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Genetic Engineering of Lignin Biosynthesis in Trees: Compromise between Wood Properties and Plant Viability

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Abstract

Lignin is the second most common terrestrial biopolymer. It provides mechanical strength to plants, confers waterproof properties to the vascular system, and plays an important role in protection against biotic and abiotic stresses. The chemical resistance of lignin impedes the conversion of plant biomass into cellulose and biofuels; this circumstance led to intense research on lignin biosynthesis. For a long time, it was believed that lignin consists almost exclusively of three monolignols. However, about thirty more minor monomers of diverse chemical nature have been discovered to date. Using genetic engineering methods, a number of transgenic trees with altered expression of lignin biosynthesis genes and the transcription factor genes that regulate this process have been obtained. Changes in the content and/or composition of lignin allowed researchers to significantly raise the efficiency of delignification and enzymatic hydrolysis of woody biomass, but these changes often led to retarded growth and distorted plant development. In search of a balance between the industrial needs and plant viability, new strategies have been proposed that are based on the inclusion of new monolignols in lignin as well as on the use of lignin-deficient natural tree forms. New physicochemical properties of lignin are expected to increase its extractability. At the same time, growth, development, and stress resistance of such transgenic plants should be studied under field conditions. The review presents the current state of research on properties and modification of lignin in woody plants. In addition, the relations between these modifications and plant viability, as well as the prospects for their commercial use, are discussed.

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REFERENCES

  1. Tian, Q., Wang, X., Li, C., Lu, W., Yang, L., Jiang, Y., and Luo, K., Functional characterization of the poplar R2R3-MYB transcription factor PtoMYB216 involved in the regulation of lignin biosynthesis during wood formation, PLoS One, 2013, vol. 8, p. e76369. https://doi.org/10.1371/journal.pone.0076369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Zagoskina, N.V., Involvement of phenolic compounds in plant protection from stress, Materialy X Mezhdunarodnogo simpoziuma “Fanol’nye soedineniya: fundamental’nye i prikladnye aspekty” (Proc. X Int. Symp. “Phenolic Compounds: Fundamental and Applied Aspects”), Moscow, 2018, p. 150.

  3. Moura, J.C., Bonine, C.A., Viana, J.D.O.F., Dornelas, M.C., and Mazzafera, P., Abiotic and biotic stresses and changes in the lignin content and composition in plants, J. Integr. Plant Biol., 2010, vol. 52, p. 360. https://doi.org/10.1111/j.1744-7909.2010.00892.x

    Article  CAS  PubMed  Google Scholar 

  4. Kitin, P., Voelker, S.L., Meinzer, F.C., Beeckman, H., Strauss, S.H., and Lachenbruch, B., Tyloses and phenolic deposits in xylem vessels impede water transport in low-lignin transgenic poplars: a study by cryo-fluorescence microscopy, Plant Physiol., 2010, vol. 154, p. 887. https://doi.org/10.1104/pp.110.156224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Saleme, M.L.S., Cesarino, I., Vargas, L., Kim, H., Vanholme, R., Goeminne, G., van Acker, R., Fonseca, F.C.A., Pallidis, A., Voorend, W., Junior, J.N., Padmakshan, D., van Doorsselaere, J., Ralph, J., and Boerjan, W., Silencing caffeoyl shikimate esterase affects lignification and improves saccharification in poplar, Plant Physiol., 2017, vol. 175, p. 1040. https://doi.org/10.1104/pp.17.00920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Grev, A.M., Wells, M.S., Samac, D.A., Martinson, K.L., and Sheaffer, C.C., Forage accumulation and nutritive value of reduced lignin and reference alfalfa cultivars, Agron. J., 2017, vol. 109, p. 2749. https://doi.org/10.2134/agronj2017.04.0237

    Article  CAS  Google Scholar 

  7. Liu, C.-J., Cai, Y., Zhang, X., Gou, M., and Yang, H., Tailoring lignin biosynthesis for efficient and sustainable biofuel production, Plant Biotechnol. J., 2014, vol. 12, p. 1154. https://doi.org/10.1111/pbi.12250

    Article  CAS  PubMed  Google Scholar 

  8. Bonawitz, N.D. and Chapple, C., The genetics of lignin biosynthesis: connecting genotype to phenotype, Annu. Rev. Genet., 2010, vol. 44, p. 337. https://doi.org/10.1146/annurev-genet-102209-163508

    Article  CAS  PubMed  Google Scholar 

  9. Al-Haddad, J.M., Kang, K.-Y., Mansfield, S.D., and Telewski, F.W., Chemical responses to modified lignin composition in tension wood of hybrid poplar (Populus tremula × Populus alba), Tree Physiol., 2013. V 33, p. 365. https://doi.org/10.1093/treephys/tpt017

    Article  CAS  PubMed  Google Scholar 

  10. Vanholme, R., Cesarino, I., Rataj, K., **ao, Y., Sundin, L., Goeminne, G., Kim, H., Cross, J., Morreel, K., Araujo, P., Welsh, L., Haustraete, J., McClellan, C., Vanholme, B., Ralph, J., et al., Caffeoyl shikimate esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis, Science, 2013, vol. 341, p. 1103. https://doi.org/10.1126/science.1241602

