Changes of lignin biosynthesis in tobacco leaves during maturation
Zhaopeng Song A , Daibin Wang B , Yabei Gao A , Changjun Li B , Houlong Jiang B , Xiaowei Zhu B and Hongying Zhang
A C
+ Author Affiliations
- Author Affiliations
A Key Laboratory for Cultivation of Tobacco Industry, College of Tobacco Science, Henan Agricultural University, Zhengzhou 450002, China.
B China Tobacco Chongqing Industrial Co., Ltd, Chongqing 400715, China.
C Corresponding author. Email: zhangying198215@163.com
Functional Plant Biology 48(6) 624-633 https://doi.org/10.1071/FP20244
Submitted: 14 August 2020 Accepted: 11 February 2021 Published: 2 March 2021
Abstract
Lignin is one of the most valuable renewable industrial materials. To elucidate the mechanism via which lignin is synthesised, we compared the lignin content, leaf hardness, cell wall thickness of palisade tissue, and gene expression patterns of lignin biosynthetic enzymes in three tobacco (Nicotiana tabacum L.) varieties during maturation. The results consistently showed that during maturation, the accumulation of lignin gradually increased in tobacco leaves, reaching a peak at full maturity (45 days after topping), and then gradually decreased. Similarly, the transcript level analysis revealed that the gene expression pattern of NtPAL, NtC4H, NtCCoAOMT and NtCOMT were relatively high, and consistent with the lignin content changes. Thus, the four genes may play regulatory roles in the synthesis of tobacco lignin. Analysis of tissue expression patterns of the lignin synthesis-related gene showed that the NtPAL, NtC4H, Nt4CL, NtHCT, NtCCoAOMT, NtCOMT, NtCCR, NtCAD, and NtPAO were all expressed in stems, roots, and leaves. NtC3H and NtF5H were specifically expressed in stems and roots, and not in leaves. Consistently, the NtC3H promoter induced high GUS expression in stems and petioles, marginal in roots, and no GUS activity in leaves. These results provide insights into molecular regulation of lignin biosynthesis in tobacco.
Keywords: lignin, promoter, gene expression, transgenic plants, palisade tissue, renewable, Nicotiana tabacum.
References
Abdel-Rahman MM, Mousa IE (2016) Effects of down regulation of lignin content in maize (Zea mays L.) plants expressing C4H3 gene in the antisense orientation. Biofuels 7, 289–294.| Effects of down regulation of lignin content in maize (Zea mays L.) plants expressing C4H3 gene in the antisense orientation.Crossref | GoogleScholarGoogle Scholar |
Abdulrazzak N, Pollet B, Ehlting J, Larsen K, Asnaghi C, Ronseau S, Proux C, Erhardt M, Seltzer V, Renou JP, Ullmann P, Pauly M, Lapierre C, Werck-Reichhart D (2006) A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growth Plant Physiology 140, 30–48.
| A coumaroyl-ester-3-hydroxylase insertion mutant reveals the existence of nonredundant meta-hydroxylation pathways and essential roles for phenolic precursors in cell expansion and plant growthCrossref | GoogleScholarGoogle Scholar | 16377748PubMed |
Abedi T, Khalil MFM, Koike K, Hagura Y, Tazoe Y, Ishida N, Kitamura K, Tanaka N (2018) Expression of the human UDP-galactose transporter gene hUGT1 in tobacco plants’ enhanced plant hardness. Journal of Bioscience and Bioengineering 126, 241–248.
| Expression of the human UDP-galactose transporter gene hUGT1 in tobacco plants’ enhanced plant hardness.Crossref | GoogleScholarGoogle Scholar | 29650365PubMed |
Anders S, Huber W (2012) ‘Differential expression of RNA-Seq data at the gene level–the DESeq package.’ (European Molecular Biology Laboratory (EMBL): Heidelberg, Germany)
Barakate A, Stephens J, Goldie A, Hunter WN, Marshall D, Hancock RD, Lapierre C, Morreel K, Boerjan W, Halpin C (2011) Syringyl lignin is unaltered by severe sinapyl alcohol dehydrogenase suppression in tobacco. The Plant Cell 23, 4492–4506.
