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Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis

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Abstract

Lignins result from the oxidative polymerization of three hydroxycinnamyl (p-coumaryl, coniferyl, and sinapyl) alcohols in a reaction mediated by peroxidases. The most important of these is the cationic peroxidase from Zinnia elegans (ZePrx), an enzyme considered to be responsible for the last step of lignification in this plant. Bibliographical evidence indicates that the arabidopsis peroxidase 72 (AtPrx72), which is homolog to ZePrx, could have an important role in lignification. For this reason, we performed a bioinformatic, histochemical, photosynthetic, and phenotypical and lignin composition analysis of an arabidopsis knock-out mutant of AtPrx72 with the aim of characterizing the effects that occurred due to the absence of expression of this peroxidase from the aspects of plant physiology such as vascular development, lignification, and photosynthesis. In silico analyses indicated a high homology between AtPrx72 and ZePrx, cell wall localization and probably optimal levels of translation of AtPrx72. The histochemical study revealed a low content in syringyl units and a decrease in the amount of lignin in the atprx72 mutant plants compared to WT. The atprx72 mutant plants grew more slowly than WT plants, with both smaller rosette and principal stem, and with fewer branches and siliques than the WT plants. Lastly, chlorophyll a fluorescence revealed a significant decrease in ΦPSII and q L in atprx72 mutant plants that could be related to changes in carbon partitioning and/or utilization of redox equivalents in arabidopsis metabolism. The results suggest an important role of AtPrx72 in lignin biosynthesis. In addition, knock-out plants were able to respond and adapt to an insufficiency of lignification.

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Abbreviations

AtPrx72:

Basic peroxidase 72 from Arabidopsis thaliana

Chl:

Chlorophyll

G:

Guaiacyl

ORF:

Open reading frame

S:

Syringyl

ZePrx:

Basic peroxidase isoenzyme from Zinnia elegans

References

  • Amthor JS (2003) Efficiency of lignin biosynthesis: a quantitative analysis. Ann Bot 91:673–695

    Article  PubMed  CAS  Google Scholar 

  • Anterola AM, Lewis NG (2002) Trends in lignin modification: a comprehensive analysis of the effects of genetic manipulations/mutations on lignification and vascular integrity. Phytochemistry 61:221–294

    Article  PubMed  CAS  Google Scholar 

  • Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576

    Article  PubMed  CAS  Google Scholar 

  • Berthet S, Demont- Caulet N, Pollet B, Bidzinski P, Cézard L, Le Bris P, Borrega N, Hervé J, Blondet E, Balzergue S, Lapierre C, Jouanin L (2011) Disruption of LACCASE4 and 17 results in tissue-specific alterations to lignification of Arabidopsis thaliana stems. Plant Cell 23:1124–1137

    Article  PubMed  CAS  Google Scholar 

  • Bilger W, Björkman O (1990) Role of the xanthophyll cycle in photoprotection elucidated by measurements of light-induced absorbance changes, fluorescence, and photosynthesis in Hedera canariensis. Photosynth Res 25:173–185

    Article  CAS  Google Scholar 

  • Boyes DC, Zayed AM, Ascenzi R, Ms Caskill AJ, Hoffman NE, Davis KR, Görlach J (2001) Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13:1499–1510

    PubMed  CAS  Google Scholar 

  • Cassab GI, Varner JE (1988) Cell-wall proteins. Annu Rev Plant Physiol 39:321–353

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • De Gara L (2004) Class III peroxidases and ascorbate metabolism in plants. Phytochem Rev 3:195–205

    Article  Google Scholar 

  • Demura T, Tashiro G, Horiguchi G, Kishimoto N, Kubo M, Matsuoka N, Minami A, Nagata- Hiwatashi M, Nakamura K, Okamura I, Sassa N, Suzuki S, Yazaki J, Kikuchi S, Fukuda H (2002) Visualization by comprehensive microarray analysis of gene expression programs during transdifferentiation of mesophyll cells into xylem cells. Proc Natl Acad Sci USA 99:15794–15799

    Article  PubMed  Google Scholar 

  • Durbeej B, Eriksson LA (2003) Formation of β-O-4 lignin models-a theoretical study. Holzforschung 57:466–478

    CAS  Google Scholar 

  • Edwards K, Johnstone C, Thompson C (1991) A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucleic Acids Res 19:1349

    Article  PubMed  CAS  Google Scholar 

  • Espiñeira JM, Novo-Uzal E, Gómez-Ros LV, Carrión JS, Merino F, Ros Barceló A, Pomar F (2011) Distribution of lignin monomers and the evolution of lignification among lower plants. Plant Biol 13:59–68

