Molecular background of cadmium tolerance in Rht dwarf wheat mutant is related to a metabolic shift from proline and polyamine to phytochelatin synthesis

. 2020 Jul ; 27 (19) : 23664-23676. [epub] 20200415

Jazyk angličtina Země Německo Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid32291640

Grantová podpora
KH 124472 Hungarian National Scientific Research Foundation

Odkazy

PubMed 32291640
PubMed Central PMC7326835
DOI 10.1007/s11356-020-08661-z
PII: 10.1007/s11356-020-08661-z
Knihovny.cz E-zdroje

Plant height is among the most important agronomic traits influencing crop yield. Wheat lines carrying Rht genes are important in plant breeding due to their both higher yield capacity and better tolerance to certain environmental stresses. However, the effects of dwarf-inducing genes on stress acclimation mechanisms are still poorly understood. Under the present conditions, cadmium stress induced different stress responses and defence mechanisms in the wild-type and dwarf mutant, and the mutant with the Rht-B1c allele exhibited higher tolerance. In the wild type after cadmium treatment, the abscisic acid synthesis increased in the leaves, which in turn might have induced the polyamine and proline metabolisms in the roots. However, in the mutant line, the slight increment in the leaf abscisic acid content accompanied by relatively high salicylic acid accumulation was not sufficient to induce such a great accumulation of proline and putrescine. Although changes in proline and polyamines, especially putrescine, showed similar patterns, the accumulation of these compounds was antagonistically related to the phytochelatin synthesis in the roots of the wild type after cadmium stress. In the dwarf genotype, a favourable metabolic shift from the synthesis of polyamine and proline to that of phytochelatin was responsible for the higher cadmium tolerance observed.

Zobrazit více v PubMed

Achard P, Genschik P. Releasing the brakes of plant growth: how GAs shut down DELLA proteins. J Exp Bot. 2009;60:1085–1092. doi: 10.1093/jxb/ern301. PubMed DOI

Al Khateeb W, Al-Qwasemeh H. Cadmium, copper and zinc toxicity effects on growth, proline content and genetic stability of Solanum nigrum L., a crop wild relative for tomato; comparative study. Physiol Mol Biol Plants. 2014;20:31–39. doi: 10.1007/s12298-013-0211-5. PubMed DOI PMC

Alcázar R, García-Martínez JL, Cuevas JC, Tiburcio AF, Altabella T. Overexpression of ADC2 in Arabidopsis induces dwarfism and late-flowering through GA deficiency. Plant J. 2005;43:425–436. doi: 10.1111/j.1365-313X.2005.02465.x. PubMed DOI

Alcázar R, Cuevas JC, Patron M, Altabella T, Tiburcio AF. Abscisic acid modulates polyamine metabolism under water stress in Arabidopsis thaliana. Physiol Plant. 2006;128:448–455. doi: 10.1111/j.1399-3054.2006.00780.x. DOI

Alonso-Ramírez A, Rodríguez D, Reyes D, Jiménez JA, Nicolás G, López-Climent M, Gómez-Cadenas A, Nicolás C. Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol. 2009;150:1335–1344. doi: 10.1104/pp.109.139352. PubMed DOI PMC

Anton A, Rékási M, Uzinger N, Széplábi G, Makó A. Modelling the potential effects of the Hungarian red mud disaster on soil properties. Water Air Soil Pollut. 2012;223:5175–5188. doi: 10.1007/s11270-012-1269-3. DOI

Asgher M, Iqbal M, Khan R, Anjum NA, Khan N. Minimizing toxicity of cadmium in plants-role of plant growth regulators. Protoplasma. 2014;252:399–413. doi: 10.1007/s00709-014-0710-4. PubMed DOI

Astolfi S, Zuchi S, Passera C. Role of sulphur availability on cadmium-induced changes of nitrogen and sulphur metabolism in maize (Zea mays L.) leaves. J. Plant Physiol. 2004;161:795–802. doi: 10.1016/j.jplph.2003.11.005. PubMed DOI

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. Phiol Plant. 1998;104:195–202. doi: 10.1034/j.1399-3054.1998.1040207.x. DOI

