eXtra Botany |
Salinity and programmed cell death: unravelling mechanisms for ion specific signalling
School of Agricultural Science, University of Tasmania, Private Bag 54, Hobart, Tas 7001, Australia
* E-mail: Sergey.Shabala{at}utas.edu.au
Programmed cell death (PCD) is a fundamental cellular process observed in eukaryotic cells of different origin (Huh et al., 2002; Buss et al., 2006; Piszczek and Gutman, 2007; Lam, 2008). Being an ordered series of events, PCD facilitates the removal of redundant, misplaced, or damaged cells and is essential for cellular differentiation and tissue homeostasis (Hoeberichts and Woltering, 2003; Chen and Dickman, 2004). Phloem differentiation, root cap and aerenchyma formation, aleurone and endosperm cell death, and leaf senescence are all known examples of PCD in plants. PCD is often associated with the occurrence of specific biochemical and morphological features such as condensation of the nucleus and cytoplasm, fragmentation of genomic DNA (‘DNA laddering’) and fragmentation of the cell into membrane-contained vesicles (apoptotic bodies) (Hoeberichts and Woltering, 2003). Other typical hallmarks of PCD in plants are an increase in caspase-like proteolytic activity and cytochrome c release from mitochondria.
Being essential for cell and tissue homeostasis and specialization, PCD also plays an important role in mediating plant adaptive responses to the environment. The most characterized type of PCD in plants is a hypersensitive response (HR) observed in plants in response to pathogen attack (Pennell and Lamb, 1997; Lam et al., 2001). Recently, PCD has also been proved to occur in response to various abiotic stresses such as salinity, cold stress, waterlogging, and hypoxia (Katsuhara and Kawasaki, 1996; Drew et al., 2000; Kratsch and Wise, 2000; Huh et al., 2002).
In contrast to the relatively well-described cell death pathway in animals, often referred to as apoptosis, mechanisms and regulation of plant PCD are still ill-defined (Hoeberichts and Woltering, 2003). It appears that the mechanism of DNA laddering varies in different species or even in different tissues of one organism (Jiang et al., 2008). A key role for caspase-like proteases has been suggested (Piszczek and Gutman, 2007), although caspase-encoding genes are not found in plants at the nucleotide sequence level (Hatsugai et al., 2004; Chichkova et al., 2004).
In this issue, Affenzeller and colleagues report salinity-induced PCD in a freshwater green algae Micrasterias denticulata. They have shown that prolonged salt stress (24 h) led to degradation of organelles by autophagy, a special form of PCD where organelles are degenerated and enclosed by membranous structures derived from ER. This finding extends the phenomenon of salinity-induced PCD, previously reported in higher plants (Katsuhara and Kawasaki, 1996; Katsuhara, 1997; Katsuhara and Shibasaka, 2000; Lin et al., 2005; Li et al., 2007a, b) and yeasts (Huh et al., 2002), to algal species. Importantly, DNA laddering, one of the hallmarks of PCD, was visible as soon as 1 h after the onset of NaCl stress (Affenzeller et al., 2009) while previous reports suggested that at least 4 h of salinity treatment was needed (Li et al., 2007a).
Another important aspect of Affenzeller and his colleagues' work was the finding that the observed DNA laddering occurred in NaCl but not in sorbitol-stressed cells. This indicates that the ionic rather then the osmotic component of salt stress led to the activation of the endonuclease resulting in PCD. To the best of my knowledge, the only previous report on such ionic specificity of PCD was by Huh et al. (2002). Although the exact mechanisms beyond this specificity remain elusive, several lines of evidence suggest that changes in the cytosolic K+/Na+ ratio may be crucial for triggering PCD in living cells.
