Physiological and Transcriptomic Response of Grey Poplar (Populus ×canescens Aiton Sm.) to Cadmium Stress

. 2020 Nov 04 ; 9 (11) : . [epub] 20201104

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

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid33158073

Grantová podpora
MZE-RO0118 Ministerstvo Zemědělství
CZ.02.1.01/0.0/0.0/16_019/0000738 Ministerstvo Školství, Mládeže a Tělovýchovy

(1) Background: Populus ×canescens (Aiton) Sm. is a fast-growing woody plant belonging to the family Salicaceae. Two poplar genotypes characterized by unique phenotypic traits (TP11 and TP20) were chosen to be characterized and tested for a physiological and transcriptomic response to Cd stress. (2) Methods: A comparative analysis of the effects of exposure to high cadmium (Cd) concentrations (10 µM and 100 µM) of TP11 and TP20 was performed. (3) Results: Neither of the tested Cd concentration negatively affected plant growth; however, the chlorophyll content significantly decreased. The potassium (K) content was higher in the shoots than in the roots. The magnesium concentrations were only slightly affected by Cd treatment. The zinc content in the shoots of TP20 was lower than that in the shoots of TP11. Cd accumulation was higher in the roots than in the shoots. After 10 days of exposure, 10 µM Cd resulted in comparable amounts of Cd in the roots and shoots of TP20. The most significant change in transcript amount was observed in endochitinase 2, 12-oxophytodienoate reductase 1 and phi classglutathione S-transferase. (4) Conclusions: Our study provided new insights for effective assessing the ability of different poplar genotypes to tolerate Cd stress and underlying Cd tolerance.

Zobrazit více v PubMed

Wu D., Yamaji N., Yamane M., Kashino-Fujii M., Sato K., Ma J.F. The HvNramp5 Transporter Mediates Uptake of Cadmium and Manganese, But Not Iron. Plant Physiol. 2016;172:1899–1910. doi: 10.1104/pp.16.01189. PubMed DOI PMC

Liu H., Zhao H., Wu L., Liu A., Zhao F.-J., Xu W. Heavy metal ATPase 3 (HMA3) confers cadmium hypertolerance on the cadmium/zinc hyperaccumulatorSedum plumbizincicola. New Phytol. 2017;215:687–698. doi: 10.1111/nph.14622. PubMed DOI

Zhang J., Martinoia E., Lee Y. Vacuolar Transporters for Cadmium and Arsenic in Plants and their Applications in Phytoremediation and Crop Development. Plant Cell Physiol. 2018;59:1317–1325. doi: 10.1093/pcp/pcy006. PubMed DOI

Garmash E., Golovko T.K. Effect of cadmium on growth and respiration of barley plants grown under two temperature regimes. Russ. J. Plant Physiol. 2009;56:343–347. doi: 10.1134/S1021443709030066. DOI

Li S., Yang W., Yang T., Chen Y., Ni W. Effects of Cadmium Stress on Leaf Chlorophyll Fluorescence and Photosynthesis ofElsholtzia argyi—A Cadmium Accumulating Plant. Int. J. Phytoremediat. 2014;17:85–92. doi: 10.1080/15226514.2013.828020. PubMed DOI

Lin L., Zhou W., Dai H., Cao F., Zhang G., Wu F. Selenium reduces cadmium uptake and mitigates cadmium toxicity in rice. J. Hazard. Mater. 2012;236:343–351. doi: 10.1016/j.jhazmat.2012.08.012. PubMed DOI

Nazar R., Iqbal N., Masood A., Khan M.I.R., Syeed S., Khan N.A. Cadmium Toxicity in Plants and Role of Mineral Nutrients in Its Alleviation. Am. J. Plant Sci. 2012;3:1476–1489. doi: 10.4236/ajps.2012.310178. DOI

Sharma P., Jha A.B., Dubey R.S., Pessarakli M. Reactive Oxygen Species, Oxidative Damage, and Antioxidative Defense Mechanism in Plants under Stressful Conditions. J. Bot. 2012;2012:1–26. doi: 10.1155/2012/217037. DOI