Balestrasse K, Gallego SM, Benavides MP, Tomaro ML. Polyamines and proline are affected by cadmium stress in nodules and roots of soybean plants. Plant Soil. 2005;270:343–353. doi: 10.1007/s11104-004-1792-0. DOI

Bates LS, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973;39:205–207. doi: 10.1007/BF00018060. DOI

Chen SL, Kao CH. Glutathione reduces the inhibition of rice seedling root growth caused by cadmium. Plant Growth Regul. 1995;16:249–252. doi: 10.1007/BF00024781. DOI

Chen J, Zhou J, Goldsbrough PB. Characterization of phytochelatin synthase from tomato. Physiol Plant. 1997;101:165–172. doi: 10.1111/j.1399-3054.1997.tb01833.x. DOI

Chmielowska-Bąk J, Gzyl J, Rucińska-Sobkowiak R, Arasimowicz-Jelonek M, Deckert J. The new insights into cadmium sensing. Front Plant Sci. 2014;5:245. doi: 10.3389/fpls.2014.00245. PubMed DOI PMC

Cona A, Rea G, Angelini R, Federico R, Tavladoraki P. Functions of amine oxidases in plant development and defence. Trends Plant Sci. 2006;11:80–88. doi: 10.1016/j.tplants.2005.12.009. PubMed DOI

DalCorso G, Farinati S, Maistri S, Furini A (2008) How plants cope with cadmium: staking all on metabolism and gene expression. J Integr Plant Biol. 10.1111/j.1744-7909.2008.00737.x PubMed

de Torres-Zabala M, Truman W, Bennett MH, Lafforgue G, Mansfield JW, Rodriguez Egea P, Bögre L, Grant M. Pseudomonas syringae pv. tomato hijacks the Arabidopsis abscisic acid signalling pathway to cause disease. EMBO J. 2007;26:1434–1443. doi: 10.1038/sj.emboj.7601575. PubMed DOI PMC

Dobrikova AG, Yotsova EK, Börner A, Landjeva SP, Apostolova EL. The wheat mutant DELLA-encoding gene (Rht-B1c) affects plant photosynthetic responses to cadmium stress. Plant Physiol Biochem. 2017;114:10–18. doi: 10.1016/j.plaphy.2017.02.015. PubMed DOI

Flintham JE, Börner A, Worland AJ, Gale MD (1997) Optimizing wheat grain yield: effects of Rht (gibberellin-insensitive) dwarfing genes. J Agr Sci 128(1):11–25. 10.1017/S0021859696003942

Gallé Á, Csiszár J, Benyó D, Laskay G, Leviczky T, Erdei L, Tari I. Isohydric and anisohydric strategies of wheat genotypes under osmotic stress: biosynthesis and function of ABA in stress responses. J Plant Physiol. 2013;170:1389–1399. doi: 10.1016/j.jplph.2013.04.010. PubMed DOI

Gallego-Giraldo L, Escamilla-Trevino L, Jackson LA, Dixon RA. Salicylic acid mediates the reduced growth of lignin down-regulated plants. Proc Natl Acad Sci U S A. 2011;108:20814–20819. doi: 10.1073/pnas.1117873108. PubMed DOI PMC

Gondor OK, Pál M, Darkó É, Janda T, Szalai G. Salicylic acid and sodium salicylate alleviate cadmium toxicity to different extents in maize (Zea mays L.) PLoS One. 2016;11:e0160157. doi: 10.1371/journal.pone.0160157. PubMed DOI PMC

Hare PD, Cress WA, Van Staden J. Proline synthesis and degradation: a model system for elucidating stress-related signal transduction. J Exp Bot. 1999;50:413–434. doi: 10.1093/jxb/50.333.413. DOI

Kısa D. Responses of phytochelatin and proline-related genes expression associated with heavy metal stress in Solanum lycopersicum. Acta Bot Croat. 2019;78:9–16. doi: 10.2478/botcro-2018-0023. DOI

