Abstract
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.
Highlights
Xylem tracheary elements (TEs) represent key anatomical features acquired by plants during evolution to survive and colonize the harsh conditions of terrestrial habitats, allowing for both water conduction throughout the plant body and mechanical support (Kenrick and Crane, 1997)
Radiolabeled phenylpropanoids have been applied to plant tissues to study the chronology of lignin precursor incorporation into the secondary walls of TEs. 3H-labeled cinnamic acid was shown to be incorporated both in apparently living and in dead xylem vessel elements of wheat (Triticum aestivum) coleoptiles (PickettHeaps, 1968), and even though somewhat contradictory results were obtained in another study in sycamore vessel elements (Wooding, 1968), it seems that addition of lignin precursors to already lignified cells can further enhance accumulation of lignin even after death of the vessel elements
The relationship between TE lignification and cell death was analyzed experimentally in differentiating Z. elegans TE cell cultures that were treated at the beginning of the cell culture period with a pharmacological inhibitor of lignin monomer biosynthesis, piperonylic acid (PA)
Summary
Xylem tracheary elements (TEs) represent key anatomical features acquired by plants during evolution to survive and colonize the harsh conditions of terrestrial habitats, allowing for both water conduction throughout the plant body and mechanical support (Kenrick and Crane, 1997). Similar conclusions were drawn from studies performed in Zinnia elegans TE cell cultures in which reduction in TE lignification by pharmacological inhibitors could be compensated for by the addition of lignin monomers to TEs undergoing lignification (Sato et al, 1993; Hosokawa et al, 2001; Tokunaga et al, 2005) None of these studies provided experimental evidence on how lignification relates to cell death of TEs. It was very interesting that bulk deposition of lignin was recently shown to occur postmortem (i.e., after TE cell death) by live-cell imaging of differentiating Arabidopsis thaliana TEs, the interdependency, if any, of TE PCD and lignification was not experimentally tested (Pesquet et al, 2010; Pesquet and Lloyd, 2011). Our specific research question is whether lignification in TEs occurs independently of cell death and how these processes affect each other to enable the formation of a functional, lignified TE
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