Cui W., Wang H., Song J., Cao X., Rogers H.J., Francis D., Jia C., Sun L., Hou M., Yang Y., et al. Cell cycle arrest mediated by Cd-induced DNA damage in Arabidopsis root tips. Ecotoxicol. Environ. Saf. 2017;145:569–574. doi: 10.1016/j.ecoenv.2017.07.074. PubMed DOI

DalCorso G., Farinati S., Maistri S., Furini A. How Plants Cope with Cadmium: Staking All on Metabolism and Gene Expression. J. Integr. Plant Biol. 2008;50:1268–1280. doi: 10.1111/j.1744-7909.2008.00737.x. PubMed DOI

Yamaguchi H., Fukuoka H., Arao T., Ohyama A., Nunome T., Miyatake K., Negoro S. Gene expression analysis in cadmium-stressed roots of a low cadmium-accumulating solanaceous plant, Solanum torvum. J. Exp. Bot. 2009;61:423–437. doi: 10.1093/jxb/erp313. PubMed DOI PMC

Garbisu C., Hernández-Allica J., Barrutia O., Alkorta I., Becerril J.M. Phytoremediation: A Technology Using Green Plants to Remove Contaminants from Polluted Areas. Rev. Environ. Health. 2002;17:173–188. doi: 10.1515/REVEH.2002.17.3.173. PubMed DOI

Reeves R.D., Van Der Ent A., Baker A.J.M. Agromining: Farming for Metals. Springer; Cham, Switzerland: 2017. Global Distribution and Ecology of Hyperaccumulator Plants; pp. 75–92.

Brown S.L., Chaney R.L., Angle J.S., Baker A.J.M. Zinc and Cadmium Uptake by Hyperaccumulator Thlaspi caerulescens and Metal Tolerant Silene vulgaris Grown on Sludge-Amended Soils. Environ. Sci. Technol. 1995;29:1581–1585. doi: 10.1021/es00006a022. PubMed DOI

Hernández-Allica J., Becerril J.M., Zárate O., Garbisu C. Assessment of the Efficiency of a Metal Phytoextraction Process with Biological Indicators of Soil Health. Plant Soil. 2006;281:147–158. doi: 10.1007/s11104-005-4081-7. DOI

Epelde L., Becerril J.M., Kowalchuk G.A., Deng Y., Zhou J., Garbisu C. Impact of Metal Pollution and Thlaspi caerulescens Growth on Soil Microbial Communities. Appl. Environ. Microbiol. 2010;76:7843–7853. doi: 10.1128/AEM.01045-10. PubMed DOI PMC

Broadhurst C.L., Chaney R.L. Growth and Metal Accumulation of an Alyssum murale Nickel Hyperaccumulator Ecotype Co-cropped with Alyssum montanum and Perennial Ryegrass in Serpentine Soil. Front. Plant Sci. 2016;7:451. doi: 10.3389/fpls.2016.00451. PubMed DOI PMC

Huang Y., Miyauchi K., Inoue C., Endo G. Development of suitable hydroponics system for phytoremediation of arsenic-contaminated water using an arsenic hyperaccumulator plant Pteris vittata. Biosci. Biotechnol. Biochem. 2015;80:1–5. doi: 10.1080/09168451.2015.1107461. PubMed DOI

Tlustoš P., Břendová K., Száková J., Najmanová J., Koubová K. The long-term variation of Cd and Zn hyperaccumulation by Noccaea spp and Arabidopsis halleri plants in both pot and field conditions. Int. J. Phytoremediat. 2016;18:110–115. doi: 10.1080/15226514.2014.981243. PubMed DOI

He J., Ma C., Ma Y., Li H., Kang J., Liu T., Polle A., Peng C., Luo Z.-B. Cadmium tolerance in six poplar species. Environ. Sci. Pollut. Res. 2013;20:163–174. doi: 10.1007/s11356-012-1008-8. PubMed DOI

Martinsen G.D., Whitham T.G., Turek R.J., Keim P. Hybrid populations selectively filter gene introgression between species. Evol. Int. J. Org. Evol. 2001;55:1325–1335. doi: 10.1111/j.0014-3820.2001.tb00655.x. PubMed DOI

