• abscisic acid (ABA);
  • drought;
  • ferns;
  • hydropassive and hydroactive;
  • leaf water status;
  • lycophytes;
  • stomatal conductance;
  • turgor

More than a century ago, Francis Darwin (1898) combined two key observations that shape current understanding of the role of leaf water status in stomatal control: that ‘the guard cells share in the general turgor of the leaf’, and that ‘guard cells may lose turgor spontaneously, …in response to a stimulus [that] may be the slight flaccidity of the rest of the leaf’. The principle of this dual action was rejected by others at the time but is evident in the data of Knight (1917) (Fig. 1), and the two components later became known respectively as ‘hydropassive’ and ‘hydroactive’ stomatal responses to leaf water deficit (Stålfelt, 1929, 1955; Raschke, 1970; Cowan, 1977). Now the discussion around this subject has been re-invigorated from a fresh perspective, one barely accessible to Francis Darwin and his contemporaries: evolution. Focusing on stomatal behaviour in ferns and lycophytes, two basal lineages of vascular plants, McAdam & Brodribb in this issue of New Phytologist (pp. 429–441) report that stomatal closure under water deficit in these plants is dominated by the passive mechanism, with the active component playing a lesser role.


Figure 1. One of the first experiments to capture the complex response of stomata to leaf water deficit, prompting the ‘theory of the action of incipient drying’(data plotted from Knight, 1917). Stomatal aperture in Helianthus tuberosus, an angiosperm, initially increased and then decreased in response to increasing leaf water deficit. As the water deficit was relieved, stomata remained closed. Because of the complex nature of the response Knight concluded that stomata were not the ‘chief factors in maintaining the water content of the leaf’. We now know that stomatal mechanics and the action of the regulatory stress hormone abscisic acid (ABA) contribute to this widely observed pattern, but new work by McAdam & Brodribb (this issue of New Phytologist, pp. 429–441) on ferns and lycophytes suggests this classical view could be biased.

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‘Now the discussion around this subject has been re-invigorated from a fresh perspective, one barely accessible to Francis Darwin and his contemporaries: evolution.’

How plants manage water deficit under drought or high evaporative demand profoundly influences primary productivity and survival in diverse environments (Boyer, 1982; Ciais et al., 2005). The stomatal control system is at the centre of this, responding rapidly to small environmental changes to optimize the exchange of water for carbon (Farquhar & Sharkey, 1982). One approach to understanding this system has been to examine the molecular signalling mechanisms by which environmental changes are sensed, integrated and translated into adjustments in stomatal aperture. From this, major inroads have been made into the hydroactive mechanism, with considerable attention to the action of the stress hormone abscisic acid (ABA) (Schroeder et al., 2001; Kim et al., 2010). Since its ability to reduce stomatal aperture was discovered (Mittelheuser & Van Steveninck, 1969), ABA has gained increasing prominence as a key player in stomatal control, particularly in relation to management of plant water deficit. However, almost all of the research into the action of ABA and the hydroactive mechanism has focused on angiosperms. Could this have biased current perceptions of the relative role of the hydroactive and hydropassive mechanisms? The findings of McAdam & Brodribb suggest this could be the case. In a group of six ferns and one lycophyte, only two of the ferns showed the classical pattern of decreasing stomatal conductance with increasing leaf ABA concentration, but all closed their stomata as leaf water potential declined, leading McAdam & Brodribb to conclude that ferns and lycophytes rely predominantly on the hydropassive mechanism.

Given that stomatal sensitivity to ABA and related molecular signalling pathways have been identified across the evolutionary spectrum of vascular plants, as well as in moss sporophytes (Chater et al., 2011; Ruszala et al., 2011), it appears that hydroactive and hydropassive stomatal control processes have operated together since stomata first evolved some 400 million yr ago. The question that emerges is whether angiosperms are generally more dependent on ABA and the hydroactive mechanism, and if so, why? To address this, one needs to consider the conditions that could have driven selection for such dependence. Increasing exposure to leaf water deficit per se is unlikely to have been a significant factor as ferns, lycophytes and angiosperms today thrive in a diverse range of moisture environments. However, selection for other stomatal performance characteristics might have increased the dependence of angiosperms on active adjustment of guard cell turgor. One possibility is illustrated in Fig. 2. In contrast to ferns and lycophytes, the epidermal cells adjacent to stomata in angiosperms typically exert a ‘mechanical advantage’ over the guard cells. This enhances dynamic performance but for stomata to close effectively under declining leaf water potential the mechanical advantage must be counteracted by active guard cell osmotic adjustment (Franks & Farquhar, 2007). ABA might serve as a signal in this mechanism. Importantly, it is shown in Fig. 2 that although the absence of the mechanical advantage (as in some ferns and lycophytes) would obviate the need for this kind of hydroactive mechanism, the improved sensitivity it provides would benefit most plants. The relative importance of hydropassive and hydroactive stomatal control in different plant species or lineages may vary as a result of a number of factors, but so far, Darwin's integrated model appears to be holding up well.


Figure 2. The benefits of active stomatal control, and why angiosperms might rely on it more than ferns. In this simulation the stomatal guard cells of the fern (or lycophyte; a, c, e) and angiosperm (b, d, f) are anatomically and functionally similar except that the turgor of epidermal cells of the angiosperm exerts a mechanical advantage over the guard cells. This mechanical advantage is common in angiosperms but typically absent in ferns and lycophytes (Franks & Farquhar, 2007). (a–f) describe the stomatal response of both types of plants to the same decline in leaf water potential, Ψ(leaf), from 0 to −1 MPa, as soil dries. Red lines show responses only via basic hydropassive control. Blue lines show the responses via hydropassive control together with a simple hydroactive control process defined here as a proportional reduction in guard cell turgor with epidermal turgor (mediated by a biochemical signal such as abscisic acid (ABA)). Without the influence of epidermal turgor (which for the fern in this example is always, but for the angiosperm is only when the epidermal cells lose turgor) the relationship between stomatal aperture and guard cell turgor (P(guard cell)) follows a saturating curve (solid black lines in a, b). At full epidermal turgor (i.e. Ψ(leaf) equal to zero) stomatal aperture at any P(guard cell) is reduced substantially in the angiosperm (dotted black line in b), with the effect diminishing as epidermal turgor declines. To achieve the same apertures when Ψ(leaf) equals zero (in this case c. 8 μm) the angiosperm requires substantially higher P(guard cell) than the fern (compare b with a), generated by higher guard cell osmotic pressure, Π(guard cell) (compare c with d). Without active control, the –1 MPa drop in Ψ(leaf) reduces P(guard cell) in the fern and angiosperm but aperture declines only in the fern, not the angiosperm (compare red line in a with red line in b). With the simple active control mechanism operating in the angiosperm, the −1 MPa drop in leaf water potential is amplified to a −3.5 MPa drop in P(guard cell) (blue line in b). The same active control mechanism reduces Π(guard cell) in the fern and the angiosperm as Ψ(leaf) declines to –1 MPa (blue lines in c, d). The fern is able to reduce stomatal conductance (gw) to zero without active control (red line in e) but can do so at higher Ψ(leaf) with the addition of active control (blue line in e). Unlike the fern, hydropassive control alone in the angiosperm cannot reduce stomatal conductance in response to the drop in Ψ(leaf) (red line in f), but with the addition of active stomatal control gw declines in a similar fashion to that of the fern (blue line in f). The mechanical advantage improves other dynamic characteristics of stomata in angiosperms (Franks & Farquhar, 2007) but may require heavier reliance on active control compared with ferns and lycophytes.

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