Response of cytokinins and nitrogen metabolism in the fronds of Pteris sp. under arsenic stress

. 2020 ; 15 (5) : e0233055. [epub] 20200515

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid32413087

Given the close relationship between cytokinins (CKs), photosynthesis and nitrogen metabolism, this study assessed the effect of arsenic (As) contamination on these metabolic components in the As-hyperaccumulators Pteris cretica L. var. Albo-lineata (Pc-A) and var. Parkerii (Pc-P) as well as the As-non-hyperaccumulator Pteris straminea Mett. ex Baker (Ps). The ferns were cultivated in a pot experiment for 23 weeks in soil spiked with As at the levels 20 and 100 mg·kg-1. For the purpose of this study, the CKs were placed into five functionally different groups according to their structure and physiological roles: bioactive forms (bCKs; CK free bases); inactive or weakly active forms (dCKs; CK N-glucosides); transport forms (tCKs; CK ribosides); storage forms (sCKs; O-glucosides); and primary products of CK biosynthesis (ppbCKs; CK nucleotides). An important finding was higher CKs total content, accumulation of sCKs and reduction of dCKs in As-hyperaccumulators in contrast to non-hyperaccumulator ferns. A significant depletion of C resources was confirmed in ferns, especially Ps, which was determined by measuring the photosynthetic rate and chlorophyll fluorescence. A fluorescence decrease signified a reduction in the C/N ratio, inducing an increase of bioactive CKs forms in Pc-P and Ps. The impact of As on N utilization was significant in As-hyperaccumulators. The glutamic acid/glutamine ratio, an indicator of primary N assimilation, diminished in all ferns with increased As level in the soil. In conclusion, the results indicate a large phenotypic diversity of Pteris species to As and suggest that the CKs composition and the glutamic acid/glutamine ratio can be used as a tool to diagnose As stress in plants.

Zobrazit více v PubMed

Zwack PJ, Rashotte AM. Interactions between cytokinin signalling and abiotic stress responses. J Exp Bot. 2015;66:4863–71. 10.1093/jxb/erv172 PubMed DOI

Hönig M, Plíhalová L, Husičková A, Nisler J, Doležal K. Role of cytokinins in senescence, antioxidant defence and photosynthesis. Int J Mol Sci. 2018;19:4045 10.3390/ijms19124045 PubMed DOI PMC

Vanstraelen M, Benková E. Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol. 2012;28:463–87. 10.1146/annurev-cellbio-101011-155741 PubMed DOI

Poschenrieder C, Cabot C, Martos S, Gallego B, Barceló J. Do toxic ions induce hormesis in plants? Plant Sci. 2013;212:15–25. 10.1016/j.plantsci.2013.07.012 PubMed DOI

Sarwat M, Naqvi AR, Ahmad P, Ashraf M, Akram NA. Phytohormones and microRNAs as sensors and regulators of leaf senescence: Assigning macro roles to small molecules. Biotechnol Adv. 2013;31:1153–71. 10.1016/j.biotechadv.2013.02.003 PubMed DOI

Verma V, Ravindran P, Kumar PP. Plant hormone-mediated regulation of stress responses. BMC Plant Biol. 2016;16:86 10.1186/s12870-016-0771-y PubMed DOI PMC

Curaba J, Singh MB, Bhalla PL. miRNAs in the crosstalk between phytohormone signalling pathways. J Exp Bot. 2014;65:1425–38. 10.1093/jxb/eru002 PubMed DOI

Zemanová V, Pavlíková D, Dobrev PI, Motyka V, Pavlík M. Endogenous phytohormone profiles in Pteris fern species differing in arsenic accumulating ability. Environ Exp Bot. 2019;166:103822 10.1016/j.envexpbot.2019.103822 DOI