Lexer C., Fay M.F., Joseph J.A., Nica M.-S., Heinze B. Barrier to gene flow between two ecologically divergent Populus species, P. alba (white poplar) and P. tremula (European aspen): The role of ecology and life history in gene introgression. Mol. Ecol. 2005;14:1045–1057. doi: 10.1111/j.1365-294X.2005.02469.x. PubMed DOI

Suvanto L.I., Latva-Karjanmaa T.B. Clone identification and clonal structure of the European aspen (Populus tremula) Mol. Ecol. 2005;14:2851–2860. doi: 10.1111/j.1365-294X.2005.02634.x. PubMed DOI

Puschenreiter M., Türktaş M., Sommer P., Wieshammer G., Laaha G., Wenzel W.W., Hauser M.-T. Differentiation of metallicolous and non-metallicolous Salix caprea populations based on phenotypic characteristics and nuclear microsatellite (SSR) markers. Plant Cell Environ. 2010;33:1641–1655. doi: 10.1111/j.1365-3040.2010.02170.x. PubMed DOI PMC

Anwar G.M., Helmey R.K., Mostafa Y.M. Assesment of genetic diversityin garlic clones using SSR and ISSR markers. [(accessed on 22 July 2019)];Egypt. J. Genet. Cytol. 2017 45:333–345. doi: 10.21608/ejgc.2016.9585. Available online: http://journal.esg.net.eg/index.php/EJGC/article/view/233. DOI

Dimsoski P., Toth G.P. Development of DNA-based microsatellite marker technology for studies of genetic diversity in stressor impacted populations. Ecotoxicology. 2001;10:229–232. doi: 10.1023/A:1016621511695. PubMed DOI

Selkoe K.A., Toonen R.J. Microsatellites for ecologists: A practical guide to using and evaluating microsatellite markers. Ecol. Lett. 2006;9:615–629. doi: 10.1111/j.1461-0248.2006.00889.x. PubMed DOI

Vieira M.L.C., Santini L., Diniz A.L., Munhoz C.D.F. Microsatellite markers: What they mean and why they are so useful. Genet. Mol. Biol. 2016;39:312–328. doi: 10.1590/1678-4685-GMB-2016-0027. PubMed DOI PMC

Wan X., Landhäusser S.M., Lieffers V.J., Zwiazek J.J. Signals controlling root suckering and adventitious shoot formation in aspen (Populus tremuloides) Tree Physiol. 2006;26:681–687. doi: 10.1093/treephys/26.5.681. PubMed DOI

Baryla A., Carrier P., Franck F., Coulomb C., Sahut C., Havaux M. Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: Causes and consequences for photosynthesis and growth. Planta. 2001;212:696–709. doi: 10.1007/s004250000439. PubMed DOI

Paunov M., Koleva L., Vassilev A., Vangronsveld J., Goltsev V. Effects of Different Metals on Photosynthesis: Cadmium and Zinc Affect Chlorophyll Fluorescence in Durum Wheat. Int. J. Mol. Sci. 2018;19:787. doi: 10.3390/ijms19030787. PubMed DOI PMC

Ondrasek G., Rengel Z., Romic D. Humic acids decrease uptake and distribution of trace metals, but not the growth of radish exposed to cadmium toxicity. Ecotoxicol. Environ. Saf. 2018;151:55–61. doi: 10.1016/j.ecoenv.2017.12.055. PubMed DOI

Zhan Y.-H., Zhang C., Zheng Q.-X., Huang Z.-A., Yu C.-L. Cadmium stress inhibits the growth of primary roots by interfering auxin homeostasis in Sorghum bicolor seedlings. J. Plant Biol. 2017;60:593–603. doi: 10.1007/s12374-017-0024-0. DOI

Schützendübel A., Nikolova P., Rudolf C., Polle A. Cadmium and H2O2-induced oxidative stress in Populus × canescens roots. Plant Physiol. Biochem. 2002;40:577–584. doi: 10.1016/S0981-9428(02)01411-0. DOI

Jiang H., Yang J., Zhang J. Effects of external phosphorus on the cell ultrastructure and the chlorophyll content of maize under cadmium and zinc stress. Environ. Pollut. 2007;147:750–756. doi: 10.1016/j.envpol.2006.09.006. PubMed DOI

Kapoor D., Kaur S., Bhardwaj R. Physiological and Biochemical Changes inBrassica junceaPlants under Cd-Induced Stress. BioMed Res. Int. 2014;2014:1–13. doi: 10.1155/2014/726070. PubMed DOI PMC

Dotaniya M.L., Meena V.D., Basak B.B., Meena R.S. Potassium Solubilizing Microorganisms for Sustainable Agriculture. Springer; New Delhi, India: 2016. Potassium Uptake by Crops as Well as Microorganisms; pp. 267–280.