Under saline conditions, strong membrane depolarization caused by Na+ uptake favours K+ efflux via depolarization-activated outward-rectifying K+ channels (Shabala et al., 2006). By contrast, isotonic mannitol or sorbitol solution causes significant membrane hyperpolarization, resulting in increased K+ uptake (Shabala et al., 2000; Shabala and Lew, 2002). This will result in a dramatic difference in cytosolic K+ level between these two types of stresses (Shabala and Cuin, 2008). In animal tissues, caspase activity is significantly increased by a low cytosolic K+ content (Hughes and Cidlowski, 1999). Assuming plant caspase-like proteases are regulated in a similar way, a decrease in the cytosolic K+ pool will activate caspase-like proteases leading to PCD after NaCl but not sorbitol treatment.
Second, no DNA laddering was detected by Affenzeller and co-authors in 0.5 mM Zn2+-pretreated cells exposed to NaCl stress. The authors explain this finding by the fact that one of the major classes of endonucleases, the so-called Ca2+-dependent endonucleases, are inhibited by elevated Zn2+ concentrations. However, it should also be noted that, similar to other divalent cations, Zn2+ is a potent blocker of both non-selective cation channels (NSCC, a major route of Na+ uptake in plant cells; Demidchik et al., 2002), and depolarization-activated outward rectifying K+ channels (Shabala et al., 2006, 2007). Thus, under saline conditions, the cytosolic K+/Na+ ratio is expected to be much higher in Zn2+-pretreated Micrasterias cells compared with untreated ones. Consistent with this idea is the finding by Li et al. (2007b) that 10 µM La3+ treatment was effective in preventing salt stress-induced PCD in rice roots. La3+ is a known NSCC channel blocker (Demidchik and Tester, 2002) and, thus, La3+ treatment was expected to have a beneficial effect on cytosolic K+/Na+ ratio under saline conditions.
In animal systems, caspase-3 is instrumental to cell apoptosis. As mentioned above, no caspase orthologues have been identified in plant genomes so far. However, up to eight distinct caspase-like enzymes have been reported in plants (Bonneau et al., 2008). Increase in the caspase-3-like activity was reported in various algal cells during PCD (Zuppini et al., 2007). Interestingly, no such increase was found by Affenzeller and co-authors in NaCl-treated Micrasterias cells. This suggests that multiple biochemical pathways may lead to PCD and calls for more thorough investigation of the signal transduction pathways involved. Reactive oxygen species (ROS) have emerged as important signals in the activation of plant PCD (Hoeberichts and Woltering, 2003). In addition, several plant hormones (e.g. ET, JA, SA, ABA, GA) may exert their respective effects on plant PCD through the regulation of ROS accumulation. Recently, heterologous expression of the animal anti-apoptotic CED-9 gene was shown to increase plant salt and oxidative stress tolerance by altering K+ and H+ flux patterns across the plasma membrane of tobacco mesophyll cells (Shabala et al., 2007), pointing to ROS-regulated ion channels as an important component of the PCD machinery in plants. More direct experiments are needed to reveal the full complexity and cross-talks between multiple pathways controlling salinity-induced PCD in plant cells.
At the moment, the following model can be suggested (Fig. 1). Under saline conditions, Na+ enters the cell through NSCC (1), causing a significant membrane depolarization (2) and resulting in a massive K+ leak (3) from the cell through depolarization-activated TEA+-sensitive KOR channels (Shabala et al., 2006; Shabala and Cuin, 2008). At the same time, salinity-induced elevation in cytosolic Ca2+ (Tracey et al., 2008) will lead to a dramatic raise in ROS level (4) resulting from [Ca2+]cyt activation of NADPH oxidase (5) via positive feedback mechanism (6; Lecourieux et al., 2002). This will cause an additional K+ efflux via ROS-activated NSCC channels (7; Demidchik et al., 2003). The resultant decrease in the cytosolic K+ pool may activate caspase-like proteases (8) leading to PCD (Fig. 1). No decline in cytosolic K+ pools (hence, no PCD) will be observed in sorbitol-treated cells, or in cells where membrane depolarization is prevented by Zn2+ or La3+ pretreatment. Several predictions can also be drawn from this model. (i) NaCl-induced PCD should be substantially attenuated (or absent) in plants lacking KOR channels (e.g. Arabidopsis gork mutants); (ii) PCD in salt-treated cells may also be prevented by more efficient scavenging of ROS by endogenous (e.g. antioxidant enzymes) or exogenous (e.g. diphenylene iodonium, mannitol) means; (iii) plants capable of better maintaining negative membrane potential under saline conditions (e.g. ones with intrinsically higher H+-ATPase activity) must be more prone to NaCl-induced PCD. Given the important adaptive significance of PCD for salinity tolerance (Huh et al., 2002), testing these predictions and validating and exploring various components of this model may be an important priority in the future.
