Functional and evolutionary comparative analysis of the DIR gene family in Nicotiana tabacum L. and Solanum tuberosum L.
Nicotiana tabacum L.
Solanum tuberosum L.
Biotic stress
Dirigent (DIR)
Expression analysis
Phylogenetic analysis
Journal
BMC genomics
ISSN: 1471-2164
Titre abrégé: BMC Genomics
Pays: England
ID NLM: 100965258
Informations de publication
Date de publication:
05 Jul 2024
05 Jul 2024
Historique:
received:
11
04
2024
accepted:
27
06
2024
medline:
6
7
2024
pubmed:
6
7
2024
entrez:
5
7
2024
Statut:
epublish
Résumé
The dirigent (DIR) genes encode proteins that act as crucial regulators of plant lignin biosynthesis. In Solanaceae species, members of the DIR gene family are intricately related to plant growth and development, playing a key role in responding to various biotic and abiotic stresses. It will be of great application significance to analyze the DIR gene family and expression profile under various pathogen stresses in Solanaceae species. A total of 57 tobacco NtDIRs and 33 potato StDIRs were identified based on their respective genome sequences. Phylogenetic analysis of DIR genes in tobacco, potato, eggplant and Arabidopsis thaliana revealed three distinct subgroups (DIR-a, DIR-b/d and DIR-e). Gene structure and conserved motif analysis showed that a high degree of conservation in both exon/intron organization and protein motifs among tobacco and potato DIR genes, especially within members of the same subfamily. Total 8 pairs of tandem duplication genes (3 pairs in tobacco, 5 pairs in potato) and 13 pairs of segmental duplication genes (6 pairs in tobacco, 7 pairs in potato) were identified based on the analysis of gene duplication events. Cis-regulatory elements of the DIR promoters participated in hormone response, stress responses, circadian control, endosperm expression, and meristem expression. Transcriptomic data analysis under biotic stress revealed diverse response patterns among DIR gene family members to pathogens, indicating their functional divergence. After 96 h post-inoculation with Ralstonia solanacearum L. (Ras), tobacco seedlings exhibited typical symptoms of tobacco bacterial wilt. The qRT-PCR analysis of 11 selected NtDIR genes displayed differential expression pattern in response to the bacterial pathogen Ras infection. Using line 392278 of potato as material, typical symptoms of potato late blight manifested on the seedling leaves under Phytophthora infestans infection. The qRT-PCR analysis of 5 selected StDIR genes showed up-regulation in response to pathogen infection. Notably, three clustered genes (NtDIR2, NtDIR4, StDIR3) exhibited a robust response to pathogen infection, highlighting their essential roles in disease resistance. The genome-wide identification, evolutionary analysis, and expression profiling of DIR genes in response to various pathogen infection in tobacco and potato have provided valuable insights into the roles of these genes under various stress conditions. Our results could provide a basis for further functional analysis of the DIR gene family under pathogen infection conditions.
Sections du résumé
BACKGROUND
BACKGROUND
The dirigent (DIR) genes encode proteins that act as crucial regulators of plant lignin biosynthesis. In Solanaceae species, members of the DIR gene family are intricately related to plant growth and development, playing a key role in responding to various biotic and abiotic stresses. It will be of great application significance to analyze the DIR gene family and expression profile under various pathogen stresses in Solanaceae species.
RESULTS
RESULTS
A total of 57 tobacco NtDIRs and 33 potato StDIRs were identified based on their respective genome sequences. Phylogenetic analysis of DIR genes in tobacco, potato, eggplant and Arabidopsis thaliana revealed three distinct subgroups (DIR-a, DIR-b/d and DIR-e). Gene structure and conserved motif analysis showed that a high degree of conservation in both exon/intron organization and protein motifs among tobacco and potato DIR genes, especially within members of the same subfamily. Total 8 pairs of tandem duplication genes (3 pairs in tobacco, 5 pairs in potato) and 13 pairs of segmental duplication genes (6 pairs in tobacco, 7 pairs in potato) were identified based on the analysis of gene duplication events. Cis-regulatory elements of the DIR promoters participated in hormone response, stress responses, circadian control, endosperm expression, and meristem expression. Transcriptomic data analysis under biotic stress revealed diverse response patterns among DIR gene family members to pathogens, indicating their functional divergence. After 96 h post-inoculation with Ralstonia solanacearum L. (Ras), tobacco seedlings exhibited typical symptoms of tobacco bacterial wilt. The qRT-PCR analysis of 11 selected NtDIR genes displayed differential expression pattern in response to the bacterial pathogen Ras infection. Using line 392278 of potato as material, typical symptoms of potato late blight manifested on the seedling leaves under Phytophthora infestans infection. The qRT-PCR analysis of 5 selected StDIR genes showed up-regulation in response to pathogen infection. Notably, three clustered genes (NtDIR2, NtDIR4, StDIR3) exhibited a robust response to pathogen infection, highlighting their essential roles in disease resistance.