Sadeghipour O. Enhancing Cadmium Tolerance in Common Bean Plants by Potassium Application. Philipp. Agric. Sci. 2018;101:167–175.

Liu S., Yang R., Tripathi D.K., Li X., Jiang M., Lv B., Ma M., Qibing C. RETRACTED: Signalling cross-talk between nitric oxide and active oxygen in Trifolium repens L. plants responses to cadmium stress. Environ. Pollut. 2018;239:53–68. doi: 10.1016/j.envpol.2018.03.106. PubMed DOI

Zhang G., Fukami M., Sekimoto H. Influence of cadmium on mineral concentrations and yield components in wheat genotypes differing in Cd tolerance at seedling stage. Field Crop. Res. 2002;77:93–98. doi: 10.1016/S0378-4290(02)00061-8. DOI

Rivetta A., Negrini N., Cocucci M. Involvement of Ca2+-calmodulin in Cd2+ toxicity during the early phases of radish (Raphanus sativus L.) seed germination. Plant Cell Environ. 1997;20:600–608. doi: 10.1111/j.1365-3040.1997.00072.x. DOI

Tkalec M., Štefanić P.P., Cvjetko P., Šikić S., Pavlica M., Balen B. The Effects of Cadmium-Zinc Interactions on Biochemical Responses in Tobacco Seedlings and Adult Plants. PLoS ONE. 2014;9:e87582. doi: 10.1371/journal.pone.0087582. PubMed DOI PMC

Courbot M., Willems G., Motte P., Arvidsson S., Roosens N., Saumitou-Laprade P., Verbruggen N. A Major Quantitative Trait Locus for Cadmium Tolerance in Arabidopsis halleri Colocalizes with HMA4, a Gene Encoding a Heavy Metal ATPase. Plant Physiol. 2007;144:1052–1065. doi: 10.1104/pp.106.095133. PubMed DOI PMC

Morel M., Crouzet J., Gravot A., Auroy P., Leonhardt N., Vavasseur A., Richaud P. AtHMA3, a P1B-ATPase Allowing Cd/Zn/Co/Pb Vacuolar Storage in Arabidopsis. Plant Physiol. 2008;149:894–904. doi: 10.1104/pp.108.130294. PubMed DOI PMC

Di Lonardo S., Capuana M., Arnetoli M., Gabbrielli R., Gonnelli C. Exploring the metal phytoremediation potential of three Populus alba L. clones using an in vitro screening. Environ. Sci. Pollut. Res. 2010;18:82–90. doi: 10.1007/s11356-010-0354-7. PubMed DOI

Nikolić N., Zoric L., Cvetković I., Pajević S., Borišev M., Orlović S. Assessment of cadmium tolerance and phytoextraction ability in young Populus deltoides L. and Populus × euramericana plants through morpho-anatomical and physiological responses to growth in cadmium enriched soil. IForest-Biogeosci. For. 2017;10:635–644. doi: 10.3832/ifor2165-010. DOI

Redovniković I.R., De Marco A., Proietti C., Hanousek K., Sedak M., Bilandžić N., JakovljeviĆ T. Poplar response to cadmium and lead soil contamination. Ecotoxicol. Environ. Saf. 2017;144:482–489. doi: 10.1016/j.ecoenv.2017.06.011. PubMed DOI

Pietrini F., Zacchini M., Iori V., Pietrosanti L., Ferretti M., Massacci A. Spatial distribution of cadmium in leaves and its impact on photosynthesis: Examples of different strategies in willow and poplar clones. Plant Biol. 2009;12:355–363. doi: 10.1111/j.1438-8677.2009.00258.x. PubMed DOI

Vollenweider P., Cosio C., Günthardt-Goerg M.S., Keller C. Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.) Environ. Exp. Bot. 2006;58:25–40. doi: 10.1016/j.envexpbot.2005.06.012. DOI