| Syringyl lignin is unaltered by severe sinapyl alcohol dehydrogenase suppression in tobacco.Crossref | GoogleScholarGoogle Scholar | 22158465PubMed |
Barros J, Serrani-Yarce JC, Chen F, Baxter D, Venables BJ, Dixon RA (2016) Role of bifunctional ammonia-lyase in grass cell wall biosynthesis. Nature Plants 2, 16050
| Role of bifunctional ammonia-lyase in grass cell wall biosynthesis.Crossref | GoogleScholarGoogle Scholar | 27255834PubMed |
Baucher M, Halpin C, Petit-Conil M, Boerjan W (2003) Lignin: Genetic engineering and impact on pulping. Critical Reviews in Biochemistry and Molecular Biology 38, 305–350.
| Lignin: Genetic engineering and impact on pulping.Crossref | GoogleScholarGoogle Scholar | 14551235PubMed |
Begović L, Abičić I, Lalić A, Lepeduš H, Cesar V, Leljak-Levanić D (2018) Lignin synthesis and accumulation in barley cultivars differing in their resistance to lodging. Plant Physiology and Biochemistry 133, 142–148.
| Lignin synthesis and accumulation in barley cultivars differing in their resistance to lodging.Crossref | GoogleScholarGoogle Scholar | 30419464PubMed |
Boerjan W, Ralph J, Baucher M (2003) Lignin Biosynthesis. Annual Review of Plant Biology 54, 519–546.
| Lignin Biosynthesis.Crossref | GoogleScholarGoogle Scholar | 14503002PubMed |
Collett JR, Billing JM, Meyer PA, Schmidt AJ, Remington AB, Hawley ER, Hofstad BA, Panisko EA, Dai Z, Hart TR, Santosa DM, Magnuson JK, Hallen RT, Jones SB (2019) Renewable diesel via hydrothermal liquefaction of oleaginous yeast and residual lignin from bioconversion of corn stover. Applied Energy 233–234, 840–853.
| Renewable diesel via hydrothermal liquefaction of oleaginous yeast and residual lignin from bioconversion of corn stover.Crossref | GoogleScholarGoogle Scholar |
Day A, Neutelings G, Nolin F, Grec S, Habrant A, Crônier D, Maher B, Rolando C, David H, Chabbert B (2009) Caffeoyl coenzyme A -methyltransferase down-regulation is associated with modifications in lignin and cell-wall architecture in flax secondary xylem. Plant Physiology and Biochemistry 47, 9–19.
| Caffeoyl coenzyme A -methyltransferase down-regulation is associated with modifications in lignin and cell-wall architecture in flax secondary xylem.Crossref | GoogleScholarGoogle Scholar | 19004632PubMed |
Edwards KD, Fernandez-Pozo N, Drake-Stowe K, Humphry M, Evans AD, Bombarely A, Allen F, Hurst R, White B, Kernodle SP, Bromley JR, Sanchez-Tamburrino JP, Lewis RS, Mueller LA (2017) A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency. BMC Genomics 18, 448
| A reference genome for Nicotiana tabacum enables map-based cloning of homeologous loci implicated in nitrogen utilization efficiency.Crossref | GoogleScholarGoogle Scholar | 28625162PubMed |
Fang X, Liu X, Zhang Y, Huang K, Li Y, Nie J, She H, Ruan R, Yuan X, Yi Z (2018) Effects of uniconazole or gibberellic acid application on the lignin metabolism in relation to lodging resistance of culm in common buckwheat (Fagopyrum esculentum M.). Journal Agronomy & Crop Science 204, 414–423.
| Effects of uniconazole or gibberellic acid application on the lignin metabolism in relation to lodging resistance of culm in common buckwheat (Fagopyrum esculentum M.).Crossref | GoogleScholarGoogle Scholar |
Fornalé S, Rencoret J, Garcia-Calvo L, Capellades M, Encina A, Santiago R, Rigau J, Gutiérrez A, Río JC, Caparros-Ruiz D (2015) Cell wall modifications triggered by the down-regulation of coumarate 3-hydroxylase-1 in maize. Plant Science 236, 272–282.
