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PtomtAPX is an autonomous lignification peroxidase during the earliest stage of secondary wall formation in Populus tomentosa Carr

Abstract

At present, a cooperative process hypothesis is used to explain the supply of enzyme (class III peroxidases and/or laccases) and substrates during lignin polymerization. However, it remains elusive how xylem cells meet the needs of early lignin rapid polymerization during secondary cell wall formation. Here we provide evidence that a mitochondrial ascorbate peroxidase (PtomtAPX) is responsible for autonomous lignification during the earliest stage of secondary cell wall formation in Populus tomentosa. PtomtAPX was relocated to cell walls undergoing programmed cell death and catalysed lignin polymerization in vitro. Aberrant phenotypes were caused by altered PtomtAPX expression levels in P. tomentosa. These results reveal that PtomtAPX is crucial for catalysing lignin polymerization during the early stages of secondary cell wall formation and xylem development, and describe how xylem cells provide autonomous enzymes needed for lignin polymerization during rapid formation of the secondary cell wall by coupling with the programmed cell death process.

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Fig. 1: Subcellular distribution analysis of PtomtAPX in P. tomentosa stems.
Fig. 2: Relocation of PtomtAPX from mitochondria to the cell wall.
Fig. 3: GC–MS and NMR analysis of reaction products of PtomtAPX.
Fig. 4: Phenotypic analysis of WT and transgenic P. tomentosa.
Fig. 5: Ultrastructural morphology of the cell wall and Raman images of lignin distribution within transverse stem sections in anti-24, overexpression OX-3 and WT plants.
Fig. 6: Relocation of PtomtAPX in different stages of fibre (F) cell differentiation during PCD.

Data availability

The data that support the findings of this study are openly available in Science Data Bank at http://cstr.cn/31253.11.sciencedb.j00001.00446. Sequence data in this article can be found in the GenBank database under accession number PtomtAPX (MG921618.1) at https://www.ncbi.nlm.nih.gov/nuccore/MG921618.1/. Source data are provided with this paper.

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Acknowledgements

This work was supported by the Natural Science Foundation of China (31971618) and National Key Research and Development Program of China (2021YFD2200900).

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Contributions

H. Lu designed the experiments; J.Z., Y.L. and C.L. performed the experiments; X.L., X.G., C.Z., D.L. and B.Y. performed statistical analysis; H. Lu, J.Z., H. Li and I.H. wrote the manuscript.

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Correspondence to Hui Li or Hai Lu.

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Nature Plants thanks the anonymous reviewers for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Tables 1 and 2.

Reporting Summary

Supplementary Video 1

Relocation of PtomtAPX-GFP fusion protein in transgenic tobacco suspension cells during PCD.

Source data

Source Data Fig. 1

Unprocessed western blots and gels for Fig. 1.

Source Data Fig. 2

Unprocessed western blots and gels for Fig. 2.

Source Data Fig. 4

Statistical source data for Fig. 4.

Source Data Fig. 5

Statistical source data for Fig. 5.

Source Data Fig. 6

Statistical source data for Fig. 6.

Source Data Fig. 6

Unprocessed western blots and gels for Fig. 6.

Source Data Table 1

Statistical source data for Table 1.

Source Data Table 2

Statistical source data for Table 2.

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Zhang, J., Liu, Y., Li, C. et al. PtomtAPX is an autonomous lignification peroxidase during the earliest stage of secondary wall formation in Populus tomentosa Carr. Nat. Plants 8, 828–839 (2022). https://doi.org/10.1038/s41477-022-01181-3

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