Cosio C., DeSantis L., Frey B., Diallo S., Keller C. Distribution of cadmium in leaves of Thlaspi caerulescens. J. Exp. Bot. 2005;56:765–775. doi: 10.1093/jxb/eri062. PubMed DOI

Kumar M., Brar A., Yadav M., Chawade A., Vivekanand V., Pareek N. Chitinases—Potential Candidates for Enhanced Plant Resistance towards Fungal Pathogens. Agriculture. 2018;8:88. doi: 10.3390/agriculture8070088. DOI

Cao J., Tan X. Comprehensive Analysis of the Chitinase Family Genes in Tomato (Solanum lycopersicum) Plants. 2019;8:52. doi: 10.3390/plants8030052. PubMed DOI PMC

Békésiová B., Hraška Š., Libantova J., Moravčíková J., Matušíková I. Heavy-metal stress induced accumulation of chitinase isoforms in plants. Mol. Biol. Rep. 2007;35:579–588. doi: 10.1007/s11033-007-9127-x. PubMed DOI

Gálusová T., Rybanský Ľ., Mészáros P., Spieß N., Piršelová B., Kuna R., Libantova J., Moravčíková J., Hauptvogel P., Matušíková I. Variable responses of soybean chitinases to arsenic and cadmium stress at the whole plant level. Plant Growth Regul. 2014;76:147–155. doi: 10.1007/s10725-014-9984-y. DOI

Breithaupt C., Kurzbauer R., Schaller F., Stintzi A., Schaller A., Huber R., Macheroux P., Clausen T. Structural Basis of Substrate Specificity of Plant 12-Oxophytodienoate Reductases. J. Mol. Biol. 2009;392:1266–1277. doi: 10.1016/j.jmb.2009.07.087. PubMed DOI

Xiang C.-B., Oliver D.J. Glutathione Metabolic Genes Coordinately Respond to Heavy Metals and Jasmonic Acid in Arabidopsis. Plant Cell. 1998;10:1539. doi: 10.1105/tpc.10.9.1539. PubMed DOI PMC

Maksymiec W., Krupa Z. The effects of short-term exposition to Cd, excess Cu ions and jasmonate on oxidative stress appearing in Arabidopsis thaliana. Environ. Exp. Bot. 2006;57:187–194. doi: 10.1016/j.envexpbot.2005.05.006. DOI

Liu T., Liu S., Guan H., Ma L., Chen Z., Gu H., Qu L. Transcriptional profiling of Arabidopsis seedlings in response to heavy metal lead (Pb) Environ. Exp. Bot. 2009;67:377–386. doi: 10.1016/j.envexpbot.2009.03.016. DOI

Velazhahan R., Datta S.K., Muthukrishnan S. Pathogenesis-Related Proteins in Plants. CRC Press; Boca Raton, FL, USA: 1999. The PR-5 family: Thaumatin-like proteins; pp. 107–129. DOI

Sarowar S., Kim Y.J., Kim E.N., Kim K.D., Hwang B.K., Islam R., Shin J.S. Overexpression of a pepper basic pathogenesis-related protein 1 gene in tobacco plants enhances resistance to heavy metal and pathogen stresses. Plant Cell Rep. 2005;24:216–224. doi: 10.1007/s00299-005-0928-x. PubMed DOI

Fecht-Christoffers M.M., Braun H.-P., Lemaitre-Guillier C., Vandorsselaer A., Horst W.J. Effect of Manganese Toxicity on the Proteome of the Leaf Apoplast in Cowpea. Plant Physiol. 2003;133:1935–1946. doi: 10.1104/pp.103.029215. PubMed DOI PMC

Júnior W.V.A., Neto C.F.D.O., Filho B.G.D.S., Amarante C.B.D., Cruz E.D., Okumura R.S., Barbosa A.V.C., De Sousa D.J.P., Teixeira J., Botelho A.D.S. Effect of cadmium on young plants of Virola surinamensis. AoB Plants. 2019;11:plz022. doi: 10.1093/aobpla/plz022. PubMed DOI PMC