    Article  PubMed  Google Scholar 

  • Fengel D, Wegener G (2003) Wood, chemistry and ultrastructure and reactions. Kassel Verlag, Ramagen

    Google Scholar 

  • Gabaldón C, López-Serrano M, Pedreño M, Ros Barceló A (2005) Cloning and molecular characterization of the basic peroxidase isoenzyme from Zinnia elegans, an enzyme involved in lignin biosynthesis. Plant Physiol 139:1138–1154

    Article  PubMed  Google Scholar 

  • Gabaldón C, López-Serrano M, Pomar F, Merino F, Cuello J, Pedreño MA, Ros Barceló A (2006) Characterization of the last step of lignin biosynthesis in Zinnia elegans suspension cell cultures. FEBS Lett 580:4311–4316

    Article  PubMed  Google Scholar 

  • Gabaldón C, Gómez-Ros LV, Núñez- Flores MJ, Esteban Carrasco A, Ros Barceló A (2007) Post-translational modifications of the basic peroxidase isoenzyme from Zinnia elegans. Plant Mol Biol 65:43–61

    Article  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    Article  CAS  Google Scholar 

  • Gómez-Ros LV, Gabaldón C, Pomar F, Merino F, Pedreño MA, Ros Barceló A (2007) Structural motifs of syringyl peroxidases predate not only the gymnosperm–angiosperm divergence but also the radiation of tracheophytes. New Phytol 173:63–78

    Article  PubMed  Google Scholar 

  • Harrison SJ, Mott EK, Parsley K, Aspinall S, Gray JC, Cottage A (2006) A rapid and robust method of identifying transformed Arabidopsis thaliana seedlings following floral dip transformation. Plant Methods 2:19

    Article  PubMed  Google Scholar 

  • Henriksen A, Mirza O, Indiani C, Teilum K, Smulevich G, Welinder KG, Gajhede M (2001) Structure of soybean seed coat peroxidase: a plant peroxidase with unusual stability and haem-apoprotein interactions. Protein Sci 10:108–115

    Article  PubMed  CAS  Google Scholar 

  • Iiyama K, Wallis AFA (1988) An improved acetyl bromide procedure for determining lignin in woods and wood pulps. Wood Sci Technol 22:271–280

    Article  CAS  Google Scholar 

  • Irshad M, Canut H, Borderies G, Pont-Lezica R, Jamet E (2008) A new picture of cell wall protein dynamics in elongating cells of Arabidopsis thaliana: confirmed actors and newcomers. BMC Plant Biol 8:94

    Article  PubMed  Google Scholar 

  • Jaroszewski L, Li Z, Cai XH, Weber C, Godzik A (2011) FFAS server: novel features and applications. Nucleic Acids Res 39:38–44

    Article  Google Scholar 

  • Kozak M (1991) Structural features in eukaryotic mRNAs that modulate the initiation of translation. J Biol Chem 266:19867–19870

    PubMed  CAS  Google Scholar 

  • Kramer DM, Johnson G, Kiirats O, Edwards GF (2004) New fluorescence parameters for the determination of Q (A) redox state and excitation energy fluxes. Photosynth Res 79:209–218

    Article  PubMed  CAS  Google Scholar 

  • Krause GH, Jahns P (2004) Non-photochemical energy dissipation determined by chlorophyll fluorescence quenching: characterization and function. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration. Chlorophyll fluorescence: A signature of photosynthesis. Springer, Dordrecht, pp 463–495

    Chapter  Google Scholar 

  • Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T (2005) Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 19:1855–1860

    Article  PubMed  CAS  Google Scholar 

  • Lagrimini LM, Gingas V, Finger F, Rothstein S, Liu T (1997) Characterization of antisense transformed plants deficient in the tobacco anionic peroxidase. Plant Physiol 114:1187–1196

    PubMed  CAS  Google Scholar 

  • Lapierre CB, Pollet C, Rolando C (1995) New insights into the molecular architecture of hardwood lignins by chemical degradative methods. Res Chem Intermed 21:397–412

    Article  CAS  Google Scholar 

  • Lebedeva OV, Ezhova TA, Musin SM, Radyukina NL, Shestakov SV (2003) PXD gene controls synthesis of three anionic peroxidase isoforms in Arabidopsis thaliana. Biol Bull 30:124–132