    Article  CAS  PubMed  Google Scholar 

  11. Wang, X., Chao, N., Zhang, M., Jiang, X., and Gai, Y., Functional characteristics of caffeoyl shikimate esterase in Larix kaempferi and monolignol biosynthesis in gymnosperms, Int. J. Mol. Sci., 2019, vol. 20, p. 6071. https://doi.org/10.3390/ijms20236071

    Article  CAS  PubMed Central  Google Scholar 

  12. Dixon, R.A. and Barros, J., Lignin biosynthesis: old roads revisited and new roads explored, Open Biol., 2019, vol. 9, p. 190215. https://doi.org/10.1098/rsob.190215

    Article  PubMed  PubMed Central  Google Scholar 

  13. del Río, J.C., Rencoret, J., Gutiérrez, A., Elder, T., Kim, H., and Ralph, J., Lignin monomers from beyond the canonical monolignol biosynthetic pathway: another brick in the wall, ACS Sustainable Chem. Eng., 2020, vol. 8, p. 4997. https://doi.org/10.1021/acssuschemeng.0c01109

    Article  CAS  Google Scholar 

  14. Ralph, J., Brunow, G., Harris, P.J., Dixon, R.A., Schatz, P.F., and Boerjan, W., Lignification: are lignins biosynthesized via simple combinatorial chemistry or via proteinaceous control and template replication? in Recent Advances in Polyphenol Research, Daayf, F. and Lattanzio, V., Eds., Chichester: Wiley-Blackwell, 2008, vol. 1, p. 36. https://doi.org/10.1002/9781444302400.ch2

  15. Chanoca, A., de Vries, L., and Boerjan, W., Lignin engineering in forest trees, Front. Plant Sci., 2019, vol. 10, p. 912. https://doi.org/10.3389/fpls.2019.00912

    Article  PubMed  PubMed Central  Google Scholar 

  16. Gui, J., Lam, P.Y., Tobimatsu, Y., Sun, J., Huang, C., Cao, S., Zhong, Y., Umezawa, T., and Li, L., Fibre-specific regulation of lignin biosynthesis improves biomass quality in Populus, New Phytol., 2020, vol. 226, p. 1074. https://doi.org/10.1111/nph.16411

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Mottiar, Y., Vanholme, R., Boerjan, W., Ralph, J., and Mansfield, S.D., Designer lignins: harnessing the plasticity of lignification, Curr. Opin. Biotechnol., 2016, vol. 37, p. 190. https://doi.org/10.1016/j.copbio.2015.10.009

    Article  CAS  PubMed  Google Scholar 

  18. Horvath, L., Peszlen, I., Peralta, P., Kasal, B., and Li, L., Mechanical properties of genetically engineered young aspen with modified lignin content and/or structure, Wood Fiber Sci., 2010, vol. 42, p. 310. https://doi.org/10.1016/j.sajb.2014.01.002

    Article  CAS  Google Scholar 

  19. Vanholme, R., De Meester, B., Ralph, J., and Boerjan, W., Lignin biosynthesis and its integration into metabolism, Curr. Opin. Biotechnol., 2019, vol. 56, p. 230. https://doi.org/10.1016/j.copbio.2019.02.018

    Article  CAS  PubMed  Google Scholar 

  20. Lu, F., Marita, J.M., Lapierre, C., Jouanin, L., Morreel, K., Boerjan, W., and Ralph, J., Sequencing around 5-hydroxyconiferyl alcohol-derived units in caffeic acid O-methyltransferase-deficient poplar lignins, Plant Physiol., 2010, vol. 153, p. 569. https://doi.org/10.1104/pp.110.154278

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Wagner, A., Tobimatsu, Y., Phillips, L., Flint, H., Torr, K., Donaldson, L., Pears, L., and Ralph, J., CCoAOMT suppression modifies lignin composition in Pinus radiata, Plant J., 2011, vol. 67, p. 119. https://doi.org/10.1111/j.1365-313X.2011.04580.x

    Article  CAS  PubMed  Google Scholar 

  22. Stewart, J.J., Akiyama, T., Chapple, C., Ralph, J., and Mansfield, S.D., The effects on lignin structure of overexpression of ferulate 5-hydroxylase in hybrid poplar, Plant Physiol., 2009, vol. 150, p. 621. https://doi.org/10.1104/pp.109.137059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Karlen, S.D., Zhang, C., Peck, M.L., Smith, R.A, Padmakshan, D., Helmich, K.E., Free, H.C.A., Lee, S., Smith, B.G., Lu, F., Sedbrook, J.C., Sibout, R., Grabber, J.H., Runge, T.M., Mysore, K.S., et al., Monolignol ferulate conjugates are naturally incorporated into plant lignins, Sci. Adv., 2016, vol. 2, p. e1600393. https://doi.org/10.1126/sciadv.1600393