Lee Y., Donghwan S., Won-Yong S., InHwan H., Youngsook L. Arabidopsis metallothioneins 2a and 3 enhance resistance to cadmium when expressed in Vicia faba guard cells. Plant Mol. Biol. 2004;54:805–815. doi: 10.1007/s11103-004-0190-6. PubMed DOI

Gullner G., Komives T., Király L., Schröder P. Glutathione S-Transferase Enzymes in Plant-Pathogen Interactions. Front. Plant Sci. 2018;9:1836. doi: 10.3389/fpls.2018.01836. PubMed DOI PMC

Khan N., Hu C.-M., Khan W.A., Hou X. Genome-Wide Identification, Classification, and Expression Divergence of Glutathione-Transferase Family in Brassica rapa under Multiple Hormone Treatments. BioMed Res. Int. 2018;2018:1–19. doi: 10.1155/2018/6023457. PubMed DOI PMC

Srivastava D., Verma G., Chauhan A.S., Pande V., Chakrabarty D. Rice (Oryza sativa L.) tau class glutathione S-transferase (OsGSTU30) overexpression in Arabidopsis thaliana modulates a regulatory network leading to heavy metal and drought stress tolerance. Metallomics. 2019;11:375–389. doi: 10.1039/C8MT00204E. PubMed DOI

Yang Q., Liu Y.-J., Zeng Q. Overexpression of three orthologous glutathione S-transferases from Populus increased salt and drought resistance in Arabidopsis. Biochem. Syst. Ecol. 2019;83:57–61. doi: 10.1016/j.bse.2019.01.001. DOI

Li L., Hou M., Cao L., Xia Y., Shen Z., Hu Z. Glutathione S-transferases modulate Cu tolerance in Oryza sativa. Environ. Exp. Bot. 2018;155:313–320. doi: 10.1016/j.envexpbot.2018.07.007. DOI

Du J., Ren J., Ye X., Hou A., Fu W., Mei F. Genome-wide identification and expression analysis of the glutathione S-transferase (GST) family under different developmental tissues and abiotic stresses in Chinese cabbage (Brassica rapa ssp. pekinensis) PeerJ. 2018 doi: 10.7287/peerj.preprints.26629v1. DOI

Lan T., Yang Z.-L., Yang X., Liu Y.-J., Wang X.-R., Zeng Q. Extensive Functional Diversification of the Populus Glutathione S-Transferase Supergene Family. Plant Cell. 2009;21:3749–3766. doi: 10.1105/tpc.109.070219. PubMed DOI PMC

Kieffer P., Dommes J., Hoffmann L., Hausman J.-F., Renaut J. Quantitative changes in protein expression of cadmium-exposed poplar plants. Proteomics. 2008;8:2514–2530. doi: 10.1002/pmic.200701110. PubMed DOI

Tognetti V.B., Van Aken O., Morreel K., Vandenbroucke K., Van De Cotte B., De Clercq I., Chiwocha S., Fenske R., Prinsen E., Boerjan W., et al. Perturbation of Indole-3-Butyric Acid Homeostasis by the UDP-Glucosyltransferase UGT74E2 Modulates Arabidopsis Architecture and Water Stress Tolerance. Plant Cell. 2010;22:2660–2679. doi: 10.1105/tpc.109.071316. PubMed DOI PMC

Hu Y.F., Zhou G., Na X.F., Yang L., Bin Nan W., Liu X., Zhang Y.Q., Li J.L., Bi Y. Cadmium interferes with maintenance of auxin homeostasis in Arabidopsis seedlings. J. Plant Physiol. 2013;170:965–975. doi: 10.1016/j.jplph.2013.02.008. PubMed DOI

Murashige T., Skoog F. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant. 1962;15:473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x. DOI

Van Der Schoot J., Pospíšková M., Vosman B., Smulders M.J.M. Development and characterization of microsatellite markers in black poplar (Populus nigra L.) Theor. Appl. Genet. 2000;101:317–322. doi: 10.1007/s001220051485. DOI

Smulders M.J.M., Van Der Schoot J., Arens P., Vosman B. Trinucleotide repeat microsatellite markers for black poplar (Populus nigra L.) Mol. Ecol. Notes. 2001;1:188–190. doi: 10.1046/j.1471-8278.2001.00071.x. DOI

