Abstract
Class III peroxidases are key enzymes involved in the last step of lignin deposition, the oxidation of monolignols prior to polymerization. These enzymes belong to large multigene families with functionally redundant members, but not all of them play a role in the lignification process. Here, we characterized the class III peroxidase gene family in the model C4 grass Setaria viridis and applied a pipeline based on expression analyses to identify family members potentially involved in lignin polymerization. A total of 154 genes encoding class III peroxidases (SvPRX1 to SvPRX154) were found in the S. viridis genome, and 70% of these genes were involved in tandem duplication events. Five SvPRX genes (SvPRX49, SvPRX58, SvPRX119, SvPRX122, and SvPRX149) were identified as potential candidates to play a role in lignification based on (1) similar expression pattern to that of secondary cell wall (SCW)-related genes in a public transcriptomic database, (2) similar expression pattern to that observed for lignin biosynthetic genes in the S. viridis elongating internode, and (3) high expression in S. viridis tissues considered key-lignification sites. The promoter region of all five genes contained SCW-related cis elements, suggesting that their expression is controlled by the same regulatory network that controls lignin deposition and further supporting a role for these genes in lignin polymerization. Comparative analysis of the primary structure of the selected SvPRXs indicated that only SvPRX58 exhibits all structural motifs characteristic of syringyl (S) peroxidases, suggesting that this peroxidase can oxidize sinapyl alcohol. Finally, in situ hybridization experiments indicated that both SvPRX49 and SvPRX58 are expressed in cell types undergoing active lignification in S. viridis internodes. The identification of peroxidase genes potentially involved in lignin polymerization in S. viridis might help developing lignin bioengineering strategies for the bioeconomy.
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References
Adler E (1977) Lignin chemistry—past, present and future. Wood Sci Technol 11:169–218. https://doi.org/10.1007/BF00365615
Almagro L, Gómez Ros LV, Belchi-Navarro S et al (2009) Class III peroxidases in plant defence reactions. J Exp Bot 60:377–390. https://doi.org/10.1093/jxb/ern277
Barros J, Serk H, Granlund I, Pesquet E (2015) The cell biology of lignification in higher plants. Ann Bot 115:1053–1074. https://doi.org/10.1093/aob/mcv046
Barros J, Escamilla-Trevino L, Song L et al (2019) 4-Coumarate 3-hydroxylase in the lignin biosynthesis pathway is a cytosolic ascorbate peroxidase. Nat Commun 10:1994. https://doi.org/10.1038/s41467-019-10082-7
Berthet S, Demont-Caulet N, Pollet B et al (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23:1124–1137. https://doi.org/10.1105/tpc.110.082792
Blaschek L, Pesquet E (2021) Phenoloxidases in plants—how structural diversity enables functional specificity. Front Plant Sci. https://doi.org/10.3389/fpls.2021.754601
Blaschek L, Murozuka E, Serk H et al (2022) Different combinations of laccase paralogs nonredundantly control the amount and composition of lignin in specific cell types and cell wall layers in Arabidopsis. Plant Cell koac344 35(2):889–909. https://doi.org/10.1093/plcell/koac344
Blee KA, Choi JW, O’Connell AP et al (2003) A lignin-specific peroxidase in tobacco whose antisense suppression leads to vascular tissue modification. Phytochemistry 64:163–176. https://doi.org/10.1016/S0031-9422(03)00212-7
Cannon SB, Mitra A, Baumgarten A et al (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol. https://doi.org/10.1186/1471-2229-4-10
Cesarino I (2019) Structural features and regulation of lignin deposited upon biotic and abiotic stresses. Curr Opin Biotechnol 56:209–214. https://doi.org/10.1016/j.copbio.2018.12.012
