Abstract
Dirigent proteins (DIRs) are a new class of proteins that were identified during the 8–8′ lignan biosynthetic pathway and involves the formation of ( +) or ( −)-pinoresinol through stereoselective coupling from E-coniferyl alcohol. These proteins are known to play a vital role in the development and stress response in plants. Various studies have reported the functional and structural characterization of dirigent gene family in different plants using in silico approaches. Here, we have summarized the importance of dirigent proteins in plants and their role in plant stress tolerance by analyzing the genome-wide analysis including gene structure, mapping of chromosomes, phylogenetic evolution, conserved motifs, gene structure, and gene duplications in important plants. Overall, this review would help to compare and clarify the molecular and evolutionary characteristics of dirigent gene family in different plants.
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Abbreviations
- DIRs:
-
Dirigent proteins
- NCBI:
-
National Center for Biotechnology Information
- SMART:
-
Simple Modular Architecture Research Tool
- PFAM:
-
Protein Families
- MEME:
-
Multiple Expectation Maximizations for Motif Elicitation
- MEGA:
-
Molecular Evolutionary Genetics Analysis
References
Abe H, Urao T, Ito T et al (2003) Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 15:63–78. https://doi.org/10.1105/tpc.006130
Apweiler R, Bairoch A, Wu CH et al (2004) UniProt: the Universal Protein knowledgebase. Nucleic Acids Res 32:2699. https://doi.org/10.1093/nar/gky092
Ascacio-Valdés JA, Buenrostro-Figueroa JJ, Aguilera-Carbo A et al (2011) Ellagitannins: biosynthesis, biodegradation and biological properties. J Med Plant Res 5:4696–4703
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713. https://doi.org/10.1007/BF00029852
Bank G Supplementary Table S1, n.d. Genomic information and identification of dirigent genes in major cucurbitaceous crops (Citrullus lanatus, Cucumis melo, Cucumis sativus, Cucurbita pepo, Cucurbita moschata and Lagenaria siceraria). Supplementary Table S2. 1–3
Borges AF, Ferreira RB, Monteiro S (2013) Transcriptomic changes following the compatible interaction Vitis vinifera-Erysiphe necator. Paving the way towards an enantioselective role in plant defence modulation. Plant Physiol Biochem 68:71–80. https://doi.org/10.1016/j.plaphy.2013.03.024
Cheng X, Li M, Li D et al (2017) Characterization and analysis of CCR and CAD gene families at the whole-genome level for lignin synthesis of stone cells in pear (Pyrus bretschneideri) fruit. Biol Open 6:1602–1613. https://doi.org/10.1242/bio.026997
Cheng X, Su X, Muhammad A et al (2018) Molecular characterization, evolution, and expression profiling of the dirigent (DIR) family genes in Chinese white pear (Pyrus bretschneideri). Front Genet 9:1–15. https://doi.org/10.3389/fgene.2018.00136
Corbin C, Drouet S, Mateljak I et al (2017) Functional characterization of the pinoresinol–lariciresinol reductase-2 gene reveals its roles in yatein biosynthesis and flax defense response. Planta 246:405–420. https://doi.org/10.1007/s00425-017-2701-0
Corbin C, Drouet S, Markulin L et al (2018) A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: from gene identification and evolution to differential regulation. Plant Mol Biol 97:73–101. https://doi.org/10.1007/s11103-018-0725-x
Dabravolski SA (2020) The resurgence of Dirigent story: time for a bacterial chapter. Curr Microbiol 77:517–521. https://doi.org/10.1007/s00284-019-01809-2
Dalisay DS, Kim KW, Lee C et al (2015) Dirigent protein-mediated lignan and cyanogenic glucoside formation in flax seed: integrated omics and MALDI mass spectrometry imaging. J Nat Prod 78:1231–1242. https://doi.org/10.1021/acs.jnatprod.5b00023
Damaj MB, Kumpatla SP, Emani C et al (2010) Sugarcane DIRIGENT and O-METHYLTRANSFERASE promoters confer stem-regulated gene expression in diverse monocots. Planta 231:1439–1458. https://doi.org/10.1007/s00425-010-1138-5
Davin LB, Wang H, Crowell AL, et al (1997) : : 275
De Kleijn MJJ, Van Der Schouw YT, Wilson PWF et al (2001) Intake of dietary phytoestrogens is low in postmenopausal women in the United States: the Framingham study. J Nutr 131:1826–1832. https://doi.org/10.1093/jn/131.6.1826
