title: Phloem-Specific Methionine Recycling Fuels Polyamine Biosynthesis in a Sulfur-Dependent Manner and Promotes Flower and Seed Development.
abstract: The Yang or Met Cycle is a series of reactions catalyzing the recycling of the sulfur (S) compound 5'-methylthioadenosine (MTA) to Met. MTA is produced as a by-product in ethylene, nicotianamine, and polyamine biosynthesis. Whether the Met Cycle preferentially fuels one of these pathways in a S-dependent manner remained unclear so far. We analyzed Arabidopsis (Arabidopsis thaliana) mutants with defects in the Met Cycle enzymes 5-METHYLTHIORIBOSE-1-PHOSPHATE-ISOMERASE1 (MTI1) and DEHYDRATASE-ENOLASE-PHOSPHATASE-COMPLEX1 (DEP1) under different S conditions and assayed the contribution of the Met Cycle to the regeneration of S for these pathways. Neither mti1 nor dep1 mutants could recycle MTA but showed S-dependent reproductive failure, which was accompanied by reduced levels of the polyamines putrescine, spermidine, and spermine in mutant inflorescences. Complementation experiments with external application of these three polyamines showed that only the triamine spermine could specifically rescue the S-dependent reproductive defects of the mutant plants. Furthermore, expressing gene-reporter fusions in Arabidopsis showed that MTI1 and DEP1 were mainly expressed in the vasculature of all plant parts. Phloem-specific reconstitution of Met Cycle activity in mti1 and dep1 mutant plants was sufficient to rescue their S-dependent mutant phenotypes. We conclude from these analyses that phloem-specific S recycling during periods of S starvation is essential for the biosynthesis of polyamines required for flowering and seed development.
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany.
authors.forename: Wolfgang
authors.identifier: http://orcid.org/0000-0002-0397-8296
authors.initials: W
authors.lastname: Zierer
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany.
authors.forename: Mohammad R
authors.initials: MR
authors.lastname: Hajirezaei
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany.
authors.forename: Kai
authors.identifier: http://orcid.org/0000-0003-1540-4086
authors.initials: K
authors.lastname: Eggert
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany.
authors.forename: Norbert
authors.identifier: http://orcid.org/0000-0003-4357-2079
authors.initials: N
authors.lastname: Sauer
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany.
authors.forename: Nicolaus
authors.identifier: http://orcid.org/0000-0002-4966-425X
authors.initials: N
authors.lastname: von Wirén
authors.affiliation: Friedrich-Alexander-Universität Erlangen-Nürnberg, Department of Biology, Molecular Plant Physiology, 91058 Erlangen, Germany (W.Z., N.S.); andMolecular Plant Nutrition (M.R.H., K.E., N.v.W.) and Metalloid Transport (B.P.), Department of Physiology and Cell Biology, Leibniz Institute of Plant Genetics and Crop Plant Research (IPK), 06466 Gatersleben, Germany pommerrenig@ipk-gatersleben.de.
authors.forename: Benjamin
authors.identifier: http://orcid.org/0000-0002-7522-7942
authors.initials: B
authors.lastname: Pommerrenig
mesh_terms: D019747:Aldose-Ketose Isomerases / Q000235:genetics / Q000378:metabolism*; D017360:Arabidopsis / Q000166:cytology / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D003839:Deoxyadenosines / Q000378:metabolism; D005030:Ethylenes / Q000378:metabolism; D035264:Flowers / Q000166:cytology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D008715:Methionine / Q000378:metabolism*; D009154:Mutation; D009928:Organ Specificity; D052585:Phloem / Q000166:cytology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D010937:Plant Growth Regulators / Q000378:metabolism*; D011073:Polyamines / Q000378:metabolism; D011700:Putrescine / Q000378:metabolism; D012639:Seeds / Q000166:cytology / Q000235:genetics / Q000254:growth & development / Q000378:metabolism; D013095:Spermidine / Q000378:metabolism; D013096:Spermine / Q000378:metabolism; D013455:Sulfur / Q000378:metabolism*; D013865:Thioglycosides; D013872:Thionucleosides / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D003839:Deoxyadenosines; D005030:Ethylenes; D010937:Plant Growth Regulators; D011073:Polyamines; D013865:Thioglycosides; D013872:Thionucleosides; C001955:5-methylthioribose; D013096:Spermine; C008500:5'-methylthioadenosine; D013455:Sulfur; C036216:ethylene; D008715:Methionine; C577260:5-methylthioribose-1-phosphate isomerase1, Arabidopsis; D019747:Aldose-Ketose Isomerases; D013095:Spermidine; D011700:Putrescine