Influence of a phyA Mutation on Polyamine Metabolism in Arabidopsis Depends on Light Spectral Conditions

. 2023 Apr 18 ; 12 (8) : . [epub] 20230418

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid37111912

Grantová podpora
NKFIH K134395 National Research, Development and Innovation Office
NKM-4/2022 Czech-Hungarian Academical Bilateral Grant

The aim of the study was to reveal the influence of phyA mutations on polyamine metabolism in Arabidopsis under different spectral compositions. Polyamine metabolism was also provoked with exogenous spermine. The polyamine metabolism-related gene expression of the wild type and phyA plants responded similarly under white and far-red light conditions but not at blue light. Blue light influences rather the synthesis side, while far red had more pronounced effects on the catabolism and back-conversion of the polyamines. The observed changes under elevated far-red light were less dependent on PhyA than the blue light responses. The polyamine contents were similar under all light conditions in the two genotypes without spermine application, suggesting that a stable polyamine pool is important for normal plant growth conditions even under different spectral conditions. However, after spermine treatment, the blue regime had more similar effects on synthesis/catabolism and back-conversion to the white light than the far-red light conditions. The additive effects of differences observed on the synthesis, back-conversion and catabolism side of metabolism may be responsible for the similar putrescine content pattern under all light conditions, even in the presence of an excess of spermine. Our results demonstrated that both light spectrum and phyA mutation influence polyamine metabolism.

Zobrazit více v PubMed

Poorter H., Niinemets Ü., Ntagkas N., Siebenkäs A., Mäenpää M., Matsubara S., Pons T. A meta-analysis of plant responses to light intensity for 70 traits ranging from molecules to whole plant performance. New Phytol. 2019;223:1073–1105. doi: 10.1111/nph.15754. PubMed DOI

Sharrock R.A. The phytochrome red/far-red photoreceptor superfamily. Genome Biol. 2008;9:230. doi: 10.1186/gb-2008-9-8-230. PubMed DOI PMC

Legris M., Ince Y.Ç., Fankhauser C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nat. Commun. 2019;10:5219. doi: 10.1038/s41467-019-13045-0. PubMed DOI PMC

Sharrock R.A., Clack T. Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol. 2002;130:442–456. doi: 10.1104/pp.005389. PubMed DOI PMC

Fankhauser C. The phytochromes, a family of red/far-red absorbing photoreceptors. J. Biol. Chem. 2001;276:11453–11456. doi: 10.1074/jbc.R100006200. PubMed DOI

Oh S., Warnasooriya S.N., Montgomery B.L. Downstream effectors of light- and phytochrome-dependent regulation of hypocotyl elongation in Arabidopsis thaliana. Plant Mol. Biol. 2013;81:627–640. doi: 10.1007/s11103-013-0029-0. PubMed DOI PMC

Wimalasekera R., Villar C., Begum T., Scherer G.F. COPPER AMINE OXIDASE1 (CuAO1) of Arabidopsis thaliana contributes to abscisic acid- and polyamine-induced nitric oxide biosynthesis and abscisic acid signal transduction. Mol. Plant. 2011;4:663–678. doi: 10.1093/mp/ssr023. PubMed DOI

Arana M.V., Tognacca R.S., Estravis-Barcalá M., Sánchez R.A., Botto J.F. Physiological and molecular mechanisms underlying the integration of light and temperature cues in Arabidopsis thaliana seeds. Plant Cell Environ. 2017;40:3113–3121. doi: 10.1111/pce.13076. PubMed DOI

Xiang S., Wu S., Jing Y., Chen L., Yu D. Phytochrome B regulates jasmonic acid-mediated defense response against Botrytis cinerea in Arabidopsis. Plant Divers. 2022;44:109–115. doi: 10.1016/j.pld.2021.01.007. PubMed DOI PMC

Desai M., Hu J. Light induces peroxisome proliferation in Arabidopsis seedlings through the photoreceptor phytochrome A, the transcription factor HY5 HOMOLOG, and the peroxisomal protein PEROXIN11b. Plant Physiol. 2008;146:1117–1127. doi: 10.1104/pp.107.113555. PubMed DOI PMC

Prerostova S., Dobrev P.I., Knirsch V., Jarosova J., Gaudinova A., Zupkova B., Prášil I.T., Janda T., Brzobohatý B., Skalák J., et al. Light quality and intensity modulate cold acclimation in Arabidopsis. Int. J. Mol. Sci. 2021;22:2736. doi: 10.3390/ijms22052736. PubMed DOI PMC

