A unique program for cell death in xylem fibers of Populus stem

Abstract

Summary Maturation of the xylem elements involves extensive deposition of secondary cell‐wall material and autolytic processes resulting in cell death. We describe here a unique type of cell‐death program in xylem fibers of hybrid aspen (Populus tremula x P. tremuloides) stems, including gradual degradative processes in both the nucleus and cytoplasm concurrently with the phase of active cell‐wall deposition. Nuclear DNA integrity, as determined by TUNEL (terminal deoxynucleotidyl transferase‐mediated dUTP nick end labeling) and Comet (single‐cell gel electrophoresis) assays, was compromised early during fiber maturation. In addition, degradation of the cytoplasmic contents, as detected by electron microscopy of samples fixed by high‐pressure freezing/freeze substitution (HPF‐FS), was gradual and resulted in complete loss of the cytoplasmic contents well before the loss of vacuolar integrity, which is considered to be the moment of death. This type of cell death differs significantly from that seen in xylem vessels. The loss of vacuolar integrity, which is thought to initiate cell degradative processes in the xylem vessels, is one of the last processes to occur before the final autolysis of the remaining cell contents in xylem fibers. High‐resolution microarray analysis in the vascular tissues of Populus stem, combined with in silico analysis of publicly available data repositories, suggests the involvement of several previously uncharacterized transcription factors, ethylene, sphingolipids and light signaling as well as autophagy in the control of fiber cell death.

Morphological classification of plant cell deaths

“…[18][19][20][21] Depending on the system, the cell wall can be largely degraded, as for example during aerenchyma formation, leaf perforations in the lace plant and petal senescence [22][23][24] or can remain intact, for example, during xylem differentiation in vascular plants or leaf remodelling in Monstera (Figure 1). [24][25][26] Examples of vacuolar cell death are found during embryo, organ and tissue morphogenesis and senescence, and include, in addition to those mentioned above, the formation of embryo-suspensor, pollen, ovary, ducts and laticifers. 19 Knockout of ATG genes was shown to accelerate Arabidopsis leaf senescence, 27,28 and ATG5 has recently been found to be required for vacuolar cell death of Arabidopsis tracheary elements.…”

AspWood: High-Spatial-Resolution Transcriptome Profiles Reveal Uncharacterized Modularity of Wood Formation in Populus tremula

“…Hand sections were taken from freshly collected stem material for analysis of cell viability using nitroblue tetrazolium (Courtois- Moreau et al, 2009). Longitudinal sections (15 mm thick) were cut using a cryo-microtome (Uggla et al, 1996) and stored at 280°C.…”

“…Formation of the secondary cell wall (SCW) and lignification occurs in all xylem cell types. Vessel elements and fibers both undergo programmed cell death, with death in vessel elements occurring earlier than in fibers (Courtois- Moreau et al, 2009), while ray cells remain alive for several years (Nakaba et al, 2012). Distinct markers defining substages of the differentiation processes are currently not available.…”

Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 Directly Regulates the Genes That Govern Programmed Cell Death and Secondary Wall Formation during Xylem Differentiation

“…The rigid secondary cell walls of xylem fiber cells and TEs provide mechanical support for the plant body. To lose their cellular contents and act as a conductive tube, TEs undergo a rapid and unique type of programmed cell death (PCD) process, which is different from cell death in xylem fibers, in the final step of their differentiation (Obara et al, 2001;Courtois-Moreau et al, 2009).…”