White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases.

Lingyun Cheng,Carroll P Vance,Junqi Liu,Bruna Bucciarelli,Jana Patton-Vogt,Susan Miller,Deborah Allan,Kelly Zinn,Jianbo Shen

doi:10.1104/pp.111.173724

Lingyun Cheng, Carroll P Vance + Show 7 more

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https://doi.org/10.1104/pp.111.173724

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Journal: Plant Physiology	Publication Date: Apr 4, 2011
Citations: 80	License type: CC BY 4.0

Affiliation: United States Department of Agriculture

Abstract

White lupin (Lupinus albus) is a legume that is very efficient in accessing unavailable phosphorus (Pi). It develops short, densely clustered tertiary lateral roots (cluster/proteoid roots) in response to Pi limitation. In this report, we characterize two glycerophosphodiester phosphodiesterase (GPX-PDE) genes (GPX-PDE1 and GPX-PDE2) from white lupin and propose a role for these two GPX-PDEs in root hair growth and development and in a Pi stress-induced phospholipid degradation pathway in cluster roots. Both GPX-PDE1 and GPX-PDE2 are highly expressed in Pi-deficient cluster roots, particularly in root hairs, epidermal cells, and vascular bundles. Expression of both genes is a function of both Pi availability and photosynthate. GPX-PDE1 Pi deficiency-induced expression is attenuated as photosynthate is deprived, while that of GPX-PDE2 is strikingly enhanced. Yeast complementation assays and in vitro enzyme assays revealed that GPX-PDE1 shows catalytic activity with glycerophosphocholine while GPX-PDE2 shows highest activity with glycerophosphoinositol. Cell-free protein extracts from Pi-deficient cluster roots display GPX-PDE enzyme activity for both glycerophosphocholine and glycerophosphoinositol. Knockdown of expression of GPX-PDE through RNA interference resulted in impaired root hair development and density. We propose that white lupin GPX-PDE1 and GPX-PDE2 are involved in the acclimation to Pi limitation by enhancing glycerophosphodiester degradation and mediating root hair development.

Highlights

White lupin (Lupinus albus) is a legume that is very efficient in accessing unavailable phosphorus (Pi)
We report the following: (1) two white lupin GPX-PDEs (GPXPDE1 and GPX-PDE2) are highly up-regulated by Pi limitation and are expressed in root hair, epidermal, and vascular cells; (2) GPX-PDE2 transcripts show rapid suppression in response to Pi resupply without a change in shoot P status, but GPX-PDE1 is less responsive; (3) GPX-PDEs are affected by photosynthate deprivation, but in opposite manners; (4) GPX-PDE1 complements a yeast gde1D mutant revealing a GPC-PDE function, and recombinant GPX-PDE2 protein has highest activity with GPI but is active with GPC; and (5) RNA interference (RNAi)-mediated knockdown of GPX-PDE1 and GPX-PDE2 impairs root hair development
Multiple alignment of the white lupin GPX-PDE1 and GPX-PDE2 deduced amino acid sequences with known GPX-PDEs showed that both GPX-PDEs have the conserved sequence nE2XD1(X)nH2D2(X)nE3XK]

Summary

Introduction

White lupin (Lupinus albus) is a legume that is very efficient in accessing unavailable phosphorus (Pi). We characterize two glycerophosphodiester phosphodiesterase (GPX-PDE) genes (GPX-PDE1 and GPX-PDE2) from white lupin and propose a role for these two GPX-PDEs in root hair growth and development and in a Pi stress-induced phospholipid degradation pathway in cluster roots Both GPX-PDE1 and GPX-PDE2 are highly expressed in Pi-deficient cluster roots, in root hairs, epidermal cells, and vascular bundles. Upon the development and use of arrays to evaluate gene expression, several studies have noted the enhanced expression of transcripts that annotate as GPX-PDEs (Uhde-Stone et al, 2003; Misson et al, 2005; Morcuende et al, 2007; Muller et al, 2007) Plant GPX-PDE enzyme was first identified in carrot (Daucus carota) cells Both intracellular and extracellular GPX-PDE activities were induced in Pi-deficient cell cultures of carrot, Arabidopsis (Arabidopsis thaliana), and sycamore (Acer pseudoplatanus; Van der Rest et al, 2002). Membrane phospholipid turnover and remodeling of the plasmalemma with galactolipids is well known in Pi-stressed plants (Andersson et al, 2003, 2005; Lee et al, 2003; Rietz et al, 2004, 2010; Misson et al, 2005; Morcuende et al, 2007; Nakamura et al, 2009)

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