Jumtee K., Bamba T., Okazawa A., Fukusaki E., Kobayashi A. Integrated metabolite and gene expression profiling revealing phytochrome A regulation of polyamine biosynthesis of Arabidopsis thaliana. J. Exp. Bot. 2008;59:1187–1200. doi: 10.1093/jxb/ern026. PubMed DOI

Jumtee K., Okazawa A., Harada K., Fukusaki E., Takano M., Kobayashi A. Comprehensive metabolite profiling of phyA phyB phyC triple mutants to reveal their associated metabolic phenotype in rice leaves. J. Biosci. Bioeng. 2009;108:151–159. doi: 10.1016/j.jbiosc.2009.03.010. PubMed DOI

Han X., Tohge T., Lalor P., Dockery P., Devaney N., Esteves-Ferreira A.A., Fernie A.R., Sulpice R. Phytochrome A and B regulate primary metabolism in Arabidopsis leaves in response to light. Front. Plant Sci. 2017;8:1394. doi: 10.3389/fpls.2017.01394. PubMed DOI PMC

Kim W., Źeljković S.C., Piskurewicz U., Megies C., Tarkowski P., Lopez-Molina L. Polyamine uptake transporter 2 (put2) and decaying seeds enhance phyA-mediated germination by overcoming PIF1 repression of germination. PLoS Genet. 2019;15:e1008292. doi: 10.1371/journal.pgen.1008292. PubMed DOI PMC

Chun L., Kawakami A., Christopher D.A. Phytochrome A mediates blue light and UV-A-dependent chloroplast gene transcription in green leaves. Plant Physiol. 2001;125:1957–1966. doi: 10.1104/pp.125.4.1957. PubMed DOI PMC

Sullivan S., Hart J.E., Rasch P., Walker C.H., Christie J.M. Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis. Front. Plant Sci. 2016;7:290. doi: 10.3389/fpls.2016.00290. PubMed DOI PMC

Warnasooriya S.N., Porter K.J., Montgomery B.L. Tissue- and isoform-specific phytochrome regulation of light-dependent anthocyanin accumulation in Arabidopsis thaliana. Plant Signal. Behav. 2011;6:624–631. doi: 10.4161/psb.6.5.15084. PubMed DOI PMC

Kong Y., Zheng Y. Phototropin is partly involved in blue-light-mediated stem elongation, flower initiation, and leaf expansion: A comparison of phenotypic responses between wild Arabidopsis and its phototropin mutants. Environ. Exp. Bot. 2020;171:103967. doi: 10.1016/j.envexpbot.2019.103967. DOI

Usami T., Mochizuki N., Kondo M., Nishimura M., Nagatani A. Cryptochromes and phytochromes synergistically regulate Arabidopsis root greening under blue light. Plant Cell Physiol. 2004;45:1798–1808. doi: 10.1093/pcp/pch205. PubMed DOI

Sheng S., Wu C., Xiang Y.C., Pu W.X., Duan S.H., Huang P.J., Cheng X.Y., Gong Y.Y., Liang Y.L., Liu L.H. Polyamine: A potent ameliorator for plant growth response and adaption to abiotic stresses particularly the ammonium stress antagonized by urea. Front. Plant Sci. 2022;13:783597. doi: 10.3389/fpls.2022.783597. PubMed DOI PMC

Pál M., Szalai G., Janda T. Speculation: Polyamines are important in abiotic stress signaling. Plant Sci. 2015;237:16–23. doi: 10.1016/j.plantsci.2015.05.003. PubMed DOI

Chen F., Li B., Li G., Charron J.-B., Dai M., Shi X., Deng X.W. Arabidopsis Phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways. Plant Cell. 2014;26:1949–1966. doi: 10.1105/tpc.114.123950. PubMed DOI PMC

Pál M., Szalai G., Gondor O.K., Janda T. Unfinished story of polyamines: Role of conjugation, transport and light-related regulation in the polyamine metabolism in plants. Plant Sci. 2021;308:110923. doi: 10.1016/j.plantsci.2021.110923. PubMed DOI

Hummel I., Bourdais G., Gouesbet G., Couée I., Malmber R.L., El Amrani A. Differential gene expression of arginine decarboxylase ADC1 and ADC2 in Arabidopsis thaliana: Characterization of transcriptional regulation during seed germination and seedling development. New Phytol. 2004;163:519–531. doi: 10.1111/j.1469-8137.2004.01128.x. PubMed DOI

Marco F., Busó E., Carrasco P. Overexpression of SAMDC1 gene in Arabidopsis thaliana increases expression of defense-related genes as well as resistance to Pseudomonas syringae and Hyaloperonospora arabidopsidis. Front. Plant Sci. 2014;5:115. doi: 10.3389/fpls.2014.00115. PubMed DOI PMC