Kocheva KV, Landjeva SP, Georgiev GI. Variation in ion leakage parameters of two wheat genotypes with different Rht-B1 alleles in response to drought. J Biosci. 2014;39:753–759. doi: 10.1007/s12038-014-9471-7. PubMed DOI

Kocheva K, Nenova V, Karceva T, Petrov P, Georgiev GI, Börner A, Landjeva S. Changes in water status, membrane stability and antioxidant capacity of wheat seedlings carrying different Rht-B1 dwarfing alleles under drought stress. J Agron Crop Sci. 2014;200:83–91. doi: 10.1111/jac.12047. DOI

Kovács V, Gondor OK, Szalai G, Darkó É, Majláth I, Janda T, Pál M. Synthesis and role of salicylic acid in wheat varieties with different levels of cadmium tolerance. J Hazard Mater. 2014;280:12–19. doi: 10.1016/j.jhazmat.2014.07.048. PubMed DOI

Leskó K, Stefanovits-Bányai É, Simon-Sarkadi L (2000) Effect of magnesium on free amino acid and polyamine content in wheat seedling exposed to cadmium stress. Acta biologica Szegediensis, Acta Biol Szeged. Univ

Liu J-H, Wang W, Wu H, Gong X, Moriguchi T. Polyamines function in stress tolerance: from synthesis to regulation. Front Plant Sci. 2015;6:827. doi: 10.3389/FPLS.2015.00827. PubMed DOI PMC

Liu S, Li M, Su L, Ge K, Li L, Li X, Liu X, Li L. Negative feedback regulation of ABA biosynthesis in peanut (Arachis hypogaea): a transcription factor complex inhibits AhNCED1 expression during water stress. Sci Rep. 2016;6:37943. doi: 10.1038/srep37943. PubMed DOI PMC

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

Lomozik L, Gasowska A, Bregier-Jarzebowska R, Jastrzab R (2005) Coordination chemistry of polyamines and their interactions in ternary systems including metal ions, nucleosides and nucleotides. Coord Chem Rev. 10.1016/j.ccr.2005.05.002

Lu Q, Chen S, Li Y, Zheng F, He B, Gu M. Exogenous abscisic acid (ABA) promotes cadmium (Cd) accumulation in Sedum alfredii Hance by regulating the expression of Cd stress response genes. Environ Sci Pollut Res. 2020;27:8719–8731. doi: 10.1007/s11356-019-07512-w. PubMed DOI

Majumdar R, Barchi B, Turlapati SA, Gagne M, Minocha R, Long S, Minocha SC. Glutamate, ornithine, arginine, proline, and polyamine metabolic interactions: the pathway is regulated at the post-transcriptional level. Front Plant Sci. 2016;7:78. doi: 10.3389/fpls.2016.00078. PubMed DOI PMC

Manohar M, Wang D, Manosalva PM, Choi HW, Kombrink E, Klessig DF. Members of the abscisic acid co-receptor PP2C protein family mediate salicylic acid-abscisic acid crosstalk. Plant Direct. 2017;1:e00020. doi: 10.1002/pld3.20. PubMed DOI PMC

Meguro A, Sato Y. Salicylic acid antagonizes abscisic acid inhibition of shoot growth and cell cycle progression in rice. Sci Rep. 2015;4:4555–4511. doi: 10.1038/srep04555. PubMed DOI PMC

Metwally A, Finkemeier I, Georgi M, Dietz K-J. Salicylic acid alleviates the cadmium toxicity in barley seedlings. Plant Physiol. 2003;132:272–281. doi: 10.1104/pp.102.018457. PubMed DOI PMC

Moschou PN, Paschalidis KA, Delis ID, Andriopoulou AH, Lagiotis GD, Yakoumakis DI, Roubelakis-Angelakis KA. Spermidine exodus and oxidation in the apoplast induced by abiotic stress is responsible for H2O2 signatures that direct tolerance responses in tobacco. Plant Cell. 2008;20:1708–1724. doi: 10.1105/tpc.108.059733. PubMed DOI PMC

Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd NP, Jones JDG. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Curr Biol. 2008;18:650–655. doi: 10.1016/j.cub.2008.03.060. PubMed DOI