    Article  CAS  Google Scholar 

  • Li Y, Kajita S, Kawai S, Katayama Y, Morohoshi N (2003a) Down-regulation of an anionic peroxidase in transgenic aspen and its effect on lignin characteristics. J Plant Res 116:175–182

    Article  PubMed  CAS  Google Scholar 

  • Li L, Zhou Y, Cheng X, Sun J, Marita JM, Ralph J, Chiang VL (2003b) Combinatorial modification of multiple lignin traits in trees through multigene cotransformation. Proc Natl Acad Sci USA 100:4939–4944

    Article  PubMed  CAS  Google Scholar 

  • Lu F, Ralph J (1996) Reactions of lignin model β-aryl ethers with acetyl bromide. Holzforschung 50:360–364

    Article  CAS  Google Scholar 

  • Marjamaa K, Kukkola E, Fagerstedt K (2009) The role of xylem class III peroxidases in lignification. J Exp Bot 60:367–376

    Article  PubMed  CAS  Google Scholar 

  • McCann MC, Defernez M, Urbanowicz BR, Tewari JC, Langewisch T, Olek A, Wells B, Wilson RH, Carpita NC (2007) Neural network analyses of infrared spectra for classifying cell wall architectures. Plant Physiol 143:1314–1326

    Article  PubMed  CAS  Google Scholar 

  • Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10:1–6

    Article  PubMed  CAS  Google Scholar 

  • Novo-Uzal E, Gómez-Ros LV, Pomar F, Bernal MA, Paradela A, Albar JP, Ros Barceló A (2009) The presence of sinapyl lignin in Ginkgo biloba cell cultures changes our views of the evolution of lignin biosynthesis. Physiol Plant 135:196–213

    Article  Google Scholar 

  • Østergaard L, Yanofsky MF (2004) Establishing gene function by mutagenesis in Arabidopsis thaliana. Plant J 39:682–696

    Article  PubMed  Google Scholar 

  • Østergaard L, Pedersen AG, Jespersen HM, Brunak S, Welinder KG (1998) Computational analyses and annotations of the Arabidopsis peroxidase gene family. FEBS Lett 433:98–102

    Article  PubMed  Google Scholar 

  • Østergaard L, Telium K, Mirza O, Mattson O, Petersen M, Welinder KG, Mundy J, Gajhede M, Henriksen A (2000) Arabidopsis ATP A2 peroxidase. Expression and high-resolution structure of a plant peroxidase with implications for lignification. Plant Mol Biol 44:231–243

    Article  PubMed  Google Scholar 

  • Passardi F, Dobias J, Valério L, Guimil S, Penel C, Dunand C (2007) Morphological and physiological traits of three major Arabidopsis thaliana accessions. J Plant Physiol 164:980–992

    Article  PubMed  CAS  Google Scholar 

  • Patzlaff A, Mclnnis S, Courtenay A, Suman C, Newman LJ, Smith C, Bevan MW, Mansfield S, Whetten RW, Sederoff RR, Campbell MM (2003) Characterisation of a pine MYB that regulates lignification. Plant J 36:743–754

    Article  PubMed  CAS  Google Scholar 

  • Pomar F, Merino F, Ros Barceló A (2002) O-4-Linked coniferyl and sinapyl aldehydes in lignifying cell walls are the main targets of the Wiesner (phloroglucinol-HCl) reaction. Protoplasma 220:17–28

    Article  PubMed  CAS  Google Scholar 

  • Quiroga M, Guerrero C, Botella MA, Ros Barceló A, Amaya I, Medina MI, Alonso FJ, de Forchetti SM, Tigier H, Valpuesta V (2000) A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiol 122:1119–1127

    Article  PubMed  CAS  Google Scholar 

  • Rana R, Langenfeld-Heyser R, Finkeldey R, Polle A (2010) FTIR spectroscopy, chemical, and histochemical characterisation of wood and lignin of five tropical timber wood species of the family of Dipterocarpaceae. Wood Sci Technol 44:225–242

    Article  CAS  Google Scholar 

  • Rogers LA, Dubos C, Surman C, Willment J, Cullis IF, Mansfield SD, Campbell MM (2005) Comparison of lignin deposition in three ectopic lignification mutants. New Phytol 168:123–140

    Article  PubMed  CAS  Google Scholar 

  • Ros Barceló A (1997) Lignification in plant cell walls. Int Rev Cytol 176:87–132

    Article  PubMed  Google Scholar 

  • Ros Barceló A, Gómez-Ros LV, Esteban Carrasco A (2007) Looking for syringyl peroxidases. Trends Plant Sci 12:486–491