Cesarino I, Araújo P, Sampaio Mayer JL et al (2012) Enzymatic activity and proteomic profile of class III peroxidases during sugarcane stem development. Plant Physiol Biochem 55:66–76. https://doi.org/10.1016/j.plaphy.2012.03.014
Cesarino I, Araujo P, Paes Leme AF et al (2013a) Suspension cell culture as a tool for the characterization of class III peroxidases in sugarcane. Plant Physiol Biochem 62:1–10. https://doi.org/10.1016/j.plaphy.2012.10.015
Cesarino I, Araujo P, Sampaio Mayer JL et al (2013b) Expression of SofLAC, a new laccase in sugarcane, restores lignin content but not S: G ratio of Arabidopsis lac17 mutant. J Exp Bot 64:1769–1781. https://doi.org/10.1093/jxb/ert045
Cesarino I, Simões MS, dos Brito M, S, et al (2016) Building the wall: recent advances in understanding lignin metabolism in grasses. Acta Physiol Plant 38:269. https://doi.org/10.1007/s11738-016-2293-5
Cesarino I, Dello Ioio R, Kirschner GK et al (2020) Plant science’s next top models. Ann Bot 126:1–23. https://doi.org/10.1093/aob/mcaa063
Choi HW, Kim YJ, Lee SC et al (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiol 145:890–904. https://doi.org/10.1104/pp.107.103325
Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408. https://doi.org/10.1093/jxb/ern318
Cosio C, Vuillemin L, De Meyer M et al (2009) An anionic class III peroxidase from zucchini may regulate hypocotyl elongation through its auxin oxidase activity. Planta 229:823–836. https://doi.org/10.1007/s00425-008-0876-0
Czégény G, Rácz A (2023) Phenolic peroxidases: Dull generalists or purposeful specialists in stress responses? J Plant Physiol 280:153884. https://doi.org/10.1016/j.jplph.2022.153884
Daudi A, Cheng Z, O’Brien JA et al (2012) The Apoplastic oxidative burst peroxidase in arabidopsis is a major component of pattern-triggered immunity. Plant Cell 24:275–287. https://doi.org/10.1105/tpc.111.093039
de Lima LGA, Ferreira SS, Simões MS et al (2023) Comprehensive expression analyses of the ABCG subfamily reveal SvABCG17 as a potential transporter of lignin monomers in the model C4 grass Setaria viridis. J Plant Physiol 280:153900. https://doi.org/10.1016/j.jplph.2022.153900
de Oliveira RR, Cesarino I, Mazzafera P, Dornelas MC (2014) Flower development in Coffea arabica L.: new insights into MADS-box genes. Plant Reprod 27:79–94. https://doi.org/10.1007/s00497-014-0242-2
Delli-Ponti R, Shivhare D, Mutwil M (2021) Using gene expression to study specialized metabolism—A Practical Guide. Front Plant Sci. https://doi.org/10.3389/fpls.2020.625035
Demarco D (2017) Histochemical Analysis of Plant Secretory Structures. Histochemistry of Single Molecules. Humana Press, New York, pp 313–330
Fernández-Pérez F, Pomar F, Pedreño MA, Novo-Uzal E (2015a) The suppression of AtPrx52 affects fibers but not xylem lignification in Arabidopsis by altering the proportion of syringyl units. Physiol Plant 154:395–406. https://doi.org/10.1111/ppl.12310
Fernández-Pérez F, Vivar T, Pomar F et al (2015b) Peroxidase 4 is involved in syringyl lignin formation in Arabidopsis thaliana. J Plant Physiol 175:86–94. https://doi.org/10.1016/j.jplph.2014.11.006
Ferreira SS, Simões MS, Carvalho GG et al (2019) The lignin toolbox of the model grass Setaria viridis. Plant Mol Biol 101:235–255. https://doi.org/10.1007/s11103-019-00897-9
Ferreira SS, Goeminne G, Simões MS et al (2022) Transcriptional and metabolic changes associated with internode development and reduced cinnamyl alcohol dehydrogenase activity in sorghum. J Exp Bot 73:6307–6333. https://doi.org/10.1093/jxb/erac300
Francoz E, Ranocha P, Nguyen-Kim H et al (2015) Roles of cell wall peroxidases in plant development. Phytochemistry 112:15–21. https://doi.org/10.1016/j.phytochem.2014.07.020
Gabaldón C, López-Serrano M, Pedreño MA, Barceló AR (2005) Cloning and molecular characterization of the basic peroxidase isoenzyme from Zinnia elegans, an enzyme involved in lignin biosynTHESis. Plant Physiol 139:1138–1154. https://doi.org/10.1104/pp.105.069674