Urano K., Yoshiba Y., Nanjo T., Igarashi Y., Seki M., Sekiguchi F., Yamaguchi-Shinozaki K., Shinozaki K. Characterization of Arabidopsis genes involved in biosynthesis of polyamines in abiotic stress responses and developmental stages. Plant Cell Environ. 2003;26:1917–1926. doi: 10.1046/j.1365-3040.2003.01108.x. DOI

Hanzawa Y., Imai A., Michael A.J., Komeda Y., Takahashi T. Characterization of the spermidine synthase-related gene family in Arabidopsis thaliana. FEBS Lett. 2002;527:176–180. doi: 10.1016/S0014-5793(02)03217-9. PubMed DOI

Planas-Portell J., Gallart M., Tiburcio A.F., Altabella T. Copper-containing amine oxidases contribute to terminal polyamine oxidation in peroxisomes and apoplast of Arabidopsis thaliana. BMC Plant Biol. 2013;13:109. doi: 10.1186/1471-2229-13-109. PubMed DOI PMC

Takahashi Y., Cong R., Sagor G.H., Niitsu M., Berberich T., Kusano T. Characterization of five polyamine oxidase isoforms in Arabidopsis thaliana. Plant Cell Rep. 2010;29:955–965. doi: 10.1007/s00299-010-0881-1. PubMed DOI

Fincato P., Moschou P.N., Ahou A., Angelini R., Roubelakis-Angelakis K.A., Federico R., Tavladoraki P. The members of Arabidopsis thaliana PAO gene family exhibit distinct tissue- and organ-specific expression pattern during seedling growth and flower development. Amino Acids. 2012;42:831–841. doi: 10.1007/s00726-011-0999-7. PubMed DOI

Kim D.W., Watanabe K., Murayama C., Izawa S., Niitsu M., Michael A.J., Berberich T., Kusano T. Polyamine oxidase5 regulates Arabidopsis thaliana growth through a thermospermine oxidase activity. Plant Physiol. 2014;165:1575–1590. doi: 10.1104/pp.114.242610. PubMed DOI PMC

Zarza X., Atanasov K.E., Marco F., Arbona V., Carrasco P., Kopka J., Fotopoulos V., Munnik T., Gómez-Cadenas A., Tiburcio A.F., et al. Polyamine oxidase 5 loss-of-function mutations in Arabidopsis thaliana trigger metabolic and transcriptional reprogramming and promote salt stress tolerance. Plant Cell Environ. 2017;40:527–542. doi: 10.1111/pce.12714. PubMed DOI

Kaszler N., Benkő P., Bernula D., Szepesi Á., Fehér A., Gémes K. Polyamine metabolism is involved in the direct regeneration of shoots from Arabidopsis lateral root primordia. Plants. 2021;10:305. doi: 10.3390/plants10020305. PubMed DOI PMC

Wimalasekera R., Schaarschmidt F., Angelini R., Cona A., Tavladoraki P., Scherer G.F. POLYAMINE OXIDASE2 of Arabidopsis contributes to ABA mediated plant developmental processes. Plant Physiol. Biochem. 2015;96:231–240. doi: 10.1016/j.plaphy.2015.08.003. PubMed DOI

Tajti J., Hamow K.Á., Majláth I., Gierczik K., Németh E., Janda T., Pál M. Polyamine-induced hormonal changes in eds5 and sid2 mutant Arabidopsis plants. Int. J. Mol. Sci. 2019;20:5746. doi: 10.3390/ijms20225746. PubMed DOI PMC

Hunter D.C., Burritt D.J. Light quality influences the polyamine content of lettuce (Lactuca sativa L.) cotyledon explants during shoot production in vitro. Plant Growth Regul. 2005;45:53–61. doi: 10.1007/s10725-004-5971-z. DOI

Gondor O.K., Tajti J., Hamow K.Á., Majláth I., Szalai G., Janda T., Pál M. Polyamine metabolism under different light regimes in wheat. Int. J. Mol. Sci. 2021;22:11717. doi: 10.3390/ijms222111717. PubMed DOI PMC

Pál M., Hamow K.Á., Rahman A., Majláth I., Tajti J., Gondor O.K., Ahres M., Gholizadeh F., Szalai G., Janda T. Light spectral composition modifies polyamine metabolism in young wheat plants. Int. J. Mol. Sci. 2022;23:8394. doi: 10.3390/ijms23158394. PubMed DOI PMC

