Skip to main content
Log in

Biosynthesis of monolignols. Genomic and reverse genetic approaches

  • Published:
Phytochemistry Reviews Aims and scope Submit manuscript

Abstract

The biosynthesis of monolignols is one of the most studied pathways of plant natural product biosynthesis. However, the pathway has recently undergone considerable revision, and it would appear that our understanding of the exact routes for synthesis of the building blocks of lignin and lignans is still not fully understood. Early studies of in vitro enzyme specificity failed to appreciate the catalytic promiscuity of some of the enzymes of the monolignol pathway, and the evolving model of a metabolic grid for monolignol biosynthesis may fail to appreciate the possible extent of metabolic channeling within the pathway. New approaches to the study of monolignol biosynthesis include genomics, advanced cellular imaging techniques, and transgenic manipulation. This article summarizes the use of these approaches to gain a better understanding of the operation of a complex metabolic pathway.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Atanassova R, Favet N, Martz F, Chabbert B, Tollier MT, Monties B, Fritig B & Legrand M (1995) Altered lignin composition in transgenic tobacco expressing O-methyltransferase sequences in sense and antisense orientation. Plant J. 8: 465–477.

    Google Scholar 

  • Bao W, O'Malley DM, Whetten R & Sederoff RR (1993) A laccase associated with lignification in loblolly pine xylem. Science 260: 672–674.

    Google Scholar 

  • Barber MS, McConnell VS & DeCaus BS (2000) Antimicrobial in-termediates of the general phenylpropanoid and lignin specific pathways. Phytochemistry 54: 53–56.

    Google Scholar 

  • Bate NJ, Orr J, Ni W, Meroni A, Nadler-Hassar T, Doerner PW, Dixon RA, Lamb CJ & Elkind Y (1994) Quantitative relation-ship between phenylalanine ammonia-lyase levels and phenyl-propanoid accumulation in transgenic tobacco identifies a rate determining step in natural product synthesis. Proc. Natl. Acad. Sci. USA 91: 7608–7612.

    Google Scholar 

  • Baucher M, BernardVailhe MA, Chabbert B, Besle JM, Opsomer C, VanMontagu M & Botterman J (1999) Down-regulation of cinnamyl alcohol dehydrogenase in transgenic alfalfa (Medicago sativa L.) and the effect on lignin composition and digestibility. Plant Mol. Biol. 39: 437–447.

    Google Scholar 

  • Bell C, Dixon RA, Farmer AD, Flores R, Inman J, Gonzales RA, Harrison MJ, Paiva NL, Scott AD, Weller JW & May GD (2001) The Medicago genome initiative: a model legume database. Nucleic Acids Res. 29: 114–117.

    Google Scholar 

  • Binns AN, Chen RH, Wood HN & Lynn DG (1987) Cell divi-sion promoting activity of naturally occuring dehydrodiconiferyl glucosides: Do cell wall components control cell division? Proc. Nat.l Acad. Sci. USA 84: 980–984.

    Google Scholar 

  • Bolwell GP & Butt VS (1983) Photoinduced changes in o-diphenol oxidase and p-coumarate hydroxylase activities in spinach beet seedlings and leaves. Phytochemistry 22: 37–45.

    Google Scholar 

  • Boudet AM & Grima-Pettenati J (1996) Lignin genetic engineering. Mol. Breeding 2: 25–39.

    Google Scholar 

  • Boudet AM, Lapierre C & Grima-Pettenati J (1995) Tansley Review No. 80. Biochemistry and molecular biology of lignification. New Phytologist 129: 203–236.

    Google Scholar 

  • Chabannes M, Barakate A, Lapierre C, Marita JM, Ralph J, Pean M, Danoun S, Halpin C, GrimaPettenati J & Boudet AM (2001) Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down-regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol de-hydrogenase (CAD) in tobacco plants. Plant J. 28: 257–270.

    Google Scholar 

  • Chabannes M, Ruel K, Yoshinaga A, Chabbert B, Jauneau A, Joseleau JP & Boudet AM (2001) In situ analysis of lignins in transgenic tobacco reveals a differential impact of individual transformations on the spatial patterns of lignin deposition at the cellular and subcellular levels. Plant J. 28: 271–282.