Gómez Ros LV, Gabaldón C, Pomar F et al (2007) Structural motifs of syringyl peroxidases predate not only the gymnosperm–angiosperm divergence but also the radiation of tracheophytes. New Phytol 173:63–78. https://doi.org/10.1111/j.1469-8137.2006.01898.x
Halpin C (2019) Lignin engineering to improve saccharification and digestibility in grasses. Curr Opin Biotechnol 56:223–229. https://doi.org/10.1016/j.copbio.2019.02.013
Hatfield R, Ralph J, Grabber JH (2008) A potential role for sinapyl p-coumarate as a radical transfer mechanism in grass lignin formation. Planta 228:919–928. https://doi.org/10.1007/s00425-008-0791-4
Hatfield RD, Rancour DM, Marita JM (2017) Grass cell walls: a story of cross-linking. Front Plant Sci 7:2056. https://doi.org/10.3389/fpls.2016.02056
Hellemans J, Mortier G, De Paepe A et al (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8:R19. https://doi.org/10.1186/gb-2007-8-2-r19
Hoffmann N, Benske A, Betz H et al (2020) Laccases and peroxidases co-localize in lignified secondary cell walls throughout stem development. Plant Physiol 184:806–822. https://doi.org/10.1104/pp.20.00473
Jacobowitz JR, Doyle WC, Weng J-K (2019) PRX9 and PRX40 are extensin peroxidases essential for maintaining tapetum and microspore cell wall integrity during arabidopsis anther development. Plant Cell 31:848–861. https://doi.org/10.1105/tpc.18.00907
Jamet E, Albenne C, Boudart G et al (2008) Recent advances in plant cell wall proteomics. Proteomics 8:893–908. https://doi.org/10.1002/pmic.200700938
Julca I, Tan QW, Mutwil M (2023) Toward kingdom-wide analyses of gene expression. Trends Plant Sci 28:235–249. https://doi.org/10.1016/j.tplants.2022.09.007
Kunieda T, Shimada T, Kondo M et al (2013) Spatiotemporal secretion of peroxidase36 Is required for seed coat mucilage extrusion in Arabidopsis. Plant Cell 25:1355–1367. https://doi.org/10.1105/tpc.113.110072
Lazzarotto F, Menguer PK, Del-Bem L-E et al (2021) Ascorbate peroxidase Neofunctionalization at the origin of APX-R and APX-L: evidence from basal archaeplastida. Antioxidants 10:597. https://doi.org/10.3390/antiox10040597
Lewis NG, Yamamoto E (1990) Lignin: occurrence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41(1):455–496
Li Y, Kajita S, Kawai S et al (2003) Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. J Plant Res 116:175–182. https://doi.org/10.1007/s10265-003-0087-5
Liszkay A, Kenk B, Schopfer P (2003) Evidence for the involvement of cell wall peroxidase in the generation of hydroxyl radicals mediating extension growth. Planta 217:658–667. https://doi.org/10.1007/s00425-003-1028-1
Liu C-J (2012) Deciphering the enigma of lignification: precursor transport, oxidation, and the topochemistry of lignin assembly. Mol Plant 5:304–317. https://doi.org/10.1093/mp/ssr121
Martin AP, Palmer WM, Brown C et al (2016) A developing Setaria viridis internode: an experimental system for the study of biomass generation in a C4 model species. Biotechnol Biofuels 9:45. https://doi.org/10.1186/s13068-016-0457-6
Martínez-Cortés T, Pomar F, Espiñeira JM et al (2012) Purification and kinetic characterization of two peroxidases of Selaginella martensii Spring. involved in lignification. Plant Physiol Biochem 52:130–139. https://doi.org/10.1016/j.plaphy.2011.12.008
Martins PK, Nakayama TJ, Ribeiro AP et al (2015) Setaria viridis floral-dip: a simple and rapid Agrobacterium-mediated transformation method. Biotechnol Rep 6:61–63. https://doi.org/10.1016/j.btre.2015.02.006
Martins PK, Mafra V, de Souza WR et al (2016) Selection of reliable reference genes for RT-qPCR analysis during developmental stages and abiotic stress in Setaria viridis. Sci Rep. https://doi.org/10.1038/srep28348
McCaig BC, Meagher RB, Dean JFD (2005) Gene structure and molecular analysis of the laccase-like multicopper oxidase (LMCO) gene family in Arabidopsis thaliana. Planta 221:619–636. https://doi.org/10.1007/s00425-004-1472-6
Mei W, Qin Y, Song W et al (2009) Cotton GhPOX1 encoding plant class III peroxidase may be responsible for the high level of reactive oxygen species production that is related to cotton fiber elongation. J Genet Genom 36:141–150. https://doi.org/10.1016/S1673-8527(08)60101-0
