Association between water and carbon dioxide transport in leaf plasma membranes: assessing the role of aquaporins

Abstract

The role of some aquaporins as CO permeable channels has been controversial. Low CO permeability of plant membranes has been criticized because of unstirred layers and other limitations. Here we measured both water and CO permeability (P , P ) using stopped flow on plasma membrane vesicles (pmv) isolated from Pisum sativum (pea) and Arabidopsis thaliana leaves. We excluded the chemical limitation of carbonic anhydrase (CA) in the vesicle acidification technique for P using different temperatures and CA concentrations. Unstirred layers were excluded based on small vesicle size and the positive correlation between vesicle diameter and P . We observed high aquaporin activity (P 0.06 to 0.22 cm s ) for pea pmv based on all the criteria for their function using inhibitors and temperature dependence. Inhibitors of P did not alter P . P ranged from 0.001 to 0.012 cm s (mean 0.0079 + 0.0007 cm s ) with activation energy of 30.2 kJ mol . Intrinsic variation between pmv batches from normally grown or stressed plants revealed a weak (R = 0.27) positive linear correlation between P and P . Despite the low P , aquaporins may facilitate CO transport across plasma membranes, but probably via a different pathway than for water.

Role of Plant Carbonic Anhydrases under Stress Conditions

“…However, biological membranes appear to have a low CO 2 permeability [75] due to a high level of protein and sterol content [74,76]. Recently, using plasma membrane vesicles of pea leaves it has been demonstrated that plasma membrane aquaporins could facilitate CO 2 transport [77]. The same data were earlier presented for tobacco, Arabidopsis, fava bean, and others [78][79][80].…”

“…This connection allows CO 2 permeability across the plasma membrane to be facilitated. Further, the decrease in the CA concentration was shown to lead to a lower CO 2 permeability in plasma membrane vesicles [77]. Therefore, it can be proposed that the functioning of plasma membrane aquaporins depends on the CA activity under both normal and stress conditions.…”

The Membrane Transport System of the Guard Cell and Its Integration for Stomatal Dynamics

“…The results are also difficult to reconcile with a publication from the same group suggesting that phosphorylation sites on both sides of the membrane are essential for the SLAC1 response to pCO 2 (Yamamoto et al, 2016). Thus, the relationships between aquaporins and carbonic anhydrases in water and CO 2 permeability are a matter of debate (Grondin et al, 2015;Zhao et al, 2016), as is their coupling to activation of the anion channel. For now, the guard cell CO 2 (HCO 3 2 ) sensors remain unknown, although it is clear that, downstream, the action overlaps with significant elements important also for ABA signaling (Chater et al, 2015;Tian et al, 2015).…”

“…Guard cells coordinate solute flux actively through a number of major transport pathways at the plasma membrane and the tonoplast during stomatal movements (Box 1;Allen et al, 1999;Chen et al, 2016;Desikan et al, 2002;Suhita et al, 2004;Yamauchi et al, 2016;Yin et al, 2009;Zhang et al, 2001;Zhao et al, 2016). Like all plant cells, guard cells use ATP to drive H + out of the cell via H + -ATPases, thereby generating a membrane voltage, negative inside, and an electrochemical potential difference (Dm H ) for the H + .…”

Internal transport of CO2 from the root‐zone to plant shoot is pH dependent

“…How plants release the root‐zone CO 2 to the atmosphere is an important question. To gain entry into plants, CO 2 could pass through aquaporins in the plasma membrane which have been shown to enhance membrane permeability to CO 2 (Hanba et al , Li et al , Zhao et al ) or directly through the lipid bilayer of the plasma membrane. After reaching the symplasm, CO 2 could diffuse through plants very quickly as evidenced by gas exchange measurements (Figs and ).…”