Aerenchyma

Death and autolysis of cells can be induced in roots of many monocot and dicot species in response to a wide range of environmental factors: these include hypoxia (Justin and Armstrong, 1991; Drew, 1997), mechanical impedance (He et al., 1996a), transient starvation of inorganic nutrients (Drew et al., 1989) and desiccation (Drew, 1979; Shone and Flood, 1983). Death occurs in primary roots usually among the cortical cells in the zone where the cells have just completed their expansion, usually a few cm behind the root tip (Campbell and Drew, 1983). The function of aerenchyma is experimentally established only for hypoxia, where the oxygen status of roots growing in O2-impoverished surroundings is improved (Drew etal., 1985). However, circumstantial evidence suggests that aerenchyma aid in root penetration of dense soil layers thereby increasing drought tolerance (Drew et al., 2000). The case for interpreting lysigenous aerenchyma formation as an example of PCD is supported by the inducibility of aerenchyma by the hormone, ethylene; by the precise, predictable pattern of localized cell death within the root cortex; and by the detection of TUNEL positive nuclei early in the induction of cell death (Gunawardena et al., 2001).

Signs of nuclear degradation in cells during root cortical death (RCD) beginning from the outside and progressing towards the stele have been detected using acridine orange staining (Henry and Deacon, 1981). Loss of nuclear staining by acridine orange correlates with other criteria of cell death, including loss of esterase activity and with loss of ability to plasmolyze (Lascaris and Deacon, 1991). RCD apparently occurs without the intervention of external environmental factors, although deficiency of inorganic nutrients can accelerate RCD (Elliott et al., 1993). It is unclear whether aerenchyma formation and RCD are the same phenomenon; however, in one study the cell death patterns for the two phenomena did not overlap (Deacon et al., 1986).

PCD in the cortex of roots of maize is triggered by ethylene. With hypoxia or mechanical impedance, the activity of enzymes involved in the biosynthetic pathway is increased resulting in increased ethylene production in the roots (Drew et al., 1979; Atwell et al., 1988; He et al., 1996a). Such PCD can be initiated by application of low concentrations of ethy-lene under normoxic conditions, while inhibitors of ethylene biosynthesis or action block aerenchyma formation in hypoxic or ethylene-treated roots, respectively (Drew et al., 1981; Jackson et al., 1985). Evidence of a signal transduction pathway leading to PCD comes from studies using agonists or antagonists of potential intermediates (He et al., 1996b).

PCD was accelerated by activation of G-proteins, blocked by inhibition of protein kinases, and induced by inhibition of protein phosphatases (thereby keeping proteins in a phospho-rylated form). Reagents that increased the concentration of intracellular Ca2+ accelerated PCD, and conversely, reagents that lowered cytosolic Ca2+ inhibited death. Direct measurements of phospholipase C activity and inositol 1,4,5, trisphosphate (He, Morgan and Drew, unpublished) also indicate the participation of phosphoinositides in signaling PCD.

In rice, PCD leading to aerenchyma formation is constitutive rather than inducible, although it is possible that ethylene still has a role (Justin and Armstrong, 1991). Death in rice seminal roots begins in isolated cells in the mid cortex, and it is first detected by a more acid cytoplasmic pH (stained with neutral red) and an inability to exclude Evans blue (Kawai et al., 1998). The authors suggest that PCD is involved in the initiation of death, but they speculate that the subsequent spreading radially from cell to cell might be necrosis (oncosis). The use of the TUNEL reaction to identify individual cells might resolve this question.

Aerenchyma formation has many features in common with PCD in TEs. Aerenchyma formation requires the dissolution of dead cells, suggesting that an array of hydrolytic enzymes would be involved. At the transmission electron microscopy (TEM) level, the initial sign of death is the collapse inwards of isolated cells in the mid cortex suggesting loss of tonoplast integrity (Campbell and Drew, 1983), as in TE differentiation. This would allow access of vacuolar enzymes to the cytoplasm and cytoplasmic acidosis. Cell dissolution is probably complete for individual cells within 24 h of the start of cell death. Cellulase activity increases in the apical zone before any microscopic signs of cell abnormality (He et al., 1994), and increased cellulase activity is always tightly coupled to cell death (He et al., 1996b). Furthermore, the requirement for an increase in cytosolic Ca2+ to initiate death in cortical cells of roots resembles that in TEs. Whether the common features signify a similar underlying mechanism remains to be determined.

Among the relatively few genes that are experimentally linked with PCD in plants, several are expressed in roots. Mutations in the root necrosis (Rn) gene in soybean cause a progressive browning of the root after germination, and death of cells beginning in the inner cortex (Kosslak et al., 1997). Maize root cortical cell delineating gene is expressed rapidly in response to mechanical impedance which induces PCD in cortical cells (Huang etal., 1998), and its expression is up regulated in genetic tumors in tobacco (Fujita et al., 1994). An animal cell death suppressor gene (see IIIA. Aleurone and Scutellum) homologue Dadl (defender against apoptotic cell death) is expressed in arabidopsis, rice and maize roots (Gallois et al., 1997; Tanaka et al., 1997; Finkelstein, Morgan and Drew, unpublished). The arabidopsis gene was shown to be functional in mutant animal cells lacking the cell death suppressor (Gallois et al., 1997), and its expression decreases in PCD of scutellum cells (Lindholm etal., 2000). Other genes in plants have been identified that have been shown to be functional as cell death suppressors (Dietrich et al., 1997; Gray et al., 1997). The existence of genes encoding death receptors, effectors, adaptors and regulators of animal apoptosis (Vaux and Korsmeyer, 1999) should encourage further genetic studies with plant systems.

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