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Tree Genetics & Genomes

, 12:22 | Cite as

A cell wall-bound anionic peroxidase, PtrPO21, is involved in lignin polymerization in Populus trichocarpa

  • Chien-Yuan Lin
  • Quanzi Li
  • Sermsawat Tunlaya-Anukit
  • Rui Shi
  • Ying-Hsuan Sun
  • Jack P. Wang
  • Jie Liu
  • Philip Loziuk
  • Charles W. Edmunds
  • Zachary D. Miller
  • Ilona Peszlen
  • David C. Muddiman
  • Ronald R. SederoffEmail author
  • Vincent L. ChiangEmail author
Original Article
Part of the following topical collections:
  1. Genome Biology

Abstract

Class III peroxidases are members of a large plant-specific sequence-heterogeneous protein family. Several sequence-conserved homologs have been associated with lignin polymerization in Arabidopsis thaliana, Oryza sativa, Nicotiana tabacum, Zinnia elegans, Picea abies, and Pinus sylvestris. In Populus trichocarpa, a model species for studies of wood formation, the peroxidases involved in lignin biosynthesis have not yet been identified. To do this, we retrieved sequences of all PtrPOs from Peroxibase and conducted RNA-seq to identify candidates. Transcripts from 42 PtrPOs were detected in stem differentiating xylem (SDX) and four of them are the most xylem-abundant (PtrPO12, PtrPO21, PtrPO42, and PtrPO64). PtrPO21 shows xylem-specific expression similar to that of genes encoding the monolignol biosynthetic enzymes. Using protein cleavage-isotope dilution mass spectrometry, PtrPO21 is detected only in the cell wall fraction and not in the soluble fraction. Downregulated transgenics of PtrPO21 have a lignin reduction of ~20 % with subunit composition (S/G ratio) similar to wild type. The transgenics show a growth reduction and reddish color of stem wood. The modulus of elasticity (MOE) of the stems of the downregulated PtrPO21-line 8 can be reduced to ~60 % of wild type. Differentially expressed gene (DEG) analysis of PtrPO21 downregulated transgenics identified a significant overexpression of PtPrx35, suggesting a compensatory effect within the peroxidase family. No significant changes in the expression of the 49 P. trichocarpa laccases (PtrLACs) were observed.

Keywords

Lignin polymerization Populus trichocarpa Lignin peroxidase LC-MS/MS Lignin systems biology 

Notes

Acknowledgments

The National Science Foundation (USA), Plant Genome Research Program (Grant DBI-0922391) to V.L.C., the NC State University Jordan Family Endowment, NIH/NCSU Molecular Biotechnology Training Program (Grant 5T32GM00-8776-08), and the NC State University Forest Biotechnology Industrial Research Consortium supported this work.

Author contributions

C.Y.L. generated the PtrPO transgenic plants. Q.L. prepared the RNAi constructs and RNAi libraries. R.S. and Y.H.S. selected the peroxidase candidate. C.Y.L. and S.T.-A. performed the transcriptome analysis. C.Y.L. and J.L. performed the lignin and cell wall composition analysis. P.L. and D.C.M. performed the PC-IDMS protein quantification. C.Y.L., C.W.E. and Z.D.M. analyzed the modulus of elasticity of the wood samples. C.Y.L., J.P.W., I.P., R.R.S. and V.L.C. wrote the manuscript.

Compliance with ethical standards

Conflict of interest

We do not have any conflict of interest to report.

Data archiving statement

The sequence of class III peroxidases for Arabidopsis thaliana (AtPrx) and Populus trichocarpa (PtrPO) reported here are achieved and publicly available at the PeroxiBase database (http://peroxibase.toulouse.inra.fr/). The genome information of P. trichocarpa is available in Phytozome (http://www.phytozome.org). The accession numbers for plant peroxidases in National Center for Biotechnology Information (NCBI; https://www.ncbi.nlm.nih.gov/) are available as follows: TPX1 (L13654), FBP1 (AF149277), ZPO-C (AB023959), ZePrx (AJ880392), TP60 (AF149251), ATP-A2 (X99952), prxA3a (Q43049), PXP3-4 (X97350), and CPWPO-C (AB210901). The accession numbers for PtrPOs are provided in Supplementary Material as Table S2.

Supplementary material

11295_2016_978_MOESM1_ESM.docx (1.1 mb)
ESM 1 (DOCX 1127 kb)

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Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  • Chien-Yuan Lin
    • 1
    • 2
  • Quanzi Li
    • 3
  • Sermsawat Tunlaya-Anukit
    • 4
  • Rui Shi
    • 1
  • Ying-Hsuan Sun
    • 5
  • Jack P. Wang
    • 1
    • 6
  • Jie Liu
    • 1
  • Philip Loziuk
    • 7
  • Charles W. Edmunds
    • 8
  • Zachary D. Miller
    • 8
  • Ilona Peszlen
    • 8
  • David C. Muddiman
    • 7
  • Ronald R. Sederoff
    • 1
    Email author
  • Vincent L. Chiang
    • 1
    • 6
    Email author
  1. 1.Forest Biotechnology Group, Department of Forestry and Environmental ResourcesNorth Carolina State UniversityRaleighUSA
  2. 2.Biosciences CenterNational Renewable Energy LaboratoryGoldenUSA
  3. 3.State Key Laboratory of Tree Genetics and BreedingChinese Academy of ForestryBeijingChina
  4. 4.SCG Packaging PLCBan PongThailand
  5. 5.Department of ForestryNational Chung-Hsing UniversityTaichungTaiwan
  6. 6.State Key Laboratory of Tree Genetics and BreedingNortheast Forestry UniversityHarbinChina
  7. 7.W.M. Keck FTMS Laboratory, Department of ChemistryNorth Carolina State UniversityRaleighUSA
  8. 8.Department of Forest BiomaterialsNorth Carolina State UniversityRaleighUSA

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