Role of Aquaporins in Determining Carbon and Nitrogen Status in Higher Plants

Abstract

Aquaporins (AQPs) are integral membrane proteins facilitating the transport of water and some small neutral molecules across cell membranes. In past years, much effort has been made to reveal the location of AQPs as well as their function in water transport, photosynthetic processes, and stress responses in higher plants. In the present review, we paid attention to the character of AQPs in determining carbon and nitrogen status. The role of AQPs during photosynthesis is characterized as its function in transporting water and CO₂ across the membrane of chloroplast and thylakoid; recalculated results from published studies showed that over-expression of AQPs contributed to 25% and 50% increases in stomatal conductance (g_s) and mesophyll conductance (g_m), respectively. The nitrogen status in plants is regulated by AQPs through their effect on water flow as well as urea and NH₄⁺ uptake, and the potential role of AQPs in alleviating ammonium toxicity is discussed. At the same time, root and/or shoot AQP expression is quite dependent on both N supply amounts and forms. Future research directions concerning the function of AQPs in regulating plant carbon and nitrogen status as well as C/N balance are also highlighted.

Keywords: aquaporins; carbon; nitrogen; transport; uptake.

Figure 1

AQPs (Aquaporins) located in the chloroplast and thylakoid membrane are associated with the facilitation of H₂O, CO₂, and H₂O₂. The figure illustrates the variety of transport functions achieved by aquaporins in the chloroplast, the arrows presented the photosynthesis process briefly. The different aquaporin subclasses and functions are identified at the right of the illustration in distinct colors and shapes. The TIPs (tonoplast intrinsic proteins) were demonstrated to be located in the thylakoid and chloroplast and facilitate the transportation of H₂O in the chloroplast, and the PIP2;1 were recently identified in the Arabidopsis envelope fraction. Still, some uncertain AQPs, such as PIP1;2, PIP1;3, PIP2;4, and PIP2;7 were also detected in envelope membrane preparations in the chloroplast, though they were considered as contaminants—this needs to be clarified in the future. The PIP1s (plasma membrane intrinsic proteins (PIPs), subgroup 1) in Arabidopsis thaliana, tobacco, and maize, and the PIP2s (PIPs, subgroup 2) in rice plant are considered as CO₂ facilitators. Moreover, AQPs facilitate transmembrane diffusion of H₂O₂ with a heterologous expression system, but the related isoforms and evidence need to be studied in the future.

Figure 2

Pathway of CO₂ diffusion to substomatal internal cavities (a) and from there to chloroplasts (b). The presence of PIPs (red) and TIPs (blue) in the plasma membrane and chloroplast envelope facilitated CO₂ transport, and PIPs and TIPs located in the thylakoid implied their role in mediating H₂O transport, which are reviewed in Section 2.2. The bar indicates 1 μm.

Figure 3

The change in photosynthesis rate (P_n), mesophyll conductance (g_m), and stomatal conductance (g_s) in up-regulated AQP (in red) and down-regulated AQP (in black) plants compared with wild type plants. The data were collected from Flexas et al. [7], Uehlein et al. [25], Uehlein et al. [42], Heckwolf et al. [43], Hanba et al. [45], Secchi and Zwieniecki [50], Tsuchihira et al. [51], Kawase et al. [52], Sade et al. [53] and Li et al. [54]. The sample number of each parameter was indicated by n.

Figure 4

Diagrammatic illustration of the water and nitrogen uptake and transport from the soil through the soil to the root (a) and further to the shoot (b). Both water and nitrogen can flow either via apoplast (dotted arrows) or symplast (solid arrows) pathways. NRT1 transporter (in red) is responsible for both NO₃⁻ uptake and radial and long-distance transport, while NRT2 transporter (in green) is only involved in NO₃⁻ uptake. For NH₄⁺, the AMT family represents the major entry pathway for root NH₄⁺ uptake, but the transporters involved in NH₄⁺ xylem loading in the root and unloading in the shoot are unknown. For water, it can flow either via the apoplast or through AQPs via the symplast, and further be transported to the shoot where it is lost to the atmosphere by transpiration from leaves.

Figure 5

Effect of different nitrogen supply amount (a–e) and nitrogen forms (f) on AQP expression in rice root (a,b,f), rice leaf (d,e), and maize root (c). Relative gene expression was presented as the fold change compared to the expression under low N supply (a–e) and NO₃⁻ supply (f). The response of leaf AQPs to N supply was shown in different rice cultivars, “Shanyou 63” (hybrid indica China, d) and “Yangdao 6” (conventional indica China, e). AQP expression in the rice was determined after treatment for 2 weeks (a,d–f) or 24 h (b), and the AQP expression in the maize was averaged from the expression determined after the treatments for 0.5 h, 1 h, 2 h, and 4 h (c). The data were extracted from Ren et al. [85] (a), Wang et al. [88] (b), Gorska and Zwieniecki [86] (c), Ding et al. [39] and Ren et al. [85] (d), Ren et al. [85] (e), Wang et al. [93] and Ding et al. [94] (f).