Putrescine catabolism via DAO contributes to proline and GABA accumulation in roots of lupine seedlings growing under salt stress

Jolanta Legocka, Ewa Sobieszczuk-Nowicka, Damian Ludwicki, Teresa Lehmann

Abstract


The levels of polyamines (PAs), proline (Pro), and γ-aminobutyric acid (GABA) as well as the activity of diamine oxidase (DAO; EC 1.4.3.6) were studied in the roots of 2-day-old lupine (Lupinus luteus L. ‘Juno’) seedlings treated with 200 mM NaCl for 24 h. The effect of adding 1 mM aminoguanidine (AG), an inhibitor of DAO activity, was also analyzed. It was found that in roots of lupine seedlings growing under salt stress, a negative correlation between Pro accumulation and putrescine (Put) content takes place. Pro level increased in roots by about 160% and, at the same time, Put content decreased by about 60%, as a result of ca. twofold increase of DAO activity. The AG added to the seedlings almost totally inhibited the activity of DAO, increased Put accumulation to control level, decreased Pro content by about 25%, and reduced GABA level by about 22%. Addition of 50 mM GABA to the lupine seedlings growing in the presence of AG and NaCl restored Pro content in roots to its level in NaCl-treated plants. In this research, the clear correlation between Put degradation and GABA and Pro accumulation was shown for the first time in the roots of seedlings growing under salt stress. This could be considered as a short-term response of a plant to high salt concentration. Our findings indicate that during intensive Pro accumulation in roots induced by salt stress, the pool of this amino acid is indirectly supported by GABA production as a result of Put degradation.

Keywords


diamine oxidase; lupine roots; polyamines; proline; salt stress; γ-aminobutyric acid

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References


Verbruggen N, Hermans C. Proline accumulation in plants: a review. Amino Acids. 2008;35:753–756. https://doi.org/10.1007/s00726-008-0061-6

Bouchereau A, Aziz A, Larher F, Martin-Tanquy J. Polyamines and environmental challenges: recent development. Plant Sci. 2009;140(2):103–125. https://doi.org/10.1016/s0168-9452(98)00218-0

Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pitchel J, Ahmad A. Role of proline under changing environments. Plant Signal Behav. 2012;7:1456–1466. https://doi.org/10.4161/psb.21949

Minocha R, Majumdar R, Minocha C. Polyamines and abiotic stress in plants: complex relationship. Front Plant Sci. 2014;5:175. https://doi.org/10.3389/fpls.2014.00175

Kinnersley AM. Gamma aminobutric acid (GABA) and plant responses to stress. Crit Rev Plant Sci. 2000;19:479–509. https://doi.org/10.1016/s0735-2689(01)80006-x

Barnett J, Naylor A. Amino acid and protein metabolism in Bermuda grass during water stress. Plant Physiol. 1966;41:1222–1230. https://doi.org/10.1104/pp.41.7.1222

Arshaf M, Foolad MR. Roles of glycine, betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot. 2007;59:206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006

Hare PD, Cress WA. Metabolic implication of stress-induced proline accumulation in plants. Plant Growth Regul. 1997;21:79–102. https://doi.org/10.1023/a:1005703923347

Aziz A, Martin-Tanguy J, Larher F. Stress-induced changes in polyamine and tyramine levels can regulate proline accumulation in tomato leaf discs treated with sodium chloride. Physiol Plant. 1998;104:195–201. https://doi.org/10.1034/j.1399-3054.1998.1040207.x

Liu JH, Nada K, Honda C, Katashiba H, Wen XP, Pang XM, et al. Polyamine biosynthesis of apple callus under salt stress: importance of arginine decarboxylase in stress response. J Exp Bot. 2006;57:2589–2599. https://doi.org/10.1093/jxb/erl018

Santa-Cruz A, Acosta M, Rus A, Bolarin MC. Short-term salt tolerance, mechanisms in differentially salt tolerant tomato species. Plant Physiol Biochem. 1999;37(1):65–71. https://doi.org/10.1016/S0981-9428(99)80068-0

Lefèvre I, Gratia E, Lutts S. Discrimination between the ionic and osmotic components of salt stress in relation to free polyamine level in rice (Oryza sativa). Plant Sci. 2001;161:943–952. https://doi.org/10.1016/s0168-9452(01)00485-x

Lin CC, Kao CM. NaCl-induced changes in putrescine content and diamine oxidase activity in roots of rice seedlings. Biol Plant. 2002;45:633–636. https://doi.org/10.1023/a:1022396408673

Benavides MP, Aizencang G, Tomaro ML. Polyamines in Helanthus annuus L. during germination under salt stress. J Plant Growth Regul. 1997;16:205–211. https://doi.org/10.1007/pl00006997