Mitchell RAC, Oszvald M, Pellny TK et al (2023) A high soluble-fibre allele in wheat encodes a defective cell wall peroxidase responsible for dimerization of ferulate moieties on arabinoxylan. bioRxiv. https://doi.org/10.1101/2023.03.08.531735
Mottiar Y, Vanholme R, Boerjan W et al (2016) Designer lignins: harnessing the plasticity of lignification. Curr Opin Biotechnol 37:190–200. https://doi.org/10.1016/j.copbio.2015.10.009
Moural TW, Lewis KM, Barnaba C et al (2017) Characterization of class III peroxidases from switchgrass1. Plant Physiol 173:417–433. https://doi.org/10.1104/pp.16.01426
Müller K, Linkies A, Vreeburg RAM et al (2009) In vivo cell wall loosening by hydroxyl radicals during cress seed germination and elongation growth. Plant Physiol 150:1855–1865. https://doi.org/10.1104/pp.109.139204
Mutwil M, Klie S, Tohge T et al (2011) PlaNet: combined sequence and expression comparisons across plant networks derived from seven species. Plant Cell 23:895–910. https://doi.org/10.1105/tpc.111.083667
Ning P, Yang G, Hu L et al (2021) Recent advances in the valorization of plant biomass. Biotechnol Biofuels 14:102. https://doi.org/10.1186/s13068-021-01949-3
Ohtani M, Demura T (2019) The quest for transcriptional hubs of lignin biosynthesis: beyond the NAC-MYB-gene regulatory network model. Curr Opin Biotechnol 56:82–87. https://doi.org/10.1016/j.copbio.2018.10.002
Østergaard L, Teilum K, Mirza O et al (2000) Arabidopsis ATP A2 peroxidase. expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Mol Biol 44:231–243. https://doi.org/10.1023/A:1006442618860
Paschoal D, Costa JL, da Silva EM et al (2022) Infection by Moniliophthora perniciosa reprograms tomato Micro-Tom physiology, establishes a sink, and increases secondary cell wall synthesis. J Exp Bot Erac. https://doi.org/10.1093/jxb/erac057
Passardi F, Longet D, Penel C, Dunand C (2004) The class III peroxidase multigenic family in rice and its evolution in land plants. Phytochemistry 65:1879–1893. https://doi.org/10.1016/j.phytochem.2004.06.023
Passardi F, Cosio C, Penel C, Dunand C (2005) Peroxidases have more functions than a Swiss army knife. Plant Cell Rep 24:255–265. https://doi.org/10.1007/s00299-005-0972-6
Raes J, Rohde A, Christensen JH et al (2003) Genome-wide characterization of the lignification toolbox in Arabidopsis. Plant Physiol 133:1051–1071. https://doi.org/10.1104/pp.103.026484
Ralph J (2010) Hydroxycinnamates in lignification. Phytochem Rev 9:65–83. https://doi.org/10.1007/s11101-009-9141-9
Ralph J, Lapierre C, Boerjan W (2019) Lignin structure and its engineering. Curr Opin Biotechnol 56:240–249. https://doi.org/10.1016/j.copbio.2019.02.019
Ren L-L, Liu Y-J, Liu H-J et al (2014) Subcellular relocalization and positive selection play key roles in the retention of duplicate genes of populus class III peroxidase family. Plant Cell 26:2404–2419. https://doi.org/10.1105/tpc.114.124750
Ring L, Yeh S-Y, Hücherig S et al (2013) Metabolic interaction between anthocyanin and lignin biosynthesis is associated with peroxidase FaPRX27 in strawberry fruit. Plant Physiol 163:43–60. https://doi.org/10.1104/pp.113.222778
Rojas-Murcia N, Hématy K, Lee Y et al (2020) High-order mutants reveal an essential requirement for peroxidases but not laccases in Casparian strip lignification. Proc Natl Acad Sci 117:29166–29177. https://doi.org/10.1073/pnas.2012728117
Ros Barceló A, Ros LVG, Carrasco AE (2007) Looking for syringyl peroxidases. Trends Plant Sci 12:486–491. https://doi.org/10.1016/j.tplants.2007.09.002
Ruprecht C, Mutwil M, Saxe F et al (2011) Large-scale co-expression approach to dissect secondary cell wall formation across plant species. Plant Physiol 2:23. https://doi.org/10.3389/fpls.2011.00023
Ruprecht C, Vaid N, Proost S et al (2017) Beyond genomics: studying evolution with gene coexpression networks. Trends Plant Sci 22:298–307. https://doi.org/10.1016/j.tplants.2016.12.011
