3 cADPR and plant response to environmental stress

Sensing, Signaling and Cell Adaptation

Lee H. C. (2002)

Hon Cheung Lee,

Cell and Molecular Response to Stress, 2002 –

https://www.sciencedirect.com/topics/immunology-and microbiology/plant-stoma

3 cADPR and plant response to environmental stress

Unlike animals, plants are immobile and cannot actively avoid adverse conditions. Various strategies were evolved in plants to handle environmental stress. A particular robust response is the regulation of stomata on leaves, pores through which gas exchange takes place. By closing the stomata, plants can conserve water during periods of drought by reducing loss through evaporation. Stomatal aperture is made up of and controlled by two parallel guard cells which are elongated in shape and are physically linked at the two ends, but not longitudinally. When water is plentiful, swelling of the guard cells induced by solute and water intake results in opening of the pore. Closure of the stomata is regulated by a plant hormone, abscisic acid (ABA), which triggers solute efflux from the guard cells and causes cell shrinkage.

A complex series of ion movements in guard cells is activated by ABA (Schroeder et al., 2001). Principal among them is cytoplasmic elevation of Ca^2 + concentration, which in turn activates anion channels in the plasma membrane of the cell. Efflux of anions depolarizes the cell and opens the outward-rectifying K⁺-channels present also in the plasma membrane. The net effect is the efflux of KC1 from the guard cell leading to reduction in turgor pressure, cell shrinkage and closure of the stomatal aperture.

A series of recent studies shows that cADPR plays a crucial role in initiating the Ca^2 + signal induced by ABA. A main source of this Ca^2 + signal is by release from the large vacuoles present in plant cells. Isolated vacuolar microsomes can respond to either cADPR or IP₃ and release Ca^2 + (Allen et al., 1995). Patch-clamp studies of individual vacuoles show the presence of cADPR-gated Ca^2 + channels in the vacuolar membrane (Allen et al., 1995; Leckie et al., 1998). Microinjection of cADPR into guard cells likewise induces Ca^2 + elevation and effects loss of turgor pressure in the injected cell (Leckie et al., 1998). Conversely, treatment of guard cells with nicotinamide, an inhibitor of the ADP-ribosyl cyclase (described above), significantly inhibits stomatal closure induced by ABA.

The ABA-induced Ca^2 + signal occurs in the form of a prolonged oscillation, which appears to be important for stomatal closure (Leckie et al., 1998; Allen et al., 2000). A plant mutant which lacks the ability to produce a Ca^2 + oscillation in response to certain stimuli also fails to close the stomata in response to the same stimuli (Allen et al., 2000). The exact mechanism of how ABA activates this Ca^2 + oscillation has not been worked out. Evidence obtained in sea urchin eggs indicates that specific interactions between the cADPR- and NAADP-sensitive Ca^2 + stores can lead to prolonged Ca^2 + oscillation (Aarhus et al., 1996; Lee, 1997; Churchill and Galione, 2001a). Indeed, plants, like the eggs, also possess both types of Ca^2 + stores. Fractionation studies show that the NAADP-sensitive Ca^2 + stores are mainly copurified with the endoplasmic reticulum (Navazio et al., 2000). The cADPR-sensitive stores, on the other hand, are associated with both the vacuolar membranes and the endoplasmic reticulum (Allen et al., 1995; Navazio et al., 2001). The pharmacology of the NAADP-sensitive mechanism in plants is also similar to that observed in animal cells, being insensitive to 8-amino-cADPR and heparin and showing potent self-desensitization (Aarhus et al., 1996; Genazzani et al., 1996; Navazio et al., 2001). It has also been shown that plant homogenates are capable of enzymatic synthesis of NAADP from NADP and nicotinic acid, as observed in animal cells (Aarhus et al., 1995b; Navazio et al., 2001). It is thus clear that both Ca^2 + signaling mechanisms, like the IP₃ mechanism, are highly conserved in evolution, testifying to their fundamental importance.

Stomatal closure represents a fast and immediate response to ABA, which is also capable of inducing long-term adaptation through expression of specific genes. This process is likewise mediated by cADPR. Microinjection of cADPR into plant cells activates expression of ABA-specific genes, such as rd29A, a desiccation-responsive gene (Wu et al., 1997), as well as kin2 and BN115, which are cold-inducible genes (Wu et al., 1997; Sangwan et al., 2001). Indeed, cADPR-induced expression of BN115 effects significant protection of the leaves to damage by freezing (Sangwan et al., 2001). The protective effect of cADPR is more specific than simply elevating cytoplasmic Ca^2 +, since A23187, a non-specific Ca^2 + ionophore, can produce much less protection, indicating a high degree of specificity of the cADPR-pathway in mediating cold-acclimatization in plants (Sangwan et al., 2001).

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