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Acknowledgements |
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This work was supported by the Grain Research and Development Corporation grant (UT00013) to Dr S Shabala.
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Abbreviations |
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KOR, depolarization-activated outward-rectifying K+ channel; NSCC, non-selective cation channel; PCD, programmed cell death; TEA, tetraethylammonium chloride.
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References |
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 Top References |
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Affenzeller MJ, Dareshouri A, Andosch A, Lutz C, Lutz-Meindl U. Salt stress-induced cell death in the unicellular green alga Micrasterias denticulata. Journal of Experimental Botany (2009) 60:939–954.
Bonneau L, Ge Y, Drury GE, Gallois P. What happened to plant caspases? Journal of Experimental Botany (2008) 59:491–499.
Buss RR, Sun W, Oppenheim RW. Adaptive roles of programmed cell death during nervous system development. Annual Review of Neuroscience (2006) 29:1–35.[CrossRef][Web of Science][Medline]
Chichkova NV, Kim SH, Titova ES, Kalkum M, Morozov VS, Rubtsov YP, Kalinina NO, Taliansky ME, Vartapetian AB. A plant caspase-like protease activated during the hypersensitive response. The Plant Cell (2004) 16:157–171.
Demidchik V, Davenport RJ, Tester M. Nonselective cation channels in plants. Annual Review of Plant Biology (2002) 53:67–107.[CrossRef][Medline]
Demidchik V, Shabala SN, Coutts KB, Tester MA, Davies JM. Free oxygen radicals regulate plasma membrane Ca2+ and K+- permeable channels in plant root cells. Journal of Cell Science (2003) 116:81–88.
Demidchik V, Tester M. Sodium fluxes through nonselective cation channels in the plasma membrane of protoplasts from Arabidopsis roots. Plant Physiology (2002) 128:379–387.
Drew MC, He CJ, Morgan PW. Programmed cell death and aerenchyma formation in roots. Trends in Plant Science (2000) 5:123–127.[CrossRef][Web of Science][Medline]
Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S, Kondo M, Nishimura M, Hara-Nishimura I. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science (2004) 305:855–858.
Hoeberichts FA, Woltering EJ. Multiple mediators of plant programmed cell death: interplay of conserved cell death mechanisms and plant-specific regulators. Bioessays (2003) 25:47–57.[CrossRef][Web of Science][Medline]
Hughes FM, Cidlowski JA. Potassium is a critical regulator of apoptotic enzymes in vitro and in vivo. Advances in Enzyme Regulation (1999) 39:157–171.[CrossRef][Web of Science][Medline]
Huh G-H, Damsz B, Matsumoto TK, Reddy MP, Rus AM, Ibeas JI, Narasimhan ML, Bressan RA, Hasegawa PM. Salt causes ion disequilibrium-induced programmed cell death in yeast and plants. The Plant Journal (2002) 29:649–659.[CrossRef][Web of Science][Medline]
Jiang AL, Cheng YW, Li JY, Zhang W. A zinc-dependent nuclear endonuclease is responsible for DNA laddering during salt-induced programmed cell death in root tip cells of rice. Journal of Plant Physiology (2008) 165:1134–1141.[CrossRef][Web of Science][Medline]
Katsuhara M, Kawasaki T. Salt stress induced nuclear and DNA degradation in meristematic cells of barley roots. Plant and Cell Physiology (1996) 37:169–173.
