Non-Cell-Autonomous Postmortem Lignification of Tracheary Elements in Zinnia elegans

• Published in: The Plant cell Vol. 25; no. 4; pp. 1314 - 1328
• Main Authors: Pesquet, Edouard, Zhang, Bo, Gorzsás, András, Puhakainen, Tuula, Serk, Henrik, Escamez, Sacha, Barbier, Odile, Gerber, Lorenz, Courtois-Moreau, Charleen, Alatalo, Edward, Paulin, Lars, Kangasjärvi, Jaakko, Sundberg, Björn, Goffner, Deborah, Tuominen, Hannele
• Format: Journal Article
• Language: English
• Published: United States American Society of Plant Biologists 01.04.2013
• Subjects: Acetylcysteine - pharmacology; Alcohol Oxidoreductases - genetics; Alcohol Oxidoreductases - metabolism; Alcohols; Aldehyde Oxidoreductases - genetics; Aldehyde Oxidoreductases - metabolism; Apoptosis; Arabidopsis - genetics; Arabidopsis - metabolism; Asteraceae - cytology; Asteraceae - genetics; Asteraceae - metabolism; Benzoates - pharmacology; Biochemistry and Molecular Biology; Biokemi och molekylärbiologi; Cell Biology; Cell culture techniques; Cell Wall - metabolism; Cell walls; Cellbiologi; Cells, Cultured; Gas Chromatography-Mass Spectrometry; Gene Expression Regulation, Plant - drug effects; Lignification; Lignin; Lignin - metabolism; Monomers; Onium Compounds - pharmacology; Plant cells; Plant Stems - cytology; Plant Stems - genetics; Plant Stems - metabolism; Plants; Plants, Genetically Modified; Reverse Transcriptase Polymerase Chain Reaction; Spectroscopy, Fourier Transform Infrared; Thiosulfates - pharmacology; Tracheoesophageal fistula; Xylem; Xylem - cytology; Xylem - genetics; Xylem - metabolism
• ISSN: 1040-4651; 1532-298X; 1532-298X
• DOI: 10.1105/tpc.113.110593

Postmortem lignification of xylem tracheary elements (TEs) has been debated for decades. Here, we provide evidence in Zinnia elegans TE cell cultures, using pharmacological inhibitors and in intact Z. elegans plants using Fourier transform infrared microspectroscopy, that TE lignification occurs postmortem (i.e., after TE programmed cell death). In situ RT-PCR verified expression of the lignin monomer biosynthetic cinnamoyl CoA reductase and cinnamyl alcohol dehydrogenase in not only the lignifying TEs but also in the unlignified non-TE cells of Z. elegans TE cell cultures and in living, parenchymatic xylem cells that surround TEs in stems. These cells were also shown to have the capacity to synthesize and transport lignin monomers and reactive oxygen species to the cell walls of dead TEs. Differential gene expression analysis in Z. elegans TE cell cultures and concomitant functional analysis in Arabidopsis thaliana resulted in identification of several genes that were expressed in the non-TE cells and that affected lignin chemistry on the basis of pyrolysis—gas chromatography/mass spectrometry analysis. These data suggest that living, parenchymatic xylem cells contribute to TE lignification in a non-cell-autonomous manner, thus enabling the postmortem lignification of TEs.