Kiran NS, Polanská L, Fohlerová R, Mazura P, Válková M, Šmeral M, et al. Ectopic over-expression of the maize β-glucosidase Zm-p60.1 perturbs cytokinin homeostasis in transgenic tobacco. J Exp Bot. 2006;57:985–96. 10.1093/jxb/erj084 PubMed DOI

Šmehilová M, Dobrůšková J, Novák O, Takáč T, Galuszka P. Cytokinin-Specific glycosyltransferases possess different roles in cytokinin homeostasis maintenance. Front Plant Sci. 2016;7:1264 10.3389/fpls.2016.01264 PubMed DOI PMC

Gelová Z, ten Hoopen P, Novák O, Motyka V, Pernisová M, Dabravolski S, et al. Antibody-mediated modulation of cytokinins in tobacco: Organ-specific changes in cytokinin homeostasis. J. Exp. Bot. 2018;69:441–54. 10.1093/jxb/erx426 PubMed DOI

Liu CJ, Zhao Y, Zhang K. Cytokinin transporters: Multisite players in cytokinin homeostasis and signal distribution. Front Plant Sci. 2019;10:693 10.3389/fpls.2019.00693 PubMed DOI PMC

Guo J, Hu X, Duan R. Interactive effects of cytokinins, light, and sucrose on the phenotypes and the syntheses of anthocyanins and lignins in cytokinin overproducing transgenic Arabidopsis. J Plant Growth Regul. 2005;24:93–101. 10.1007/s00344-005-0005-2 DOI

Connor EF, Bartlett L, O'Toole S, Byrd S, Biskar K, Orozco J. The mechanism of gall induction makes galls red. Arthropod-Plant Interact. 2012;6:489–95. 10.1007/s11829-012-9210-7 DOI

McGaw BA, Horgan R. Cytokinin catabolism and cytokinin oxidase. Phytochemistry. 1983;22:1103–5. 10.1016/0031-9422(83)80200-3 DOI

Kopečný D, Pethe C, Šebela M, Houba-Hérin N, Madzak C, Majira A, et al. High-level expression and characterization of Zea mays cytokinin oxidase/dehydrogenase in Yarrowia lipolytica. Biochimie. 2005;87:1011–22. 10.1016/j.biochi.2005.04.006 PubMed DOI

Brzobohatý B, Moore I, Kristoffersen P, Bako L, Campos N, Schell J, et al. Release of active cytokinin by a β-glucosidase localized to the maize root meristem. Science. 1993;262:1051–4. 10.1126/science.8235622 PubMed DOI

Shoaib M, Yang W, Shan Q, Sajjad M, Zhang A. Genome-wide identification and expression analysis of new cytokinin metabolic genes in bread wheat (Triticum aestivum L.). PeerJ. 2019;7:e6300 10.7717/peerj.6300 PubMed DOI PMC

Ananieva K, Ananiev ED, Doncheva S, Georgieva K, Tzvetkova N, Kamínek M, et al. Senescence progression in a single darkened cotyledon depends on the light status of the other cotyledon in Cucurbita pepo (zucchini) seedlings: Potential involvement of cytokinins and cytokinin oxidase/dehydrogenase activity. Physiol Plant. 2008;134:609–23. 10.1111/j.1399-3054.2008.01161.x PubMed DOI

Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, Nagato Y, et al. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 2007;445:652–5. 10.1038/nature05504 PubMed DOI

Sakakibara H, Takei K, Hirose N. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 2006;11:440–8. 10.1016/j.tplants.2006.07.004 PubMed DOI

Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, Sakakibara H. Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot. 2008;59:75–83. 10.1093/jxb/erm157 PubMed DOI

Neuberg M, Pavlíková D, Žižková E, Motyka V, Pavlík M. Different types of N nutrition and their impact on endogenous cytokinin levels in Festulolium and Trifolium pratense L. Plant Soil Environ. 2011;57:381–7. 10.17221/152/2011-PSE DOI