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. del Rıo, J.C., Marques, G., Rencoret, J., Martınez, A.T., and Gutierrez, A., Occurrence of naturally acetylated lignin units, J. Agric. Food Chem., 2007, vol. 55, p. 5461. https://doi.org/10.1021/jf0705264

    Article  CAS  PubMed  Google Scholar 

  25. Karlen, S.D., Smith, R.A., Kim, H., Padmakshan, D., Bartuce, A., Mobley, J.K., Free, H.C.A., Smith, B.G., Harris, P.J., and Ralph, J., Highly decorated lignins in leaf tissues of the Canary Island date palm Phoenix canariensis, Plant Physiol., 2017, vol. 175, p. 1058. https://doi.org/10.1104/pp.17.01172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Kim, H., Li, Q., Karlen, S.D., Smith, R.A., Shi, R., Liu, J., Yang, C., Tunlaya-Anukit, S., Jack, P. Wang, J.P., Chang, H.-M., Sederoff, R.R., Ralph, J., and Chiang, V.L., Monolignol benzoates incorporate into the lignin of transgenic Populus trichocarpa depleted in C3H and C4H, ACS Sustainable Chem. Eng., 2020, vol. 8, p. 3644. https://doi.org/10.1021/acssuschemeng.9b06389

    Article  CAS  Google Scholar 

  27. van Acker, R., Déjardin, A., Desmet, S., Hoengenaert, L., Vanholme, R., Morreel, K., Laurans, F., Kim, H., Santoro, N., Foster, C., Goeminne, G., Légée, F., Lapierre, C., Pilate G., Ralph, J., et al., Different routes for conifer- and sinapaldehyde and higher saccharification upon deficiency in the dehydrogenase CAD, Plant Physiol., 2017, vol. 175, p. 1018. https://doi.org/10.1104/pp.17.00834

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Ralph, J., MacKay, J.J., Hatfield, R.D., O’Malley, D.M., Whetten, R.W., and Sederoff, R.R., Abnormal lignin in a loblolly pine mutant, Science, 1997, vol. 277, p. 235. https://doi.org/10.1126/science.277.5323.235

    Article  CAS  PubMed  Google Scholar 

  29. Gui, J., Luo, L., Zhong, Y., Sun, J., Umezawa, T., and Li, L., Phosphorylation of LTF1, an MYB transcription factor in Populus, acts as a sensory switch regulating lignin biosynthesis in wood cell, Mol. Plant, 2019, vol. 12, p. 1325. https://doi.org/10.1016/j.molp.2019.05.008

    Article  CAS  PubMed  Google Scholar 

  30. Jervis, J., Hildreth, S.B., Sheng, X., Beers, E.P., Brunner, A.M., and Helm, R.F., A metabolomic assessment of NAC154 transcription factor overexpression in field grown poplar stem wood, Phytochemistry, 2015, vol. 115, p. 112. https://doi.org/10.1016/j.phytochem.2015.02.013

    Article  CAS  PubMed  Google Scholar 

  31. Zhong, R., McCarthy, R.L., Lee, C., and Ye, Z.-H., Dissection of the transcriptional program regulating secondary wall biosynthesis during wood formation in poplar, Plant Physiol., 2011, vol. 157, p. 1452. https://doi.org/10.1104/pp.111.181354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Yang, Y., Yoo, C.G., Rottmann, W., Winkeler, K.A., Collins, C.M., Gunter, L.E., Jawdy, S.S., Yang, X., Pu, Y., Ragauskas, A.J., Tuskan, G.A., and Chen, J.G., PdWND3A, a wood-associated NAC domain-containing protein, affects lignin biosynthesis and composition in Populus, BMC Plant Biol., 2019, vol. 19: 486. https://doi.org/10.1186/s12870-019-2111-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lebedev, V.G., Subbotina, N.M., Maluchenko, O.P., Lebedeva, T.N., Krutovsky, K.V., and Shestibratov, K.A., Transferability and polymorphism of SSR markers located in flavonoid pathway genes in Fragaria and Rubus species, Genes, 2020, vol. 11, p. 11.https://doi.org/10.3390/genes11010011

    Article  CAS  Google Scholar 

  34. Soler, M., Plasencia, A., Lepikson-Neto, J., Camargo, E.L.O., Dupas, A., Ladouce, N., Pesquet, E., Mounet, F., Larbat, R., and Grima-Pettenati, J., The woody-preferential gene EgMYB88 regulates the biosynthesis of phenylpropanoid-derived compounds in wood, Front. Plant Sci., 2016, vol. 7: e1422. https://doi.org/10.3389/fpls.2016.01422

    Article  Google Scholar 

  35. Li, C., Wang, X., Lu, W., Liu, R., Tian, Q., Sun, Y., and Luo, K., A poplar R2R3-MYB transcription factor, PtrMYB152, is involved in regulation of lignin biosynthesis during secondary cell wall formation, Plant Cell, Tissue Organ Cult., 2014, vol. 119, p. 553. https://doi.org/10.1007/s11240-014-0555-8