CONCLUSION
CONCLUSIONS
The genome-wide identification, evolutionary analysis, and expression profiling of DIR genes in response to various pathogen infection in tobacco and potato have provided valuable insights into the roles of these genes under various stress conditions. Our results could provide a basis for further functional analysis of the DIR gene family under pathogen infection conditions.
Identifiants
pubmed: 38970011
doi: 10.1186/s12864-024-10577-8
pii: 10.1186/s12864-024-10577-8
doi:
Substances chimiques
Plant Proteins
0
Types de publication
Journal Article
Comparative Study
Langues
eng
Sous-ensembles de citation
IM
Pagination
671Subventions
Organisme : Longyan Tobacco Company
ID : LK-2022Y06
Organisme : Longyan Tobacco Company
ID : LK-2022Y02
Organisme : Longyan Tobacco Company
ID : LK-2022Y06
Informations de copyright
© 2024. The Author(s).
Références
Sun HR, Zhang JN, Ren M, Wang YF. Genome-wide identification and expression analysis of DIR gene family in tomato (Solanum lycopersicum). J Agricultural Biotechnol. 2023;31(1):36–49.
Davin LB, Wang HB, Crowell AL, et al. Stereoselec-tive bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science. 1997;275(5298):362–6.
pubmed: 8994027
doi: 10.1126/science.275.5298.362
Ralph S, Park JY, Bohlmann J, et al. 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. 2006;60(1):21–40.
pubmed: 16463097
doi: 10.1007/s11103-005-2226-y
Chen JL, Zhang ZJ, Liu XY, et al. Genome-wide identification and analysis of dirigent gene family in moso bamboo (Phyllostachys edulis). Plant Physiol J. 2019;55(9):1406–17.
Shi H, Liu Z, Zhu L, Zhang C, Chen Y, Zhou Y, et al. Overexpression of cotton (Gossypium hirsutum) dirigent1 gene enhances lignification that blocks the spread of Verticillium Dahliae. Acta Biochim Biophys Sin. 2012;44:555–64.
pubmed: 22595512
doi: 10.1093/abbs/gms035
Ma QH, Liu YC. TaDIR13, a dirigent protein from wheat, promotes lignan biosynthesis and enhances pathogen resistance. Plant Mol Biology Report. 2014;33(1):143–52.
doi: 10.1007/s11105-014-0737-x
Wang Y, Fristensky BJMB. Transgenic canola lines expressing pea defense gene DRR206 have resistance to aggressive blackleg isolates and to Rhizoctonia solani. Mol Breeding. 2001;8:263–71.
doi: 10.1023/A:1013706400168
Nobile PM, Bottcher A, Mayer JLS, et al. Identification, classification and transcriptional profiles of dirigent domain-containing proteins in sugarcane. Mol Genet Genomics. 2017;292(6):1323–40.
pubmed: 28699001
doi: 10.1007/s00438-017-1349-6
Arasan SKT, Park JI, Ahmed NU, et al. Characterization and expression analysis of dirigent family genes related to stresses in Brassica. Plant Physiol Biochem. 2013;67:144–53.
doi: 10.1016/j.plaphy.2013.02.030
Sahani PA, Ujinwal M, Singh S, et al. Genome wide in silico characterization of dirigent protein family in flax (Linum Usitatissmum L). Plant Archives. 2018;18:61–8.
Song M, Peng X. Genome-wide identification and characterization of DIR genes in Medicago truncatula. Biochem Genet. 2019;57(4):487–506.
pubmed: 30649641
doi: 10.1007/s10528-019-09903-7
Cheng X, Su XQ, Muhammad A, et al. Molecular characterization, evolution, and expression profiling of the dirigent (DIR) family genes in Chinese white pear (Pyrus Bretschneideri). Front Genet. 2018;9:136.
pubmed: 29713336
pmcid: 5911567
doi: 10.3389/fgene.2018.00136
Hosmani PS, Kamiya T, Danku J, Naseer S, Geldner N, Guerinot ML, et al. 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. 2013;110:14498–503.
pubmed: 23940370
pmcid: 3761638
doi: 10.1073/pnas.1308412110
Ma XF, Xu WY, Liu T, et al. Functional characterization of soybean (Glycine max) DIRIGENT genes reveals an important role of GmDIR27 in the regulation of pod dehiscence. Genomics. 2021;113(1 Pt 2):979–90.
