Abstract
Background and Aims
Polyamines (PAs) play important roles in drought tolerance, but the physiological significance of putrescine (Put) conversion into other forms of PAs is not clear in filling grain embryos of wheat (Triticum aestivum L.) plants under drought stress.
Methods
The changes in the levels of three main free PAs, Put, spermidine (Spd), and spermine (Spm), covalently conjugated PAs (perchloric acid-soluble), and covalently bound PAs (perchloric acid-insoluble), were investigated in embryos of filling grains, in two wheat cultivars, Longmai No. 079 (drought-tolerant) and Wanmai No. 52 (drought-sensitive). Furthermore, the activities of arginine decarboxylase, S-adenosylmethionine decarboxylase, and transglutaminase, which affect free Put biosynthesis, Spd and Spm biosynthesis from Put, and conversion of free PAs into bound PAs, respectively, were also determined. Exogenous PAs and PA biosynthesis inhibitors were also applied in the experiment.
Results
Under drought stress, the levels of conjugated PAs did not significantly differ between the two cultivars. However, the levels of free Spd, free Spm and bound Put increased more markedly (p < 0.05) in drought-tolerant Longmai No. 079 than in drought-sensitive Wanmai No. 52, suggesting that free Spd and Spm, and bound Put, which were converted from free Put, were possibly involved in drought tolerance. Exogenous Spd treatment enhanced the drought-induced increases in endogenous Spd and Spm contents in drought-sensitive Wanmai No. 52, and increased drought tolerance, as judged by the decrease in flag leaf relative plasma membrane permeability and increases in flag leaf relative water content, 1000-grain weight and grain number per spike. Methylglyoxal-bis guanylhydrazone and o-phenanthrolin inhibited drought-induced increases in free Spd, Spm, and bound-Put contents in drought-tolerant Longmai No. 079, and decreased in drought tolerance.
Conclusions
Collectively, the conversions of free Put into free Spd, Spm, and bound Put in filling grain embryos enhanced the tolerance of wheat plants to drought stress.
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Code availability
Not applicable.
Data Availability
The datasets generated during and analysed during the current study are available from the corresponding author on reasonable request.
References
Ahmad A, Ali A (2019) Improvement of postharvest quality, regulation of antioxidants capacity and softening enzymes activity of cold-stored carambola in response to polyamines application. Postharvest Biol Tech 148:208–217. https://doi.org/10.1016/j.postharvbio.2018.10.017
Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Let 28:1867–1876. https://doi.org/10.1007/s10529-006-9179-3
Alcázar R, Bueno M, Tiburcio AF (2020) Polyamines: Small amines with large effects on plant abiotic stress tolerance. Cells 9:2373. https://doi.org/10.3390/cells9112373
Bais HP, Sudha GS, Rarishankar GA (2000) Putrescine and silver nitrate influences shoot multiplication, in vitro flowering and endogenous titers of polyamines in Cichorium intybus L. cv. lucknow local. J Plant Growth Regul 19:238–248. https://doi.org/10.1007/s003440000012
Bányai J, Maccaferri M, Cané MA, Monostori I, Spitkó T, Kuti C, Mészáros K, Láng L, Pál M, Karsai I (2017) Phenotypical and physiological study of near-isogenic durum wheat lines under contrasting water regimes. S Afr J Bot 108: 248–255. https://doi.org/10.1016/j.sajb.2016.11.001
Beshamgan ES, Sharifi M, Zarinkamar F (2019) Crosstalk among polyamines, phytohormones, hydrogen peroxide, and phenylethanoid glycosides responses in Scrophularia striata to Cd stress. Plant Physiol Biochem 143: 129–141. https://doi.org/10.1016/j.plaphy.2019.08.028
Bradford MM (1976) A rapid and sensitive methods for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binging. Anal Biochem 72:248–254. https://doi.org/10.1046/j.0960-7412.2001.01200.x
