Callose: a multifunctional (1, 3)-β–d-glucan involved in morphogenesis and function of angiosperm stomata

The radial callose fibrillar arrays deposited in the periclinal cell walls of the kidney- shaped GCs of the fern Asplenium nidus, which are co-aligned with the radial cellulose microfibrils, possibly participate in stomatal opening, reinforcing the role of the latter in the tangential periclinal GC wall expansion that is critical for stomatal opening [10, 27]. This suggestion has been experimentally supported [27].

Callose is absent from the periclinal cell walls of the functional kidney–shaped GCs of the dicotyledonous V. sinensis. It is localized at the polar VW ends as well as in the thickenings deposited at the junctions of the dorsal cell walls (Fig. 1 L, M). It is well known that during stomatal opening, the polar VW ends of the kidney-shaped stomata are under intense mechanical stress [3, 17, 28, 29]. Callose, functioning as a stiffening material, probably strengthens the polar VW ends to withstand the mechanical forces generated during stomatal opening [8]. If the VW ends are not stiff enough, the stomatal pore will not open successfully.

Gensler [19] considering the presence of callose in the periclinal cell walls of the kidney-shaped GCs of the fern Asplenium nidus [18, 27] has assumed that callose creates a protonic electrical circuit at the periclinal cell walls of the GCs. Such a circuit would facilitate proton transfer between different parts of the VW and further provide a driving force for concomitant potassium ion entry and exit between GCs and subsidiary cells. In this way, callose could participate in the stomata function mechanism. However, this view cannot be applied in kidney-shaped GCs of V. sinensis, because callose is absent from their periclinal cell walls.

Although both the dicotyledonous V. sinensis and the fern A. nidus have kidney-shaped stomata, callose displays a different distribution pattern between the two. It implies that it plays a different role during stomatal movement in them. In V. sinensis, callose is absent from the periclinal cell walls of the GCs [8], while it is present at these cell walls of A. nidus GCs [18, 27]. These differences may be related not only to the particular morphology of the GCs but also to the chemical composition of the cell walls of the GCs of these two plants. In A. nidus, the GCs display swollen polar ends facing the substomatal cavity and intense cell wall thickenings at the junction sites of the polar VW ends with the external periclinal cell wall [30]. These cell wall regions are traversed by many cellulose microfibrils arranged parallel to the epidermal surface [30]. These structural features are absent from the GCs of V. sinensis. Furthermore, while the GC walls of the dicotyledonous, as V. sinensis, are rich in pectins [8, 17], they seem to participate in a lower degree in the cell wall composition of A. nidus GCs [17]. According to Shtein et al. [16, 17], the ferns, including A. nidus, use crystalline cellulose as a localized strengthening material in the central region of the GCs that participates in stomatal movement. This notion is further supported by the presence of callose at the exact same sites. On the contrary, in dicotyledonous stomata, the role of crystalline cellulose and callose is probably served by pectins located at the respective regions [17]. Nevertheless, in A. nidus stomata too, the callose deposited at the cell wall thickenings of the polar VW ends [18, 27] probably reinforces the specific regions in order to withstand the mechanical forces exerted during stomatal opening, as it has already been suggested in V. sinensis stomata [8].

During opening of the dumbbell-shaped grass stomata, the bulbous GC ends swell and become deformed. The radial cellulose microfibrils in both the periclinal cell walls of the bulbous GC ends, which diverge from the edge of the central canal towards their ends [20] and the pairs of terminal central canal thickenings, seem to control the pattern of expansion and deformation of the bulbous GC ends. The swelling of the bulbous GC ends appears asymmetrical, being more intense towards the VW than towards the dorsal cell wall (Fig. 1H; compare to Fig. 1G). The mechanical forces generated by the elevated GC turgor are finally exerted on both the polar VW ends and on the terminal canal thickenings, to induce stomatal opening. It is achieved when the central canals are displaced to some extent ‘‘into the subsidiary cells’’ [31, 32] (Fig. 1G; compare to Fig. 1H). When the bulbous ends of the GCs swell, the terminal cell wall thickenings that emerge from the central canal and enter the junctions of the periclinal cell wall with the lateral ones in the bulbous GC ends (arrowheads in Fig. 1) probably enforce the central canals to move towards the subsidiary cells, acting like “levers”. This becomes possible because the central canal and the terminal cell wall thickenings in each GC constitute a united system [20]. At the same time mechanical forces applied on the VW ends also contribute to the lateral displacement of the central canals.

The development of this particular mechanism of stomatal movement became probably necessary because of the unique morphology of the dumbbell-shaped stomata of the Poaceae. Usually, in Z. mays, the junctions of the VW with the transverse cell walls display large gaps, through which cytoplasm, plastids and mitochondria can move from one GC to the other [20]. However, this VW discontinuity enables GCs to be synchronized and to function as one cell during stomatal movement. In addition, the osmotic and turgor pressure ‘‘synchronization’’ between the GCs and the subsidiary cells, ‘‘see-sawing’’ according to Franks and Farquhar [31], is also functionally important. The increase of the GC turgor, keeping pace with the decrease of that of the subsidiary cells makes feasible the change of the shape of the latter cells to ‘‘accept the lateral central canal displacement’’ [31, 32] (Fig. 1F; compare to Fig. 1E and  J; compare to Fig. 1I). As Franks and Farquhar [31] and Nunes et al. [33] pointed out, the four-celled dumbbell-shaped stomatal complexes of Poaceae, due to their unique structure, became able to attain wider pore apertures and faster response to environmental changes than any other stomatal type.

Callose enrichment of the central canal cell walls as well as those of bulbous GC ends (Fig. 1C–E), increases their stiffening making them rigid enough to secure the lateral displacement of the central canal ‘‘into the subsidiary cells’’ [8]. Especially, callose deposition in the terminal thickenings of the central canal increases their stiffness to fulfil the critical role in stomatal opening suggested above. The endings of the cell wall thickenings of the central canal display high degree of cellulose crystallinity [28], so Rui et al. [6] concluded that the cell wall in these regions display intense stiffness. Obviously, this stiffness is further increased by the presence of callose. Callose detection at the cell wall of the intervening cell adjacent to the polar end of the open stomata [8] is probably a response to mechanical forces exerted on it during increase in volume/deformation of the bulbous GC ends. In addition, the presence of callose in the lateral GC cell wall of the central canal, (Fig. 1F), may have either a sealing function for the preservation of GC and/or the subsidiary cell turgor or more possibly it is formed as the result of mechanical stresses imposed on this cell wall during the lateral movement of the GC central canal. The above consideration allows the suggestion that the extensive GC callose depositions significantly reinforce the rigidity of the dumbbell-shaped stomata during stomatal opening and closure.

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