    Article  CAS  Google Scholar 

  36. Legay, S., Sivadon, P., Blervacq, A.S., Pavy, N., Baghdady, A., Tremblay, L., Levasseur, C., Ladouce, N., Lapierre, C., and Séguin, A., EgMYB1, an R2R3 MYB transcription factor from eucalyptus negatively regulates secondary cell wall formation in Arabidopsis and poplar, New Phytol., 2010, vol. 188, p. 774. https://doi.org/10.1111/j.1469-8137.2010.03432.x

    Article  CAS  PubMed  Google Scholar 

  37. Yang, L., Zhao, X., Ran, L.Y., Li, C.F., Fan, D., and Luo, K.M., PtoMYB156 is involved in negative regulation of phenylpropanoid metabolism and secondary cell wall biosynthesis during wood formation in poplar, Sci. Rep., 2017, vol. 7, p. 41209. https://doi.org/10.1038/srep41209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Zhong, R. and Ye, Z.H., Complexity of the transcriptional network controlling secondary wall biosynthesis, Plant Sci., 2014, vol. 229, p. 193. https://doi.org/10.1016/j.plantsci.2014.09.009

    Article  CAS  PubMed  Google Scholar 

  39. Zhang, J., **e, M., Tuskan, G.A., Muchero, W., and Chen, J.-G., Recent advances in the transcriptional regulation of secondary cell wall biosynthesis in the woody plants, Front. Plant Sci., 2018, vol. 9, p. 1535. https://doi.org/10.3389/fpls.2018.01535

    Article  PubMed  PubMed Central  Google Scholar 

  40. **e, M., Muchero, W., Bryan, A.C., Yee, K., Guo, H.-B., Zhang, J., Tschaplinski, T.J., Singan, V.R., Lindquist, E., Payyavula, R.S., Barros-Rios, J., Dixon, R., Engle, N., Sykes, R.W., Davis, M., et al., A 5-enolpyruvylshikimate 3-phosphate synthase functions as a transcriptional repressor in Populus, Plant Cell, 2018, vol. 30, p. 1645. https://doi.org/10.1105/tpc.18.00168

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Chen, H., Wang, J.P., Liu, H.Z., Li, H.Y., Lin, Y.-C.J., Shi, R., Yang, C., Gao, J., Zhou, C., Li, Q., Sederoff, R.R., Li, W., and Chiang, V.L., Hierarchical transcription factor and chromatin binding network for wood formation in black cottonwood (Populus trichocarpa), Plant Cell, 2019, vol. 31, p. 602. https://doi.org/10.1105/tpc.18.00620

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Cesarino, I., Structural features and regulation of lignin deposited upon biotic and abiotic stresses, Curr. Opin. Biotechnol., 2019, vol. 56, p. 209. https://doi.org/10.1016/j.copbio.2018.12.012

    Article  CAS  PubMed  Google Scholar 

  43. Mast, S.W., Donaldson, L.A., Torr, K., Phillips, L., Flint, H., West, M., Strabala, T.J., and Wagner, A., Exploring the ultrastructural localization and biosyn-thesis of β(1,4)-galactan in Pinus radiata compression wood, Plant Physiol., 2009, vol. 150, p. 573. https://doi.org/10.1104/pp.108.134379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Gorshkova, T., Mokshina, N., Chernova, T., Ibragimova, N., Salnikov, V., Mikshina, P., Tryfona, T., Banasiak, A., Immerzeel, P., Dupree, P., and Mellerowicz, E.J., Aspen tension wood fibers contain β(1→4)-galactans and acidic arabinogalactans retained by cellulose microfibrils in gelatinous walls, Plant Physiol., 2015, vol. 169, p. 2048. https://doi.org/10.1104/pp.15.00690

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Mourasobczak, J., Souza, U., and Mazzafera, P., Drought stress and changes in the lignin content and composition in Eucalyptus, BMC Proc., 2011, vol. 5, p. 103. https://doi.org/10.1186/1753-6561-5-S7-P103

    Article  Google Scholar 

  46. Srivastava, S., Vishwakarma, R.K., Arafat, Y.A., Gupta, S.K., and Khan, B.M., Abiotic stress induces change in cinnamoyl CoA reductase (CCR) protein abundance and lignin deposition in develo** seedlings of Leucaena leucocephala, Physiol. Mol. Biol. Plants, 2015, vol. 21, p. 197. https://doi.org/10.1007/s12298-015-0289-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Xu, C., Fu, X., Liu, R., Guo, L., Ran, L., Li, C., Tian, Q., Jiao, B., Wang, B., and Luo, K., PtoMYB170 positively regulates lignin deposition during wood formation in poplar and confers drought tolerance in transgenic Arabidopsis, Tree Physiol., 2017, vol. 37, p. 1713. https://doi.org/10.1093/treephys/tpx093

    Article  CAS  PubMed  Google Scholar 

  48. Khaledian, Y., Maali-Amiri, R., and Talei, A., Phenylpropanoid and antioxidant changes in chickpea plants during cold stress, Russ. J. Plant Physiol., 2015, vol. 62, p. 772. https://doi.org/10.1134/S1021443715060102

