Enhanced Photosynthesis and Growth in atquac1 Knockout Mutants Are Due to Altered Organic Acid Accumulation and an Increase in Both Stomatal and Mesophyll Conductance

Abstract

Stomata control the exchange of CO 2 and water vapor in land plants. Thus, whereas a constant supply of CO 2 is required to maintain adequate rates of photosynthesis, the accompanying water losses must be tightly regulated to prevent dehydration and undesired metabolic changes. Accordingly, the uptake or release of ions and metabolites from guard cells is necessary to achieve normal stomatal function. The AtQUAC1, an R-type anion channel responsible for the release of malate from guard cells, is essential for efficient stomatal closure. Here, we demonstrate that mutant plants lacking AtQUAC1 accumulated higher levels of malate and fumarate. These mutant plants not only display slower stomatal closure in response to increased CO 2 concentration and dark but are also characterized by improved mesophyll conductance. These responses were accompanied by increases in both photosynthesis and respiration rates, without affecting the activity of photosynthetic and respiratory enzymes and the expression of other transporter genes in guard cells, which ultimately led to improved growth. Collectively, our results highlight that the transport of organic acids plays a key role in plant cell metabolism and demonstrate that AtQUAC1 reduce diffusive limitations to photosynthesis, which, at least partially, explain the observed increments in growth under well-watered conditions.

Rethinking Guard Cell Metabolism

“…Further insights into the importance of carboxylates in the connection between stomatal behavior and leaf primary metabolism come from two recent studies where higher stomatal conductance was observed in plants with increased accumulation of malate (Gago et al, 2016;Medeiros et al, 2016). Plants lacking a functional AtALMT12 malate channel not only displayed slower stomatal closure, as mentioned above (Meyer et al, 2010), but also were characterized by changes in organic acid accumulation and increased stomatal and mesophyll conductance (Medeiros et al, 2016).…”

Stomatal Biology of CAM Plants

“…Guard cell metabolism in C 3 , C 4 , and CAM plants continues to be a fast-paced area of research with many critical questions awaiting resolution (Daloso et al, 2016;Santelia and Lunn, 2017). The similarities between guard cell metabolism in C 3 plants and the metabolism of mesophyll cells of CAM plants are striking, which led Cockburn (1981) to suggest that a transfer of guard cell-like metabolism to mesophyll cells was a central event in evolutionary origins of CAM.…”

“…More recent work has highlighted the importance of organic acids in C 3 guard cell function (e.g. Wang and Blatt, 2011;Penfield et al, 2012;Daloso et al, 2015;Medeiros et al, 2016).…”

Ion Transport at the Vacuole during Stomatal Movements

“…It is assumed that starch conversion to sugars, but also the import of sugars via the plasma membrane, is required to achieve or maintain open stomata, replacing or adding to K salts as osmotica (Daloso et al, 2016;Santelia and Lawson, 2016;Santelia, 2017). How might sugars be imported into and released from the guard cell vacuole?…”

“…(1) Nagy et al (2009); (2) Klein et al (2003) Arabidopsis guard cell Mal 22 concentration increases during stomatal opening 2-to 3-fold and generally correlates with stomatal aperture (Monda et al, 2011;Ding et al, 2014;Takahashi et al, 2015;Medeiros et al, 2016). We have gained good understanding of the importance of individual transport processes at the vacuole.…”