Takács Z., Poór P., Tari I. Comparison of polyamine metabolism in tomato plants exposed to different concentrations of salicylic acid under light or dark conditions. Plant Physiol. Biochem. 2016;108:266–278. doi: 10.1016/j.plaphy.2016.07.020. PubMed DOI

Majumdar R., Shao L., Turlapati S.A., Minocha S.C. Polyamines in the life of Arabidopsis: Profiling the expression of S-adenosylmethionine decarboxylase (SAMDC) gene family during its life cycle. BMC Plant Biol. 2017;17:264. doi: 10.1186/s12870-017-1208-y. PubMed DOI PMC

Devlin P.F., Halliday K.J., Harberd N.P., Whitelam G.C. The rosette habit of Arabidopsis thaliana is dependent upon phytochrome action: Novel phytochromes control internode elongation and flowering time. Plant J. 1996;10:1127–1134. doi: 10.1046/j.1365-313X.1996.10061127.x. PubMed DOI

Eskins K. Light-quality effects on Arabidopsis development. Red, blue and far-red regulation of flowering and morphology. Physiol. Plant. 1992;86:439–444. doi: 10.1111/j.1399-3054.1992.tb01341.x. DOI

Kurepin L.V., Walton L.J., Hayward A., Emery R.J.N., Pharis R.P., Reid D.M. Interactions between plant hormones and light quality signaling in regulating the shoot growth of Arabidopsis thaliana seedlings. Botany. 2012;90:237–246. doi: 10.1139/b11-108. DOI

Liu T., Dobashi H., Kim D.W., Sagor G.H., Niitsu M., Berberich T., Kusano T. Arabidopsis mutant plants with diverse defects in polyamine metabolism show unequal sensitivity to exogenous cadaverine probably based on their spermine content. Physiol. Mol. Biol. Plants. 2014;20:151–159. doi: 10.1007/s12298-014-0227-5. PubMed DOI PMC

Dai Y.R., Galston A.W. Simultaneous phytochrome controlled promotion and inhibition of arginine decarboxylase activity in buds and epicotyls of etiolated peas. Plant Physiol. 1981;67:266–269. doi: 10.1104/pp.67.2.266. PubMed DOI PMC

Yoshida I., Yamagata H., Hirasawa E. Signal transduction controlling the blue- and red-light mediated gene expression of S-adenosylmethionine decarboxylase in Pharbitis nil. J. Exp. Bot. 2002;53:1525–1529. PubMed

Yadav A., Singh D., Lingwan M., Yadukrishnan P., Masakapalli S.K., Datta S. Light signaling and UV-B-mediated plant growth regulation. J. Integr. Plant Biol. 2020;62:1270–1292. doi: 10.1111/jipb.12932. PubMed DOI

Chen D., Shao Q., Yin L., Younis A., Zheng B. Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Front. Plant Sci. 2019;9:1945. doi: 10.3389/fpls.2018.01945. PubMed DOI PMC

Sakamoto A., Terui Y., Uemura T., Igarashi K., Kashiwagi K. Polyamines regulate gene expression by stimulating translation of histone acetyltransferase mRNAs. J. Biol. Chem. 2020;295:8736–8745. doi: 10.1074/jbc.RA120.013833. PubMed DOI PMC

Alonso J.M., Stepanova A.N., Leisse T.J., Kim C.J., Chen H., Shinn P., Stevenson D.K., Zimmerman J., Barajas P., Cheuk R., et al. Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science. 2003;301:653–657. doi: 10.1126/science.1086391. PubMed DOI

Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT. Methods. 2001;25:402–408. doi: 10.1006/meth.2001.1262. PubMed DOI

Jubault M., Hamon C., Gravot A., Lariagon C., Delourme R., Bouchereau A., Manzanares-Dauleux M.J. Differential regulation of root arginine catabolism and polyamine metabolism in clubroot-susceptible and partially resistant Arabidopsis genotypes. Plant Physiol. 2008;146:2008–2019. doi: 10.1104/pp.108.117432. PubMed DOI PMC

Kamada-Nobusada T., Hayashi M., Fukazawa M., Sakakibara H., Nishimura M. A putative peroxisomal polyamine oxidase, AtPAO4, is involved in polyamine catabolism in Arabidopsis thaliana. Plant Cell Physiol. 2008;49:1272–1282. doi: 10.1093/pcp/pcn114. PubMed DOI

Sagor G.H.M., Kusano T., Berberich T. A polyamine oxidase from Selaginella lepidophylla (SelPAO5) can replace AtPAO5 in Arabidopsis through converting thermospermine to norspermidine instead to spermidine. Plants. 2019;8:99. doi: 10.3390/plants8040099. PubMed DOI PMC

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...