    Google Scholar 

  • Chapple CCS, Vogt T, Ellis BE & Somerville CR (1992) An Arabidopsis mutant defective in the general phenylpropanoid pathway. Plant Cell 4: 1413–1424.

    Google Scholar 

  • Chen F, Yasuda S & Fukushima K (1999) Evidence for a novel bio-synthetic pathway that regulates the ratio of syringyl to guaiacyl residues in lignin in the differentiating xylem of Magnolia kobus DC. Planta 207: 597–603.

    Google Scholar 

  • Cook D, R. (1999) Medicago truncatula-a model in the making! Curr. Opinion Plant Biol. 2: 301–304.

    Google Scholar 

  • Cukovic D, Ehlting J, VanZiffle J & Douglas CJ (2001) Structure and evolution of 4-coumarate: coenzyme A ligase (4CL)gene families. Biol. Chem. 382: 645–654.

    Google Scholar 

  • Davin LB & Lewis NG (1992) Phenylpropanoid metabolism: bio-synthesis of monolignols, lignans and neolignans, lignins and suberins. Rec. Adv. Phytochem. 26: 325–375.

    Google Scholar 

  • Delay D, Dyé F, Wisniewski JP & Delmotte F (1994) Synthesis and Agrobacterium vir-inducing activities of coniferyl alcohol â-glycosides. Phytochemistry 36: 289–298.

    Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu C-J, M.S. R & Wang L (2002) The phenylpropanoid pathway and plant defense-a genomics perspective. Mol. Plant Pathol. 3: 371–390.

    Google Scholar 

  • Dixon RA, Chen F, Guo D & Parvathi K (2001) The biosynthesis of monolignols: a "metabolic grid", or independent pathways to guaiacyl and syringyl units? Phytochemistry 57: 1069–1084.

    Google Scholar 

  • Dixon RA, Lamb CJ, Masoud S, Sewalt VJH & Paiva NL (1996) Metabolic engineering: prospects for crop improvement through the genetic manipulation of phenylpropanoid biosynthesis and defense responses-a review. Gene 179: 61–71.

    Google Scholar 

  • Ehlting J, Buttner D, Wang Q, Douglas CJ, Somssich IE & Kom-brink E (1999) Three 4-coumarate: coenzyme A ligases in Ara-bidopsis thaliana represent two evolutionarily divergent classes in angiosperms. Plant J. 19: 9–20.

    Google Scholar 

  • Ehlting J, Shin JJK & Douglas CJ (2001) Identification of 4-coumarate: coenzyme A ligase (4CL) substrate recognition domains. Plant J. 27: 455–465.

    Google Scholar 

  • Felton GW, Korth KL, Bi JL, Wesley SV, Huhman DV, Mathews MC, Murphy JB, Lamb C & Dixon RA (1999) Inverse relation-ship between systemic resistance of plants to microorganisms and to insect herbivory. Current Biol. 9: 317–320.

    Google Scholar 

  • Franke R, Hemm MR, Denault JW, Ruegger MO, Humphreys JM & Chapple C (2002) Changes in secondary metabolism and de-position of an unusual lignin in the ref8 mutant of Arabidopsis. Plant J. 30: 47–59.

    Google Scholar 

  • Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO & Chapple C (2002) The Arabidopsis REF8 gene encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J. 30: 33–45.

    Google Scholar 

  • Franke R, McMichael CM, Meyer K, Shirley AM, Cusumano JC & Chapple C (2000) Modified lignin in tobacco and poplar plants over-expressing the Arabidopsis gene encoding ferulate 5-hydroxylase. Plant J. 22: 223–234.

    Google Scholar 

  • Guo D, Chen F, Inoue K, Blount JW & Dixon RA (2000) Down-regulation of caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O -methyltransferase in transgenic alfalfa (Medicago sativa L.): impacts on lignin structure and implications for the biosynthesis of G and S lignin. Plant Cell 13: 73–88.

    Google Scholar 

  • Halpin C, Knight ME, Foxon GA, Campbell MM, Boudet AM, Boon JJ, Chabbert B, Tollier MT & Schuch W (1994) Manip-.305 ulation of lignin quality by downregulation of cinnamyl alcohol dehydrogenase. Plant J. 6: 339–350.

    Google Scholar 

  • Hibino T, Yakabe K, Kawazu T, Shibata D & Higuchi T (1995) Increase of cinnamaldehyde groups in lignin of transgenic to-bacco plants carrying an antisense gene for cinnamyl alcohol dehydrogenase. Biosci. Biotech. Biochem. 59: 929–931.

    Google Scholar 

  • Hoffmann L, Maury S, Martz F, Geoffroy P & Legrand M (2003) Purification, cloning, and properties of an acyltransferase con-trolling shikimate and quinate ester intermediates in phenylpro-panoid metabolism. J. Biol. Chem. 278: 95–103.

    Google Scholar 

  • Hu W-J, Harding SA, Lung J, Popko JL, Ralph J, Stokke DD, Tsai C-J & Chiang VL (1999) Repression of lignin biosynthesis pro-motes cellulose accumulation and growth of transgenic trees. Nature Biotech. 17: 808–812.

    Google Scholar 

  • Humphreys JM & Chapple C (2002) Rewriting the lignin roadmap. Curr. Opinion Plant Biol. 5: 224–229.

    Google Scholar 

  • Humphreys JM, Hemm MR & Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cyto-chrome P450-dependent monooxygenase. Proc. Natl. Acad. Sci.USA 96: 10045–10050.

    Google Scholar 

  • Inoue K, Parvathi K & Dixon RA (2000) Substrate preferences of caffeic acid/5-hydroxyferulic acid 3-O-methyltransferases in de-veloping stems of alfalfa (Medicago sativa L.). Arch. Biochem. Biophys. 375: 175–182.

    Google Scholar 

  • Joshi CP & Chiang VL (1998) Conserved sequence motifs in plant S-adenosyl-L-methionine-dependent methyltransferases. Plant Mol. Biol. 37: 663–674.

    Google Scholar 

  • Jouanin L, Goujon T, deNadai V, Martin MT, Mila I, Vallet C, Pollet B, Yoshinaga A, Chabbert B, PetitConil M & Lapierre C (2000) Lignification in transgenic poplars with extremely re-duced caffeic acid O-methyltransferase activity. Plant Physiol. 123: 1363–1373.

    Google Scholar 

  • Kajita S, Katayama Y & Omori S (1996) Alterations in the bio-synthesis of lignin in transgenic plants with chimeric genes for 4-coumarate: Coenzyme A ligase. Plant Cell Physiol. 37: 957–965.

    Google Scholar 

  • Knobloch KH & Hahlbrock K (1975) Isoenzymes pf p-coumarate: CoA ligase from cell suspension cultures of Glycine max. Eur. J. Biochem. 52: 311–320.

    Google Scholar 

  • Lam TBT, Iiyama K & Stone BA (1996) Caffeic acid: O-methyltransferases and the biosynthesis of ferulic acid in primary cell walls of wheat seedlings. Phytochemistry 41: 1507–1510.

    Google Scholar 

  • Lee D & Douglas CJ (1996) Two divergent members of a tobacco 4-coumarate:coenzyme A Ligase (4CL) gene family. Plant Physiol. 112: 193–2205.

    Google Scholar 

  • Lee D, Meyer K, Chapple C & Douglas CJ (1997) Antisense suppression of 4-coumarate:coenzyme A ligase activity in Ar-abidopsis leads to altered lignin subunit composition. Plant Cell 9: 1985–1998.

    Google Scholar 

  • Lewis NG, Davis LB & Sarkanen S (1999) The Nature and Func-tion of Lignins. In: Comprehensive Natural Products Chem-istry, Vol. 3, DHR Barton & K Nakanishi (eds) (pp. 617–745.) Elsevier, Oxford.

    Google Scholar 

  • Li L, Cheng XF, Leshkevich J, Umezawa T, Harding SA & Chi-ang VL (2001) The last step of syringyl monolignol biosynthesis in angiosperms is regulated by a novel gene encoding sinapyl alcohol dehydrogenase. Plant Cell 13: 1567–1585.

    Google Scholar 

  • Li L, Popko JL, Umezawa T & Chiang VL (2000) 5-Hydroxyconiferyl aldehyde modulates enzymatic methylation for syringyl monolignol formation, a new view of monolignol biosynthesis in angiosperms. J. Biol. Chem. 275: 6537–6545.

    Google Scholar 

  • Li L, Popko JL, Zhang X-H, Osakabe K, Tsai C-J, Joshi CP & Chiang VL (1997) A novel multifunctional O-methyltransferase implicated in a dual methylation pathway associated with lignin biosynthesis in loblolly pine. Proc. Natl. Acad. Sci. USA 94: 5461–5466.

    Google Scholar 

  • Maher EA, Bate NJ, Ni W, Elkind Y, Dixon RA & Lamb CJ (1994) Increased disease susceptibility of transgenic tobacco plants with suppressed levels of preformed phenylpropanoid products. Proc. Natl. Acad. Sci. USA. 91: 7802–7806.

    Google Scholar 

  • Marita JM, Ralph J, Hatfield RD & Chapple C (1999) NMR characterization of lignins in Arabidopsis altered in the activ-ity of ferulate 5-hydroxylase. Proc. Natl. Acad. Sci. USA 96: 12382-12332.

    Google Scholar 

  • Marita JM, Ralph J, Hatfield RD, Guo D, Chen F & Dixon RA (2002) Structural and compositional modifications in lignin of transgenic alfalfa down-regulated in caffeic acid 3-O-methyltransferase and caffeoyl CoA 3-O-methyltransferase.Phytochemistry 62: 53–65.

    Google Scholar 

  • Martin C & Paz-Ares J (1997) MYB transcription factors in plants. Trends Genet. 13: 67–73.

    Google Scholar 

  • Masuta C, Tanaka H, Uehara K, Kuwata S, Koiwai A & Noma M (1995) Broad resistance to plant viruses in transgenic plants conferred by antisense inhibition of a host gene essential in S-adenosylmethionine-dependent transmethylation reactions. Proc. Natl. Acad. Sci. USA 92: 6117–6121.

    Google Scholar 

  • Matsui N, Fukushima K, Yasuda S & Terashima N (1994) On the behavior of monolignol glucosides in lignin biosynthesis. Holzforschung 48: 375–380.

    Google Scholar 

  • Maury S, Geoffroy P & Legrand M (1999) Tobacco O-methyltransferases involved in phenylpropanoid metabolism. The different caffeoyl-coenzyme A/5-hydroxyferuloyl-coenzyme A 3/5-O-methyltransferase and caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase classes have distinct substrate specificities and expression patterns.Plant Physiol. 121: 215–223.

    Google Scholar 

  • Mazur W & Adlercreutz H. (1998) Naturally occurring oestrogens in food. Pure Appl. Chem. 70: 1759–1776.

    Google Scholar 

  • Meyer K, Shirley AM, Cusumano JC, Bell-Lelong DA & Chapple C (1998) Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis. Proc. Natl. Acad. Sci. USA 95: 6619–6623.

    Google Scholar 

  • Neish AC (1968) Monomeric intermediates in the biosynthesis of lignin. In: K Freudenberg & AC Neish (eds) Constitution and Biosynthesis of Lignin. (pp. 2–43). Springer-Verlag, Berlin.

    Google Scholar 

  • Ni W, Paiva NL & Dixon RA (1994) Reduced lignin in transgenic plants containing an engineered caffeic acid O-methyltransferase antisense gene. Transgenic Res. 3: 120–126.

    Google Scholar 

  • O'Connell A, Bolwell P & Schuch W (1998) Impact of forest tree biotechnology on the pulp and paper-making processes in the 21st century. In: K Lindsey (ed) Transgenic Plant Research. (pp. 175–186.) Harwood Academic Publ, Chur.

