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In BriefIN BRIEF
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Good Neighbor Hypothesis of Lignification Holds for Xylem Cells, but Not for Interfascicular Fibers

Kathleen L. Farquharson
Kathleen L. Farquharson
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Published October 2013. DOI: https://doi.org/10.1105/tpc.113.251010

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Lignin is a key adaptation that enables plants to live and thrive in terrestrial environments. In addition to allowing plants to grow to great heights, this complex phenolic compound reinforces the secondary walls of water-conducting cells and forms a protective barrier. Lignin precursors (i.e., monolignols) are synthesized in the cytoplasm through the phenylpropanoid pathway (Humphreys and Chapple, 2002); however, it is unclear how these compounds reach their final destination (Liu et al., 2011). Although lignification is largely considered to be a postmortem phenomenon (Hosokawa et al., 2001), it appears to begin prior to programmed cell death (Pickett-Heaps, 1968). The finding that Zinnia elegans cells undergo postmortem lignification in culture gave rise to the good neighbor hypothesis, which proposes that lignin precursors are synthesized in nonlignified cells and exported to the walls of adjacent lignifying cells (Hosokawa et al., 2001; Tokunaga et al., 2005; Pesquet et al., 2013).

In a new study, Smith et al. (pages 3988–3999) rigorously tested the good neighbor hypothesis of lignification in planta in the model plant Arabidopsis thaliana. They analyzed the timing of lignification relative to programmed cell death in Arabidopsis roots using a radiolabeled precursor of monolignols, tritiated Phe (3H-Phe). After a 2-h incubation in medium containing 3H-Phe and cycloheximide, which prevents 3H-Phe from being assimilated into newly translated proteins, Arabidopsis seedlings were high-pressure frozen, sectioned, and analyzed by microautoradiography. The immobilized radiolabeled metabolites localized to the spiral wall thickenings of protoxylem tracheary elements and were particularly abundant in living or recently dead tracheary elements. Closer inspection using transmission electron microscopy revealed high levels of radiolabel in the secondary cell walls of living cells and low levels in dead tracheary elements, which would have already undergone significant lignification prior to labeling. These observations show that lignification occurs both before and after cell death. Furthermore, the finding that radiolabel levels were low in the cytoplasm suggests that flux through the phenylpropanoid pathway is high.

To establish which cells contribute to lignification in planta, the authors silenced monolignol biosynthesis specifically in tracheary elements and fibers using artificial microRNA technology and examined the distribution of lignin in the roots and stems of the resulting transgenic plants. Whereas lignification still occurred in the tracheary elements and xylary fibers of the silenced plants, lignin in interfascicular fibers was markedly reduced (see figure). This shows that lignification of interfascicular fibers occurs in a cell-autonomous manner. Thus, whereas xylem cells have good neighbors that facilitate lignification even after cell death, interfascicular fibers have an autonomous lignification system. The authors propose that xylem parenchyma cells, which are in close contact with xylem cells but not with interfascicular fibers, are these good neighbors.

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Interfascicular fibers undergo cell-autonomous lignification. Interfascicular fibers in the stem of (left) a wild-type Arabidopsis plant and (right) an Arabidopsis plant silenced for monolignol biosynthesis specifically in cells that develop lignified secondary walls. Phloroglucinol-HCl staining (red) revealed that cell wall lignification was greatly reduced in interfascicular fibers of the silenced line. Arrows indicate secondary cell wall thickenings. Bars = 5 μm. (Adapted from Smith et al. [2013], Figures 6B and 6F.)

Footnotes

  • www.plantcell.org/cgi/doi/10.1105/tpc.113.251010

References

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    OpenUrlAbstract/FREE Full Text
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    1. Humphreys J.M.,
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    1. Pickett-Heaps J.D.
    (1968). Radiographic investigations using lignin precursors. Protoplasma 65: 181–205.
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    Neighboring parenchyma cells can contribute to Arabidopsis xylem lignification, while lignification of interfascicular fibers is cell autonomous. Plant Cell 25: 3988–3999.
  6. ↵
    1. Tokunaga N.,
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    (2005). Involvement of extracellular dilignols in lignification during tracheary element differentiation of isolated Zinnia mesophyll cells. Plant Cell Physiol. 46: 224–232.
    OpenUrlAbstract/FREE Full Text
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Good Neighbor Hypothesis of Lignification Holds for Xylem Cells, but Not for Interfascicular Fibers
Kathleen L. Farquharson
The Plant Cell Oct 2013, 25 (10) 3635; DOI: 10.1105/tpc.113.251010

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Good Neighbor Hypothesis of Lignification Holds for Xylem Cells, but Not for Interfascicular Fibers
Kathleen L. Farquharson
The Plant Cell Oct 2013, 25 (10) 3635; DOI: 10.1105/tpc.113.251010
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The Plant Cell Online: 25 (10)
The Plant Cell
Vol. 25, Issue 10
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