pubmed: 33144217
doi: 10.1016/j.ygeno.2020.10.033
Khan A, Li RJ, Sun JT, Ma F, Zhang HX, Jin JH, et al. Genome-wide analysis of dirigent gene family in pepper (Capsicum annuum L.) and characterization of CaDIR7 in biotic and abiotic stresses. Sci Rep. 2018;8(1):5500.
pubmed: 29615685
pmcid: 5883049
doi: 10.1038/s41598-018-23761-0
Zhang K, Xing W, Sheng S, Yang D, Zhen F, Jiang H, Yan C, Jia L. Genome-wide identification and expression analysis of eggplant DIR gene family in response to biotic and abiotic stresses. Horticulturae. 2022;8:732.
doi: 10.3390/horticulturae8080732
Liao YR, Liu SB, Jiang YY, et al. Genome-wide analysis and environmental response profiling of dirigent family genes in rice (Oryza sativa). Genes Genomics. 2017;39(1):47–62.
doi: 10.1007/s13258-016-0474-7
Luo R, Pan W, Liu W, Tian Y, Zeng Y, Li Y, Li Z, Cui L. The barley DIR gene family: an expanded gene family that is involved in stress responses. Front Genet. 2022. https://doi.org/10.3389/fgene.2022.1042772 .
doi: 10.3389/fgene.2022.1042772
pubmed: 36778912
pmcid: 9772685
Kim K-W, Smith CA, Daily MD, Cort JR, Davin LB, Lewis NG. Trimeric structure of (+)-pinoresinol forming dirigent protein at 1.95 Å resolution with three isolated active sites. J Biol Chem. 2015;290:1308–18.
pubmed: 25411250
doi: 10.1074/jbc.M114.611780
Corbin C, Drouet S, Markulin L, Auguin D, Lainé É, Davin LB, Cort JR, Lewis NG, Hano C. A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: from gene identification and evolution to differential regulation. Plant Mol Biol. 2018;97(1–2):73–101.
pubmed: 29713868
doi: 10.1007/s11103-018-0725-x
Wang Y, Tang H, Debarry JD, Tan X, Li J, Wang X, Lee TH, Jin H, Marler B, Guo H, et al. MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012;40:e49.
pubmed: 22217600
pmcid: 3326336
doi: 10.1093/nar/gkr1293
Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13:1194–202.
pubmed: 32585190
doi: 10.1016/j.molp.2020.06.009
Shi R, Jin J, Nifong JM, Shew D, Lewis R. Homoeologous chromosome exchange explains the creation of a QTL affecting soil-borne pathogen resistance in tobacco. Plant Biotechnol J. 2022;20(1):47–58.
pubmed: 34453871
doi: 10.1111/pbi.13693
Yabuuchi E, Kosako Y, Yano I, Hotta H, Nishiuchi Y. Transfer of two Burkholderia and an Alcaligenes species to Ralstonia gen. Nov.: proposal of Ralstonia pickettii (Ralston, Palleroni and Doudoroff 1973) comb. Nov., Ralstonia solanacearum (Smith, 1896) comb. Nov. and Ralstonia eutropha (Davis 1969) comb. Nov. Microbiol Immunol. 1995;39(11):897–904.
pubmed: 8657018
doi: 10.1111/j.1348-0421.1995.tb03275.x
Jenkins SF, Averrre CW. Root diseases of vegetables in hydroponic culture systems in North Carolina greenhouse. Plant Dis. 1983;9(67):968–70.
doi: 10.1094/PD-67-968
Tan W, Wu YH. Pathology of tobacco. Beijing, China: Agriculture; 2003.
Jose J, Éva C, Bozsó Z, Hamow KÁ, Fekete Z, Fábián A, Bánfalvi Z, Sági L. Global transcriptome and targeted metabolite analyses of roots reveal different defence mechanisms against Ralstonia solanacearum infection in two resistant potato cultivars. Front Plant Sci. 2023. https://doi.org/10.3389/fpls.2022.1065419 .
doi: 10.3389/fpls.2022.1065419
pubmed: 36733596
pmcid: 9889091
Al Harethi AA, Abdullah QYM, Al Jobory HJ, et al. First report of molecular identification of Phytophthora infestans causing potato late blight in Yemen. Sci Rep. 2023;13:16365.
pubmed: 37773211
pmcid: 10541906
doi: 10.1038/s41598-023-43510-2
Cannon SB, Mitra A, Baumgarten A, Young ND, May G. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. 2004;4:10.
pubmed: 15171794
pmcid: 446195
doi: 10.1186/1471-2229-4-10
Moore RC, Purugganan MD. The early stages of duplicate gene evolution. Proc Natl Acad Sci U S A. 2003;100(26):15682–7.