Saha P, Blumwald E (2016) Spike-dip transformation of Setaria viridis. Plant J Cell Mol Biol 86:89–101. https://doi.org/10.1111/tpj.13148
Sasaki S, Nishida T, Tsutsumi Y, Kondo R (2004) Lignin dehydrogenative polymerization mechanism: a poplar cell wall peroxidase directly oxidizes polymer lignin and produces in vitro dehydrogenative polymer rich in beta-O-4 linkage. FEBS Lett 562:197–201. https://doi.org/10.1016/S0014-5793(04)00224-8
Sato Y, Demura T, Yamawaki K et al (2006) Isolation and characterization of a novel peroxidase gene ZPO-C whose expression and function are closely associated with lignification during tracheary element differentiation. Plant Cell Physiol 47:493–503. https://doi.org/10.1093/pcp/pcj016
Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209:1395–1402. https://doi.org/10.1111/nph.13738
Shigeto J, Itoh Y, Hirao S et al (2015) Simultaneously disrupting AtPrx2, AtPrx25 and AtPrx71 alters lignin content and structure in Arabidopsis stem. J Integr Plant Biol 57:349–356. https://doi.org/10.1111/jipb.12334
Simões MS, Ferreira SS, Grandis A et al (2020b) Differentiation of tracheary elements in sugarcane suspension cells involves changes in secondary wall deposition and extensive transcriptional reprogramming. Front Plant Sci 11:2093. https://doi.org/10.3389/fpls.2020.617020
Simões MS, Carvalho GG, Ferreira SS et al (2020a) Genome-wide characterization of the laccase gene family in Setaria viridis reveals members potentially involved in lignification. Planta 251:46
Sung BM, Carvalho GG, Wairich A, Cesarino I (2021) Searching for novel transcriptional regulators of lignin deposition within the PIRIN family in the model C4 grass Setaria viridis. Trop Plant Biol 14:93–105. https://doi.org/10.1007/s12042-021-09283-6
Tobimatsu Y, Schuetz M (2019) Lignin polymerization: how do plants manage the chemistry so well? Curr Opin Biotechnol 56:75–81. https://doi.org/10.1016/j.copbio.2018.10.001
Tognolli M, Penel C, Greppin H, Simon P (2002) Analysis and expression of the class III peroxidase large gene family in Arabidopsis thaliana. Gene 288:129–138. https://doi.org/10.1016/S0378-1119(02)00465-1
Umezawa T (2018) Lignin modification in planta for valorization. Phytochem Rev 17:1305–1327. https://doi.org/10.1007/s11101-017-9545-x
Vanholme R, Morreel K, Ralph J, Boerjan W (2008) Lignin engineering. Curr Opin Plant Biol 11:278–285. https://doi.org/10.1016/j.pbi.2008.03.005
Vanholme R, Storme V, Vanholme B et al (2012) A systems biology view of responses to lignin biosynthesis perturbations in Arabidopsis. Plant Cell 24:3506–3529. https://doi.org/10.1105/tpc.112.102574
Vanholme R, Cesarino I, Rataj K et al (2013) Caffeoyl Shikimate Esterase (CSE) is an enzyme in the lignin biosynthetic pathway in Arabidopsis. Science 341:1103–1106. https://doi.org/10.1126/science.1241602
Vanholme R, De Meester B, Ralph J, Boerjan W (2019) Lignin biosynthesis and its integration into metabolism. Curr Opin Biotechnol 56:230–239. https://doi.org/10.1016/j.copbio.2019.02.018
Vermaas JV, Petridis L, Qi X et al (2015) Mechanism of lignin inhibition of enzymatic biomass deconstruction. Biotechnol Biofuels 8:217. https://doi.org/10.1186/s13068-015-0379-8
Volpi e Silva N, Mazzafera P, Cesarino I (2019) Should I stay or should I go: are chlorogenic acids mobilized towards lignin biosynthesis? Phytochemistry 166:112063. https://doi.org/10.1016/j.phytochem.2019.112063
Wang Y, Wang X, Paterson AH (2012) Genome and gene duplications and gene expression divergence: a view from plants. Ann N Y Acad Sci 1256:1–14. https://doi.org/10.1111/j.1749-6632.2011.06384.x
Wang J, Feng J, Jia W et al (2015a) Lignin engineering through laccase modification: a promising field for energy plant improvement. Biotechnol Biofuels 8:145. https://doi.org/10.1186/s13068-015-0331-y
Wang Y, Bouchabke-Coussa O, Lebris P et al (2015b) LACCASE5 is required for lignification of the brachypodium distachyon culm. Plant Physiol 168:192–204. https://doi.org/10.1104/pp.114.255489
