Blue Light Induces a Distinct Starch Degradation Pathway in Guard Cells for Stomatal Opening

Stomatal pores form a crucial interface between the leaf mesophyll and the atmosphere, controlling water and carbon balance in plants [1]. Major advances have been made in understanding the regulatory networks and ion fluxes in the guard cells surrounding the stomatal pore [2]. However, our knowledg...

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Bibliographic Details
Published in:Current biology 2016-02, Vol.26 (3), p.362-370
Main Authors: Horrer, Daniel, Flütsch, Sabrina, Pazmino, Diana, Matthews, Jack S.A., Thalmann, Matthias, Nigro, Arianna, Leonhardt, Nathalie, Lawson, Tracy, Santelia, Diana
Format: Article
Language:English
Subjects:
Arabidopsis - metabolism
Arabidopsis - radiation effects
Light
Plant Leaves - physiology
Plant Stomata - physiology
Starch - metabolism
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Summary:Stomatal pores form a crucial interface between the leaf mesophyll and the atmosphere, controlling water and carbon balance in plants [1]. Major advances have been made in understanding the regulatory networks and ion fluxes in the guard cells surrounding the stomatal pore [2]. However, our knowledge on the role of carbon metabolism in these cells is still fragmentary [3–5]. In particular, the contribution of starch in stomatal opening remains elusive [6]. Here, we used Arabidopsis thaliana as a model plant to provide the first quantitative analysis of starch turnover in guard cells of intact leaves during the diurnal cycle. Starch is present in guard cells at the end of night, unlike in the rest of the leaf, but is rapidly degraded within 30 min of light. This process is critical for the rapidity of stomatal opening and biomass production. We exploited Arabidopsis molecular genetics to define the mechanism and regulation of guard cell starch metabolism, showing it to be mediated by a previously uncharacterized pathway. This involves the synergistic action of β-amylase 1 (BAM1) and α-amylase 3 (AMY3)—enzymes that are normally not required for nighttime starch degradation in other leaf tissues. This pathway is under the control of the phototropin-dependent blue-light signaling cascade and correlated with the activity of the plasma membrane H+-ATPase. Our results show that guard cell starch degradation has an important role in plant growth by driving stomatal responses to light. [Display omitted] •Starch in guard cells is degraded within 30 min of light to promote stomatal opening•A distinct set of hydrolytic enzymes mediates starch degradation in guard cells•Phototropin signaling and proton pumping control starch degradation in guard cells•Guard cell starch drives plant growth through the control of stomatal aperture Horrer et al. report quantitative analysis of starch turnover in guard cells of intact Arabidopsis leaves and show it to be an ideal system to study guard cell carbohydrate metabolism. Molecular genetic analyses show that guard cells integrate blue-light-induced proton pumping with starch degradation to control stomatal opening and plant growth.
ISSN:0960-9822
1879-0445
DOI:10.1016/j.cub.2015.12.036