pubmed: 14671323
pmcid: 307628
doi: 10.1073/pnas.2535513100
Wang R, Du C, Gu G, et al. Genome-wide identification and expression analysis of the ADH gene family under diverse stresses in tobacco (Nicotiana tabacum L). BMC Genomics. 2024;25:13.
pubmed: 38166535
pmcid: 10759372
doi: 10.1186/s12864-023-09813-4
Qin M, Zhang B, Gu G, Yuan J, Yang X, Yang J, Xie X. Genome-wide analysis of the G2-like transcription factor genes and their expression in different senescence stages of tobacco (Nicotiana tabacum L). Front Genet. 2021;31(12):626352.
doi: 10.3389/fgene.2021.626352
Si C, Zhan D, Wang L, Sun X, Zhong Q, Yang S. Systematic investigation of TCP gene family: genome-wide identification and light-regulated gene expression analysis in pepino (Solanum Muricatum). Cells. 2023;12:1015.
pubmed: 37048089
pmcid: 10093338
doi: 10.3390/cells12071015
Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016;14(16):86.
doi: 10.1186/s12870-016-0771-y
Atkinson NJ, Urwin PE. The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot. 2012;63:3523–43.
pubmed: 22467407
doi: 10.1093/jxb/ers100
Zhao F, Niu K, Tian X, Du W. Triticale improvement: mining of genes related to yellow rust resistance in triticale based on transcriptome sequencing. Front Plant Sci. 2022;9(13):883147.
doi: 10.3389/fpls.2022.883147
Yao J, Allen C. Chemotaxis is required for virulence and competitive fitness of the bacterial wilt pathogen Ralstonia solanacearum. J Bacteriol. 2006;188:3697–708.
pubmed: 16672623
pmcid: 1482862
doi: 10.1128/JB.188.10.3697-3708.2006
Vasse J, Frey P, Trigalet A. Microscopic studies of intercellular infection and protoxylem invasion of tomato roots by Pseudomonas solanacearum. Mol Plant–Microbe Interact. 1995;8(2):241–51.
doi: 10.1094/MPMI-8-0241
Edwards KD, et al. A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genomics. 2017;18:1–14.
doi: 10.1186/s12864-017-3791-6
Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, et al. The Sol Genomics Network (SGN)--from genotype to phenotype to breeding. Nucleic Acids Res. 2015;43:D1036–41.
pubmed: 25428362
doi: 10.1093/nar/gku1195
Jian Y, Yan W, Xu J, Duan S, Li G, Jin L. Genome-wide simple sequence repeat markers in potato: abundance, distribution, composition, and polymorphism. DNA Res. 2021. https://doi.org/10.1093/dnares/dsab020 .
doi: 10.1093/dnares/dsab020
pubmed: 34609514
pmcid: 8641542
Ivica, Letunic. Peer Bork. 20 years of the SMART protein domain annotation resource. Nucleic Acids Res. 2018;46:D493–496.
doi: 10.1093/nar/gkx922
Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, et al. CDD: NCBI’s conserved domain database. Nucleic Acids Res. 2015;43:D222–6.
pubmed: 25414356
doi: 10.1093/nar/gku1221
Horton P, et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res. 2007;35:1–3.
doi: 10.1093/nar/gkm259
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 2002;30(1):325–7.
pubmed: 11752327
pmcid: 99092
doi: 10.1093/nar/30.1.325
Ma WX, Noble WS, Bailey TL. Motif-based analysis of large nucleotide data sets using MEME-ChIP. Nat Protoc. 2014;9(6):1428–50.
pubmed: 24853928
pmcid: 4175909
doi: 10.1038/nprot.2014.083
Bailey TL, Johnson J, Grant CE, Noble WS. The MEME suite. Nucleic Acids Res. 2015;43:39–49.
doi: 10.1093/nar/gkv416
Gao W, Chen R, Pan M, et al. Early transcriptional response of seedling roots to Ralstonia solanacearum in tobacco (Nicotiana tabacum L). Eur J Plant Pathol. 2019;155(2):527–36.
doi: 10.1007/s10658-019-01788-x
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(– Delta Delta C(T)) method. Methods. 2001;25(4):402–8.
pubmed: 11846609
doi: 10.1006/meth.2001.1262
Qin M, Luo W, Zheng Y, Guan H, Xie X. Genome-wide identification and expression analysis of the PHD-finger gene family in Solanum tuberosum. PLoS ONE. 2019. https://doi.org/10.1371/journal.pone.0226964 .
doi: 10.1371/journal.pone.0226964
pubmed: 31887174
pmcid: 6936845