Chen D, Shao Q, Yin L, Younis A, Zheng B (2019) Polyamine function in plants: Metabolism, regulation on development, and roles in abiotic stress responses. Front Plant Sci 9:1945. https://doi.org/10.3389/fpls.2018.01945
Del Duca S, Beninati S, Serafini-Fracassini D (1995) Polyamines in chloroplasts: identification of their glutamyl and acetyl derivatives. Biochem J 305:233–237. https://doi.org/10.1042/bj3050233
Del Duca S, Serafini-Fracassini D, Cai G (2014) Senescence and programmed cell death in plants: Polyamine action mediated by transglutaminase. Front Plant Sci 5:120. https://doi.org/10.3389/fpls.2014.00120
Di Tomaso JM, Shaff JE, Kochian LV (1989) Putrescine-induced wounding and its effects on membrane integrity and ion transport processes in roots of intact corn seedlings. Plant Physiol 90:988–995. https://doi.org/10.1104/pp.90.3.988
Du HY, Liu GT, Hua CM, Liu DX, He YY, Liu HP, Kurtenbach R, Ren DT (2021) Exogenous melatonin alleviated chilling injury in harvested plum fruit via affecting the levels of polyamines conjugated to plasma membrane. Postharvest Biol Tec 179:111585. https://doi.org/10.1016/j.postharvbio.2021.111585
Du HY, Liu DX, Liu GT, Liu HP, Sun HL, Li CH, Kurtenbach R (2022) Conjugated polyamines are involved in conformation stability of plasma membrane from maturing maize grain embryos under drought stress. Environ Exp Bot 194:104726. https://doi.org/10.1016/j.envexpbot.2021.104726
Dutra NT, Silveira V, Azevedo IG, Gomes-Neto LR, Facanha AR, Steiner N, Guerra MP, Floh EIS, Santa-Catarina C (2013) Polyamines affect the cellular growth and structure of pro-embryogenic masses in Araucaria angustifolia embryogenic cultures through the modulation of proton pump activities and endogenous levels of polyamines. Physiol Plant 148:121–132. https://doi.org/10.1111/j.1399-3054.2012.01695.x
Ebeed HT, Hassan NM, Keshta MM, Hassanin OS (2019) Comparative analysis of seed yield and biochemical attributes in different sunflower genotypes under different levels of irrigation and salinity. Egypt J Bot 59: 339–355. https://doi.org/10.21608/ejbo.2019.5043.1205
Ebmeyer H, Fiedler-Wiechers K, Hoffmann CM (2021) Drought tolerance of sugar beet–evaluation of genotypic differences in yield potential and yield stability under varying environmental conditions. Eur J Agron 125:126262. https://doi.org/10.1016/j.eja.2021.126262
Farooq M, Wahid A, Lee DJ (2009) Exogenously applied polyamines increase drought tolerance of rice by improving leaf water status, photosynthesis and membrane properties. Acta Physiol Plant 31:937–945. https://doi.org/10.1007/s11738-009-0307-2
Gardiner DM, Kazan K, Praud S, Torney FJ, Rusu A, Manners JM (2010) Early activation of wheat polyamine biosynthesis during Fusarium head blight implicates putrescine as an inducer of trichothecene mycotoxin production. BMC Plant Biol 10:289. https://doi.org/10.1186/1471-2229-10-289
Gondor OK, Tajti J, Hamow KÁ, Majláth I, Szalai G, Janda T, Pál M (2021) Polyamine metabolism under different light regimes in wheat. Int J Mol Sci 22:11717. https://doi.org/10.3390/ijms222111717
Gonzalez ME, Jasso-Robles FI, Flores-Hernández E, Rodríguez-Kessler M, Pieckenstain FL (2021) Current status and perspectives on the role of polyamines in plant immunity. Ann Appl Biol 178:244–255. https://doi.org/10.1111/aab.12670
Gupta K, Dey A, Gupta B (2013) Plant polyamines in abiotic stress responses. Acta Physiol Plant 35:2015–2036. https://doi.org/10.1007/s11738-013-1239-4
Hashem AM, Moore S, Chen S, Hu C, Zhao Q, Elesawi IE, Feng Y, Topping JF, Liu J, Lindsey K (2021) Putrescine depletion affects arabidopsis root meristem size by modulating auxin and cytokinin signaling and ROS accumulation. Int J Mol Sci 22:4094. https://doi.org/10.3390/ijms22084094