Pavlíková D, Pavlík M, Procházková D, Zemanová V, Hnilička F, Wilhelmová N. Nitrogen metabolism and gas exchange parameters associated with zinc stress in tobacco expressing an ipt gene for cytokinin synthesis. J Plant Physiol. 2014a;171:559–64. 10.1016/j.jplph.2013.11.016 PubMed DOI

Pavlíková D, Zemanová V, Procházková D, Pavlík M, Száková J, Wilhelmová N. The long-term effect of zinc soil contamination on selected free amino acids playing an important role in plant adaptation to stress and senescence. Ecotox Environ Safe. 2014b;100:166–70. 10.1016/j.ecoenv.2013.10.028 PubMed DOI

Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wirén N, Bangerth F. Root-derived cytokinins as long-distance signals for NO3—induced stimulation of leaf growth. J Exp Bot. 2005;56:1143–52. 10.1093/jxb/eri107 PubMed DOI

Okazaki K, Oka N, Shinano T, Osaki M, Takebe M. Differences in the metabolite profiles of spinach (Spinacia oleracea L.) leaf in different concentrations of nitrate in the culture solution. Plant Cell Physiol. 2008;49:170–7. 10.1093/pcp/pcm173 PubMed DOI

Finnegan PM, Chen W. Arsenic toxicity: the effects on plant metabolism. Front Physiol. 2012;3: 182 10.3389/fphys.2012.00182 PubMed DOI PMC

Shahid MA, Balal RM, Khan N, Zotarelli L, Liu G.D., Sarkhosh A, et al. Selenium impedes cadmium and arsenic toxicity in potato by modulating carbohydrate and nitrogen metabolism. Ecotox Environ Safe. 2019;180:588–99. 10.1016/j.ecoenv.2019.05.037 PubMed DOI

Singh N, Ma LQ, Vu JC, Raj A. Effects of arsenic on nitrate metabolism in arsenic hyperaccumulating and non-hyperaccumulating ferns. Environ. Pollut. 2009;157:2300–5. 10.1016/j.envpol.2009.03.036 PubMed DOI

Chakrabarty D, Trivedi PK, Misra P, Tiwari M, Shri M, Shukla D, et al. Comparative transcriptome analysis of arsenate and arsenite stresses in rice seedlings. Chemosphere. 2009:74:688–702. 10.1016/j.chemosphere.2008.09.082 PubMed DOI

Singh VP, Singh S, Kumar J, Prasad SM. Hydrogen sulfide alleviates toxic effects of arsenate in pea seedlings through up-regulation of the ascorbate-glutathione cycle: Possible involvement of nitric oxide. J Plant Physiol. 2015:181:20–9. 10.1016/j.jplph.2015.03.015 PubMed DOI

Campos NV, Araújo TO, Arcanjo-Silva S, Freitas-Silva L, Azevedo AA, Nunes-Nesi A. Arsenic hyperaccumulation induces metabolic reprogramming in Pityrogramma calomelanos to reduce oxidative stress. Physiol Plant. 2016;157:135–46. 10.1111/ppl.12426 PubMed DOI

Bittsánszky A, Pilinszky K, Gyulai G, Komives T. Overcoming ammonium toxicity. Plant Sci. 2015;231:184–90. 10.1016/j.plantsci.2014.12.005 PubMed DOI

Zemanová V, Pavlík M, Pavlíková D, Tlustoš P. The changes of contents of selected free amino acids associated with cadmium stress in Noccaea caerulescens and Arabidopsis halleri. Plant Soil Environ. 2013;59:417–22. 10.17221/403/2013-PSE DOI

Pavlíková D, Zemanová V, Pavlík M. The contents of free amino acids and elements in As-hyperaccumulator Pteris cretica and non-hyperaccumulator Pteris straminea during reversible senescence. Plant Soil Environ. 2017;63:455–60. 10.17221/606/2017-PSE DOI