| Cell wall modifications triggered by the down-regulation of coumarate 3-hydroxylase-1 in maize.Crossref | GoogleScholarGoogle Scholar | 26025540PubMed |
Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM, Chapple C (2002) Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of Arabidopsis The Plant Journal 30, 47–59.
| Changes in secondary metabolism and deposition of an unusual lignin in the ref8 mutant of ArabidopsisCrossref | GoogleScholarGoogle Scholar | 11967092PubMed |
Gao YB, Wan GTX, Zheng XY, Bai JY, Zhou ZY, Zhao DF, Zhao GB, Qiu K (2019) Changes in lignin metabolism and water retention of tobacco leaves and their correlation analysis during maturity Xi Nan Nong Ye Xue Bao 32, 1543–1548.
Goyal HB, Seal D, Saxena RC (2008) Biol.-fuels from thermochemical conversion of renewable resources: A review. Renewable & Sustainable Energy Reviews 12, 504–517.
| Biol.-fuels from thermochemical conversion of renewable resources: A review.Crossref | GoogleScholarGoogle Scholar |
Grinberg M, Perl-Treves R, Palevsky E, Shomer I, Soroker V (2005) Interaction between cucumber plants and the broad mite, Polyphagotarsonemus latus: from damage to defense gene expression. Entomologia Experimentalis et Applicata 115, 135–144.
| Interaction between cucumber plants and the broad mite, Polyphagotarsonemus latus: from damage to defense gene expression.Crossref | GoogleScholarGoogle Scholar |
Hatfield RD, Marita JM (2017) Maize Development: Cell wall changes in leaves and sheaths. American Journal of Plant Sciences 08, 1248–1263.
| Maize Development: Cell wall changes in leaves and sheaths.Crossref | GoogleScholarGoogle Scholar |
Hazwan Hussin M, Aziz AA, Iqbal A, Ibrahim MNM, Latif NHA (2019) Development and characterization novel bio-adhesive for wood using kenaf core (Hibiscus cannabinus) lignin and glyoxal. International Journal of Biological Macromolecules 122, 713–722.
| Development and characterization novel bio-adhesive for wood using kenaf core (Hibiscus cannabinus) lignin and glyoxal.Crossref | GoogleScholarGoogle Scholar | 30399384PubMed |
Hilal M, Parrado MF, Rosa M, Gallardo M, Orce L, Massa EM, González JA, Prado FE (2004) Epidermal lignin deposition in quinoa cotyledons in response to UV-B radiation. Photochemistry and Photobiology 79, 205–210.
| Epidermal lignin deposition in quinoa cotyledons in response to UV-B radiation.Crossref | GoogleScholarGoogle Scholar | 15068034PubMed |
Hildebrandt J, Budzinski M, Nitzsche R, Weber A, Krombholz A, Thrän D, Bezama A (2019) Assessing the technical and environmental performance of wood-based fiber laminates with lignin based phenolic resin systems. Resources, Conservation and Recycling 141, 455–464.
| Assessing the technical and environmental performance of wood-based fiber laminates with lignin based phenolic resin systems.Crossref | GoogleScholarGoogle Scholar |
Hu D, Liu XB, She HZ, Gao Z, Ruan RW, Wu DQ, Yi ZL (2017) The lignin synthesis related genes and lodging resistance of Fagopyrum esculentum. Biologia Plantarum 61, 138–146.
| The lignin synthesis related genes and lodging resistance of Fagopyrum esculentum.Crossref | GoogleScholarGoogle Scholar |
Jefferson RA (1987) Assaying chimeric genes in plants: The GUS gene fusion system. Plant Molecular Biology Reporter 5, 387–405.
| Assaying chimeric genes in plants: The GUS gene fusion system.Crossref | GoogleScholarGoogle Scholar |
Jones L, Ennos AR, Turner SR (2001) Cloning and characterization of irregular xylem4 (irx4): a severelylignin-deficient mutant of Arabidopsis. The Plant Journal 26, 205–216.