Hassan N, Ebeed H, Aljaarany A (2020) Exogenous application of spermine and putrescine mitigate adversities of drought stress in wheat by protecting membranes and chloroplast ultra-structure. Physiol Mol Biol Plants 26:233–245. https://doi.org/10.1007/s12298-019-00744-7
Hussain SS, Ali M, Ahmad M, Siddique KHM (2011) Polyamines: natural and engineered abiotic and biotic stress tolerance in plants. Biotechnol Adv 29:300–311. https://doi.org/10.1016/j.biotechadv.2011.01.003
Icekson I, Apelbaum A (1987) Evidence for transglutaminase activity in plant tissue. Plant Physiol 84:972–974. https://doi.org/10.1104/pp.84.4.972
Jahan MS, Wang Y, Shu S, Zhong M, Chen Z, Wu J, Sun J, Guo S (2019) Exogenous salicylic acid increases the heat tolerance in tomato (Solanum lycopersicum L.) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Sci Hortic 247:421–429. https://doi.org/10.1016/j.scienta.2018.12.047
Janicka-Russak M, Kabala K, Mlodzinska E, Klobus G (2010) The role of polyamines in the regulation of the plasma membrane and the tonoplast proton pumps under salt stress. J Plant Physiol 167:261–269. https://doi.org/10.1016/j.jplph.2009.010
Jing JG, Guo SY, Li YF, Li WH (2020) The alleviating effect of exogenous polyamines on heat stress susceptibility of different heat resistant wheat (Triticum aestivum L.) varieties. Sci Rep 10:7467. https://doi.org/10.1038/s41598-020-64468-5
Kasukabe Y, He L, Nada K, Misawa S, Ihara I, Tachibana S (2004) Over-expression of spermidine synthase enhances tolerance to multiple environmental stress and up-regulates the expression of various stress-regulated genes in transgenic Arabidopsis thaliana. Plant Cell Physiol 45:712–722. https://doi.org/10.1093/pcp/pch083
Kaur G, Asthir B (2017) Molecular responses to drought stress in plants. Biol Plant 61:201–209. https://doi.org/10.1007/s10535-016-0700-9
Kaur-Sawhney R, Shin M (1982) Relation of polyamines synthesized titer to aging and senescence in oat leaves. Plant Physiol 69:405–410. https://doi.org/10.1104/pp.69.2.405
Kong L, Attree SM, Fowke LC (1998) Effects of polyethylene glycol and methylglyoxal bis (guanylhydrazone) on endogenous polyamine levels and osmotic embryo maturation in white spruce. Plant Sci 133:211–220. https://doi.org/10.1016/S0168-9452(98)00040-5
Kubis J (2008) Exogenous spermidine differentially alters activities of some scavenging system enzymes, H2O2 and superoxide radical levels in water-stressed cucumber leaves. J Plant Physiol 165:397–406. https://doi.org/10.1016/j.jplph.2007.02.005
Lechowska K, Wojtyla Ł, Quinet M, Kubala S, Lutts S, Garnczarska M (2022) Endogenous polyamines and ethylene biosynthesis in relation to germination of osmoprimed brassica napus seeds under salt stress. Int J Mol Sci 23:349. https://doi.org/10.3390/ijms23010349
Liu Y, Gu D, Wu W, Wen X, Liao Y (2013a) The relationship between polyamines and hormones in the regulation of wheat grain filling. PLoS ONE 8:e78196. https://doi.org/10.1371/journal.pone.0078196
Liu Y, Wen XX, Gu DD, Guo Q, Zeng A, Li CJ, Liao YC (2013b) Effect of polyamine on grain filling of winter wheat and its physiological mechanism. Acta Agron Sin 39:712–719. https://doi.org/10.3724/SP.J.1006.2013.00712
Liu Y, Liang HY, Lv XK, Liu DD, Wen XX, Liao YC (2016) Effect of polyamines on the grain filling of wheat under drought stress. Plant Physiol Biochem 100:113–129. https://doi.org/10.1016/j.plaphy.2016.01.003
Luo J, Wei B, Han J, Liao Y, Liu Y (2019) Spermidine increases the sucrose content in inferior grain of wheat and thereby promotes its grain filling. Front Plant Sci 10:1309. https://doi.org/10.3389/fpls.2019.01309
Lutts S, Hausman J, Quinet M, Lefèvre I (2013) Polyamines and their roles in the alleviation of ion toxicities in plants. In: Ahmad P, Azooz M, Prasad M (Eds) Ecophysiology and Responses of Plants under Salt Stress. Springer: New York, NY, USA, pp 315–353.
