Transpiration from shoots triggers diurnal changes in root aquaporin expression

Climate Change Research Team, National Agricultural Research Center for Tohoku Region, Morioka, Japan.
Plant Cell and Environment (Impact Factor: 6.96). 03/2011; 34(7):1150-63. DOI: 10.1111/j.1365-3040.2011.02313.x
Source: PubMed


Root hydraulic conductivity (Lp(r)) 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 12h light/12h dark regime, Lp(r) 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 2h after light initiation. When darkness was extended for 12h 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 Lp(r) during the day.

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    • "This highlights the need for genome-wide studies on the expression of aquaporins in relation to water status in field-grown plants in order to drive a more informative and precise conclusion on how to manipulate aquaporin genes to improve plant productivity. Sakurai-Ishikawa et al. [45] have shown that most of root aquaporins in rice were upregulated during periods of high transpiration demand (beginning of the light period) probably to maintain a positive plant water status. However, the relevance of this information to plant responses in the field is limited because the authors grew the plants under non-saturating conditions of 370 ␮mole m −2 s −1 light intensity and 75% relative humidity (RH), where stomatal depression did not occur but rather the rates of transpiration increased progressively during the whole light period. "
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    ABSTRACT: This study aimed at specifying the reasons of unbalanced water relations of rice in the field at midday which results in slowing down photosynthesis and reducing water use efficiency (WUE) in japonica and indica rice under well-watered and droughted conditions. Leaf relative water content (RWC) decreased in the well-watered plants at midday in the field, but more dramatically in the droughted indica (75.6 and 71.4%) than japonica cultivars (85.5 and 80.8%). Gas exchange was measured at three points during the day (9:00, 13:00 and 17:00). Leaf internal CO2 (Ci) was not depleted when midday stomatal depression was highest indicating that Ci was not limiting to photosynthesis. Most aquaporins were predominantly expressed in leaves suggesting higher water permeability in leaves than in roots. The expression of leaf aquaporins was further induced by drought at 9:00 without comparable responses in roots. The data suggests that aquaporin expression in the root endodermis was limiting to water uptake. Upon removal of the radial barriers to water flow in roots, transpiration increased instantly and photosynthesis increased after 4 h resulting in increasing WUE after 4 h, demonstrating that WUE in rice is largely limited by the inadequate aquaporin expression profiles in roots.
    Plant Science 10/2014; 227. DOI:10.1016/j.plantsci.2014.08.006 · 3.61 Impact Factor
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    • "Applying a shoots-topping treatment to grapevine and soybean plants, Vandeleur et al. (2014) observed a significant reduction in root hydraulic conductance that mediated by changes in AQP expression and activity, and proposed a hydraulic signal propagated rapidly from shoots to roots potentially because of the decline of plant transpiration and the release of xylem tension. It has been shown that alterations of leaf transpiration may trigger rapid changes in root hydraulics across multiple species (Vandeleur et al. 2009; Kudoyarova et al. 2011; Sakurai-Ishikawa et al. 2011). We found no significant differences in Lprc measured on excised root segments and roots of intact plants (Supporting Information Fig. S1), indicating the changes in root hydraulics caused by shoot decapitation may not involve changes in Lprc (Vandeleur et al. 2014), at least within the time (10 min) of the cell pressure probe measurements in the present study. "
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    ABSTRACT: It has long been recognized that inhibition of plant water transport by either osmotic stress or salinity is mediated by aquaporins (AQPs), but the function and regulation of AQPs are highly variable among distinct isoforms and across different species. In this study, cucumber seedlings were subjected to PEG or NaCl stress for duration of 2h or 24h. The 2h treatment with PEG or NaCl had non-significant effect on the expression of plasma membrane AQP (CsPIPs) in roots, indicating the decrease in hydraulic conductivity of roots (Lpr) and root cells (Lprc) measured in these conditions were due to changes in AQP activity. After both 2h and 24h PEG or NaCl exposure, the decrease in hydraulic conductivity of leaves (Kleaf) and leaf cells (Lplc) could be attributed to a down-regulation of the two most highly expressed isoforms, CsPIP1;2 and CsPIP2;4. In roots, both Lpr and Lprc were further reduced after 24h PEG exposure, but partially recovered after 24h NaCl treatment, which were consistent with changes in the expression of CsPIP genes. Overall, the results demonstrated differential responses of CsPIPs in mediating water transport of cucumber seedlings, and the regulatory mechanisms differed according to applied stresses, stress durations, and specific organs.
    Plant Cell and Environment 03/2014; 38(3). DOI:10.1111/pce.12319 · 6.96 Impact Factor
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    • "The Output graph summarizes observations from various plants (Vandeleur et al., 2014). Increased transpiration increases root aquaporin expression and activity and L pr (Levin et al., 2009; Sakurai-Ishikawa et al., 2011; Laur and Hacke, 2013), and the signal may be an increase in xylem tension that is rapidly transmitted to roots (McElrone et al., 2007); alternatively, phloem ABA may increase and stimulate root aquaporin activity (Kudoyarova et al., 2011). The method of signal transduction is unknown. "
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    ABSTRACT: Plant growth and development are dependent on tight regulation of water movement. Water diffusion across cell membranes is facilitated by aquaporins that provide plants with the means to rapidly and reversibly modify water permeability. This is done by changing aquaporin density and activity in the membrane, including post-translational modifications and protein interaction that act on their trafficking and gating. At the whole organ level aquaporins modify water conductance and gradients that impact on whole plant water flow, and are used to cope with ever-changing environmental conditions. Molecular, physiological, and biophysical approaches have demonstrated that variations in root and leaf hydraulic conductivity can be accounted for by aquaporins but this must be integrated with anatomical considerations. It is becoming evident that stomatal regulation is not paramount in controlling plant water status. This Update integrates these data and emphasizes the central role played by aquaporins in regulating plant water relations.
    Plant physiology 01/2014; 164(4). DOI:10.1104/pp.113.233791 · 6.84 Impact Factor
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