title: Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance.
abstract: The family of polyamine oxidases (PAO) in Arabidopsis (AtPAO1-5) mediates polyamine (PA) back-conversion, which reverses the PA biosynthetic pathway from spermine and its structural isomer thermospermine (tSpm) into spermidine and then putrescine. Here, we have studied the involvement of PA back-conversion in Arabidopsis salinity tolerance. AtPAO5 is the Arabidopsis PAO gene member most transcriptionally induced by salt stress. Two independent loss-of-function mutants (atpao5-2 and atpao5-3) were found to exhibit constitutively higher tSpm levels, with associated increased salt tolerance. Using global transcriptional and metabolomic analyses, the underlying mechanisms were studied. Stimulation of abscisic acid and jasmonate (JA) biosynthesis and accumulation of important compatible solutes, such as sugars, polyols and proline, as well as TCA cycle intermediates were observed in atpao5 mutants under salt stress. Expression analyses indicate that tSpm modulates the transcript levels of several target genes, including many involved in the biosynthesis and signalling of JA, some of which are already known to promote salinity tolerance. Transcriptional modulation by tSpm is isomer-dependent, thus demonstrating the specificity of this response. Overall, we conclude that tSpm triggers metabolic and transcriptional reprogramming that promotes salt stress tolerance in Arabidopsis.
authors.affiliation: Department of Natural Products, Plant Biology and Soil Science, Laboratory of Plant Physiology Faculty of Pharmacy, University of Barcelona, Barcelona, Spain.|Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Xavier
authors.initials: X
authors.lastname: Zarza
authors.affiliation: Department of Natural Products, Plant Biology and Soil Science, Laboratory of Plant Physiology Faculty of Pharmacy, University of Barcelona, Barcelona, Spain.
authors.forename: Kostadin E
authors.initials: KE
authors.lastname: Atanasov
authors.affiliation: Departamento de Biología Vegetal, Facultad de Farmacia, Universidad de Valencia, Burjassot, Spain.
authors.forename: Francisco
authors.initials: F
authors.lastname: Marco
authors.affiliation: Departamento de Ciencias Agrarias y del Medio Natural, Universitat Jaume I, Campus Riu Sec, E-12071, Castelló de la Plana, Spain.
authors.forename: Vicent
authors.initials: V
authors.lastname: Arbona
authors.affiliation: Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias Biológicas, Universidad de Valencia, Burjassot, Spain.
authors.forename: Pedro
authors.initials: P
authors.lastname: Carrasco
authors.affiliation: Max Planck Institute for Molecular Plant Physiology, Golm, Germany.
authors.forename: Joachim
authors.initials: J
authors.lastname: Kopka
authors.affiliation: Department of Agricultural Sciences, Biotechnology and Food Science, Cyprus University of Technology, P.O. Box 50329, Limassol, Cyprus.
authors.forename: Vasileios
authors.initials: V
authors.lastname: Fotopoulos
authors.affiliation: Department of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, Amsterdam, The Netherlands.
authors.forename: Teun
authors.initials: T
authors.lastname: Munnik
authors.affiliation: Departamento de Ciencias Agrarias y del Medio Natural, Universitat Jaume I, Campus Riu Sec, E-12071, Castelló de la Plana, Spain.
authors.forename: Aurelio
authors.initials: A
authors.lastname: Gómez-Cadenas
authors.affiliation: Department of Natural Products, Plant Biology and Soil Science, Laboratory of Plant Physiology Faculty of Pharmacy, University of Barcelona, Barcelona, Spain.
authors.forename: Antonio F
authors.initials: AF
authors.lastname: Tiburcio
authors.affiliation: Department of Natural Products, Plant Biology and Soil Science, Laboratory of Plant Physiology Faculty of Pharmacy, University of Barcelona, Barcelona, Spain.
authors.forename: Rubén
authors.initials: R
authors.lastname: Alcázar
mesh_terms: D000040:Abscisic Acid / Q000378:metabolism; D017360:Arabidopsis / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics* / Q000378:metabolism; D029681:Arabidopsis Proteins / Q000235:genetics* / Q000378:metabolism; D002952:Citric Acid Cycle; D003517:Cyclopentanes / Q000378:metabolism; D020869:Gene Expression Profiling; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D063990:Gene Ontology; D006861:Hydrogen Peroxide / Q000378:metabolism; D007477:Ions; D000073658:Loss of Function Mutation / Q000235:genetics*; D055442:Metabolome; D005810:Multigene Family; D050891:Oxidoreductases Acting on CH-NH2 Group Donors / Q000235:genetics* / Q000378:metabolism; D054883:Oxylipins / Q000378:metabolism; D010641:Phenotype; D025341:Principal Component Analysis; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D055049:Salt Tolerance / Q000235:genetics*; D012964:Sodium / Q000378:metabolism; D012965:Sodium Chloride / Q000494:pharmacology*; D013096:Spermine / Q000031:analogs & derivatives / Q000378:metabolism; D013312:Stress, Physiological / Q000187:drug effects / Q000235:genetics*; D014158:Transcription, Genetic / Q000187:drug effects; D059467:Transcriptome / Q000235:genetics; D000097667:Polyamine Oxidase
chemical_list: D000040:Abscisic Acid; D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D006861:Hydrogen Peroxide; D007477:Ions; D050891:Oxidoreductases Acting on CH-NH2 Group Donors; D054883:Oxylipins; D012333:RNA, Messenger; D012964:Sodium; D012965:Sodium Chloride; D013096:Spermine; C011006:jasmonic acid; C021097:thermospermine; C000624495:PAO5 protein, Arabidopsis; D000097667:Polyamine Oxidase
keywords: jasmonates; metabolomics; polyamines; salt tolerance; thermospermine