Martin-Tanguy J (2001) Metabolism and function of polyamines in plants: recent development (new approaches). Plant Growth Regul 34:135–148. https://doi.org/10.1023/A:1013343106574
Musetti R, Scaramagli S, Vighi C, Pressaao L, Torrigiani P, Favali MA (1999) The involvement of polyamines in phytoplasma-infected periwinkle (Catharanthus roseus L.) plants. Plant Biosyst 133:37–45. https://doi.org/10.1080/11263509909381530
Nam KH, Lee SH, Lee JH (1997) Differential expression of ADC mRNA during development and upon acid stress in soybean (Glycine max) hypocotyls. Plant Cell Physiol 38:1156–1166. https://doi.org/10.1093/oxfordjournals.pcp.a029101
Ouyang W, Yin X, Yang J, Struik PC (2020) Comparisons with wheat reveal root anatomical and histochemical constraints of rice under water-deficit stress. Plant Soil 452:547–568. https://doi.org/10.1007/s11104-020-04581-6
Pál M, Szalai G, Gondor OK, Janda T (2021) Unfinished story of polyamines: role of conjugation, transport and light-related gegulation in the polyamine metabolism in plants. Plant Sci 308:110923. https://doi.org/10.1016/j.plantsci.2021.110923
Paschalidis KA, Roubelakis-Angelakis KA (2005) Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs / tissues of the tobacco plant. Correlations with age, cell division/expansion, and differentiation. Plant Physiol 138:142–152. https://doi.org/10.1104/pp.104.055483
Pedrol N, Ramos P, Reigosa MJ (2000) Phenotypic plasticity and acclimation to water deficits in velvet-grass: A long-term greenhouse experiment. Changes in leaf morphology, photosynthesis and stress-induced metabolites. J Plant Physiol 157:383–393. https://doi.org/10.1016/S0176-1617(00)80023-1
Pottosin I, Shabala S (2014) Polyamines control of cation transport across plant membranes: Implications for ion homeostasis and abiotic stress signaling. Front Plant Sci 5:154. https://doi.org/10.3389/fpls.2014.00154
Pottosin I, Olivas-Aguirre M, Dobrovinskaya O, Zepeda-Jazo I, Shabala S (2021) Modulation of ion transport across plant membranes by polyamines: Understanding specific modes of action under stress. Front Plant Sci 11:616077. https://doi.org/10.3389/fpls.2020.616077
Puga-Hermida MT, Gallardo M, Matilla AJ (2003) The zygotic embryogenesis and ripening of Brassica rapa seeds provokes important alterations in the levels of free and conjugated abscisic acid and polyamines. Physiol Plant 117:279–288. https://doi.org/10.1034/j.1399-3054.2003.00033.x
Quinet M, Ndayiragije A, Lefèvre I, Lambillotte B, Dupont-Gillain CC, Lutts S (2010) Putrescine differently influences the effect of salt stress on polyamine metabolism and ethylene synthesis in rice cultivars differing in salt resistance. J Exp Bot 61:2719–2733. https://doi.org/10.1093/jxb/erq118
Rabiti AL, Betti L, Bortolotti G, Marini F, Canova A, Bagni N, Torrigiani P (1998) Shout-term polyamine response in TMV-inoculated hypersensitive and susceptible tobacco plants. New Phytol 139:549–553. https://doi.org/10.1046/j.1469-8137.1998.00205.x
Rakić T, Pešić M, Kostić N, Andrejić G, Fira D, Dželetović Ž, Stanković S, Lozo J (2021) Rhizobacteria associated with Miscanthus x Giganteus improve metal accumulation and plant growth in the flotation tailings. Plant Soil 462:349–363. https://doi.org/10.1007/s11104-021-04865-5
Rodriguez SDC, López B, Chaves AR (2001) Effect of different treatments on the evolution of polyamines during refrigerated storage of eggplants. J Agric Food Chem 49:4700–4705. https://doi.org/10.1021/jf0001031
