Members of rice plasma membrane intrinsic proteins subfamily are involved in arsenite permeability and tolerance in plants

Abstract

Rice accumulates high level of arsenic (As) in its edible parts and thus plays an important role in the transfer of As into the food chain. However, the mechanisms of As uptake and its detoxification in rice are not well understood. Recently, members of the Nodulin 26-like intrinsic protein (NIP) subfamily of plant aquaporins were shown to transport arsenite in rice and Arabidopsis. Here we report that members of the rice plasma membrane intrinsic protein (PIP) subfamily are also involved in As tolerance and transport. Based on the homology search with the mammalian AQP9 and yeast Fps1 arsenite transporters, we identified and cloned five rice PIP gene subfamily members. qRT-PCR analysis of PIPs in rice root and shoot tissues revealed a significant down regulation of transcripts encoding OsPIP1;2, OsPIP1;3, OsPIP2;4, OsPIP2;6, and OsPIP2;7 in response to arsenite treatment. Heterologous expression of OsPIP2;4, OsPIP2;6, and OsPIP2;7 in Xenopus laevis oocytes significantly increased the uptake of arsenite. Overexpression of OsPIP2;4, OsPIP2;6, and OsPIP2;7 in Arabidopsis yielded enhanced arsenite tolerance and higher biomass accumulation. Further, these transgenic plants showed no significant accumulation of As in shoot and root tissues in long term uptake assays. Whereas, short duration exposure to arsenite caused both active influx and efflux of As in the roots. The data suggests a bidirectional arsenite permeability of rice PIPs in plants. These rice PIPs genes will be highly useful for engineering important food and biofuel crops for enhanced crop productivity on contaminated soils without increasing the accumulation of toxic As in the biomass or edible tissues.

Roles of Aquaporins in Setaria viridis Stem Development and Sugar Storage

“…We hypothesize that in stem tissues SvPIP2;1 is involved in cell growth and that SvNIP2;2 may facilitate water movement and potentially the flow of other solutes into the apoplasm to sustain solute transportation by bulk-flow, and possibly ‘recycle’ water used for solute delivery back to the xylem. It is expected that SvPIP2;1 could have additional roles, as other PIP water channels have been shown to also be permeable to CO 2 , hydrogen peroxide, urea, sodium and arsenic (Siefritz et al, 2001; Uehlein et al, 2003; Mosa et al, 2012; Bienert and Chaumont, 2014; Byrt et al, 2016b). SvNIP2;2 could have roles such as transporting neutral solutes to the apoplasm, as previous studies report silicic acid, urea, and boric acid permeability for other NIPS (Bienert et al, 2008; Ma et al, 2008; Ma and Yamaji, 2008; Li et al, 2009; Deshmukh et al, 2013).…”

Arabidopsis thaliana NIP7;1 is involved in tissue arsenic distribution and tolerance in response to arsenate

“…The rice aquaporin NIP2;1/Lsi1 can efflux AsIII from rice roots, [18] and enhanced efflux of AsIII was observed in transgenic Arabidopsis roots expressing the rice PIP OsPIP2;6 when treated with AsV [9]. Bidirectional transport of AsIII through NIPs could contribute differentially to AsIII and AsV tolerance and detoxification in plants, and hence, may have implications for As tolerance in crops grown in aerobic soils where AsV predominates.…”

“…Members of the NIP (nodulin-26-like intrinsic proteins) and PIP (plasma membrane intrinsic proteins) subfamilies of aquaporins have been shown to facilitate AsIII transport in plants in Abbreviations NIPs, nodulin-26-like intrinsic proteins; RGR, relative growth rate; WT, wild-type. addition to transporting essential nutrients such as silicon and boron [7][8][9][10][11][12][13].…”

Arsenic translocation in rice cultivation and its implication for human health

“…Certain studies report that As III predominates in 80% of the analyzed sap samples in different rice species, including in those grown in As V -rich soils; this suggests that reduction occurs in the root cells before passing to the xylem and the rest of the plant parts (Su et al, 2010). Other studies demonstrate the role played by the rice plasma membrane intrinsic proteins (OsPiP) in the permeability of As III (Mosa et al, 2012).…”