Zemanová V, Pavlík M, Pavlíková D. Cadmium toxicity induced contrasting patterns of concentrations of free sarcosine, specific amino acids and selected microelements in two Noccaea species. PLoS One. 2017;12:e0177963 10.1371/journal.pone.0177963 PubMed DOI PMC

Foyer CH, Noctor G. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antioxid Redox Signal. 2009;11:861–905. 10.1089/ars.2008.2177 PubMed DOI

Havlová M, Dobrev PI, Motyka V, Štorchová H, Libus J, Dobrá J, et al. The role of cytokinins in responses to water deficit in tobacco plants over-expressing trans-zeatin O-glucosyltransferase gene under 35S or SAG12 promoters. Plant Cell Environ. 2008;31:341–53. 10.1111/j.1365-3040.2007.01766.x PubMed DOI

Kosová K, Prášil IT, Vítámvás P, Dobrev P, Motyka V, Floková K, et al. Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol. 2012;169:567–76. 10.1016/j.jplph.2011.12.013 PubMed DOI

Macková H, Hronková M, Dobrá J, Turečková V, Novák O, Lubovská Z, et al. Enhanced drought and heat stress tolerance of tobacco plants with ectopically enhanced cytokinin oxidase/dehydrogenase gene expression. J Exp Bot. 2013;64:2805–15. 10.1093/jxb/ert131 PubMed DOI PMC

Žižková E, Dobrev PI, Muhovski Y, Hošek P, Hoyerová K, Haisel D, et al. Tomato (Solanum lycopersicum L.) SIIPT3 and SIIPT4 isopentenyltransferases mediate salt stress response in tomato. BMC Plant Biol. 2015;15:85 10.1186/s12870-015-0415-7 PubMed DOI PMC

Ripullone F, Grassi G, Lauteri M, Borghetti M. Photosynthesis-nitrogen relationships: Interpretation of different patterns between Pseudotsuga menziesii and Populus × euroamericana in a mini-stand experiment. Tree Physiol. 2003;23:137–44. 10.1093/treephys/23.2.137 PubMed DOI

Li Q, Yang X, Wang H, Wang H, He S. Endogenous trans-zeatin content in plants with different metal-accumulating ability: a field survey. Environ Sci Pollut Res. 2016;23:23422–35. 10.1007/s11356-016-7544-x PubMed DOI

Zhang X, Yang X, Wang H, Li Q, Wang H, Li Y. A significant positive correlation between endogenous trans-zeatin content and total arsenic in arsenic hyperaccumulator Pteris cretica var. nervosa. Ecotox Environ Safe. 2017;138:199–205. 10.1016/j.ecoenv.2016.12.031 PubMed DOI

Li Q, Wang H, Wang H, Li Y, Wang Z, Zhang X. Effect of arsenate on endogenous levels of cytokinins with different existing forms in two Pteris species. Plant Physiol Biochem. 2018;132:652–9. 10.1016/j.plaphy.2018.10.009 PubMed DOI

Mohan TC, Castrillo G, Navarro C, Zarco-Fernández S, Ramireddy E, Mateo C, et al. Cytokinin determines thiol-mediated arsenic tolerance and accumulation. Plant Physiol. 2016;171:1418–26. 10.1104/pp.16.00372 PubMed DOI PMC

Zemanová V, Pavlík M, Pavlíková D, Hnilička F, Vondráčková S. Responses to Cd stress in two Noccaea species (Noccaea praecox and Noccaea caerulescens) originating from two contaminated sites in Mežica, Slovenia and Redlschlag, Austria. Arch Environ Contam Toxicol. 2016;70:464–74. 10.1007/s00244-015-0198-8 PubMed DOI

ter Braak CJF, Smilauer P. CANOCO reference manual and CanoDraw for Windows user's guide: software for canonical community ordination (version 4.5). Microcomputer Power; Ithaca, 2002