Scaramagli S, Biondi S, Leone A, Grillo S, Torrigiani P (2000) Acclimation to low-water potential in potato cell suspension cultures leads to changes in putressine metabolism. Plant Physiol Biochem 38:345–351. https://doi.org/10.1016/S0981-9428(00)00750-6
Serafini-Fracassini D, Del Duca S, Beninati S (1995) Plant transglutaminase. Phytochemistry 40:355–365. https://doi.org/10.1016/0031-9422(95)00243-Z
Shinozaki S, Ogata T, Horiuchi S (2000) Endogenous polyamines in the pericarp and seed of the grape berry during development and ripening. Sci Hort 83:33–41. https://doi.org/10.1016/S0304-4238(99)00064-3
Sobieszczuk-Nowicka E, Paluch-Lubawa E, Mattoo AK, Arasimowicz-Jelonek M, Gregersen PL, Pacak A (2019) Polyamines—A new metabolic switch: Crosstalk with networks involving senescence, crop improvement, and mammalian cancer therapy. Front Plant Sci 10:859. https://doi.org/10.3389/fpls.2019.00859
Tiburcio AF, Campos JL, Figueras X (1993) Recent advances in the understanding of polyamines functions during plant development. Plant Growth Regul 12:331–340. https://doi.org/10.1007/BF00027215
Tomosugi M, Ichihara K, Saito K (2006) Polyamines are essential for the synthesis of 2-ricinoleoyl phosphatidic acid in developing seeds of castor. Planta 223:349–358. https://doi.org/10.1007/s00425-005-0083-1
Upadhyay RK, Fatima T, Handa AK, Mattoo AK (2021) Differential association of free, conjugated, and bound forms of polyamines and transcript abundance of their biosynthetic and catabolic genes during drought/salinity stress in tomato (Solanum lycopersicum L.) leaves. Front Plant Sci 12: 743568. https://doi.org/10.3389/fpls.2021.743568.
Yamaguchi K, Takahashi Y, Berberich T, Imai A, Takahashi T, Michael AJ, Kusano T (2007) A protective role for the polyamine spermine against drought stress in Arabidopsis. Biochem Biophys Res Commun 352:486–490. https://doi.org/10.1016/j.bbrc.2006.11.041
Yang JC, Zhang JH, Liu K, Wang ZQ, Liu LJ (2007) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555. https://doi.org/10.1093/jxb/erm032
Zarza X, Wijk RV, Shabala L, Hunkeler A, Lefebvre M, Rodriguez-Villalón A, Shabala S, Tiburcio AF, Heilmann I, Munnik T (2020) Lipid kinases PIP5K7 and PIP5K9 are required for polyamine triggered K+ efflux in Arabidopsis roots. Plant J 104:416–432. https://doi.org/10.1111/tpj.14932
Zhong M, Wang Y, Zhang Y, Shu S, Sun J, Guo S (2019) Overexpression of transglutaminase from cucumber in tobacco increases salt tolerance through regulation of photosynthesis. Int J Mol Sci 20:894. https://doi.org/10.3390/ijms20040894
Zhong M, Song R, Wang Y, Shu S, Sun J, Guo S (2020) TGase regulates salt stress tolerance through enhancing bound polyamines-mediated antioxidant enzymes activity in tomato. Environ Exp Bot 179:104191. https://doi.org/10.1016/j.envexpbot.2020.104191
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National Natural Science Foundation of China (Grant No.: 31271627) and Natural Science Foundation of Henan province (Grant No.: 222300420394).
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HPL and HYD conceived the project; HYD and GTL performed the experiment (except enzyme activity detection); DXL detected enzyme activity; HYD and GTL wrote original draft; HPL and RK reviewed and edited the MS. Authors have already read the MS and agreed to being published in the final version.
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Du, H., Liu, G., Liu, D. et al. Significance of putrescine conversion in filling grain embryos of wheat plants subjected to drought stress. Plant Soil 484, 589–610 (2023). https://doi.org/10.1007/s11104-022-05823-5
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DOI: https://doi.org/10.1007/s11104-022-05823-5