Attenuation of Phosphate Starvation Responses by Phosphite in Arabidopsis

Abstract

When inorganic phosphate is limiting, Arabidopsis has the facultative ability to metabolize exogenous nucleic acid substrates, which we utilized previously to identify insensitive phosphate starvation response mutants in a conditional genetic screen. In this study, we examined the effect of the phosphate analog, phosphite (Phi), on molecular and morphological responses to phosphate starvation. Phi significantly inhibited plant growth on phosphate-sufficient (2 mm) and nucleic acid-containing (2 mm phosphorus) media at concentrations higher than 2.5 mm. However, with respect to suppressing typical responses to phosphate limitation, Phi effects were very similar to those of phosphate. Phosphate starvation responses, which we examined and found to be almost identically affected by both anions, included changes in: (a) the root-to-shoot ratio; (b) root hair formation; (c) anthocyanin accumulation; (d) the activities of phosphate starvationinducible nucleolytic enzymes, including ribonuclease, phosphodiesterase, and acid phosphatase; and (e) steady-state mRNA levels of phosphate starvation-inducible genes. It is important that induction of primary auxin response genes by indole-3-acetic acid in the presence of growth-inhibitory Phi concentrations suggests that Phi selectively inhibits phosphate starvation responses. Thus, the use of Phi may allow further dissection of phosphate signaling by genetic selection for constitutive phosphate starvation response mutants on media containing organophosphates as the only source of phosphorus.Phosphorus is an essential structural constituent of many biomolecules and plays a pivotal role in energy conservation and metabolic regulation. Inorganic orthophosphate (Pi), the assimilated form of phosphorus, is often a limiting macronutrient in both terrestrial and aquatic ecosystems. As a consequence, assimilation, storage, and metabolism of Pi are highly regulated processes that directly affect plant growth (Theodorou and Plaxton, 1993;Raghothama, 1999). To cope with low Pi availability, plants have evolved sophisticated developmental and metabolic adaptations to enhance Pi acquisition from the rhizosphere. Such strategies include morphological changes in root architecture and associations with symbiotic mycorrhizal fungi to accelerate soil exploration as well as biochemical responses to chemically increase Pi availability from insoluble salt complexes and organophosphates present in recalcitrant soil matter (McCully, 1999;Raghothama, 1999). Despite numerous studies on adaptive responses to Pi limitation, little is known about the underlying molecular processes or regulatory genes that are involved in the Pi starvation response of plants.On the other hand, genetic and molecular studies have provided much insight into the microbial response to Pi limitation. When faced with low Pi availability, both Escherichia coli and Saccharomyces cerevisiae activate a multigene emergency rescue system to scavenge traces of usable phosphorus from the surrounding medium. Both systems are known as a p...

Phosphite accelerates programmed cell death in phosphate-starved oilseed rape ( Brassica napus ) suspension cell cultures

“…With 2 mM Phi, no growth or APase induction occurred following subculture of the B. napus cells into the )Pi medium. This corroborates recent studies documenting the detrimental influence of Phi on )Pi, but not +Pi, vascular plants (including B. napus suspension cells; Carswell et al 1996Carswell et al , 1997Foerster et al 1998;Ticconi et al 2001;Varadarajan et al 2002) andyeast (McDonald et al 2001b). 31 P-NMR spectroscopy has demonstrated substantial intracellular Phi accumulation by )Pi plant and yeast cells cultured in the presence of Phi (Carswell et al 1996;McDonald et al 2001b).…”

“…Although Phi is non-metabolic, it greatly exacerbates the harmful effects of Pi deficiency by specifically preventing the derepression of plant and yeast genes encoding PSI proteins (i.e., APase, high-affinity plasmalemma Pi transporters, etc. ; Carswell et al 1997;Plaxton 1999;McDonald et al 2001aMcDonald et al , 2001bTicconi et al 2001;Abel et al 2002;Varadarajan et al 2002). Phi's prevention of the otherwise massive enhancement of Pi influx capacity that occurs in )Pi B. napus suspension cells provided a rationale for the approx.…”

“…; Plaxton 1999;Abel et al 2002). Although Phi is not a substrate in enzyme-catalyzed phosphoryl transfer reactions, other plant and yeast Pi-binding proteins, such as Pi transporters participating in Pi uptake or signal transduction components involved in sensing Pi status, do not appear to effectively discriminate between the Pi and Phi anions (Carswell et al 1997;McDonald et al 2001b;Ticconi et al 2001;Varadarajan et al 2002). Examination of the influence of Phi on two yeast pho regulon mutants indicated that Phi targets PHO84, a high-affinity Pi transporter and putative component of a Pi-sensor complex (McDonald et al 2001b).…”

“…In fact, low Phi concentrations are quite deleterious to the development of Pi-starved ()Pi), but not Pi-sufficient (+Pi), vascular plants (Carswell et al 1996(Carswell et al , 1997Foerster et al 1998;Ticconi et al 2001;Varadarajan et al 2002) and yeast (Saccharomyces cerevisiae) (McDonald et al 2001b). Phi treatment negates the acclimation of plants and yeast to Pi deficiency by specifically preventing the derepression of genes encoding proteins typical of their Pi starvation response (i.e., repressible acid phosphatase (APase), high-affinity plasmalemma Pi transporters, etc.…”

Alteration in growth and thylakoid membrane lipid composition of Azolla caroliniana under phosphate deficiency

“…Furthermore, Adalberto et al (2004) and KhozinGoldberg and Cohen (2006) reported that under P-deficiency, chlorophyll synthesis was severely retarded in Azolla caroliniana and Monodus subterraneus, respectively. However, Ticconi et al (2001) reported that total chlorophyll content did not significantly differ between Arabidopsis seedlings grown on P-deficient or P-sufficient medium. In present experiments, the decrease in Ch a+b in P-deficient plants was mostly related to the decrease in Chl a.…”