Effenberger I, Zhang B, Li L et al (2015) Dirigent proteins from cotton (Gossypium sp.) for the atropselective synthesis of gossypol. Angew Chemie - Int Ed 54:14660–14663. https://doi.org/10.1002/anie.201507543
Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609. https://doi.org/10.1105/tpc.12.4.599
Funatsuki H, Suzuki M, Hirose A et al (2014) Molecular basis of a shattering resistance boosting global dissemination of soybean. Proc Natl Acad Sci U S A 111:17797–17802. https://doi.org/10.1073/pnas.1417282111
Gasper R, Effenberger I, Kolesinski P et al (2016) Dirigent protein mode of action revealed by the crystal structure of AtDIR6. Plant Physiol 172:2165–2175. https://doi.org/10.1104/pp.16.01281
Grotewold E, Drummond BJ, Bowen B, Peterson T (1994) The myb-homologous P gene controls phlobaphene pigmentation in maize floral organs by directly activating a flavonoid biosynthetic gene subset. Cell 76:543–553. https://doi.org/10.1016/0092-8674(94)90117-1
Halls SC, Lewis NG (2002) Secondary and quaternary structures of the (+)-pinoresinol-forming dirigent protein. Biochemistry 41:9455–9461. https://doi.org/10.1021/bi0259709
Halls SC, Davin LB, Kramer DM, Lewis NG (2004) Kinetic study of coniferyl alcohol radical binding to the (+)-pinoresinol forming dirigent protein. Biochemistry 43:2587–2595. https://doi.org/10.1021/bi035959o
Hosmani PS, Kamiya T, Danku J et al (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 U S A 110:14498–14503. https://doi.org/10.1073/pnas.1308412110
Itzhaki H, Woodson WR (1993) Characterization of an ethylene-responsive glutathione S-transferase gene cluster in carnation. Plant Mol Biol 22:43–58. https://doi.org/10.1007/BF00038994
Jin-long G, Li-ping X, Jing-ping F et al (2012) A novel dirigent protein gene with highly stem-specific expression from sugarcane, response to drought, salt and oxidative stresses. Plant Cell Rep 31:1801–1812. https://doi.org/10.1007/s00299-012-1293-1
Kamioka H (2019) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Japanese Pharmacol Ther 47:1177–1185
Kazenwadel C, Klebensberger J, Richter S et al (2013) Optimized expression of the dirigent protein AtDIR6 in Pichia pastoris and impact of glycosylation on protein structure and function. Appl Microbiol Biotechnol 97:7215–7227. https://doi.org/10.1007/s00253-012-4579-x
Khan A, Li RJ, Sun JT et al (2018) Genome-wide analysis of dirigent gene family in pepper (Capsicum annuum L.) and characterization of CaDIR7 in biotic and abiotic stresses. Sci Rep 8:1–21. https://doi.org/10.1038/s41598-018-23761-0
Kim JK, Cao J, Wu R (1992) Regulation and interaction of multiple protein factors with the proximal promoter regions of a rice high pl α-amylase gene. MGG Mol Gen Genet 232:383–393. https://doi.org/10.1007/BF00266241
Kim MK, Jeon JH, Fujita M et al (2002) The western red cedar (Thuja plicata) 8–8′ DIRIGENT family displays diverse expression patterns and conserved monolignol coupling specificity. Plant Mol Biol 49:199–214. https://doi.org/10.1023/A:1014940930703
Kim KW, Smith CA, Daily MD et al (2015) Trimeric structure of (+)-pinoresinol-forming dirigent protein at 1.95 A˚ resolution with three isolated active sites. J Biol Chem 290:1308–1318. https://doi.org/10.1074/jbc.M114.611780
Ko JH, Beers EP, Han KH (2006) Global comparative transcriptome analysis identifies gene network regulating secondary xylem development in Arabidopsis thaliana. Mol Genet Genomics 276:517–531. https://doi.org/10.1007/s00438-006-0157-1
Kumar S, Stecher G, Tamura K (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/MOLBEV/MSW054
Lacombe E, Van Doorsselaere J, Boerjan W et al (2000) Characterization of cis-elements required for vascular expression of the cinnamoyl CoA reductase gene and for protein-DNA complex formation. Plant J 23:663–676. https://doi.org/10.1046/j.1365-313X.2000.00838.x
Lescot M, Déhais P, Thijs G et al (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. https://doi.org/10.1093/nar/30.1.325
Li N, Zhao M, Liu T et al (2017) A novel soybean dirigent gene GmDIR22 contributes to promotion of lignan biosynthesis and enhances resistance to Phytophthora sojae. Front Plant Sci 8:1–12. https://doi.org/10.3389/fpls.2017.01185
Li L, Sun W, Zhou P, et al (2021) Genome-wide characterization of dirigent proteins in populus: gene expression variation and expression pattern in response to Marssonina brunnea and phytohormones. Forests 12:. https://doi.org/10.3390/f12040507
