • Ralph J, Brunow G, Harris PJ, Dixon RA, Schatz PF, Boerjan W (2008a) Lignification: are lignins biosynthesized via simple combinatorial chemistry or via proteinaceous control and template replication? In: Daayf F, Lattanzio V (eds) Recent advances in polyphenol research, vol 1. Wiley-Blackwell, Oxford

    Google Scholar 

  • Ralph J, Kim H, Lu F, Grabber JH, Leplé JC, Berrio-Sierra J, Derikvand MM, Jouanin L, Boerjan W, Lapierre C (2008b) Identification of the structure and origin of a thioacidolysis marker compound for ferulic acid incorporation into angiosperm lignins (and an indicator for cinnamoyl CoA reductase deficiency). Plant J 53(2):368–379. doi:10.1111/j.1365-313X.2007.03345.x

    Article  CAS  PubMed  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339(1):62–66

    Article  CAS  PubMed  Google Scholar 

  • Riaño-Pachón DM, Mattiello L (2017) Draft genome sequencing of the sugarcane hybrid SP80-3280 [version 2; referees: 2 approved]. F1000Research 6:861. doi:10.12688/f1000research.11859.2

    Article  PubMed  PubMed Central  Google Scholar 

  • Saleem M, Kim HJ, Ali MS, Lee YS (2005) An update on bioactive plant lignans. Nat Prod Rep 22(6):696–716. doi:10.1039/b514045p

    Article  CAS  PubMed  Google Scholar 

  • Scheible WR, Morcuende R, Czechowski T, Fritz C, Osuna D, Palacios-Rojas N, Schindelasch D, Thimm O, Udvardi MK, Stitt M (2004) Genome-wide reprogramming of primary and secondary metabolism, protein synthesis, cellular growth processes, and the regulatory infrastructure of Arabidopsis in response to nitrogen. Plant Physiol 136(1):2483–2499. doi:10.1104/pp.104.047019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seneviratne HK, Dalisay DS, Kim KW, Moinuddin SG, Yang H, Hartshorn CM, Davin LB, Lewis NG (2015) Non-host disease resistance response in pea (Pisum sativum) pods: biochemical function of DRR206 and phytoalexin pathway localization. Phytochemistry 113:140–148. doi:10.1016/j.phytochem.2014.10.013

    Article  CAS  PubMed  Google Scholar 

  • Shi H, Liu Z, Zhu L, Zhang C, Chen Y, Zhou Y, Li F, Li X (2012) Overexpression of cotton (Gossypium hirsutum) dirigent1 gene enhances lignification that blocks the spread of Verticillium dahliae. Acta Biochim Biophys Sin (Shanghai) 44(7):555–564. doi:10.1093/abbs/gms035

    Article  CAS  Google Scholar 

  • Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22(21):2688–2690. doi:10.1093/bioinformatics/btl446

    Article  CAS  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(10):2731–2739. doi:10.1093/molbev/msr121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uchida K, Akashi T, Aoki T (2017) The missing link in leguminous pterocarpan biosynthesis is a dirigent domain-containing protein with isoflavanol dehydratase activity. Plant Cell Physiol 58(2):398–408. doi:10.1093/pcp/pcw213

    Article  PubMed  PubMed Central  Google Scholar 

  • Umezawa T (2011) Stereoselectivity of the biosynthesis of norlignans and related compounds. The biological activity of phytochemicals, vol 41. Springer, New York, pp 179–197

    Chapter  Google Scholar 

  • Vettore AL, da Silva FR, Kemper EL, Souza GM, da Silva AM, Ferro MI, Henrique-Silva F, Giglioti EA, Lemos MV, Coutinho LL, Nobrega MP, Carrer H, França SC, Bacci Júnior M, Goldman MH, Gomes SL, Nunes LR, Camargo LE, Siqueira WJ, Van Sluys MA, Thiemann OH, Kuramae EE, Santelli RV, Marino CL, Targon ML, Ferro JA, Silveira HC, Marini DC, Lemos EG, Monteiro-Vitorello CB, Tambor JH, Carraro DM, Roberto PG, Martins VG, Goldman GH, de Oliveira RC, Truffi D, Colombo CA, Rossi M, de Araujo PG, Sculaccio SA, Angella A, Lima MM, de Rosa Júnior VE, Siviero F, Coscrato VE, Machado MA, Grivet L, Di Mauro SM, Nobrega FG, Menck CF, Braga MD, Telles GP, Cara FA, Pedrosa G, Meidanis J, Arruda P (2003) Analysis and functional annotation of an expressed sequence tag collection for tropical crop sugarcane. Genome Res 13(12):2725–2735. doi:10.1101/gr.1532103

