title: The Apoplastic Copper AMINE OXIDASE1 Mediates Jasmonic Acid-Induced Protoxylem Differentiation in Arabidopsis Roots.
abstract: Polyamines are involved in key developmental processes and stress responses. Copper amine oxidases oxidize the polyamine putrescine (Put), producing an aldehyde, ammonia, and hydrogen peroxide (H2O2). The Arabidopsis (Arabidopsis thaliana) amine oxidase gene At4g14940 (AtAO1) encodes an apoplastic copper amine oxidase expressed at the early stages of vascular tissue differentiation in roots. Here, its role in root development and xylem differentiation was explored by pharmacological and forward/reverse genetic approaches. Analysis of the AtAO1 expression pattern in roots by a promoter::green fluorescent protein-β-glucuronidase fusion revealed strong gene expression in the protoxylem at the transition, elongation, and maturation zones. Methyl jasmonate (MeJA) induced AtAO1 gene expression in vascular tissues, especially at the transition and elongation zones. Early protoxylem differentiation was observed upon MeJA treatment along with Put level decrease and H2O2 accumulation in wild-type roots, whereas Atao1 loss-of-function mutants were unresponsive to the hormone. The H2O2 scavenger N,N(1)-dimethylthiourea reversed the MeJA-induced early protoxylem differentiation in wild-type seedlings. Likewise, Put, which had no effect on Atao1 mutants, induced early protoxylem differentiation in the wild type, this event being counteracted by N,N(1)-dimethylthiourea treatment. Consistently, AtAO1-overexpressing plants showed lower Put levels and early protoxylem differentiation concurrent with H2O2 accumulation in the root zone where the first protoxylem cells with fully developed secondary wall thickenings are found. These results show that the H2O2 produced via AtAO1-driven Put oxidation plays a role in MeJA signaling leading to early protoxylem differentiation in root.
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Sandip A
authors.initials: SA
authors.lastname: Ghuge
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Andrea
authors.initials: A
authors.lastname: Carucci
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Renato A
authors.initials: RA
authors.lastname: Rodrigues-Pousada
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Alessandra
authors.initials: A
authors.lastname: Tisi
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Stefano
authors.initials: S
authors.lastname: Franchi
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Paraskevi
authors.initials: P
authors.lastname: Tavladoraki
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.).
authors.forename: Riccardo
authors.identifier: http://orcid.org/0000-0002-1399-1187
authors.initials: R
authors.lastname: Angelini
authors.affiliation: Dipartimento di Scienze, Università degli Studi Roma Tre, 00146 Rome, Italy (S.A.G., A.Ca., A.T., S.F., P.T., R.A., A.Co.);Department of Life, Health, and Environmental Sciences, Università dell'Aquila, 67100 L'Aquila, Italy (R.A.R.-P.); andIstituto Nazionale Biostrutture e Biosistemi, 00136 Rome, Italy (P.T., R.A., A.Co.) alessandra.cona@uniroma3.it.
authors.forename: Alessandra
authors.initials: A
authors.lastname: Cona
mesh_terms: D000085:Acetates / Q000494:pharmacology; D006631:Amine Oxidase (Copper-Containing) / Q000235:genetics / Q000378:metabolism*; D017360:Arabidopsis / Q000166:cytology / Q000187:drug effects / Q000201:enzymology* / Q000235:genetics; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism*; D002454:Cell Differentiation / Q000187:drug effects*; D003300:Copper / Q000378:metabolism*; D003517:Cyclopentanes / Q000494:pharmacology*; D018506:Gene Expression Regulation, Plant / Q000187:drug effects; D006861:Hydrogen Peroxide / Q000378:metabolism; D009154:Mutation / Q000235:genetics; D054883:Oxylipins / Q000494:pharmacology*; D018517:Plant Roots / Q000166:cytology* / Q000187:drug effects / Q000254:growth & development; D030821:Plants, Genetically Modified; D011700:Putrescine / Q000378:metabolism; D013890:Thiourea / Q000031:analogs & derivatives / Q000494:pharmacology; D052584:Xylem / Q000166:cytology* / Q000187:drug effects
chemical_list: D000085:Acetates; D029681:Arabidopsis Proteins; D003517:Cyclopentanes; D054883:Oxylipins; C011006:jasmonic acid; D003300:Copper; C038983:1,3-dimethylthiourea; C072239:methyl jasmonate; D006861:Hydrogen Peroxide; C000605231:AO1 copper amine oxidase, Arabidopsis; D006631:Amine Oxidase (Copper-Containing); D013890:Thiourea; D011700:Putrescine