Maiale S, Sanchez DH, Guirado A, Vidal A, Ruiz O. Spermine accumulation under salt stress. J Plant Physiol. 2004;161:35–42. https://doi.org/10.1078/0176-1617-01167

Fait A, Fromm H, Walter D, Galili G, Fernie AR. Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci. 2008;13:14–19. https://doi.org/10.1016/j.tplants.2007.10.005

Michaeli S, Fromm H. Closing the loop the GABA shunt in plants: are GABA metabolism and entwined? Front Plant Sci. 2015;6:419. https://doi.org/10.3389/fpls.2015.00419

Baum G, Chen Y, Arazi T, Takasuji H, Fromm H. A plant glutamate decarboxylase containing a calmodulin binding domain. Cloning, sequence and functional analysis. J Biol Chem. 1993;268:19610–19617.

Shelp BJ, Bozzo GG, Trobacher CP, Zarei A, Deyman KL, Brikis CJ. Hypothesis/review: contribution of putrescine to 4-aminobutyrate (GABA) production in response to abiotic stress. Plant Sci. 2012;193–194:130–135. https://doi.org/10.1016/j.plantsci.2012.06.001

Tonton G, Kevers C, Faivre-Rampant O, Graziani M, Gaspar T. Effect of NaCl and manitol iso-osmotic stresses on proline and free polyamine levels in embryogenic Fraximus augustifolia callus. J Plant Physiol. 2004;161:701–708. https://doi.org/10.1078/0176-1617-01096

Xing SG, Jun YB, Hau ZW, Liang LY. Higher accumulation of γ-aminobutyric acid induced by salt stress throught stimulating the activity of diamine oxidases in Glycine max (L.) Merr. roots. Plant Physiol Biochem. 2007;45:560–566. https://doi.org/10.1016/j.plaphy.2007.05.007

Su GX, Bai X. Contribution of putrescine degradation to proline accumulation in soybean leaves under salinity. Biol Plant. 2008;52:796–799. https://doi.org/10.1007/s10535-008-0156-7

Yang R, Yin Y, Gu Z. Polyamine degradation pathway regulating growth and GABA accumulation in germinating fava bean under hypoxia-NaCl stress. J Agric Sci Technol. 2015;17:311–320

Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillian CC, Lutts S. Putrescine differentially influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot. 2010;61(10):2719–2733. https://doi.org/10.1093/jxb/erq118

Campestre MP, Bordenave CD, Origone AC, Menendez AB, Ruiz OA, Rodriguez AA, et al. Polyamine catabolism is involved in response to salt stress in soybean hypocotyls. J Plant Physiol. 2011;168:1234–1240. https://doi.org/10.1016/j.jplph.2011.01.007

DiTomaso JM, Hart JJ, Kochian LV. Transport kinetics and metabolism of exogenously applied putrescine in roots of intact maize seedlings. Plant Physiol. 1992;98:611–620. https://doi.org/10.1104/pp.98.2.611

Duhaze C, Gouzerh G, Gagneul D, Larher F, Bouchereau A. The conversion of spermidine to putrescine and 1,3-diaminopropane in the roots of Limonium tataricum. Plant Sci. 2002;163:639–646. https://doi.org/10.1016/S0168-9452(02)00172-3

Rastogi R, Davies PJ. Polyamine metabolism in ripening tomato fruit. Identification of metabolites of putrescine and spermidine. Plant Physiol. 1989;94:1449–14455. https://doi.org/10.1104/pp.94.3.1449

Kumar PP, Thorpe TA. Putrescine metabolism in excised cotyledons of Pinus radiata cultured in vitro. Physiol Plant. 1989;76:521–526. https://doi.org/10.1111/j.1399-3054.1989.tb05472.x

Verbruggen N, Villarroel R, van Montagu M. Osmoregulation of a pyrroline-5-carboxylate reductase gene in Arabidopsis thaliana. Plant Physiol. 1993;103:771–781. https://doi.org/10.1104/pp.103.3.771

Chiang HH, Dandekar AM. Regulation of proline accumulation in Arabidopsis thaliana (L.) Heynh during development and response to desiccation. Plant Cell Environ. 1995;18:1280–1290. https://doi.org/10.1111/j.1365-3040.1995.tb00187.x

Marcé M, Brown DS, Capell T, Figueras X, Tiburcio AF. Rapid high performance liquid chromatographic method for the quantitation of polyamines as their dansyl derivatives: application to plant and animal tissues. J Chromatogr B Biomed Sci Appl. 1995;666:329–335. https://doi.org/10.1016/0378-4347(94)00586-t

Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39:205–207. https://doi.org/10.1007/bf00018060

Chmielewska K, Rodziewicz P, Swarcewicz B, Sawikowska A, Krajewski P, Marczak Ł, et al. Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Front Plant Sci. 2016;7:1108. https://doi.org/10.3389/fpls.2016.01108

Delauney AJ, Verma DPS. Proline biosynthesis and osmoregulation in plants. Plant J. 1993;4:215–223. https://doi.org/10.1046/j.1365-313x.1993.04020215.x

Mohapatra S, Minocha R, Long S, Minocha SC. Transgenic manipulation of single polyamine in poplar cells affect the accumulation of all amino acids. Amino Acids. 2010;38:1117–1129. https://doi.org/10.1007/s00726-009-0322-z

Hu CA, Delauney AJ, Verma DPS. A bifunctional Δ’-enzyme-pyrroline-5-carboxylate synthetase catalyzes the first two steps in proline biosynthesis in plants. Proc Natl Acad Sci USA. 1992;89:9354–9358. https://doi.org/10.1073/pnas.89.19.9354

Moschou PN, Paschalidis KA, Roubelakis-Angelakis KA. Polyamine catabolism. Plant Signal Behav. 2008;3:1061–1066. https://doi.org/10.4161/psb.3.12.7172

Shelp BJ, Bown AW, McLean MD. Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci. 1999;4:446–452. https://doi.org/10.1016/s1360-1385(99)01486-7

Watke KV, Kad TD Zanan RL, Nadaf AB. Mechanism of 2-acetyl-1-pyrroline biosynthesis in Brassica latifolia Roxb. flowers. Physiology and Molecular Biology of Plants. 2011;17:231–237. https://doi.org/10.1007/s12298-011-0075-5

Renault H, El Amrani A, Palanivelu R, Updegraff EP, Yu AS, Renou JP, et al. GABA accumulation causes cell elongation defects and decrease in expression of gene encoding secreted and cell wall-related proteins in Arabidopsis thaliana. Plant Cell Physiol. 2011;52:894–908. https://doi.org/10.1093/pcp/pcr041

Batushansky A, Kirma M, Grillich N, Toubiana D, Pham PA, Balbo I, et al. Combined transcriptomics and metabolomics of Arabidopsis thaliana seedlings exposed to exogenous GABA suggest its role in plants is predominantly metabolic. Mol Plant. 2014;7:1065–1068. https://doi.org/10.1093/mp/ssu017

Sobieszczuk-Nowicka E, Kubala S, Zmienko A, Małecka A, Legocka J. From accumulation to degradation reprogramming polyamine metabolism facilitates dark-induced senescence in barley leaf cells. Front Plant Sci. 2016;6:1198. https://doi.org/10.3389/fpls.2015.01198

Pavan GM, Danani A, Pricl S, Smith DK. Modeling the multivalent recognition between dendritic molecules and DNA: understanding how ligand “sacrifice” and screening can enhance binding. J Am Chem Soc. 2009;131:9686–9694. https://doi.org/10.1021/ja901174k

Legocka J, Sobieszczuk-Nowicka, E Wojtyla Ł, Samardakiewicz S. Lead-stress induced changes in the content of free, thylakoid- and chromatin-bound polyamines, photosynthetic parameters and ultrastructure in greening barley leaves. J Plant Physiol. 2015;186–187:15–24. https://doi.org/10.1016/j.jplph.2015.07.010

Ha HC, Sirisoma N, Kuppusamy P, Zweier JL, Woster PM, Castro RA Jr. The natural polyamine spermine function directly as a free radical scavenger. Proc Natl Acad Sci USA. 1998;95:11140–11145. https://doi.org/10.1073/pnas.95.19.11140

Borell A, Carbonell L, Farras R, Puig-Parellada P, Tiburcio AF. Polyamines inhibit lipid peroxidation in senescing oat leaves. Physiol Plant. 1997;99:385–390. https://doi.org/10.1111/j.1399-3054.1997.tb00551.x

Benavides MP, Gallego SM, Comba ME, Tomaro ML. Relationship between polyamines and paraquat toxicity in sunflower leaf discs. Plant Growth Regul. 2000;31:215–224. https://doi.org/10.1023/a:1006316926002

Velikova V, Yardanow Y, Edreva E. Oxidative stress and some antioxidant system in acid-rain-treated bean plants: protective role of exogenous polyamines. Plant Sci. 2000;151:59–66. https://doi.org/10.1016/s0168-9452(99)00197-1

Nayyar H, Chander S. Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci. 2004;190:355–365. https://doi.org/10.1111/j.1439-037x.2004.00106.x