Liao Y, Liu S, Jiang Y et al (2017) Genome-wide analysis and environmental response profiling of dirigent family genes in rice (Oryza sativa). Genes and Genomics 39:47–62. https://doi.org/10.1007/s13258-016-0474-7
Liu J, Stipanovic RD, Bell AA et al (2008) Stereoselective coupling of hemigossypol to form (+)-gossypol in moco cotton is mediated by a dirigent protein. Phytochemistry 69:3038–3042. https://doi.org/10.1016/j.phytochem.2008.06.007
Liu Z, Wang X, Sun Z et al (2021) Evolution, expression and functional analysis of cultivated allotetraploid cotton DIR genes. BMC Plant Biol 21:1–16. https://doi.org/10.1186/s12870-021-02859-0
Ma QH, Liu YC (2015) TaDIR13, a dirigent protein from wheat, promotes lignan biosynthesis and enhances pathogen resistance. Plant Mol Biol Report 33:143–152. https://doi.org/10.1007/s11105-014-0737-x
Ma X, Xu W, Liu T et al (2021) Functional characterization of soybean (Glycine max) DIRIGENT genes reveals an important role of GmDIR27 in the regulation of pod dehiscence. Genomics 113:979–990. https://doi.org/10.1016/j.ygeno.2020.10.033
Merkouropoulos G, Barnett DC, Shirsat AH (1999) The Arabidopsis extensin gene is developmentally regulated, is induced by wounding, methyl jasmonate, abscisic and salicylic acid, and codes for a protein with unusual motifs. Planta 208:212–219. https://doi.org/10.1007/s004250050552
Mitchell AL, Attwood TK, Babbitt PC et al (2019) InterPro in 2019: improving coverage, classification and access to protein sequence annotations. Nucleic Acids Res 47:D351–D360. https://doi.org/10.1093/nar/gky1100
Morita A, Yokota H, Ishka MR, Ghanati F (2006) Changes in peroxidase activity and lignin content of cultured tea cells in response to excess manganese. Soil Sci Plant Nutr 52:26–31. https://doi.org/10.1111/j.1747-0765.2006.00006.x
Nash J, Luehrsen KR, Walbot V (1990) Bronze-2 gene of maize: reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell 2:1039–1049. https://doi.org/10.1105/tpc.2.11.1039
Oomah BD (2001) Flaxseed as a functional food source. J Sci Food Agric 81:889–894. https://doi.org/10.1002/jsfa.898
Paniagua C, Bilkova A, Jackson P et al (2017) Dirigent proteins in plants: modulating cell wall metabolism during abiotic and biotic stress exposure. J Exp Bot 68:3287–3301. https://doi.org/10.1093/jxb/erx141
Pastuglia M, Roby D, Dumas C, Cock JM (1997) Rapid induction by wounding and bacterial infection of an S gene family receptor-like kinase gene in Brassica oleracea. Plant Cell 9:49–60. https://doi.org/10.1105/tpc.9.1.49
Pellegrini N, Valtueña S, Ardigò D et al (2010) Intake of the plant lignans matairesinol, secoisolariciresinol, pinoresinol, and lariciresinol in relation to vascular inflammation and endothelial dysfunction in middle age-elderly men and post-menopausal women living in Northern Italy. Nutr Metab Cardiovasc Dis 20:64–71. https://doi.org/10.1016/j.numecd.2009.02.003
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 60:21–40. https://doi.org/10.1007/s11103-005-2226-y
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 68:1975–1991. https://doi.org/10.1016/j.phytochem.2007.04.042
Reboledo G, del Campo R, Alvarez A et al (2015) Physcomitrella patens activates defense responses against the pathogen colletotrichum gloeosporioides. Int J Mol Sci 16:22280–22298. https://doi.org/10.3390/ijms160922280
Rivière C, Pawlus AD, Mérillon JM (2012) Natural stilbenoids: distribution in the plant kingdom and chemotaxonomic interest in Vitaceae. Nat Prod Rep 29:1317–1333. https://doi.org/10.1039/c2np20049j
Rogers LA, Dubos C, Surman C et al (2005) Comparison of lignin deposition in three ectopic lignification mutants. New Phytol 168:123–140. https://doi.org/10.1111/j.1469-8137.2005.01496.x
Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523. https://doi.org/10.1046/j.1365-313X.1997.11030513.x
Rushton PJ, Torres JT, Parniske M et al (1996) Interaction of elicitor-induced DNA-binding proteins with elicitor response elements in the promoters of parsley PR1 genes. EMBO J 15:5690–5700. https://doi.org/10.1002/j.1460-2075.1996.tb00953.x
Sakai T, Takahashi Y, Nagata T (1996) Analysis of the promoter of the auxin-inducible gene, parC, of tobacco. Plant Cell Physiol 37:906–913. https://doi.org/10.1093/oxfordjournals.pcp.a029038