Katsuhara M, Shibasaka M. Cell death and growth recovery of barley after transient salt stress. Journal of Plant Research (2000) 113:239–243.[CrossRef][Web of Science]
Katsuhara M. Apoptosis-like cell death in barley roots under salt stress. Plant and Cell Physiology (1997) 38:1091–1093.
Kratsch HA, Wise RR. The ultrastructure of chilling stress. Plant, Cell and Environment (2000) 23:337–350.
Lam E, Kato N, Lawton M. Programmed cell death, mitochondria and the plant hypersensitive response. Nature (2001) 411:848–853.[CrossRef][Medline]
Lam E. Programmed cell death in plants: orchestrating an intrinsic suicide program within walls. Critical Reviews in Plant Sciences (2008) 27:413–423.[CrossRef][Web of Science]
Lecourieux D, Mazars C, Pauly N, Ranjeva R, Pugin A. Analysis and effects of cytosolic free calcium increases in response to elicitors in Nicotiana plumbaginifolia cells. The Plant Cell (2002) 14:2627–2641.
Li JY, Jiang AL, Chen HY, Wang Y, Zhang W. Lanthanum prevents salt stress-induced programmed cell death in rice root tip cells by controlling early induction events. Journal of Integrative Biology (2007b) 49:1024–1031.[CrossRef]
Li JY, Jiang AL, Zhang W. Salt stress-induced programmed cell death in rice root tip cells. Journal of Integrative Plant Biology (2007a) 49:481–486.[CrossRef][Web of Science]
Lin J, Wang Y, Wang G. Salt stress-induced programmed cell death via Ca2+ -mediated mitochondrial permeability transition in tobacco protoplasts. Plant Growth Regulation (2005) 45:243–250.[CrossRef][Web of Science]
Pennell RI, Lamb C. Programmed cell death in plants. The Plant Cell (1997) 9:1157–1168.[CrossRef][Web of Science][Medline]
Piszczek E, Gutman W. Caspase-like proteases and their role in programmed cell death in plants. Acta Physiologiae Plantarum (2007) 29:391–398.[CrossRef][Web of Science]
Shabala S, Babourina OK, Newman IA. Ion-specific mechanisms of osmoregulation in bean mesophyll cells. Journal of Experimental Botany (2000) 51:1243–1253.
Shabala S, Cuin TA. Potassium transport and plant salt tolerance. Physiologia Plantarum (2008) 133:651–669.[CrossRef][Medline]
Shabala S, Cuin TA, Prismall L, Nemchinov LG. Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta (2007) 227:189–197.[CrossRef][Web of Science][Medline]
Shabala S, Demidchik V, Shabala L, Cuin TA, Smith SJ, Miller AJ, Davies JM, Newman IA. Extracellular Ca2+ ameliorates NaCl-induced K+ loss from Arabidopsis root and leaf cells by controlling plasma membrane K+- permeable channels. Plant Physiology (2006) 141:1653–1665.
Shabala S, Lew RR. Turgor regulation in osmotically stressed Arabidopsis epidermal root cells. Direct support for the role of inorganic ion uptake as revealed by concurrent flux and cell turgor measurements. Plant Physiology (2002) 129:290–299.
Tracy FE, Gilliham M, Dodd AN, Webb AAR, Tester M. NaCl-induced changes in cytosolic free Ca2+ in Arabidopsis thaliana are heterogeneous and modified by external ionic composition. Plant, Cell and Environment (2008) 31:1063–1073.[Medline]
Zuppini A, Andreoli C, Baldan B. Heat stress: an inducer of programmed cell death in Chlorella saccharophila. Plant and Cell Physiology (2007) 48:1000–1009.
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