| Cloning and characterization of irregular xylem4 (irx4): a severelylignin-deficient mutant of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 11389761PubMed |
Kai D, Tan MJ, Chee PL, Chua YK, Yap YL, Loh XJ (2016) Towards lignin-based functional materials in a sustainable world. Green Chemistry 18, 1175–1200.
| Towards lignin-based functional materials in a sustainable world.Crossref | GoogleScholarGoogle Scholar |
Khakdan F, Nasiri J, Ranjbar M, Alizadeh H (2017) Water deficit stress fluctuates expression profiles of 4Cl, C3H, COMT, CVOMT and EOMT genes involved in the biosynthetic pathway of volatile phenylpropanoids alongside accumulation of methylchavicol and methyleugenol in different Iranian cultivars of basil. Journal of Plant Physiology 218, 74–83.
| Water deficit stress fluctuates expression profiles of 4Cl, C3H, COMT, CVOMT and EOMT genes involved in the biosynthetic pathway of volatile phenylpropanoids alongside accumulation of methylchavicol and methyleugenol in different Iranian cultivars of basil.Crossref | GoogleScholarGoogle Scholar | 28787649PubMed |
Khalil MFM, Kajiura H, Fujiyama K, Koike K, Ishida N, Tanaka N (2010) The impact of the overexpression of human UDP-galactose transporter gene hUGT1 in tobacco plants. Journal of Bioscience and Bioengineering 109, 159–169.
| The impact of the overexpression of human UDP-galactose transporter gene hUGT1 in tobacco plants.Crossref | GoogleScholarGoogle Scholar |
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nature Methods 12, 357–360.
| HISAT: a fast spliced aligner with low memory requirements.Crossref | GoogleScholarGoogle Scholar | 25751142PubMed |
Kitin P, Voelker SL, Meinzer FC, Beeckman H, Strauss SH, Lachenbruch B (2010) Tyloses and phenolic deposits in xylem vessels impede water transport in low-lignin transgenic poplars: A study by cryo-fluorescence microscopy. Plant Physiology 154, 887–898.
| Tyloses and phenolic deposits in xylem vessels impede water transport in low-lignin transgenic poplars: A study by cryo-fluorescence microscopy.Crossref | GoogleScholarGoogle Scholar | 20639405PubMed |
Lee SC, Tran TMT, Choi JW, Won K (2019) Lignin for white natural sunscreens. International Journal of Biological Macromolecules 122, 549–554.
| Lignin for white natural sunscreens.Crossref | GoogleScholarGoogle Scholar | 30416095PubMed |
Li C, Zhao X, Wang A, Huber GW, Zhang T (2015a) Catalytic transformation of lignin for the production of chemicals and fuels. Chemical Reviews 115, 11559–11624.
| Catalytic transformation of lignin for the production of chemicals and fuels.Crossref | GoogleScholarGoogle Scholar | 26479313PubMed |
Li Y, Kim JI, Pysh L, Chapple C (2015b) Four isoforms of Arabidopsis 4-coumarate:CoA ligase have overlapping yet distinct roles in phenylpropanoid metabolism. Plant Physiology 169, 2409–2421.
| Four isoforms of Arabidopsis 4-coumarate:CoA ligase have overlapping yet distinct roles in phenylpropanoid metabolism.Crossref | GoogleScholarGoogle Scholar | 26491147PubMed |
Li W, Zhang H, Li X, Zhang F, Liu C, Du Y, Gao X, Zhang Z, Zhang X, Hou Z, Zhou H, Sheng X, Wang G, Guo Y (2017) Integrative metabolomic and transcriptomic analyses unveil nutrient remobilization events in leaf senescence of tobacco. Scientific Reports 7, 12126
| Integrative metabolomic and transcriptomic analyses unveil nutrient remobilization events in leaf senescence of tobacco.Crossref | GoogleScholarGoogle Scholar | 28935979PubMed |
Li S, Xueqiang S, Muhammad A, Yanming S, Guohui L, Xi C, Yi L, Yongping C, Qing J (2018) Effects of dfferent pollens on primary metabolism and lignin biosynthesis in pear. International Journal of Molecular Sciences 19, 2273
| Effects of dfferent pollens on primary metabolism and lignin biosynthesis in pear.Crossref | GoogleScholarGoogle Scholar |
Norgren M, Edlund H (2014) Lignin: Recent advances and emerging applications. Current Opinion in Colloid & Interface Science 19, 409–416.
