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

item CHENG, LINGYUN - China Agricultural University
item Bucciarelli, Bruna
item LIU, JUNQI - University Of Minnesota
item ZINN, KELLY - University Of Minnesota
item Miller, Susan - Sue
item PATTON-VOGT, JANA - Duquesne University
item ALLAN, DEBORAH - University Of Minnesota
item SHEN, JIANBO - China Agricultural University
item Vance, Carroll

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/4/2011
Publication Date: 7/1/2011
Citation: Cheng, L., Bucciarelli, B., Liu, J., Zinn, K., Miller, S.S., Patton-Vogt, J., Allan, D., Shen, J., Vance, C.P. 2011. White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiology. 156(3):1131-1148.

Interpretive Summary: Phosphorus (P) is a critical nutrient for crop growth quantity and quality. Agriculture faces two issues with P fertilizer. Application of too much P fertilizer results in water pollution while insufficient P fertilizer results in poor crop growth. A major goal in agriculture is to improve P acquisition and use by crop plants. White lupin plants grown in P-deficient conditions show many adaptations for acquiring and using P including: formation of large masses of cluster lateral roots; exudation of enzymes from roots that can solubilize bound forms of P; and release of organic acids from roots that liberate unavailable P. In some plant species the internal stored pools of P are recycled under P deficiency. Research reported here investigated whether genes involved in P recycling were activated in white lupin cluster roots grown in P-deficient conditions. We were particularly interested in genes involved in the recycling of phospholipids. We isolated and characterized two genes that encode glycerophosphodiester phosphodiesterases (GPXPDEs) enzymes. We showed that the two GPXPDE genes encode enzymes that have different substrate specificity. One form could degrade glycerophosphoinositol while the other degraded glycerophosphocholine. The genes were most highly expressed in P-deficiency induced cluster lateral roots and that exposure to light was part of the regulation of gene expression. The function of the GPXPDEs appears to be to recycle P and to produce inositol and choline. We also found that if the GPXPDE genes do not work effectively, plant root hair formation is impaired. This research is important because we have found two novel, unique genes that help recycle P in P-deficient plants and that regulate, in part, root hair formation. These genes may be useful in improving P acquisition and use.

Technical Abstract: White lupin (Lupinus albus L.) is a phosphate (Pi) deficiency tolerant legume which 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 a novel 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 not only Pi availability but also amounts of 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 (GPC) while GPX-PDE2 shows activity with glycerophosphoinositol (GPI). Cell free protein extracts from Pi-deficient cluster roots display high GPX-PDE enzyme activity for both GPC and GPI. Knockdown of expression of GPX-PDE through RNAi resulted in impaired root hair development. We propose that white lupin GPX-PDE1 and GPX-PDE2 are involved in the adaptation to Pi-limitation by enhancing glycerophosphodiester degradation and mediating root hair development.