White Lupin Cluster Root Acclimation to Phosphorus Deficiency and Root Hair Development Involve Unique Glycerophosphodiester Phosphodiesterases    

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.

Genetic Manipulation of a “Vacuolar” H+-PPase: From Salt Tolerance to Yield Enhancement under Phosphorus-Deficient Soils

“…This observed vigorous root development displayed by AtAVP1-OX plants under Pi limitation resembles, somewhat, the behavior of white lupin (Lupinus albus), a noted Pi scavenger. As part of a complex response to limiting Pi, white lupin develops proteoid roots (densely clustered lateral roots with abundant root hairs) that significantly enhance both the surface area for Pi uptake and rhizosphere acidification capacity (Yan et al, 2002;Cheng et al, 2011). Of particular note is the fact that AtAVP1-OX plants displayed a stronger root acidification capacity than control plants when challenged with Pi limitation (Yang et al, 2007).…”

Phosphate homeostasis in the yeast Saccharomyces cerevisiae, the key role of the SPX domain‐containing proteins

“…Of note, despite lacking the SPX domain, two glycerophosphodiester phosphodiesterases have recently been involved in maintaining cellular phosphate homeostasis in plants [63,64].…”

An RNA-Seq Transcriptome Analysis of Orthophosphate-Deficient White Lupin Reveals Novel Insights into Phosphorus Acclimation in Plants

“…One of the most studied is the formation of cluster roots, which are closely spaced tertiary lateral rootlets that resemble bottle brushes (Neumann and Martinoia, 2002;Vance et al, 2003;Shane and Lambers, 2005;Neumann, 2010;Lambers et al, 2011). White lupin (Lupinus albus), which forms cluster roots, has become a model plant for the study of P i acquisition due to its exceptional ability to acquire nutrients unavailable to most other plants (Neumann and Martinoia, 2002;Vance et al, 2003;Tian et al, 2009;Zhu et al, 2009;Cheng et al, 2011aCheng et al, , 2011b. Cluster roots increase the root surface area for enhanced P i absorption and exude organic anions (Johnson et al, 1996;Massonneau et al, 2001;Sas et al, 2001;Wang et al, 2007) and acid phosphatases (Gilbert et al, 1999;Miller et al, 2001) that release P i from sparingly soluble inorganic and organic compounds.…”

“…The complex network of regulatory genes necessary to sense and respond to P i deficiency has only recently been addressed. Regulatory components identified so far include transcription factors (TFs), SPX (for SYG1, Pho81, XPR1) subfamily proteins, plant hormones, noncoding RNAs, and protein modifiers, including proteins involved in SUMOylation, phosphorylation, dephosphorylation, protein translocation, and epigenetic modifications (Nilsson et al, 2010;Smith et al, 2010;Yang and Finnegan, 2010;Cheng et al, 2011aCheng et al, , 2011bChiou and Lin, 2011;Kuo and Chiou, 2011).…”