The ER A Stress Responsive Compartment

Unfavourable radiation, water stress, severe temperature changes, wounding, and attacks by pathogens are possible environmental strain situations that plants have to cope with. The ER organization of affected cells may alter if the parameters involved in the signal transmitting cascade, like the proton and/or Ca2+ concentration, change. Morphological variations, in principle, concern a dynamic shift between the two major ER modifications, tubules, and lamellar sheets, frequently preceded or accompanied by motility changes (Table 3).

The influence of light on ER morphology has hitherto only been addressed in the alga Acetabularia (Liebe and Menzel 1994). Microscopy studies indicate that blue and UV light may affect ER organization in higher plants but detailed studies, e.g. on dose dependence, are missing. Regarding harsh water stress, plasmolysis studies showed that parts of the cortical ER adhere so strongly to the PM that they remain attached to the cell wall, forming a "Hechtian reticulum" linked to the protoplast by Hechtian strands (Oparka et al. 1994; Stickens and Verbelen 1996). The fate of the ER organization within the shrinking protoplast has not been addressed in these studies and

Table 3 Stress-induced changes in ER organization: formation of lamellar sheets from tubular elements or the disintegration of lamellar sheets to short tubules

Applied stress Morphological changes Refs.

Breakdown of Formation of lamellar sheets lamellar sheets

Natural stress Low temperature High temperature (> 35 °C) Pathogen attack Water stress (dehydration) Artificial stress Lowering the intracellular pH (< 6.8)

Increasing the intracellular pH (> 7.5)

Perturbation of Ca2+ distribution

— +++ e a Quader et al. 1989 b Quader et al. 1996

c Leckie et al. 1995; Reichel and Beachy 1998; Takemoto et al. 2003 d Quader and Fast 1990 e Quader 1990; Bergfeld and Schopfer 1984

awaits thorough investigation. Stacks of lamellar ER are, however, induced by less severe water stress, which are reversed to ER tubules after stress release (Bergfeld and Schopfer 1984).

A low temperature, around 4 °C, causes in onion epidermal cells the disintegration of lamellar ER sheets to tubules and the disappearance of long tubular strands, leading to a distinct increase of short ER tubules (Quader et al. 1989). Although the peripheral polygonal network is hardly recognizable because of the vigorous meandering tubular elements it can, however, be assumed that it is retained. Contrary to chilling, elevated temperatures (35-40 °C) cause the formation of large lamellar ER sheets within the polygonal network and deeper in the cytoplasm, often leading to lamellar stacks (Quader et al. 1996). The disappearing long tubular strands most likely contribute to the genesis of the ER lamellae. The ER organization regains normal patterning after reverting the chilling or high temperature regime to about 20 °C within a suitable period (Quader et al. 1989; Quader et al. 1996).

Attacks of pathogenic viruses and fungi also cause the formation of large lamellar sheets. They temporarily form after infecting transgenic N. ben-thamiana with tobacco mosaic virus and turn back into tER elements in later stages of infection (Reichel and Beachy 1998). The authors suggest that the virus movement protein may play a role in the formation of the lamellar sheets. A similar reorganization of the ER has been observed in epidermal cells of pea after infection with the powdery mildew fungus Erysiphe pisi (Leckie et al. 1995) and of A. thaliana cotyledons infected with different oomycete pathogens (Takemoto et al. 2003). A dense ER seems to occur around the penetration site of the fungus, which has been discussed as a compact network of lamellar ER merging into a compressed reticulum of ER tubules resembling perforated ER sheets (see above; Hepler 1981; Ridge et al. 1999). Little is known about the function of the ER accumulating around haustorial necks, but a mere function in membrane lipid and protein synthesis in relation to the formation of the haustorium has been excluded because ER accumulation occurred also in cells without haustoria (Takemoto et al. 2003).

Wounding or treatment with the defence hormone methyl jasmonate induces in epidermal cells of rosette leaves of transgenic Arabidopsis plants the formation of so-called ER bodies, besides the known ER modifications (Gunning 1998; Hawes et al. 2001; Matsushima et al. 2003). Leaves which have not been wounded or treated with the hormone do not show these structures in which defence proteins seem to accumulate (Matsushima et al. 2003; see also Hara-Nishimura and Shimada, this volume).

Pathogenic attacks involve the partial degradation of the host cell wall. Enzymes derived from pathogens as pectinases, cellulases, hemicellulases, and proteinases selectively lyse cell wall components and thus may mimic a pathogen attack. Pectinase and protein K treatment caused the formation of large lamellar ER sheets similar to the infection by a pathogen, whereas cellu-

lases and hemicellulases did not significantly affect ER organization in onion bulb scale epidermal cells (Quader et al. 1996).

Systematic investigations to solve the molecular basis for the stress-induced changes of ER morphology are rather scarce. Low and high temperature, as well as the stress exerted through pathogen attack, not only affects ER organization but is also often accompanied by the inhibition of actomyosin-dependent intracellular movement. As already pointed out, an intact actomyosin system is required not only to pull ER tubules out of the polygonal network and to push the long ER strands deeper into the cytoplasm, but also to keep them in a stretched mode (see Sect. 2). Disassembly of the AF backbone, and also the inhibition of the motor protein myosin, results in the formation of lamellar ER sheets. Myosin carries out a dual function: besides being a motor for motility it also serves as a link between AFs and the ER tubules keeping the latter stretched. Without a functional actomyosin system, only the ER tubules of the polygonal network which are linked to fixed sites may maintain their stretched shape (Knebel et al. 1990). Ca2+ in connection with calmodulin (Shimmen et al. 2000) and protons (Nachmias et al. 1987) are known to control myosin activity. Artificially lowering the cytoso-lic pH by weak acid loading causes the breakdown of lamellar ER sheets into tubules (Quader and Fast 1990), whereas artificial cytosolic alkalinization by weak base loading leads to the opposite response: the formation of lamellar ER sheets (Quader et al. 1996). The long tER strands retract during both lowering and raising of the cytosolic pH.

The ionic situation, and here in particular the equilibrium of proton and calcium cations across the ER membrane, apparently plays an important role in ER organization. Interestingly, after lowering the cytosolic pH ER tubules can obviously not fuse to lamellar ER sheets, even when they are arranged in a highly compact manner.

The disintegration of the lamellar ER sheets to ER tubules by low temperature resembles the effect achieved by lowering the cytosolic pH. The latter has been shown to drop in suspension-cultured mung bean cells from 7.4 to 6.3 within an 18-h chilling period (Yoshida 1994). The induced disintegration of the lamellar ER sheets may therefore be due to the acidification of the cytoplasm by low temperature.

Individual or stacks of large lamellar ER sheets are formed in onion epidermal cells after interference with the cellular Ca2+ distribution, e.g. through application of the Ca2+ ionophore calcimycin, selective Ca2+-chelating drugs, or calmodulin antagonists (Quader 1990). Motility is suppressed and organelles like mitochondria often accumulate in the area of the formed ER sheets. ER organization of perturbed cells recovers after washing out the drugs (Quader 1990). At the beginning, tubular ER loops develop at the rim of the ER sheets, which successively become pulled away as long tER strands to other areas of the cell (see Fig. 2d). Recovery is inhibited in the presence of actomyosin blocking substances (Quader 1990). The actomyosin system is, however, only indispensable for the movement of ER tubules, because calcimycin-induced lamellar ER sheets disintegrate to tubules after artificially lowering the cytosolic pH by weak acid loading with calcimycin and actomyosin-inhibiting drugs still present (Quader et al. 1996).

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