| Lignin: Recent advances and emerging applications.Crossref | GoogleScholarGoogle Scholar |
Ragauskas AJ, Beckham GT, Biddy MJ, Richard C, Fang C, Davis MF, Davison BH, Dixon RA, Paul G, Martin K (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 344, 1246843
| Lignin valorization: improving lignin processing in the biorefinery.Crossref | GoogleScholarGoogle Scholar | 24833396PubMed |
Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids. Phytochemistry Reviews 3, 29–60.
| Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenyl- propanoids.Crossref | GoogleScholarGoogle Scholar |
Reddy DD (2013) Tobacco stem ash as an adsorbent for removal of methylene blue from aqueous solution: equilibrium, kinetics, and mechanism of adsorption. Water, Air, and Soil Pollution 224, 1–12.
Reiter WD (2002) Biosynthesis and properties of the plant cell wall. Current Opinion in Plant Biology 5, 536–542.
| Biosynthesis and properties of the plant cell wall.Crossref | GoogleScholarGoogle Scholar | 12393017PubMed |
Ren CQ, Chen XH, Zhang SJ, Jia YC, Duan WJ, Yang TZ (2009) Comparison of drought resistance characteristics of different flue-cured tobacco varieties. Xibei Zhiwu Xuebao 29, 2019–2025.
Renault H, De MM, Jonasson G, Lara P, Nelson DR, Nilsson I, André F, Von HG, Werck-Reichhart D (2017) Gene duplication leads to altered membrane topology of a cytochrome P450 enzyme in seed plants. Molecular Biology and Evolution 34, 2041–2056.
| Gene duplication leads to altered membrane topology of a cytochrome P450 enzyme in seed plants.Crossref | GoogleScholarGoogle Scholar | 28505373PubMed |
Roopan SM (2017) An overview of natural renewable bio-polymer lignin towards nano and biotechnological applications. International Journal of Biological Macromolecules 103, 508–514.
| An overview of natural renewable bio-polymer lignin towards nano and biotechnological applications.Crossref | GoogleScholarGoogle Scholar | 28528952PubMed |
Ruegger M, Meyer K, Cusumano JC, Chapple C (1999) Regulation of ferulate-5-hydroxylase expression in Arabidopsis in the context of sinapate ester biosynthesis. Plant Physiology 119, 101–110.
| Regulation of ferulate-5-hydroxylase expression in Arabidopsis in the context of sinapate ester biosynthesis.Crossref | GoogleScholarGoogle Scholar | 9880351PubMed |
Schmittgen TD (2001) Real-time quantitative PCR. Methods (San Diego, Calif.) 25, 383–385.
| Real-time quantitative PCR.Crossref | GoogleScholarGoogle Scholar |
Schutyser W, Renders T, Van den Bosch S, Koelewijn S-F, Beckham GT, Sels BF (2018) Chemicals from lignin: an interplay of lignocellulose fractionation, depolymerisation, and upgrading. Chemical Society Reviews 47, 852–908.
| Chemicals from lignin: an interplay of lignocellulose fractionation, depolymerisation, and upgrading.Crossref | GoogleScholarGoogle Scholar | 29318245PubMed |
Sewalt VJH, Ni W, Jung HG, Dixon RA (1997) Lignin impact on fiber degradation: increased enzymatic digestibility of genetically engineered tobacco (Nicotiana tabacum) stems reduced in lignin content. Journal of Agricultural and Food Chemistry 45, 1977–1983.
