Vacuolar H+-Translocating Pyrophosphatase Is Induced by Anoxia or Chilling in Seedlings of Rice

Abstract

Many plants are subjected to temporary anoxia or hypoxia as a result of flooding, waterlogging, or ice encasement. Among crop plants, rice (Oryza sativa L.) is the most tolerant of anoxic conditions (Mocquot et al., 1981), and corn (Zea mays L.) is also moderately tolerant (Johnson et al., 1989). In seedlings of these species, a number of metabolic changes have been observed in response to hypoxia, and evidence has been presented that at least some of these responses are adaptive, i.e. they increase the ability of the plant to survive the stress (Johnson et al., 1989). In anoxic conditions, cessation of oxidative phosphorylation typically results in a marked decrease in ATP levels (Raymond et al., 1985). This can be alleviated in tolerant species by an increase in alcoholic, lactic, and other fermentation pathways (Kennedy et al., 1992; Menegus et al., 19931, and many of the proteins induced by hypoxia are enzymes of these glycolytic pathways (Bailey-Serres et al., 1988). Chilling likewise creates energy stress (Stewart and Guinn, 1969) due to mitochondrial dysfunction (Lyons and Raison, 1970), and like hypoxia chilling induces alcohol dehydrogenase in corn and rice seedlings (Christie et al., 1991). 1-514-398-5069. 1As an additional adaptation to energy stress, glycolytic enzyme reactions consuming ATP can be at least partially replaced by reactions utilizing PPi as an energy source. In rice, anoxia induces an increase in SUC synthase (Ricard et al., 1991) as well as an increase in PPi:Fru-6-P l-phosphotransferase but not phosphofructokinase (Mertens et al., 1990). Since anoxia also induces an increase in Fru-2,6-bisphosphate (Mertens et al., 1990), which activates PPi: Fru-6-P 1-phosphotransferase in the glycolytic rather than the reverse direction (Enomoto et al., 1992), these effects of anoxia favor glycolytic pathways utilizing PPi over those consuming ATP. In corn, it has been noted that, although many glycolytic enzymes are induced by hypoxia, none of these are kinases (Bailey-Serres et al., 1988). Cytosolic PPi levels seem to be independent of those of ATP (Dancer et al., 1990) and unaffected by anoxic stress (Dancer and ap Rees, 1989). Moreover, the cytoplasmic acidification that commonly results from anaerobic metabolism tends to increase the free energy of hydrolysis of PPi but has the opposite effect on the free energy of ATP hydrolysis (Davies et al., 1993). It appears therefore that PPi metabolism may play an important role in plant adaptation to anoxia.The V-PPase (Rea and Poole, 1993) represents another enzyme that might advantageously replace an ATP-consuming one (the V-ATPase) in anoxia or chilling stress. These parallel proton pumps are ubiquitous in the plant kingdom, although present in differing proportions in various tissues and species. The reaction stoichiometries of the two enzymes (Davies et al., 1992;Schmidt and Briskin, 1993) permit them to generate approximately equal proton gradients (Hedrich et al., 1989) across the vacuolar membrane, and calculations of free energy changes (Davie...

Proton Transport in Maize Tonoplasts Supported by Fructose-1,6-Bisphosphate Cleavage. Pyrophosphate-Dependent Phosphofructokinase as a Pyrophosphate-Regenerating System

“…A simultaneous up-regulation in the levels of H ϩ -PPase and PFP have been detected during anoxia in rice (Oryza sativa) seedlings (Mertens et al, 1990;Carystinos et al, 1995;Drew, 1997). Table I shows that the levels of PFP and H ϩ -PPase activities detected in different plants (Hajirezaei et al, 1994;Nielsen and Stitt, 2001) were sufficient in our assays to promote the formation of a H ϩ gradient.…”

The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development

“…Although DET3 appears to be a single-copy gene, we cannot exclude functional redundancy due to the presence of the H + -pyrophosphatase, a second proton pump specific to plants and phototrophic bacteria (Rea and Poole 1993). For instance, in det3 roots the H + -pyrophosphatase, which is highly active under anoxic conditions (Carystinos et al 1995), could be responsible for the lack of a strong root growth phenotype. Finally, we have shown that the hypocotyl elongation defect is conditional and most likely due to an increased V-ATPase assembly that is at least partially independent of the presence of DET3.…”

Transcript Profiling of the Anoxic Rice Coleoptile

“…PPi is also needed for the activity of the PPi-dependent vacuolar H 1 translocase (H 1 -PPase; Fig. 2; Carystinos et al, 1995). Activity of PEP carboxylase (PEPC) is repressed under anoxia (Fig.…”