Németh M, Janda T, Horváth E, Páldi E, Szalai G. Exogenous salicylic acid increases polyamine content but may decrease drought tolerance in maize. Plant Sci. 2002;162:569–574. doi: 10.1016/S0168-9452(01)00593-3. DOI

Nenova VR, Kocheva KV, Petrov PI, Georgiev GI, Karceva TV, Börner A, Landjeva SP. Wheat Rht-B1 dwarfs exhibit better photosynthetic response to water deficit at seedling stage compared to the wild type. J Agron Crop Sci. 2014;200:434–443. doi: 10.1111/jac.12090. DOI

Pál M, Horváth E, Janda T, Páldi E, Szalai G. Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physiol Plant. 2005;125:356–364. doi: 10.1111/j.1399-3054.2005.00545.x. DOI

Pál M, Horváth E, Janda T, Páldi E, Szalai G (2006) Physiological changes and defense mechanisms induced by cadmium stress in maize. J Plant Nutr Soil Sci. 10.1002/jpln.200520573

Pál M, Szalai G, Janda T (2015) Speculation: polyamines are important in abiotic stress signaling. Plant Sci. 10.1016/j.plantsci.2015.05.003 PubMed

Pál M, Csávás G, Szalai G, Oláh T, Khalil R, Yordanova R, Gell G, Birinyi Z, Németh E, Janda T. Polyamines may influence phytochelatin synthesis during Cd stress in rice. J Hazard Mater. 2017;340:272–280. doi: 10.1016/j.jhazmat.2017.07.016. PubMed DOI

Pál M, Janda T, Szalai G. Interactions between plant hormones and thiol-related heavy metal chelators. Plant Growth Regul. 2018;85:173–185. doi: 10.1007/s10725-018-0391-7. DOI

Pál M, Tajti J, Szalai G, Peeva V, Végh B, Janda T. Interaction of polyamines, abscisic acid and proline under osmotic stress in the leaves of wheat plants. Sci Rep. 2018;8:1–12. doi: 10.1038/s41598-018-31297-6. PubMed DOI PMC

Pál M, Ivanovska B, Oláh T, Tajti J, Hamow KÁ, Szalai G, Khalil R, Vanková R, Dobrev P, Misheva SP, Janda T. Role of polyamines in plant growth regulation of Rht wheat mutants. Plant Physiol Biochem. 2019;137:189–202. doi: 10.1016/j.plaphy.2019.02.013. PubMed DOI

Paolacci AR, Tanzarella OA, Porceddu E, Ciaffi M. Identification and validation of reference genes for quantitative RT-PCR normalization in wheat. BMC Mol Biol. 2009;10:11. doi: 10.1186/1471-2199-10-11. PubMed DOI PMC

Sanita di Toppi L, Gabbrielli R. Response to cadmium in higher plants. Environ Exp Bot. 1999;41:105–130. doi: 10.1016/S0098-8472(98)00058-6. DOI

Sharma SS, Schat H, Vooijs R. In vitro alleviation of heavy metal-induced enzyme inhibition by proline. Phytochemistry. 1998;49:1531–1535. doi: 10.1016/S0031-9422(98)00282-9. PubMed DOI

Siripornadulsil S, Traina S, Verma DPS, Sayre RT. Molecular mechanisms of proline-mediated tolerance to toxic heavy metals in transgenic microalgae. Plant Cell. 2002;14:2837–2847. doi: 10.1105/tpc.004853. PubMed DOI PMC

Sofo A, Vitti A, Nuzzaci M, Tataranni G, Scopa A, Vangronsveld J, Remans T, Falasca G, Altamura MM, Degola F, Sanità di Toppi L. Correlation between hormonal homeostasis and morphogenic responses in Arabidopsis thaliana seedlings growing in a Cd/Cu/Zn multi-pollution context. Physiol Plant. 2013;149:487–498. doi: 10.1111/ppl.12050. PubMed DOI

Stroiński A, Chadzinikolau T, Gizewska K, Zielezińska M. ABA or cadmium induced phytochelatin synthesis in potato tubers. Biol Plant. 2010;54:117–120. doi: 10.1007/s10535-010-0017-z. DOI