    Article  CAS  Google Scholar 

  49. Seong, E.S., Jeon, M.R., Choi, J.H., Yoo, J.H., Lee, J.G., Na, J.K., Kim, N.Y., and Yu, C.Y., Overexpression of S-adenosylmethionine synthetase enhances tolerance to cold stress in tobacco, Russ. J. Plant Physiol., 2020, vol. 67, p. 242. https://doi.org/10.1134/S1021443720020144

    Article  CAS  Google Scholar 

  50. Gallego-Giraldo, L., Pose, S., Pattathil, S., Peralta, A.G., Hahn, M.G., Ayre, B.G., Sunuwar, J., Hernandez, J., Patel, M., and Shah, J., Elicitors and defense gene induction in plants with altered lignin compositions, New Phytol., 2018, vol. 219, p. 1235. https://doi.org/10.1111/nph.15258

    Article  CAS  PubMed  Google Scholar 

  51. Bjurhager, I., Olsson, A.-M., Zhang, B., Gerber, L., Kumar, M., Berglund, L.A., Burgert, I., Sundberg, B., and Salmen, L., Ultrastructure and mechanical properties of Populus wood with reduced lignin content caused by transgenic down-regulation of cinnamate 4‑hydroxylase, Biomacromolecules, 2010, vol. 11, p. 2359. https://doi.org/10.1021/bm100487e

    Article  CAS  PubMed  Google Scholar 

  52. Sykes, R.W., Gjersing, E.L., Foutz, K., Rottmann, W.H., Kuhn, S.A., Foster, C.E. Ziebell, A., Turner, G.B., Decker, S.R., Hinchee, M.A.W., and Davis, M.F., Down-regulation of p-coumaroyl quinate/shikimate 3′-hydroxylase (C3′H) and cinnamate 4-hydroxylase (C4H) genes in the lignin biosynthetic pathway of Eucalyptus urophylla × E. grandis leads to improved sugar release, Biotechnol. Biofuels., 2015, vol. 8, p. 128. https://doi.org/10.1186/s13068-015-0316-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Seppanen, S.K., Pasonen, H.L., Vauramo, S., Vahala, J., Toikka, M., Kilpelainen, I., Setala, H., Teeri, T.H., Timonen, S., and Pappinen, A., Decomposition of the leaf litter and mycorrhiza forming ability of silver birch with a genetically modified lignin biosynthesis pathway, Appl. Soil Ecol., 2007, p. 36, vol. 100. https://doi.org/10.1016/j.apsoil.2006.12.002

  54. Voelker, S.L., Lachenbruch, B., Meinzer, F.C., Jourdes, M., Ki, C., Patten, A.M., Davin, L.B., Lewis, N.G., Tuskan, G.A., Gunter, L., Decker, S.R., Selig, M.J., Sykes, R., Himmel, M.E., Kitin, P., et al., Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar, Plant Physiol., 2010, vol. 154, p. 874. https://doi.org/10.1104/pp.110.159269

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Wagner, A., Donaldson, L., Kim, H., Phillips, L., Flint, H., Steward, D., Torr, K., Koch, G., Schmitt, U., and Ralph, J., Suppression of 4-coumarate-CoA ligase in the coniferous gymnosperm Pinus radiata, Plant Physiol., 2009, vol. 149, p. 370. https://doi.org/10.1104/pp.108.125765

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Shestibratov, K., Lebedev, V., Podrezov, A., and Salmova, M., Transgenic aspen and birch trees for Russian plantation forests, BMC Proc., 2011, vol. 5, p. 124. https://doi.org/10.1186/1753-6561-5-S7-P124

    Article  Google Scholar 

  57. Kovalitskaya, Y., Dayanova, L., Azarova, A., and Shestibratov, K., RNA interference-mediated down-regulation of 4-coumarate: coenzyme A ligase in Populus tremula alters lignification and plant growth, Int. J. Environ. Sci. Educ., 2016, vol. 11, p. 12259.

    Google Scholar 

  58. Coleman, H.D., Park, J.-Y., Nair, R., Chapple, C., and Mansfield, S.D., RNAi-mediated suppression of p-coumaroyl-CoA 3-hydroxylase in hybrid poplar impacts lignin deposition and soluble secondary metabolism, Proc. Natl. Acad. Sci. U.S.A., 2008, vol. 105, p. 4501. https://doi.org/10.1073/pnas.0706537105

    Article  PubMed  PubMed Central  Google Scholar 

  59. Coleman, H.D., Samuels, A.L., Guy, R.D., and Mansfield, S.D., Perturbed lignification impacts tree growth in hybrid poplar—a function of sink strength, vascular integrity, and photosynthetic assimilation, Plant Physiol., 2008, vol. 148, p. 1229. https://doi.org/10.1104/pp.108.125500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Zhou, X., Ren, S., Lu, M., Zhao, S., Chen, Z., Zhao, R., and Lv, J., Preliminary study of cell wall structure and its mechanical properties of C3H and HCT RNAi transgenic poplar sapling, Sci. Rep., 2018, vol. 8: 10508. https://doi.org/10.1038/s41598-018-28675-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Wang, H., Xue, Y., Chen, Y., Li, R., and Wei, J., Lignin modification improves the biofuel production potential in transgenic Populus tomentosa, Ind. Crop Prod., 2012, vol. 37, p. 170. https://doi.org/10.1016/j.indcrop.2011.12.014

    Article  CAS  Google Scholar 

  62. Leple, J.-C., Dauwe, R., Morreel, K., Storme, V., Lapierre, C., Pollet, B., Naumann, A., Kang, K.-Y., Kim, H., Ruel, K., Lefebvre, A., Joseleau, J.-P., Grima-Pettenati, J., De Rycke, R., Andersson- Gunnera, S., et al., Down regulation of cinnamoyl-coenzyme a reductase in poplar: multiple-level phenoty** reveals effects on cell wall polymer metabolism and structure, Plant Cell, 2007, vol. 19, p. 3669. https://doi.org/10.1105/tpc.107.054148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Zhang, W.B., Wei, R., Chen, S., Jiang, J., Li, H.Y., Huang, H.J., Yang, G., Wang, S., Wei, H.R., and Liu, G.F., Functional characterization of CCR in birch (Betula platyphylla × Betula pendula) through overexpression and suppression analysis, Physiol. Plant., 2015, vol. 154, p. 283. https://doi.org/10.1111/ppl.12306

    Article  CAS  PubMed  Google Scholar 

  64. Jouanin, L., Goujon, T., de Nadaı, V., Martin, M.-T., Mila, I., Vallet, C., Pollet, B., Yoshinaga, A., Chabbert, B., Petit-Conil, M., and Lapierre, C., Lignification in transgenic poplars with extremely reduced caffeic acid O-methyltransferase activity, Plant Physiol., 2000, vol. 123, p. 1363. https://doi.org/10.1104/pp.123.4.1363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Lapierre, C., Pilate, G., Pollet, B., Mila, I., Leple, J.-C., Jouanin, L., Kim, H., and Ralph, J., Signatures of cinnamyl alcohol dehydrogenase deficiency in poplar lignins, Phytochemistry, 2004, vol. 65, p. 313. https://doi.org/10.1016/j.phytochem.2003.11.007

    Article  CAS  PubMed  Google Scholar 

  66. Fan, D., Li, C., Fan, C., Hu, J., Li, J., Yao, S., Lu, W., Yan, Y., and Luo, K., MicroRNA6443-mediated regulation of ferulate 5-hydroxylase gene alters lignin composition and enhances saccharification in Populus tomentosa, New Phytol., 2020, vol. 226, p. 410. https://doi.org/10.1111/nph.16379

    Article  CAS  PubMed  Google Scholar 

  67. Li, S., Zhang, Y., **n, X., Ding, C., Lv, F., Mo, W., **a, Y., Wang, S., Cai, J., Sun, L., Du, M., Dong, C., Gao, X., Dai, X., Zhang, J., and Sun, J., The osmotin-like protein gene PdOLP1 is involved in secondary cell wall biosynthesis during wood formation in poplar, Int. J. Mol. Sci., 2020, vol. 21, p. e3993. https://doi.org/10.3390/ijms21113993

    Article  CAS  PubMed  Google Scholar 

  68. Zhou, X., Jacobs, T.B., Xue, L.J., Harding, S.A., and Tsai, C.J., Exploiting SNPs for biallelic CRISPR mutations in the outcrossing woody perennial Populus reveals 4-coumarate:CoA ligase specificity and redundancy, New Phytol., 2015, vol. 208, p. 298. https://doi.org/10.1111/nph.13470

    Article  CAS  PubMed  Google Scholar 

  69. Tsai, C.-J., Xu, P., Xue, L.-J., Hu, H., Nyamdari, B., Naran, R., Zhou, X., Goeminne, G., Gao, R., Gjersing, E., Dahlen, J., Pattathil, S., Hahn, M.G., Davis, M.F., Ralph, J., et al., Compensatory guaiacyl lignin biosynthesis at the expense of syringyl lignin in 4CL1-knockout poplar, Plant Physiol., 2020, vol. 183, p. 123. https://doi.org/10.1104/pp.19.01550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Takata, N., Awano, T., Nakata, M.T., Sano, Y., Sakamoto, S., Mitsuda, N., and Taniguchi, T., Populus NST/SND orthologs are key regulators of secondary cell wall formation in wood fibers, phloem fibers and xylem ray parenchyma cells, Tree Physiol., 2019, vol. 39, p. 514. https://doi.org/10.1093/treephys/tpz004

    Article  CAS  PubMed  Google Scholar 

  71. Min, D., Li, Q., Jameel, H., Chiang, V., and Chang, H.M., The cellulase mediated saccharification on wood derived from transgenic low-lignin lines of black cottonwood (Populus trichocarpa), Appl. Biochem. Biotechnol., 2012, vol. 168, p. 947. https://doi.org/10.1007/s12010-012-9833-2

    Article  CAS  PubMed  Google Scholar 

  72. Studer, M.H., DeMartini, J.D., Davis, M.F., Sykes, R.W., Davison, B., Keller, M., Tuskan, G.A., and Wyman, C.E., Lignin content in natural Populus variants affects sugar release, Proc. Natl. Acad. Sci. U.S.A., 2011, vol. 108, p. 6300. https://doi.org/10.1073/pnas.1009252108

    Article  PubMed  PubMed Central  Google Scholar 

  73. Zhou, S., Runge, T., Karlen, S.D., Ralph, J., Gonzales-Vigil, E., and Mansfield, S.D., Chemical pul** advantages of Zip-lignin hybrid poplar, ChemSusChem, 2017, vol. 10, p. 3565. https://doi.org/10.1002/cssc.201701317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Özparpucu, M., Gierlinger, N., Cesarino, I., Burgert, I., Boerjan, W., and Reggeberg, M., Significant influence of lignin on axial elastic modulus of poplar wood at low microfibril angles under wet conditions, J. Exp. Bot., 2019, vol. 70, p. 4039. https://doi.org/10.1093/jxb/erz180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Voelker, S.L., Lachenbruch, B., Meinzer, F.C., Kitin, P., and Strauss, S.H., Transgenic poplars with reduced lignin show impaired xylem conductivity, growth efficiency and survival, Plant Cell Environ., 2011, vol. 34, p. 655. https://doi.org/10.1111/j.1365-3040.2010.02270.x

    Article  PubMed  Google Scholar 

  76. Marchin, R.M., Stout, A.T., Davis, A.A., and King, J.S., Transgenically altered lignin biosynthesis affects photosynthesis and water relations of field grown Populus trichocarpa, Biomass Bioenergy, 2017, vol. 98, p. 15. https://doi.org/10.1016/j.biombioe.2017.01.013

    Article  CAS  Google Scholar 

  77. Mahon, E.L., Shawn, D., and Mansfield, S.D., Tailor-made trees: engineering lignin for ease of processing and tomorrow’s bioeconomy, Curr. Opin. Biotechnol., 2019, vol. 56, p. 147. https://doi.org/10.1016/j.copbio.2018.10.014

    Article  CAS  PubMed  Google Scholar 

  78. Wilkerson, C. G., Mansfield, S. D., Lu, F., Withers, S., Park, J.-Y., Karlen, S.D., Gonzales-Vigil, E., Padmakshan, D., Unda, F., Rencoret, J., and Ralph, J., Monolignol ferulate transferase introduces chemically labile linkages into the lignin backbone, Science, 2014, vol. 344, p. 90. https://doi.org/10.1126/science.1250161

    Article  CAS  PubMed  Google Scholar 

  79. Vanholme, R., Morreel, K., Darrah, C., Oyarce, P., Grabber, J.H., Ralph, J., and Boerjan, W., Metabolic engineering of novel lignin in biomass crops, New Phytol., 2012, vol. 196, p. 978. https://doi.org/10.1111/j.1469-8137.2012.04337.x

    Article  CAS  PubMed  Google Scholar 

  80. Cai, Y., Zhang, K., Kim, H., Hou, G., Zhang, X., Yang, H., Feng, H., Miller, L., Ralph, J., and Liu, C.-J., Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase, Nat. Commun., 2016, vol. 7, p. 11989. https://doi.org/10.1038/ncomms11989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  81. Vanholme, B., Cesarino, I., Goeminne, G., Kim, H., Marroni, F., van Acker, R., Vanholme, R., Morreel, K., Ivens, B., Pinosio, S., Morgante, M., Ralph, J., Bastien, C., and Boerjan, W., Breeding with rare defective alleles (BRDA): a natural Populus nigra HCT mutant with modified lignin as a case study, New Phytol., 2013, vol. 198, p. 765. https://doi.org/10.1111/nph.12179

    Article  CAS  PubMed  Google Scholar 

  82. Yamamoto, M., Tomiyama, H., Koyama, A., Okuizumi, H., Liu, S., Vanholme, R., Goeminne, G., Hirai, Y., Shi, H., Takata, N., Ikeda, T., Uesugi, M., Kim, H., Sakamoto, S., Mitsuda, N., et al., A century-old mystery unveiled: Sekizaisou is a natural lignin mutant, Plant Physiol., 2020, vol. 182, p. 1821. https://doi.org/10.1104/pp.19.01467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Elissetche, J.P., Valenzuela, S., García, R., Norambuena, M., Iturra, C., Rodríguez, J., Mendonça, R.T., and Balocchi, C., Transcript abundance of enzymes involved in lignin biosynthesis of Eucalyptus globulus genotypes with contrasting levels of pulp yield and wood density, Tree Genet. Genome, 2011, vol. 7, p. 697. https://doi.org/10.1007/s11295-011-0367-5

    Article  Google Scholar 

  84. Tuskan, G.A., Muchero, W., Tschaplinski, T.J., and Ragauskas, A.J., Population-level approaches reveal novel aspects of lignin biosynthesis, content, composition and structure, Curr. Opin. Biotechnol., 2019, vol. 56, p. 250. https://doi.org/10.1016/j.copbio.2019.02.017

    Article  CAS  PubMed  Google Scholar 

  85. Lebedev, V.G., Muratova, S.A., and Shestibratov, K.A., Field experiments and commercialization of biotechnological forms of forest wood plants, Lesovedenie, 2015, no. 5, p. 388.

  86. Danielsen, L., Lohaus, G., Sirrenberg, A., Karlovsky, P., Bastien, C., Pilate, G., and Polle, A., Ectomycorrhizal colonization and diversity in relation to tree biomass and nutrition in a plantation of transgenic poplars with modified lignin biosynthesis, PLoS One, 2013, vol. 8, p. e59207. https://doi.org/10.1371/journal.pone.0059207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Pilate, G., Guiney, E., Holt, K., Petit-Conil, M., Lapierre, C., Leple, J. C., Pollet, B., Mila, I., Webster, E.A., Marstorp, H.G., Hopkins, D.W., Jouanin, L., Boerjan, W., Schuch, W., Cornu, D., and Halpin, C., Field and pul** performances of transgenic trees with altered lignification, Nat. Biotechnol., 2002, vol. 20, p. 607. https://doi.org/10.1038/nbt0602-607

    Article  CAS  PubMed  Google Scholar 

  88. Novaes, E., Kirst, M., Chiang, V., Winter-Sederoff, H., and Sederoff, R., Lignin and biomass: a negative correlation for wood formation and lignin content in trees, Plant Physiol., 2010, vol. 154, p. 555. https://doi.org/10.1104/pp.110.161281

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Coleman, H.D., Canovas, F.M., Man, H., Kirby, E.G., and Mansfield, S.D., Enhanced expression of glutamine synthetase (GS1a) confers altered fibre and wood chemistry in field grown hybrid poplar (Populus tremula × alba) (717-1B4), Plant Biotechnol. J., 2012, vol. 10, p. 883. https://doi.org/10.1111/j.1467-7652.2012.00714.x

    Article  CAS  PubMed  Google Scholar 

  90. Lebedev, V.G., Faskhiev, V.N., Belyi, V.A., and Shestibratov, K.A., Analysis of the composition of lignins in transgenic aspen plants with the glutamine synthetase GS gene by two-dimensional NMR, Materialy IX Mezhdunarodnogo simpoziuma “Fanol’nye soedineniya: fundamental’nye i prikladnye aspekty” (Proc. IX Int. Symp. “Phenolic Compounds: Fundamental and Applied Aspects”), Moscow, 2015, p. 342.

  91. Komarov, A.S., Chertov, O.G., Bykhovets, S.S., Priputina, I.V., Shanin, V.N., Vidyagina, E.O., Lebedev, V.G., and Shestibratov, K.A., Impact of aspen plantations with a short cutting rotation on the biological cycle of carbon and nitrogen in the boreal forests: a model experiment, Matem. Biol. Bioinf., 2015, vol. 10, p. 398. https://doi.org/10.17537/2015.10.398

    Article  Google Scholar 

  92. Lebedev, V.G., Larionova, A.A., Bykhovets, S.S., Shanin, V.N., Komarov, A.S., and Shestibratov, K.A., Modeling biogeochemical nitrogen and carbon cycles on forest plantations with transgenic trees, Materialy Vserossiiskoi konferentsii s mezhdunarodnym uchastiem “Fundamental’nye i prikladnye problemy sovremennoi eksperimental’noi biologii rastenii” (Proc. All-Russ. Conf. with Int. Participation “Fundamental and Applied Problems of Mdoern Experimental Plant Biology”), Moscow, 2015, p. 415.

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This work was supported by the Russian Foundation for Basic Research, project no. 19-116-50103.

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  1. Branch of Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Pushchino, Russia

    V. G. Lebedev & K. A. Shestibratov

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Translated by A. Bulychev

Abbreviations: 4CL—4-coumarate CoA-ligase; C3′H—p-coumaroyl shikimate 3-hydroxylase; C4H—cinnamate 4-hydroxylase; CAD—cinnamyl-alcohol dehydrogenase; CCoAOMT—caffeoyl-CoA-O-methyltransferase; CCR—cinnamoyl CoA-reductase; COMT—caffeic acid O-methyltransferase; CSE—caffeoyl shikimate esterase; F5H—ferulate 5-hydroxylase; HCT—shikimate hydroxycinnamoyl transferase; PAL—phenylalanine ammonia lyase; RNAi—RNA interference TF—transcription factor.

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Lebedev, V.G., Shestibratov, K.A. Genetic Engineering of Lignin Biosynthesis in Trees: Compromise between Wood Properties and Plant Viability. Russ J Plant Physiol 68, 596–612 (2021). https://doi.org/10.1134/S1021443721030109

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