Press Releases
Sep. 1, 2011

First elucidation of the Biological Role of the Proton-pyrophosphatase (H+-PPase) in plants

Presenters
  • Hirokazu Tsukaya (Graduate School of Science, The University of Tokyo)
  • Ali Ferjani (Department of Biology, Tokyo Gakugei University)
  • Gorou Horiguchi (Department of Life Science, Rikkyo University)
  • Masayoshi Maeshima (Graduate School of Bioagricultural Sciences, Nagoya University)
  • Shoji Segami (Graduate School of Bioagricultural Sciences, Nagoya University)
  • Yukari Muto (Graduate School of Bioagricultural Sciences, Nagoya University,
    current affiliation: Showa Sangyo Co., Research and Development Center)

Abstract

ATP provides the energy for most of the energy-consuming activities of the cell in all living organisms. ATP is hydrolyzed within the cell into two ways, either to produce (ADP + Pi) or (AMP + PPi), and energy. Pyrophosphate (PPi), being toxic to the cell itself at high levels, is efficiently hydrolyzed by enzymes called pyrophosphatases (PPases). In plants, unlike animals or yeast, there is no cytosolic PPases, instead a unique vacuolar membrane bound H+-PPase is responsible for PPi degradation and vacuole acidification as well. A previous report claimed that the latter function, namely the vacuolar acidification, is the major role of this PPase.

Here, we discovered that upon seed germination, seedlings of the H+-PPase defective fugu5 mutant failed to produce sucrose from lipid stores due to high cytosolic PPi, which is released by active metabolism in imbibed seeds. The addition of sucrose or specific removal of cytosolic PPi in the fugu5 mutant, by the expression of the yeast cytosolic PPase IPP1, rescued both cellular and morphological phenotypes of fugu5 (Figure 1). Therefore, in contrast to the previous belief that favored a major role of plant H+-PPase as a proton pump, here we suggest based on solid evidence, that the removal of PPi is the central role of the plant H+-PPase.

Importantly, the growth of the transgenic lines was significantly improved (AVP1pro:IPP1 ; Figure 1 bottom panels), suggesting that the IPP1 gene may represent a powerful tool for genetic engineering of plants with higher yield and increased biomass production.

Paper information

Title:
Keep an Eye on PPi: The Vacuolar-Type H+-Pyrophosphatase Regulates Postgerminative Development in Arabidopsis.
Author:
Ferjani, A., Segami, S., Horiguchi, G., Muto, Y., Maeshima, M., & Tsukaya, H.
Journal:
Plant Cell (DOI: 10.1105/tpc.111.085415, published online on 29 August 2011)
Figure 1

Figure 1. Arabidopsis fugu5 mutant is defective in the vacuolar H+-PPase AVP1. In the absence of an exogenous nutrient source (sucrose), fugu5 mutant cotyledons display altered morphology (top panels) plus changes in cell size and number. Expression of the yeast cytosolic PPase IPP1 rescued both the morphological phenotype (bottom panels) and cellular abnormalities. Bar = 2 mm.

Figure 2

Supplement. Gluconeogenesis is a hot spot for PPi production. Fatty acids from triacylglycerol are converted to acetyl-CoA by β-oxidation and then to succinate by the glyoxylate cycle operating in glyoxysomes. PPi is generated by the reaction of fatty acyl-CoA synthase (a). During gluconeogenesis from phosphoenolpyruvate, PPi is generated by the reaction of PPi-dependent phosphofructokinase (b). PPi is also produced by the reaction of UDP-Glc pyrophosphorylase (c), which provides UDP-Glc. Syntheses of macromolecules such as DNA, RNA, proteins and cellulose also generate PPi as a by-product (d). PPi in the cytosol is consumed by H+-PPase/AVP1/FUGU5.