    Google Scholar 

  • Osakabe K, Tsao CC, Li L, Popko JL, Umezawa T, Carraway DT, Smeltzer RH, Joshi CP & Chiang VL (1999) Coniferyl al-dehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms. Proc. Natl. Acad. Sci. USA 96: 8955–8960.

    Google Scholar 

  • Parvathi K, Chen F, Guo D, Blount JW & Dixon RA (2001) Sub-strate preferences of O-methyltransferases in alfalfa suggest new pathways for 3-O-methylation of monolignols. Plant J. 25: 193–202.

    Google Scholar 

  • Piquemal J, Chamayou S, Nadaud I, Beckert M, Barriere Y, Mila I, Lapierre C, Rigau J, Puigdomenech P, Jauneau A, Digonnet C, Boudet A-M, Goffner D & Pichon M (2002) Down-regulation of caffeic acid O-methyltransferase in maize revisited using a transgenic approach. Plant Physiol. 130: 1675–1685.

    Google Scholar 

  • Piquemal J, Lapierre C, Myton K, O'Connell A, Schuch W, Grima-Pettenati J & Boudet AM (1998) Down-regulation of cinnamoyl-CoA reductase induces significant changes of lignin profiles in transgenic tobacco plants. Plant J. 13: 71–83.

    Google Scholar 

  • Quackenbush J, Liang F, Holt I, Pertea G & Upton J (2000) The TIGR gene indices: reconstruction and representation of expressed gene sequences. Nucleic Acids Res. 28: 141–145.

    Google Scholar 

  • Rae AL, Manners JM, Jones RJ, McIntyre CL & Lu DY (2001) Antisense suppression of the lignin biosynthetic enzyme, caf-feate O-methyltransferase, improves in vitro digestibility of the tropical pasture legume, Stylosanthes humilis. Australian J. Plant Physiol. 28: 289–297.

    Google Scholar 

  • Ralph J, MacKay JJ, Hatfield RD, O'Malley DM, Whetten RW & Sederoff RR (1997) Abnormal lignin in a loblolly pine mutant. Science 277: 235–239.

    Google Scholar 

  • Rasmussen S & Dixon RA (1999) Transgene-mediated and elicitor-induced perturbation of metabolic channeling at the entry point into the phenylpropanoid pathway. Plant Cell 11: 1537–1551.

    Google Scholar 

  • Sato Y, Sugiyama M, Górecki RJ, Fukuda H & Komamine A (1993) Interrelationship between lignin deposition and the activities of peroxidase isoenzymes in differentiating tracheary elements of Zinnia. Planta 189: 584–589.

    Google Scholar 

  • Schoch G, Goepfert S, Morant M, Hehn A, Meyer D, Ullmann P & Werck-Reichart D (2001) CYP98A3 from Arabidopsis thali-ana is a 3'-hydroxylase of phenolic esters, a missing link in the phenylpropanoid pathway. J. Biol. Chem. 276: 36566–36574.

    Google Scholar 

  • Sewalt VJH, Ni W, Blount JW, Jung HG, Howles PA, Masoud SA, Lamb C & Dixon RA (1997) Reduced lignin content and altered lignin composition in transgenic tobacco down-regulated in expression of phenylalanine ammonia-lyase or cinnamate 4-hydroxylase. Plant Physiol. 115: 41–50.

    Google Scholar 

  • Shen B, Li C & Tarczynski MC (2002) High free-methionine and decreased lignin content result from a mutation in the Ara-bidopsis S-adenosyl-L-methionine synthetase 3 gene. Plant J. 29: 371–380.

    Google Scholar 

  • Stewart D, Yahiaoui N, McDougall GJ, Myton K, Marque C, Boudet AM & Haigh J (1997) Fourier-transform infrared and Raman spectroscopic evidence for the incorporation of cin-namaldehydes into the lignin of transgenic tobacco (Nicotiana tabacum L.) plants with reduced expression of cinnamyl alcohol dehydrogenase. Planta 201: 311–318.

    Google Scholar 

  • Tamagnone L, Merida A, Parr A, Mackay S, Culianez-Macia FA, Roberts K & Martin C (1998) The AmMYB308 and AmMYB330 transcription factors from antirrhinum regulate phenylpropanoid and lignin biosynthesis in transgenic tobacco. Plant Cell 10: 135–154.