Wang HB, Ye ZH, Shu WS, Li WC, Wong MH, Lan CY. Arsenic uptake and accumulation in fern species growing at arsenic-contaminated sites of southern China: Field surveys. Int J Phytoremediat. 2006;8:1–11. 10.1080/16226510500214517 PubMed DOI

Agnihotri A, Seth CS. Exogenously applied nitrate improves the photosynthetic performance and nitrogen metabolism in tomato (Solanum lycopersicum L. cv Pusa Rohini) under arsenic (V) toxicity. Physiol Mol Biol Plants. 2016; 22:341–9. 10.1007/s12298-016-0370-2 PubMed DOI PMC

Pavlík M, Pavlíková D, Staszková L, Neuberg M, Kaliszová R, Száková J, et al. The effect of arsenic contamination on amino acids metabolism in Spinacia oleracea L. Ecotox Environ Safe. 2010; 73:1309–13. 10.1016/j.ecoenv.2010.07.008 PubMed DOI

Takei K, Sakakibara H, Taniguchi M, Sugiyama T. Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: Implication of cytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol. 2001;42:85–93. 10.1093/pcp/pce009 PubMed DOI

Kiran NS, Benková E, Reková A, Dubová J, Malbeck J, Palme K, et al. Retargeting a maize β-glucosidase to the vacuole—Evidence from intact plants that zeatin-O-glucoside is stored in the vacuole. Phytochemistry. 2012; 79:67–77. 10.1016/j.phytochem.2012.03.012 PubMed DOI

Ronzan M, Piacentini D, Fattorini L, Federica DR, Caboni E, Eiche E, et al. Auxin-jasmonate crosstalk in Oryza sativa L. root system formation after cadmium and/or arsenic exposure. Environ Exp Bot. 2019;165:59–69. 10.1016/j.envexpbot.2019.05.013 DOI

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling T. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 2003;15:2532–50. 10.1105/tpc.014928 PubMed DOI PMC

Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T. New insights into the biology of cytokinin degradation. Plant Biol. 2006;8:371–81. 10.1055/s-2006-923928 PubMed DOI

Pavlík M, Zemanová V, Pavlíková D, Kyjaková P, Hlavsa T Regulation of odd-numbered fatty acid content plays an important part in the metabolism of the hyperaccumulator Noccaea spp. adapted to oxidative stress. J Plant Physiol. 2017;208:94–101. 10.1016/j.jplph.2016.09.014 PubMed DOI

Lea PJ, Sodek L, Parry MAJ, Shewry PR, Halford NG. Asparagine in plants. Ann Appl Biol. 2007;150:1–26. 10.1111/j.1744-7348.2006.00104.x DOI

Guiboileau A, Sormani R, Meyer C, Masclaux-Daubresse C. Senescence and death of plant organs: Nutrient recycling and developmental regulation. C R Biol. 2010;333:382–91. 10.1016/j.crvi.2010.01.016 PubMed DOI

Foyer CH, Noctor G, Hodges M. Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J Exp Bot. 2011;62:1467–82. 10.1093/jxb/erq453 PubMed DOI

Gough SP, Westergren T, Hansson M. Chlorophyll biosynthesis in higher plants. Regulatory aspects of 5-aminolevulinate formation. J Plant Biol. 2003;46:135–60. 10.1007/BF03030443 DOI

Cortleven A, Nitschke S, Klaumünzer M, AbdElgawad H, Asard H, Grimm B., et al. A novel protective function for cytokinin in the light stress response is mediated by the ARABIDOPSIS HISTIDINE KINASE2 and ARABIDOPSIS HISTIDINE KINASE3 receptors. Plant Physiol. 2014;164:1470–83. 10.1104/pp.113.224667 PubMed DOI PMC

Danilova MN, Kudryakova NV, Voronin PY, Oelmüller R, Kusnetsov VV, Kulaeva ON. Membrane receptors of cytokinin and their regulatory role in Arabidopsis thaliana plant response to photooxidative stress under conditions of water deficit. Russ J Plant Physiol. 2014;61: 434–442. 10.1134/S1021443714040062 DOI