| Lignin impact on fiber degradation: increased enzymatic digestibility of genetically engineered tobacco (Nicotiana tabacum) stems reduced in lignin content.Crossref | GoogleScholarGoogle Scholar |
Shin EJ, Ji HK, Chang SP, Won K (2009) UV absorbing, antioxidant, and antibacterial activities of commercial lignins. Journal of Bioscience and Bioengineering 108, S56
| UV absorbing, antioxidant, and antibacterial activities of commercial lignins.Crossref | GoogleScholarGoogle Scholar |
Si S, Chen Y, Fan C, Hu H, Li Y, Huang J, Liao H, Hao B, Li Q, Peng L (2015) Lignin extraction distinctively enhances biomass enzymatic saccharification in hemicelluloses-rich Miscanthus species under various alkali and acid pretreatments. Bioresource Technology 183, 248–254.
| Lignin extraction distinctively enhances biomass enzymatic saccharification in hemicelluloses-rich Miscanthus species under various alkali and acid pretreatments.Crossref | GoogleScholarGoogle Scholar | 25746301PubMed |
Song ZP, Wang JN, Sun M, Wu JC, Gong CR, Liu GS (2016) Effects of organic fertilizer applications on starch changes in tobacco (Nicotiana tabacum L.) leaves during maturation. Soil Science and Plant Nutrition 62, 173–179.
| Effects of organic fertilizer applications on starch changes in tobacco (Nicotiana tabacum L.) leaves during maturation.Crossref | GoogleScholarGoogle Scholar |
Tobimatsu Y, Schuetz M (2019) Lignin polymerization: how do plants manage the chemistry so well? Current Opinion in Biotechnology 56, 75–81.
| Lignin polymerization: how do plants manage the chemistry so well?Crossref | GoogleScholarGoogle Scholar | 30359808PubMed |
Tobimatsu Y, Chen F, Nakashima J, Escamilla-Treviño LL, Jackson L, Dixon RA, Ralph J (2013) Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin Polymers in seed coats. The Plant Cell 25, 2587–2600.
| Coexistence but independent biosynthesis of catechyl and guaiacyl/syringyl lignin Polymers in seed coats.Crossref | GoogleScholarGoogle Scholar | 23903315PubMed |
Vanholme R, Morreel K, Darrah C, Oyarce P, Grabber JH, Ralph J, Boerjan W (2012) Metabolic engineering of novel lignin in biomass crops. New Phytologist 196, 978–1000.
| Metabolic engineering of novel lignin in biomass crops.Crossref | GoogleScholarGoogle Scholar |
Wang SJ, Ren LQ, Yan L, Han ZW, Yange Y (2010) Mechanical characteristics of typical plant leaves. Journal of Bionics Engineering 7, 294–300.
| Mechanical characteristics of typical plant leaves.Crossref | GoogleScholarGoogle Scholar |
Wang C, Hu D, Liu X, She H, Ruan R, Yang H, Yi Z, Wu D (2015) Effects of uniconazole on the lignin metabolism and lodging resistance of culm in common buckwheat (Fagopyrum esculentum M.). Field Crops Research 180, 46–53.
| Effects of uniconazole on the lignin metabolism and lodging resistance of culm in common buckwheat (Fagopyrum esculentum M.).Crossref | GoogleScholarGoogle Scholar |
Xu C, Arancon RAD, Labidi J, Luque R (2014) Lignin depolymerisation strategies: towards valuable chemicals and fuels. Chemical Society Reviews 43, 7485–7500.
| Lignin depolymerisation strategies: towards valuable chemicals and fuels.Crossref | GoogleScholarGoogle Scholar | 25287249PubMed |
Xu ZW, Zhang XQ, Hu YW, Wei X, Zhang YY, Guo CB, Yang LJ, Xia ZL (2018) Characteristics of leaf water retention capacity in flue-cured tobacco at different growth stages. Zhongguo Yancao Kexue 39, 17–24.
Zhou M, Sharma BK, Li J, Zhao J, Xu J, Jiang J (2019) Catalytic valorization of lignin to liquid fuels over solid acid catalyst assisted by microwave heating. Fuel 239, 239–244.
| Catalytic valorization of lignin to liquid fuels over solid acid catalyst assisted by microwave heating.Crossref | GoogleScholarGoogle Scholar |