    Article  PubMed  PubMed Central  Google Scholar 

  • Vicentini R, Bottcher A, Dos Santos Brito M, Dos Santos AB, Creste S, de Andrade Landell MG, Cesarino I, Mazzafera P (2015) Correction: large-scale transcriptome analysis of two sugarcane genotypes contrasting for lignin content. PLoS One 10(9):e0137698. doi:10.1371/journal.pone.0137698

    Article  PubMed  PubMed Central  Google Scholar 

  • Weidenbach D, Esch L, Möller C, Hensel G, Kumlehn J, Höfle C, Hückelhoven R, Schaffrath U (2016) Polarized defense against fungal pathogens is mediated by the jacalin-related lectin domain of modular poaceae-specific proteins. Mol Plant 9(4):514–527. doi:10.1016/j.molp.2015.12.009

    Article  CAS  PubMed  Google Scholar 

  • Wu R, Shang H, Zhu Y, Qi D, Deng X (2009) Cloning and expression analysis of a dirigent protein gene from the resurrection plant Boea hygrometrica. Prog Nat Sci 19(3):347–352. doi:10.1016/j.pnsc.2008.07.010

    Article  CAS  Google Scholar 

  • Xia ZQ, Costa MA, Proctor J, Davin LB, Lewis NG (2000) Dirigent-mediated podophyllotoxin biosynthesis in Linum flavum and Podophyllum peltatum. Phytochemistry 55(6):537–549

    Article  CAS  PubMed  Google Scholar 

  • Yue F, Lu F, Regner M, Sun R, Ralph J (2017) Lignin-derived thioacidolysis dimers: reevaluation, new products, authentication, and quantification. Chemsuschem 10(5):830–835. doi:10.1002/cssc.201700101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhu L, Zhang X, Tu L, Zeng F, Nie Y, Guo X (2007) Isolation and characterization of two novel dirigent-like genes highly induced in cotton (Gossypium barbadense and G. hirsutum) after infection by Verticillium dahliae. J Plant Pathol 89(1):41–45

    CAS  Google Scholar 

  • Ziegler J, Hamberg M, Miersch O, Parthier B (1997) Purification and characterization of allene oxide cyclase from dry corn seeds. Plant Physiol 114(2):565–573

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We acknowledge Fundação de Amparo a Pesquisa do Estado de São Paulo (FAPESP) for financial support (2008/58035-6) and fellowships granted to PMN (2010/08232-0 and 2012/08540-1) and MSB (2010/11476-8). We thank Laerti Reis Roque for technical support, Pedro Araújo for advice in the in situ hybridization experiments and Larissa M. Andrade for figure preparation. AB and PM thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Coordination for the Improvement of Higher Education Personnel) and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, National Council for Scientific and Technological Development) for Ph.D. and Research fellowships, respectively.

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Correspondence to Paula Macedo Nobile, Diego Mauricio Riaño-Pachón or Paulo Mazzafera.

Additional information

Communicated by S. Hohmann.

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Below is the link to the electronic supplementary material.

Data S1. The sugarcane DIR domain-containing protein amino acid sequences in Fasta format (FASTA 86 kb)

438_2017_1349_MOESM2_ESM.fasta.clstr

Data S2. The sugarcane DIR domain-containing protein sequences obtained from different databases clustered with at least 96% of identity (FASTA.CLSTR 16 kb)

Data S3. Percent Identity Matrix of Dir-c amino acid sequences generated by Clustal2.1 (XLSX 91 kb)

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Supplementary material 5 (PDF 674 kb)

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Nobile, P.M., Bottcher, A., Mayer, J.L.S. et al. Identification, classification and transcriptional profiles of dirigent domain-containing proteins in sugarcane. Mol Genet Genomics 292, 1323–1340 (2017). https://doi.org/10.1007/s00438-017-1349-6

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  • DOI: https://doi.org/10.1007/s00438-017-1349-6

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