Cortleven A, Schmülling T. Regulation of chloroplast development and function by cytokinin. J Exp Bot. 2015;66:4999–5013. 10.1093/jxb/erv132 PubMed DOI

Cortleven A, Marg I, Yamburenko MV, Schlicke H, Hill K, Grimm B, et al. Cytokinin regulates the etioplast-chloroplast transition through the two-component signaling system and activation of chloroplast-related genes. Plant Physiol. 2016;172:464–78. 10.1104/pp.16.00640 PubMed DOI PMC

Danilova MN, Doroshenko AS, Zabrodin DA, Kudryakova NV, Oelmüller R, Kusnetsov VV. Cytokinin membrane receptors modulate transcript accumulation of plastid encoded genes. Russ J Plant Physiol. 2017; 64:301–9. 10.1134/S1021443717030062 DOI

Guo Q, Turnbull MH, Song J, Roche J, Novak O, Späth J, et al. Depletion of carbohydrate reserves limits nitrate uptake during early regrowth in Lolium perenne L. J Exp Bot. 2017;68:1569–83. 10.1093/jxb/erx056 PubMed DOI PMC

Wang HB, Xie F, Yao YZ, Zhao B, Xiao QQ, Pan YH, et al. The effects of arsenic and induced-phytoextraction methods on photosynthesis in Pteris species with different arsenic-accumulating abilities. Environ Exp Bot. 2012;75:298–306. 10.1016/j.envexpbot.2011.08.002 DOI

Chernyad'ev II. The protective action of cytokinins on the photosynthetic machinery and productivity of plants under stress (review). Appl Biochem Microbiol. 2009;45:351–62. 10.1134/S0003683809040012 PubMed DOI

Brouquisse R, James F, Pradet A, Raymond P. Asparagine metabolism and nitrogen distribution during protein degradation in sugar-starved maize root tips. Planta. 1992;188:384–95. 10.1007/BF00192806 PubMed DOI

Lea PJ, Miflin BJ. Glutamate synthase and the synthesis of glutamate in plants. Plant Physiol Biochem. 2003;41:555–64. 10.1016/S0981-9428(03)00060-3 DOI

Forde BG, Lea PJ. Glutamate in plants: metabolism, regulation, and signalling. J Exp Bot. 2007;58:2339–58. 10.1093/jxb/erm121 PubMed DOI

Pavlík M, Pavlíková D, Zemanová V, Hnilička F, Urbanová V, Száková J. Trace elements present in airborne particulate matter-stressors of plant metabolism. Ecotox Environ Safe. 2012;79:101–7. 10.1016/j.ecoenv.2011.12.009 PubMed DOI

Pathare V, Srivastava S, Suprasanna P. Evaluation of effects of arsenic on carbon, nitrogen, and sulfur metabolism in two contrasting varieties of Brassica juncea. Acta Physiol Plant. 2013;35:3377–89. 10.1007/s11738-013-1370-2 DOI

Schmidt AC, Mattusch J, Reisser W, Wennrich R. Evaluation of the influence of arsenic species on the nitrogen metabolism of a model angiosperm: nasturtium, Tropaeolum majus. Appl Organomet Chem. 2005;19:590–9. 10.1002/aoc.869 DOI

Hodges M, Flesch V, Gálvez S, Bismuth E. Higher plant NADP+-dependent isocitrate dehydrogenases, ammonium assimilation and NADPH production. Plant Physiol Biochem. 2003;41:577–85. 10.1016/S0981-9428(03)00062-7 DOI

Kruse J, Hansch R, Mendel RR, Rennenberg H. The role of root nitrate reduction in the systemic control of biomass partitioning between leaves and roots in accordance to the C/N-status of tobacco plants. Plant Soil. 2010;332:387–403. 10.1007/s11104-010-0305-6 DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...