Aquaporin gene expression and apoplastic water flow in bur oak (Quercus macrocarpa) leaves in relation to the light response of leaf hydraulic conductance

Abstract

It has previously been shown that hydraulic conductance in bur oak leaves (Quercus macrocarpa Michx.), measured with the high pressure flow meter technique (HPFM), can significantly increase within 30 min following exposure to high irradiance. The present study investigated whether this increase could be explained by an increase in the cell-to-cell pathway and whether the response is linked to changes in the transcript level corresponding to aquaporin genes. Four cDNA sequences showing high similarity to members of the aquaporin gene family from other plant species were characterized from bur oak leaves and the expression levels of these cDNA sequences were examined in leaves by quantitative real-time PCR (QRT-PCR). No change was found in the relative transcript abundance corresponding to these four putative aquaporin genes in leaves with light-induced high hydraulic conductance (exposed to high irradiance) compared to leaves with low hydraulic conductance (exposed to low irradiance). However, in sun leaves that were exposed to different light levels prior to leaf collection (full sunlight, shade, and covered with aluminium foil for 16 h), the relative transcript levels of two of the putative aquaporin genes increased several-fold in shaded leaves compared to the sun-exposed or covered leaves. When the leaves were pressure-infiltrated with the apoplastic tracer dye trisodium 3-hydroxy-5,8,10-pyrenetrisulphonate (PTS3, 0.02%), there was no change in the PTS3 concentration of leaf exudates collected in ambient light or in high irradiance, but there was a small apoplastic acidification. There was also no change in PTS3 concentration between the leaves infiltrated under high irradiance with 0.02% PTS3 or with 0.1 mM HgCl2 in 0.02% PTS3. The results suggest that the putative aquaporin genes that were identified in the present study probably do not play a role in the light responses of hydraulic conductance at the transcript level, but they may function in regulating water homeostasis in leaves adapted to different light conditions. In addition, it is shown that high irradiance induced changes in the pH of the apoplast and that there does not appear to be a significant shift to the cell-to-cell mediated water transport in bur oak leaves exposed to high irradiance as measured by the apoplastic tracer dye.

Aquaporins: Highly Regulated Channels Controlling Plant Water Relations

“…This has indicated no change in apoplastic flow in response to light (see below) in Quercus macrocarpa or Populus tremuloides (Voicu et al, 2009;Voicu and Zwiazek, 2010), while in grapevine a greater degree of apoplastic flow was observed with drought treatment that corresponded to reduced K leaf and reduced inhibition of K leaf by mercury (Pou et al, 2013). Switching of water pathways involving apoplastic and symplastic transport may allow for some flexibility in responses to water stress (Morillon and Chrispeels, 2001).…”

“…Contributions from apoplast versus symplast flow in leaves can also be made using specific fluorescent tracer dyes (Voicu et al, 2009;Pou et al, 2013). This has indicated no change in apoplastic flow in response to light (see below) in Quercus macrocarpa or Populus tremuloides (Voicu et al, 2009;Voicu and Zwiazek, 2010), while in grapevine a greater degree of apoplastic flow was observed with drought treatment that corresponded to reduced K leaf and reduced inhibition of K leaf by mercury (Pou et al, 2013).…”

“…In J. regia, the rapid response in K leaf correlates with increase in transcript of both PIP2 and PIP1 isoforms and is blue light dependent but unrelated to stomatal aperture (Cochard et al, 2007;Baaziz et al, 2012). The effect of light on K leaf and aquaporin expression is not always observed (Scoffoni et al, 2008;Voicu et al, 2009;Rockwell et al, 2011). There is an interaction with dehydration (Guyot et al, 2012), and anoxia can reduce K leaf (Rockwell et al, 2011) as it does in roots.…”

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

“…This corresponds to average 16% and 31% enhancements of K leaf , respectively, across the eight species in our data set for which we measured K ox . These effects could contribute to the observed effects of light on K leaf , in addition to other mechanisms such as increased aquaporin activity (Cochard et al, 2007;Scoffoni et al, 2008;Voicu et al, 2009). Second, a major role for vapor transport implies that a great deal of water may evaporate from cells deep within the leaf.…”

Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins

“…Light-dependent hydraulic conductance of leaves has tentatively been associated with the transcriptional regulation of two PIP homologs in walnut (Juglans regia) (Cochard et al, 2007). However, no such regulation was found in bur oak (Quercus macrocarpa) (Voicu et al, 2009), and an aquaporin-independent response of shoot hydraulics to irradiance has been reported in laurel (Laurus nobilis) (Nardini et al, 2010). Combined physiological and genetic studies can be used to dissect the role of individual aquaporin genes in plant water transport (Javot et al, 2003;Da Ines et al, 2010;Postaire et al, 2010;Péret et al, 2012).…”