Ectopic expression of a rice plasma membrane intrinsic protein (OsPIP1;3) promotes plant growth and water uptake

Abstract

Plasma membrane intrinsic proteins (PIPs) are known to be major facilitators of the movement of a number of substrates across cell membranes. From a drought-resistant cultivar of Oryza sativa (rice), we isolated an OsPIP1;3 gene single-nucleotide polymorphism (SNP) that is mostly expressed in rice roots and is strongly responsive to drought stress. Immunocytochemistry showed that OsPIP1;3 majorly accumulated on the proximal end of the endodermis and the cell surface around the xylem. Expression of GFP-OsPIP1;3 alone in Xenopus oocytes or rice protoplasts showed OsPIP1;3 mislocalization in the endoplasmic reticulum (ER)-like neighborhood, whereas co-expression of OsPIP2;2 recruited OsPIP1;3 to the plasma membrane and led to a significant enhancement of water permeability in oocytes. Moreover, reconstitution of 103His-OsPIP1;3 in liposomes demonstrated water channel activity, as revealed by stopped-flow light scattering. Intriguingly, by patch-clamp technique, we detected significant NO 3 À conductance of OsPIP1;3 in mammalian cells. To investigate the physiological functions of OsPIP1;3, we ectopically expressed the OsPIP1;3 gene in Nicotiana benthamiana (tobacco). The transgenic tobacco plants exhibited higher photosynthesis rates, root hydraulic conductivity (Lp r ) and water-use efficiency, resulting in a greater biomass and a higher resistance to water deficit than the wild-type did. Further experiments suggested that heterologous expression of OsPIP1;3 in cyanobacterium altered bacterial growth under different conditions of CO 2 gas supply. Overall, besides shedding light on the multiple functions played by OsPIP1;3, this work provides insights into the translational value of plant AQPs.

Aquaporins are main contributors to root hydraulic conductivity in pearl millet [Pennisetum glaucum (L) R. Br.]

“…These findings support the observations of [31]. More recently, overexpression of rice OsPIP1-3 enhanced water use efficiency in transgenic tobacco plants [19]. However, this response may well be linked to higher photosynthesis rates due to improved nitrate uptake and transport rather than hydraulics.…”

“…For instance, the F-H-T-R signature observed in the PgPIP (Table 2), which seems strictly conserved across PIP from different species, has been associated with water and H 2 O 2 permeability [14,26,27,63]. Furthermore, PgPIP1-3 carries the same ar/R motif and similar Froger's residues as OsPIP1-3, which has been recently shown to transport nitrate (NO 3 − ) [19]. The H-I-G-R signature observed in PgTIP2-1, PgTIP2-2 and PgTIP2-3, that is conserved in TIP2 from Arabidopsis, maize and rice, supposedly allows permeability to water, NH 3 , urea and H 2 O 2 .…”

“…) and carbon dioxide (CO 2 ), some TIP isoforms to ammonia (NH 3 ) and urea, and some NIP to small organic solutes or mineral nutrients [14][15][16][17][18][19]. AQP possess wide range of physiological functions and have now been identified in a number of crop species such as rice, maize, tomato, cotton, sorghum, foxtail millet, watermelon and cannabis [20][21][22][23][24][25].…”

Phosphorylation influences water and ion channel function of AtPIP2;1

“…Aquaporins are membrane‐bound channel proteins that facilitate the passive bidirectional movement of water and other small molecules across biological membranes (Chaumont & Tyerman, 2017). Substrates currently known to be transported by aquaporins include gases (O 2 ; Zwiazek et al, 2017, CO 2 ; Otto et al, 2010; Uehlein, Lovisolo, Siefritz, & Kaldenhoff, 2003; Uehlein et al, 2012), metalloids (silicon; Ma et al, 2006, boron; Takano et al, 2006, arsenic; Li et al, 2009), reactive oxygen species (H 2 O 2 ; Bienert et al, 2007; Dynowski, Schaaf, Loque, Moran, & Ludewig, 2008a; Hooijmaijers et al, 2012; Rodrigues et al, 2017), monovalent ions (Na + ; Byrt et al, 2017; Kourghi et al, 2017; Weaver, Shomer, Louis, & Roberts, 1994; NO 3 − ; Liu et al, 2020), and other neutral substrates (urea; Dynowski, Mayer, Moran, & Ludewig, 2008b, glycerol; Gerbeau, Guclu, Ripoche, & Maurel, 1999, ammonia; Loqué, Ludewig, Yuan, & von Wirén, 2005). As facilitators of transmembrane water transport, members of the Plasma membrane Intrinsic Protein (PIP) subfamily have roles in mediating water uptake at the root–soil interface, in transcellular water flow, and in regulating hydraulic conductivity in response to abiotic stresses (for reviews, see Chaumont & Tyerman, 2014; Maurel et al, 2015; Gambetta, Knipfer, Fricke, & McElrone, 2017).…”

A Survey of Barley PIP Aquaporin Ionic Conductance Reveals Ca2+-Sensitive HvPIP2;8 Na+ and K+ Conductance

“…Anion and cation transport properties have been reported for subsets of plant PIPs when expressed and tested in heterologous systems. For example, the rice ( Oryza sativa ) OsPIP1;3, which is upregulated in roots under drought stress, has recently been shown to be able to transport nitrate anions when expressed in mammalian HEK293 cells, and to also function as a water channel [ 10 ]. This aquaporin may be orthologous to the animal AQP6 that shows anion transport activity, though normally not water channel activity [ 11 ].…”