title: Keep an eye on PPi: the vacuolar-type H+-pyrophosphatase regulates postgerminative development in Arabidopsis.
abstract: Postgerminative growth of seed plants requires specialized metabolism, such as gluconeogenesis, to support heterotrophic growth of seedlings until the functional photosynthetic apparatus is established. Here, we show that the Arabidopsis thaliana fugu5 mutant, which we show to be defective in AVP1 (vacuolar H(+)-pyrophosphatase), failed to support heterotrophic growth after germination. We found that exogenous supplementation of Suc or the specific removal of the cytosolic pyrophosphate (PPi) by the heterologous expression of the cytosolic inorganic pyrophosphatase1 (IPP1) gene from budding yeast (Saccharomyces cerevisiae) rescued fugu5 phenotypes. Furthermore, compared with the wild-type and AVP1(Pro):IPP1 transgenic lines, hypocotyl elongation in the fugu5 mutant was severely compromised in the dark but recovered upon exogenous supply of Suc to the growth media. Measurements revealed that the peroxisomal β-oxidation activity, dry seed contents of storage lipids, and their mobilization were unaffected in fugu5. By contrast, fugu5 mutants contained ~2.5-fold higher PPi and ~50% less Suc than the wild type. Together, these results provide clear evidence that gluconeogenesis is inhibited due to the elevated levels of cytosolic PPi. This study demonstrates that the hydrolysis of cytosolic PPi, rather than vacuolar acidification, is the major function of AVP1/FUGU5 in planta. Plant cells optimize their metabolic function by eliminating PPi in the cytosol for efficient postembryonic heterotrophic growth.
authors.affiliation: Department of Biology, Tokyo Gakugei University, Koganei-shi, Tokyo 184-8501, Japan. ferjani@u-gakugei.ac.jp
authors.forename: Ali
authors.initials: A
authors.lastname: Ferjani
authors.forename: Shoji
authors.initials: S
authors.lastname: Segami
authors.forename: Gorou
authors.initials: G
authors.lastname: Horiguchi
authors.forename: Yukari
authors.initials: Y
authors.lastname: Muto
authors.forename: Masayoshi
authors.initials: M
authors.lastname: Maeshima
authors.forename: Hirokazu
authors.initials: H
authors.lastname: Tsukaya
mesh_terms: D017360:Arabidopsis / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D018548:Cotyledon / Q000201:enzymology / Q000235:genetics / Q000254:growth & development; D003600:Cytosol / Q000201:enzymology / Q000378:metabolism; D003624:Darkness; D011756:Diphosphates / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant; D018525:Germination; D005943:Gluconeogenesis; D052836:Heterotrophic Processes; D006863:Hydrogen-Ion Concentration; D018546:Hypocotyl / Q000254:growth & development; D043564:Inorganic Pyrophosphatase / Q000235:genetics / Q000378:metabolism*; D009154:Mutation; D010084:Oxidation-Reduction; D020675:Peroxisomes / Q000378:metabolism; D010641:Phenotype; D030821:Plants, Genetically Modified; D012441:Saccharomyces cerevisiae / Q000201:enzymology / Q000235:genetics; D029701:Saccharomyces cerevisiae Proteins / Q000235:genetics / Q000378:metabolism*; D036226:Seedlings / Q000201:enzymology / Q000235:genetics / Q000254:growth & development; D013395:Sucrose / Q000494:pharmacology*; D014617:Vacuoles / Q000201:enzymology* / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D011756:Diphosphates; D029701:Saccharomyces cerevisiae Proteins; C107241:diphosphoric acid; D013395:Sucrose; C505048:AVP1 protein, Arabidopsis; C470575:IPP1 protein, S cerevisiae; D043564:Inorganic Pyrophosphatase