Do phosphoinositides regulate membrane water permeability of tobacco protoplasts by enhancing the aquaporin pathway?

Xiaohong Ma, Arava Shatil-Cohen, Shifra Ben-Dor, Noa Wigoda, Imara Y. Perera, Yang Ju Im, Sofia Diminshtein, Ling Yu, Wendy F. Boss, Menachem Moshelion, Nava Moran*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

11 Scopus citations

Abstract

Main conclusion: Enhancing the membrane content of PtdInsP2, the already-recognized protein-regulating lipid, increased the osmotic water permeability of tobacco protoplasts, apparently by increasing the abundance of active aquaporins in their membranes. While phosphoinositides are implicated in cell volume changes and are known to regulate some ion channels, their modulation of aquaporins activity has not yet been reported for any organism. To examine this, we compared the osmotic water permeability (Pf) of protoplasts isolated from tobacco (Nicotiana tabacum) cultured cells (NT1) with different (genetically lowered or elevated relative to controls) levels of inositol trisphosphate (InsP3) and phosphatidyl inositol [4,5] bisphosphate (PtdInsP2). To achieve this, the cells were transformed with, respectively, the human InsP3 5-phosphatase (‘Ptase cells’) or human phosphatidylinositol (4) phosphate 5-kinase (‘PIPK cells’). The mean Pf of the PIPK cells was several-fold higher relative to that of controls and Ptase cells. Three results favor aquaporins over the membrane matrix as underlying this excessive Pf: (1) transient expression of the maize aquaporin ZmPIP2;4 in the PIPK cells increased Pf by 12–30 μm s−1, while in the controls only by 3–4 μm s−1. (2) Cytosol acidification—known to inhibit aquaporins—lowered the Pf in the PIPK cells down to control levels. (3) The transcript of at least one aquaporin was elevated in the PIPK cells. Together, the three results demonstrate the differences between the PIPK cells and their controls, and suggest a hitherto unobserved regulation of aquaporins by phosphoinositides, which could occur through direct interaction or indirect phosphoinositides-dependent cellular effects.

Original languageAmerican English
Pages (from-to)741-755
Number of pages15
JournalPlanta
Volume241
Issue number3
DOIs
StatePublished - Mar 2014

Bibliographical note

Publisher Copyright:
© 2014, Springer-Verlag Berlin Heidelberg.

Keywords

  • BY2
  • Lipid
  • Osmotic water permeability coefficient
  • P
  • Signaling
  • Synthetic-biology

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