Stroiński A, Gizewska K, Zielezińska M. Abscisic acid is required in transduction of cadmium signal to potato roots. Biol Plant. 2013;57:121–127. doi: 10.1007/s10535-012-0135-x. DOI

Szalai G, Krantev A, Yordanova R, Popova LP, Janda T. Influence of salicylic acid on phytochelatin synthesis in Zea mays during cd stress. Turk J Bot. 2013;37:708–714. doi: 10.3906/bot-1210-6. DOI

Tajti J, Janda T, Majláth I, Szalai G, Pál M. Comparative study on the effects of putrescine and spermidine pre-treatment on cadmium stress in wheat. Ecotoxicol Environ Saf. 2018;148:546–554. doi: 10.1016/j.ecoenv.2017.10.068. PubMed DOI

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

Thomas JC, Perron M, Davies EC. Genetic responsiveness to copper in the ice plant, Mesembryanthemum crystallinum. Plant Sci. 2004;167:259–266. doi: 10.1016/J.PLANTSCI.2004.03.022. DOI

Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turk J Bot. 10.3906/bot-1112-16

Vrhovsek U, Masuero D, Gasperotti M, Franceschi P, Caputi L, Viola R, Mattivi F. A versatile targeted metabolomics method for the rapid quantification of multiple classes of phenolics in fruits and beverages. J Agric Food Chem. 2012;60:8831–8840. doi: 10.1021/jf2051569. PubMed DOI

Wen W, Deng Q, Jia H, Wei L, Wei J, Wang H, Yang L, Cao W, Ma Z. Sequence variations of the partially dominant della gene Rht-B1c in wheat and their functional impacts. J Exp Bot. 2013;64:3299–3312. doi: 10.1093/jxb/ert183. PubMed DOI PMC

Xiong H, Guo H, Xie Y, Zhao L, Gu J, Zhao S, Li J, Liu L. RNAseq analysis reveals pathways and candidate genes associated with salinity tolerance in a spaceflight-induced wheat mutant. Sci Rep. 2017;7(1):2731. doi: 10.1038/s41598-017-03024-0. PubMed DOI PMC

Xu J, Yin H, Li X. Protective effects of proline against cadmium toxicity in micropropagated hyperaccumulator, Solanum nigrum L. Plant Cell Rep. 2009;28:325–333. doi: 10.1007/s00299-008-0643-5. PubMed DOI

Xu H, Liu Q, Yao T, Fu XD. Shedding light on integrative GA signaling. Curr Opin Plant Biol. 2014;21:89–95. doi: 10.1016/j.pbi.2014.06.010. PubMed DOI

Xue B, Zhang A, Jiang M. Involvement of polyamine oxidase in abscisic acid-induced cytosolic antioxidant defense in leaves of maize. J Integr Plant Biol. 2009;51:225–234. doi: 10.1111/j.1744-7909.2008.00766.x. PubMed DOI

Yoda H, Yamaguchi Y, Sano H. Induction of hypersensitive cell death by hydrogen peroxide produced through polyamine degradation in tobacco plants. Plant Physiol. 2003;132:1973–1981. doi: 10.1104/pp.103.024737. PubMed DOI PMC

Zentella R, Zhang Z-L, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, Sun T. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell. 2007;19:3037–3057. doi: 10.1105/tpc.107.054999. PubMed DOI PMC

Zhu FX, Jiang T, Wang ZW, Lei GJ, Shi YZ, Li GX, Zheng SJ. Gibberellic acid alleviates cadmium toxicity by reducing nitric oxide accumulation and expression of IRT1 in Arabidopsis thaliana. J Hazard Mater. 2012;239:302–307. doi: 10.1016/j.jhazmat.2012.08.077. PubMed DOI

Zitka O, Krystofova O, Sobrova P, Adam V, Zehnalek J, Beklova M, Kizek R. Phytochelatin synthase activity as a marker of metal pollution. J Hazard Mater. 2011;192:794–800. doi: 10.1016/j.jhazmat.2011.05.088. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace