Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots

Abstract

Low phosphate (Pi) availability is one of the major constraints for plant productivity in natural and agricultural ecosystems. Plants have evolved a myriad of developmental and biochemical mechanisms to increase internal Pi uptake and utilization efficiency. One important biochemical pathway leading to an increase in internal Pi availability is the hydrolysis of phospholipids. Hydrolyzed phospholipids are replaced by nonphosphorus lipids such as galactolipids and sulfolipids, which help to maintain the functionality and structure of membrane systems. Here we report that a member of the Arabidopsis phospholipase D gene family (PLDZ2) is gradually induced upon Pi starvation in both shoots and roots. From lipid content analysis we show that an Arabidopsis pldz2 mutant is defective in the hydrolysis of phospholipids and has a reduced capacity to accumulate galactolipids under limiting Pi conditions. Morphological analysis of the pldz2 root system shows a premature change in root architecture in response to Pi starvation. These results show that PLDZ2 is involved in the eukaryotic galactolipid biosynthesis pathway, specifically in hydrolyzing phosphatidylcholine and phosphatidylethanolamine to produce diacylglycerol for digalactosyldiacylglycerol synthesis and free Pi to sustain other Pi-requiring processes.phosphate starvation ͉ phospholipids ͉ root architecture ͉ sulfolipids P hosphate (Pi) influences virtually all developmental and biochemical processes in plants. Pi is not only a constituent of key cell molecules such as ATP, nucleic acids, and phospholipids, but it is also a pivotal metabolic regulator of many processes including energy transfer, protein activation, and carbon and nitrogen metabolism. However, Pi availability can be one of the major constraints for plant growth in both natural and agricultural ecosystems because of its low mobility and high absorption capacity in the soil. As a response to this limitation, plants have evolved a range of developmental, biochemical, and symbiotic adaptive strategies to cope with low Pi availability (1, 2). In Arabidopsis, a general, 3-fold strategy to cope with low Pi availability has been described. (i) The release and uptake of Pi from external sources that are not readily available for plant uptake. This mechanism includes the transcriptional activation of high-affinity Pi transporters and the excretion of RNases, acid phosphatases, and organic acids (3-5). (ii) Changes in the architecture of the root system that reflect alterations in cell length, root meristem activity, root hair elongation, and an increased number of lateral roots (6, 7). These changes presumably increase the exploratory capacity of the root and the absorptive surface area. (iii) Optimization of Pi utilization due to a wide range of metabolic alterations, and the mobilization of Pi from internal reserves by the hydrolysis of nucleic acids, proteins, and the recycling of Pi from membrane phospholipids.During Pi deprivation, the total content of diverse phospholipids such as phosphatidylcholin...

Quantitative Profiling of Arabidopsis Polar Glycerolipids in Response to Phosphorus Starvation. Roles of Phospholipases Dζ1 and Dζ2 in Phosphatidylcholine Hydrolysis and Digalactosyldiacylglycerol Accumulation in Phosphorus-Starved Plants

“…In addition, the PLDz1 and z2 double knockout displayed shorter primary roots and had a lower concentration of PA in roots than wildtype plants under the same phosphorus-limited conditions. Another study showed that PLDz2 was involved in lipid turnover in a phosphorus-limited condition (Cruz-Ramirez et al, 2006). These results suggest that PLDz1 and z2 play a role in regulating root development in response to phosphorus limitation, but their roles, especially their potential additive roles, in the turnover of phospholipids and galactolipid accumulation during phosphorus starvation have not been investigated prior to this study (to our knowledge).…”

The role of phospholipase D in plant stress responses

“…In contrast, PLD derived PA in animals has been reported to be dephosphorylated by lipid phosphate phosphatases to yield DAG (Pyne, et al, 2005). An intriguing exemption is the proposed function of the ζ-class (PX-PH) PLDs in the plant response to phosphate starvation (Cruz-Ramirez et al, 2006). This work suggests that these animal-like PLDs in plants work together with PA phosphatase to generate free phosphate and DAG.…”

The plasma membrane proteome of Medicago truncatula roots as modified by arbuscular mycorrhizal symbiosis

“…The response of membrane lipid composition to Pi starvation essentially may comprise the degradation of phospholipids to release Pi, and the synthesis of glycolipids as nonphosphorus lipids to substitute for those phospholipids (Siebers et al 2015). The role of phospholipase D in the breakdown of PM phospholipids during phosphate deficiency actually was established in oat and thale cress (Andersson et al 2005;Cruz-Ramírez et al 2006). Likewise, the content of SGs as phosphorous-free glycolipids that replace phospholipids is known to increase in the PM as a response to phosphate starvation (Andersson et al 2005).…”