    Article  Google Scholar 

  • Schreiber U (2004) Pulse- Amplitude- Modulation (PAM) fluorometry and saturation pulse method: An overview. In: Papageorgiou GC, Govindjee (eds) Advances in photosynthesis and respiration. Chlorophyll fluorescence: A signature of photosynthesis. Springer, Dordrecht, pp 279–319

    Chapter  Google Scholar 

  • Sibout R, Eudes A, Mouille G, Pollet B, Lapierre C, Jouanin L, Séguin A (2005) Cinnamyl alcohol dehydrogenase-C and -D are the primary genes involved in lignin biosynthesis in the floral stem of Arabidopsis. Plant Cell 17:2059–2076

    Article  PubMed  CAS  Google Scholar 

  • Smith C, Rodgers M, Zimmerlin A, Ferdinando D, Bolwell G (1994) Tissue and subcellular immunolocalization of enzymes of lignin synthesis in differentiating and wounded hypocotyl tissue of French bean (Phaseolus vulgaris L). Planta 192:155–164

    Article  CAS  Google Scholar 

  • Valério L, De Meyer M, Penel C, Dunand C (2004) Expression analysis of the Arabidopsis peroxidase multigenic family. Phytochemistry 65:1331–1342

    Article  PubMed  Google Scholar 

  • Voelker SL, Lachenbruch B, Meinzer FC, Jourdes M, Ki C, Patten AM, Davin LB, Lewis NG, Tuskan GA, Gunter L, Decker SR, Selig MJ, Sykes R, Himmel ME, Kitin P, Shevchenko O, Strauss SH (2010) Antisense down-regulation of 4CL expression alters lignification, tree growth, and saccharification potential of field-grown poplar. Plant Physiol 154:874–886

    Article  PubMed  CAS  Google Scholar 

  • Walling LL (2006) Recycling or regulation? The role of amino-terminal modifying enzymes. Curr Opin Plant Biol 9:227–233

    Article  PubMed  CAS  Google Scholar 

  • Welinder KG, Justesen AF, Kjaersgard IV, Jensen RB, Rasmussen SK, Jespersen HM, Duroux L (2002) Structural diversity and transcription of class III peroxidases from Arabidopsis thaliana. Eur J Biochem 269:6063–6081

    Article  PubMed  CAS  Google Scholar 

  • Zhong R, Ripperger A, Ye ZH (2000) Ectopic deposition of lignin in the pith of stems of two Arabidopsis mutants. Plant Physiol 123:59–70

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work has been funded with support from the Spanish MICINN and the European Commission FEDER (BFU2006-11577 and BFU2009-08151) and from the Fundación Séneca, Agencia de Ciencia y Tecnología de la Región de Murcia en el marco de II PCTRM 2007-10 (08610/PI/08). Joaquín Herrero and Francisco Fernández-Pérez hold a fellowship (FPU) from the MICINN and Esther Novo-Uzal holds a JdC grant from MICINN (Spain).

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Authors and Affiliations

  1. Department of Plant Biology, University of Alcalá, 28871, Alcalá de Henares (Madrid), Spain

    Joaquín Herrero, Tatiana Yebra, Alfredo Guéra & José Miguel Zapata

  2. Department of Plant Biology, University of Murcia, 30100, Murcia, Spain

    Francisco Fernández-Pérez, Esther Novo-Uzal, Mª Ángeles Pedreño & Juan Cuello

  3. Department of Animal Biology, Plant Biology and Ecology, University of La Coruña, 15071, La Coruña, Spain

    Federico Pomar

  4. Department of Plant Biology, Complutense University, 28040, Madrid, Spain

    Alberto Esteban-Carrasco

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  1. Joaquín Herrero
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  2. Francisco Fernández-Pérez
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  3. Tatiana Yebra
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  4. Esther Novo-Uzal
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  5. Federico Pomar
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  6. Mª Ángeles Pedreño
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  7. Juan Cuello
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  8. Alfredo Guéra
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  9. Alberto Esteban-Carrasco
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  10. José Miguel Zapata
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Correspondence to Joaquín Herrero.

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F. Fernandez-Perez and T. Yebra contributed equally to this work.

In memoriam of Prof. Alfonso Ros Barceló, to be able to continue with your work is an honor.

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Herrero, J., Fernández-Pérez, F., Yebra, T. et al. Bioinformatic and functional characterization of the basic peroxidase 72 from Arabidopsis thaliana involved in lignin biosynthesis. Planta 237, 1599–1612 (2013). https://doi.org/10.1007/s00425-013-1865-5

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