    Google Scholar 

  • Terashima N, Fukushima K, He L-F & Takabe K (1993) Compre-hensive model of the lignified plant cell wall. In: HG Jung, DR Buxton, RD Hatfield & J Ralph (eds) Forage cell wall structure and digestibility. ASA-CSSA-SSSA, Madison, pp. 247–270.

    Google Scholar 

  • Tsai CJ, Popko JL, Mielke MR, Hu WJ, Podila GK & Chiang VL (1998) Suppression of O-methyltransferase gene by homolog-ous sense transgene in quaking aspen causes red-brown wood phenotypes. Plant Physiol. 117: 101–112.

    Google Scholar 

  • Ulbrich B & Zenk MH (1979) Partial purification and properties of hydroxycinnamoyl-CoA: quinate hydroxycinnamoyl transferase from higher plants. Phytochemistry 18: 929–933.

    Google Scholar 

  • Urao T, Yamaguchi-Shinozaki K, Urao S & Shinozaki K (1993) An Arabidopsis myb homolog is induced by dehydration stress and its gene product binds to the conserved MYB recognition sequence. Plant Cell 5: 1529–1539.

    Google Scholar 

  • Van Doorsselaere J, Baucher M, Chognot E, Chabbert B, Tollier M-T, Petit-Conil M, Leplé J-C, Pilate G, Cornu D, Monties B, Van Montagu M, Inzé D, Boerjan W & Jouanin L (1995) A novel lignin in poplar trees with a reduced caffeic acid/5-hydroxyferulic acid O-methyltransferase activity. Plant J. 8: 855–864.

    Google Scholar 

  • Vignols F, Rigau J, Torres MA, Capellades M & Puigdoménech P (1995) The brown midrib3 (bm3) mutation in maize occurs in the gene encoding caffeic acid O-methyltransferase. Plant Cell 7: 407–416.

    Google Scholar 

  • Vincent JR & Nicholson RL (1987) Evidence for isoenzymes of 4-hydroxycinnamic acid: CoA ligase in maize mesocotyls and their response to infection by Helminthosporium maydis race O. Physiol. Mol. Plant Pathol. 30: 121–129.

    Google Scholar 

  • Wesley VS, Helliwell CA, Smith NA, Wang MB, Rouse DT, Liu Q, Gooding PS, S.P. S, Abbott D, Stoutjesdijk PA, Robinson SP, Gleave AP, Green AG & Waterhouse PM (2001) Construct design for efficient, effective and high-throughput gene silencing in plants. Plant J. 27: 581–590.

    Google Scholar 

  • Whetten R & Sederoff R (1991) Genetic engineering of wood. For. Ecol. Manage. 43: 301–316.

    Google Scholar 

  • Yamauchi K, Y asuka S, Hamada K, Tsutsumi S & Fukushima K (2003) Multiform biosynthetic pathway of syringl lignin in angiosperms. Planta 216: 496–501.

    Google Scholar 

  • Ye ZH, Kneusel RE, Matern U & Varner JE (1994) An alternative methylation pathway in lignin biosynthesis in Zinnia. Plant Cell 6: 1427–1439.

    Google Scholar 

  • Zhong R, Morrison I, W.H., Negrel J & Ye ZH (1998) Dual methyl-ation pathways in lignin biosynthesis. Plant Cell 10: 2033–2045.

    Google Scholar 

  • Zubieta C, Kota P, Ferrer J-L, Dixon RA & Noel J (2002) Struc-tural basis for the modulation of lignin monomer methylation by caffeic acid/5-hydroxyferulic acid 3/5-O-methyltransferase. Plant Cell 14: 1265–1277.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Dixon, R.A., Srinivasa Reddy, M. Biosynthesis of monolignols. Genomic and reverse genetic approaches. Phytochemistry Reviews 2, 289–306 (2003). https://doi.org/10.1023/B:PHYT.0000045486.50637.37

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/B:PHYT.0000045486.50637.37

Navigation