Tuskan G.A., Gunter L.E., Yang Z.K., Yin T., Sewell M.M., DiFazio S.P. Characterization of microsatellites revealed by genomic sequencing of Populus trichocarpa. Can. J. For. Res. 2004;34:85–93. doi: 10.1139/x03-283. DOI

Loo M.V., Joseph J.A., Heinze B., Fay M.F., Lexer C. Clonality and spatial genetic structure in Populus × canescens and its sympatric backcross parent P. alba in a Central European hybrid zone. New Phytol. 2008;177:506–516. PubMed

Politov D.V., Belokon M.M., Belokon Y.S., Polyakova T.A., Shatokhina A.V., Mudrik E.A., Azarova A.B., Filippov M.V., Shestibratov K.A. Application of Microsatellite Loci for Molecular Identification of Elite Genotypes, Analysis of Clonality, and Genetic Diversity in Aspen Populus tremula L. (Salicaceae) Int. J. Plant Genom. 2015;2015:1–11. doi: 10.1155/2015/261518. PubMed DOI PMC

Pokorna E., Cizkova L., Machova P., Cvrckova H., Burianek V., Komarkova M. Characterization of genetic diversity of local population of grey poplar (Populus × canescens Aiton Sm.) using SSR marers and phenotypic evaluation. Rep. For. Res. 2018;63:281–289.

Guichoux E., Lagache L., Wagner S., Chaumeil P., Léger P., Lepais O., Lepoittevin C., Malausa T., Revardel E., Salin F., et al. Current trends in microsatellite genotyping. Mol. Ecol. Resour. 2011;11:591–611. doi: 10.1111/j.1755-0998.2011.03014.x. PubMed DOI

Vandesompele J., De Preter K., Pattyn F., Poppe B., Van Roy N., De Paepe A., Speleman F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002;3 doi: 10.1186/gb-2002-3-7-research0034. PubMed DOI PMC

Brentner L.B., Mukherji S.T., Merchie K.M., Yoon J.M., Schnoor J.L., Van Aken B. Expression of glutathione S-transferases in poplar trees (Populus trichocarpa) exposed to 2,4,6-trinitrotoluene (TNT) Chemosphere. 2008;73:657–662. doi: 10.1016/j.chemosphere.2008.07.059. PubMed DOI

Basa B., Solti Á., Sárvári É., Tamás L. Housekeeping gene selection in poplar plants under Cd-stress: Comparative study for real-time PCR normalisation. Funct. Plant Biol. 2009;36:1079–1087. doi: 10.1071/FP09073. PubMed DOI

Kieffer P., Schröder P., Dommes J., Hoffmann L., Renaut J., Hausman J.-F. Proteomic and enzymatic response of poplar to cadmium stress. J. Proteom. 2009;72:379–396. doi: 10.1016/j.jprot.2009.01.014. PubMed DOI

He J., Li H., Luo J., Ma C., Li S., Qu L., Gai Y., Jiang X., Janz D., Polle A., et al. A Transcriptomic Network Underlies Microstructural and Physiological Responses to Cadmium in Populus × canescens. Plant Physiol. 2013;162:424–439. doi: 10.1104/pp.113.215681. PubMed DOI PMC

Kohler A., Blaudez D., Chalot M., Martin F. Cloning and expression of multiple metallothioneins from hybrid poplar. New Phytol. 2004;164:83–93. doi: 10.1111/j.1469-8137.2004.01168.x. PubMed DOI

Gaudet M., Pietrini F., Beritognolo I., Iori V., Zacchini M., Massacci A., Mugnozza G.S., Sabatti M. Intraspecific variation of physiological and molecular response to cadmium stress in Populus nigra L. Tree Physiol. 2011;31:1309–1318. doi: 10.1093/treephys/tpr088. PubMed DOI

Sumanta N., Haque C., Nishika J., Suprakash R. Spectrophotometric Analysis of Chlorophylls and Carotenoids from Commonly Grown Fern Species by Using Various Extracting Solvents. Res. J. Chem. Sci. 2014;4:63–69.

Hoagland D.R., Arnon D.I. Growing Plants without Soil by the Water-Culture Method. Grow Plants Soil Water-Cult Method. [(accessed on 15 September 2020)];1938 Available online: https://www.cabdirect.org/cabdirect/abstract/19381900944.

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...