Satake H, Koyama T, Bahabadi SE et al (2015) Essences in metabolic engineering of lignan biosynthesis. Metabolites 5:270–290. https://doi.org/10.3390/metabo5020270
Seneviratne HK, Dalisay DS, Kim KW et al (2015) Non-host disease resistance response in pea (Pisum sativum) pods: biochemical function of DRR206 and phytoalexin pathway localization. Phytochemistry 113:140–148. https://doi.org/10.1016/j.phytochem.2014.10.013
Shin R, Burch AY, Huppert KA et al (2007) The Arabidopsis transcription factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453. https://doi.org/10.1105/tpc.107.050963
Skriver K, Olsen FL, Rogers JC, Mundy J (1991) Cis-acting DNA elements responsive to gibberellin and its antagonist abscisic acid. Proc Natl Acad Sci U S A 88:7266–7270. https://doi.org/10.1073/pnas.88.16.7266
Solano R, Nieto C, Avila J et al (1995) Dual DNA binding specificity of a petal epidermis-specific MYB transcription factor (MYB.Ph3) from Petunia hybrida. EMBO J 14:1773–1784. https://doi.org/10.1002/j.1460-2075.1995.tb07166.x
Song M, Peng X (2019) Genome-wide identification and characterization of DIR genes in Medicago truncatula. Biochem Genet 57:487–506. https://doi.org/10.1007/s10528-019-09903-7
Tamagnone L, Merida A, Parr A et al (1998) The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10:135–154. https://doi.org/10.1105/tpc.10.2.135
Thamil Arasan SK, Park JI, Ahmed NU et al (2013) Characterization and expression analysis of dirigent family genes related to stresses in Brassica. Plant Physiol Biochem 67:144–153. https://doi.org/10.1016/j.plaphy.2013.02.030
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 58:398–408. https://doi.org/10.1093/pcp/pcw213
Umezawa T, Davin LB, Yamamoto E, et al (1990) Lignan biosynthesis in Forsythia species. J Chem Soc Chem Commun 1405–1408. https://doi.org/10.1039/C39900001405
Wang Y, Cao Y, Liang X et al (2022) A dirigent family protein confers variation of Casparian strip thickness and salt tolerance in maize. Nat Commun 13:1–14. https://doi.org/10.1038/s41467-022-29809-0
White AJ, Alison Dunn M, Brown K, Hughes MA (1994) Comparative analysis of genomic sequence and expression of a lipid transfer protein gene family in winter barley. J Exp Bot 45:1885–1892. https://doi.org/10.1093/jxb/45.12.1885
Wu R, Wang L, Wang Z et al (2009) Cloning and expression analysis of a dirigent protein gene from the resurrection plant Boea hygrometrica. Prog Nat Sci 19:347–352. https://doi.org/10.1016/j.pnsc.2008.07.010
Xu W, Liu T, Zhang H, Zhu H (2021) Mungbean DIRIGENT gene subfamilies and their expression profiles under salt and drought stresses. Front Genet 12:1–15. https://doi.org/10.3389/fgene.2021.658148
Yadav V, Wang Z, Yang X et al (2021) Comparative analysis, characterization and evolutionary study of dirigent gene family in Cucurbitaceae and expression of novel dirigent peptide against powdery mildew stress. Genes (basel) 12:1–26. https://doi.org/10.3390/genes12030326
Yamamoto S, Nakano T, Suzuki K, Shinshi H (2004) Elicitor-induced activation of transcription via W box-related cis-acting elements from a basic chitinase gene by WRKY transcription factors in tobacco. Biochim Biophys Acta - Gene Struct Expr 1679:279–287. https://doi.org/10.1016/j.bbaexp.2004.07.005
Zhan ZJ, Ying YM, Ma LF, Shan WG (2011) Natural disesquiterpenoids. Nat Prod Rep 28:594–629. https://doi.org/10.1039/c0np00050g
Zhu L, Zhang X, Tu L et al (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 89:41–45
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PK has contributed substantially in writing the draft and preparing the manuscript; GR has contributed to the conceptualization and drawing of the hypothesis for the study; RJ has contributed to the making of tables and figures for the manuscript; MG and VK have contributed to critically revising the work; GR has contributed in study design and manuscript editing. All authors have read and approved the final manuscript.
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Kapoor, P., Rakhra, G., Kumar, V. et al. Insights into the functional characterization of DIR proteins through genome-wide in silico and evolutionary studies: a systematic review. Funct Integr Genomics 23, 166 (2023). https://doi.org/10.1007/s10142-023-01095-z
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DOI: https://doi.org/10.1007/s10142-023-01095-z