Abstract
Bundle sheath extensions (BSEs) are key features of leaf structure with currently little-understood functions. To test the hypothesis that BSEs reduce the hydraulic resistance from the bundle sheath to the epidermis (r(be)) and thereby accelerate hydropassive stomatal movements, we compared stomatal responses with reduced humidity and leaf excision among 20 species with heterobaric or homobaric leaves and herbaceous or woody life forms. We hypothesized that low r(be) due to the presence of BSEs would increase the rate of stomatal opening (V) during transient wrong-way responses, but more so during wrong-way responses to excision (V(e)) than humidity (V(h)), thus increasing the ratio of V(e) to V(h). We predicted the same trends for herbaceous relative to woody species given greater hydraulic resistance in woody species. We found that V(e), V(h), and their ratio were 2.3 to 4.4 times greater in heterobaric than homobaric leaves and 2.0 to 3.1 times greater in herbaceous than woody species. To assess possible causes for these differences, we simulated these experiments in a dynamic compartment/resistance model, which predicted larger V(e) and V(e)/V(h) in leaves with smaller r(be). These results support the hypothesis that BSEs reduce r(be). Comparison of our data and simulations suggested that r(be) is approximately 4 to 16 times larger in homobaric than heterobaric leaves. Our study provides new evidence that variations in the distribution of hydraulic resistance within the leaf and plant are central to understanding dynamic stomatal responses to water status and their ecological correlates and that BSEs play several key roles in the functional ecology of heterobaric leaves.
Highlights
Bundle sheath extensions (BSEs) are key features of leaf structure with currently little-understood functions
An alternative explanation is that the hydraulic resistance between the epidermis and the bulk leaf tissue, including the xylem, can be very large, consistent with the observation that epidermal turgor pressure responded to humidity at the perturbed surface but not at the unperturbed surface in V. faba (Mott, 2007; turgor was not measured for X. strumarium)
Where wrong-way responses” (WWRs) were observed, we found wide ranges for most WWR parameters
Summary
Bundle sheath extensions (BSEs) are key features of leaf structure with currently little-understood functions. The similarity of stomatal responses to hydraulic supply and demand (Saliendra et al, 1995; Comstock and Mencuccini, 1998; Cochard et al, 2002) suggests that part of the regulation of gs results from negative feedback from water status within the leaf (Buckley, 2005) The resolution of these questions may require greater focus on functional aspects of leaf anatomy, in During natural transpiration, water potentials may vary greatly over small spatial scales within leaves, because of large and varying resistances in the pathways for water flow to the sites of evaporation (Mott, 2007; Zwieniecki et al, 2007; Peak and Mott, 2011). It is surprising that the role of BSEs in stomatal control has received so little attention
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