Wang Y, Wang Q, Zhao Y et al (2015c) Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene 566:95–108. https://doi.org/10.1016/j.gene.2015.04.041
Withers S, Lu F, Kim H et al (2012) Identification of grass-specific enzyme that acylates monolignols with p-coumarate. J Biol Chem 287:8347–8355. https://doi.org/10.1074/jbc.M111.284497
Yu KMJ, Oliver J, McKinley B et al (2022) Bioenergy sorghum stem growth regulation: intercalary meristem localization, development, and gene regulatory network analysis. Plant J 112:476–492. https://doi.org/10.1111/tpj.15960
Zhang Q, Cheetamun R, Dhugga KS et al (2014) Spatial gradients in cell wall composition and transcriptional profiles along elongating maize internodes. BMC Plant Biol 14:27. https://doi.org/10.1186/1471-2229-14-27
Zhang J, Liu Y, Li C et al (2022) PtomtAPX is an autonomous lignification peroxidase during the earliest stage of secondary wall formation in Populus tomentosa Carr. Nat Plants 8:828–839. https://doi.org/10.1038/s41477-022-01181-3
Zhao Q, Nakashima J, Chen F et al (2013) LACCASE is necessary and nonredundant with peroxidase for lignin polymerization during vascular development in Arabidopsis. Plant Cell 25:3976–3987. https://doi.org/10.1105/tpc.113.117770
Zhong R, Ye Z-H (2012) MYB46 and MYB83 Bind to the SMRE sites and directly activate a suite of transcription factors and secondary wall biosynthetic genes. Plant Cell Physiol 53:368–380. https://doi.org/10.1093/pcp/pcr185
Zhong R, Lee C, Ye Z-H (2010) Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol Plant 3:1087–1103. https://doi.org/10.1093/mp/ssq062
Zhou J, Lee C, Zhong R, Ye Z-H (2009) MYB58 and MYB63 are transcriptional activators of the lignin biosynthetic pathway during secondary cell wall formation in Arabidopsis. Plant Cell 21:248–266. https://doi.org/10.1105/tpc.108.063321
Zhu Y, Li L (2021) Multi-layered regulation of plant cell wall thickening. Plant Cell Physiol 62:1867–1873. https://doi.org/10.1093/pcp/pcab152
Zhu T, Xin F, Wei S et al (2019) Genome-wide identification, phylogeny and expression profiling of class III peroxidases gene family in Brachypodium distachyon. Gene 700:149–162. https://doi.org/10.1016/j.gene.2019.02.103
Zipor G, Duarte P, Carqueijeiro I et al (2015) In planta anthocyanin degradation by a vdacuolar class III peroxidase in Brunfelsia calycina flowers. New Phytol 205:653–665. https://doi.org/10.1111/nph.13038
Acknowledgements
This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) via research grant n° 2019/25587-0. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. IC is indebted to Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the research fellowship 302927/2018-2. MSS was funded by CAPES for a predoctoral fellowship. GGC was funded by CNPq-PIBIC for a scientific initiation fellowship. SSF was funded by FAPESP for a postdoctoral fellowship (Processo Fapesp n° 2016/06917-1).
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Fundação de Amparo à Pesquisa do Estado de São Paulo, 2019/25587-0,Igor Cesarino,2016/06917-1, Sávio Siqueira Ferreira,Conselho Nacional de Desenvolvimento Científico e Tecnológico, 302927/2018-2, Igor Cesarino
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MSS: conducted most of the experiments, analyzed data and complemented the writing. GGC and SSF: performed experiments and analyzed data. IC: conceived and designed the experiments and wrote the article. All authors read and approved the final manuscript.
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Simões, M.S., Carvalho, G.G., Ferreira, S.S. et al. Toward the identification of class III peroxidases potentially involved in lignification in the model C4 grass Setaria viridis. Theor. Exp. Plant Physiol. 35, 111–131 (2023). https://doi.org/10.1007/s40626-023-00273-5
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DOI: https://doi.org/10.1007/s40626-023-00273-5