Transpiration from shoots triggers diurnal changes in root aquaporin expression

Abstract

Root hydraulic conductivity (Lpr) and aquaporin amounts change diurnally. Previously, these changes were considered to be spontaneously driven by a circadian rhythm. Here, we evaluated the new hypothesis that diurnal changes could be triggered and enhanced by transpirational demand from shoots. When rice plants were grown under a 12 h light/12 h dark regime, Lpr was low in the dark and high in the light period. Root aquaporin mRNA levels also changed diurnally, but the amplitudes differed among aquaporin isoforms. Aquaporins, such as OsPIP2;1, showed moderate changes, whereas root-specific aquaporins, such as OsPIP2;5, showed temporal and dramatic induction around 2 h after light initiation. When darkness was extended for 12 h after the usual dark period, no such induction was observed. Furthermore, plants under 100% relative humidity (RH) showed no induction even in the presence of light. These results suggest that transpirational demand triggers a dramatic increase in gene expressions such as OsPIP2;5. Immunocytochemistry showed that OsPIP2;5 accumulated on the proximal end of the endodermis and of the cell surface around xylem. The strong induction by transpirational demand and the polar localization suggest that OsPIP2;5 contributes to fine adjustment of radial water transport in roots to sustain high Lpr during the day.

Rapid changes in root hydraulic conductivity and aquaporin expression in rice (Oryza sativaL.) in response to shoot removal – xylem tension as a possible signal

“…These data suggest that OsPIP2;5 not only governs the longer term (hours to days) response of root Lp in rice to changes in transpirational water flow but is also involved in the shorter term response (minutes to hours). Figure 5 summarizes the findings of Ahamed et al (2012), Sakurai-Ishikawa et al (2011) and the present study on rice, and also includes the only comparable study on another plant species, soybean (Glycine max. L) by Vandeleur et al (2014).…”

“…Previous studies (Sakurai et al, 2005(Sakurai et al, , 2008Guo et al, 2006;Sakurai-Ishikawa et al, 2011) and our own preliminary experiments (not shown) on the Bala rice cultivar analysed showed that all three PIP1 genes and all PIP2 genes except OsPIP2;7 and OsPIP2;8 are expressed in roots at significant, or at least reproducibly detectable levels. Therefore, the latter two rice PIP genes were not included in the present analyses.…”

“…The present data provide the most direct evidence so far for the idea that xylem tension is involved in the rapid transcriptional response of root AQPs to sudden changes in the plant transpiration rate (Vandeleur et al, 2014) and that a wounding effect does not play any major role in such a response. Sakurai-Ishikawa et al (2011) concluded for rice that diurnal changes in root AQP expression and Lp are not so much due to a circadian clock but rather to diurnal changes in the transpiration rate, with rates being high (day) at times when root AQP expression and Lp are high. Similarly, Ahamed et al (2012) observed for rice that the increase in root AQP expression and Lp FIG.…”

“…There is increasing evidence which points to a role for AQPs in also regulating the root hydraulic response to rather sudden changes in shoot transpirational water loss or to 'catastrophic' events such as injury and removal of the shoot (Levin et al, 2009;Almeida-Rodriguez et al, 2011;Sakurai-Ishikawa et al, 2011;Vandeleur et al, 2014). Sakurai-Ishikawa et al (2011) reported for rice that the gene expression level of OsPIP2;4 and OsPIP2;5 increased in roots when plants were transferred from high (90 %) to low relative humidity (45 %). The increase in AQP expression occurred parallel to an increase in plant transpiration rate and root water uptake.…”

“…Frensch and Steudle, 1989;Zhu and Steudle, 1991;Steudle and Peterson, 1998;Steudle, 2000;Bramley et al, 2009;Fricke, 2010, 2011;Aroca et al, 2012). There is increasing evidence which points to a role for AQPs in also regulating the root hydraulic response to rather sudden changes in shoot transpirational water loss or to 'catastrophic' events such as injury and removal of the shoot (Levin et al, 2009;Almeida-Rodriguez et al, 2011;Sakurai-Ishikawa et al, 2011;Vandeleur et al, 2014). Sakurai-Ishikawa et al (2011) reported for rice that the gene expression level of OsPIP2;4 and OsPIP2;5 increased in roots when plants were transferred from high (90 %) to low relative humidity (45 %).…”