Miscanthus x giganteus (Mxg) is a promising second-generation biofuel crop with high production of energetic biomass. Our aim was to determine the level of plant stress of Mxg grown in poor quality soils using non-invasive physiological parameters and to test whether the stress could be reduced by application of plant growth regulators (PGRs). Plant fitness was quantified by measuring of leaf fluorescence using 24 indexes to select the most suitable fluorescence indicators for quantification of this type of abiotic stress. Simultaneously, visible stress signs were observed on stems and leaves and differences in variants were revealed also by microscopy of leaf sections. Leaf fluorescence analysis, visual observation and changes of leaf anatomy revealed significant stress in all studied subjects compared to those cultivated in good quality soil. Besides commonly used Fv/Fm (potential photosynthetic efficiency) and P.I. (performance index), which showed very low sensitivity, we suggest other fluorescence parameters (like dissipation, DIo/RC) for revealing finer differences. We can conclude that measurement of leaf fluorescence is a suitable method for revealing stress affecting Mxg in poor soils. However, none of investigated parameters proved significant positive effect of PGRs on stress reduction. Therefore, direct improvement of soil quality by fertilization should be considered for stress reduction and improving the biomass quality in this type of soils.

Clinical Research Centre Medical University of Białystok 15 089 Białystok Poland

Department of Biology Faculty of Science Jan Evangelista Purkyně University in Ústí nad Labem 400 96 Ústí nad Labem Czech Republic

Department of Environmental Chemistry and Technology Faculty of Environment Jan Evangelista Purkyně University in Ústí nad Labem 400 96 Ústí nad Labem Czech Republic

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United Nations Sustainable development knowledge platform. [(accessed on 7 August 2019)]; Available online: https://sustainabledevelopment.un.org/?menu=1300.

Gerwin W., Repmann F., Galatsidas S., Vlachaki D., Gounaris N., Baumgarten W., Volkmann C., Keramitzis D., Kiourtsis F., Freese D. Assessment and quantification of marginal lands for biomass production in Europe using soil-quality indicators. Soil. 2018;4:267–290. doi: 10.5194/soil-4-267-2018. DOI

Hodkinson T.R., Renvoize S. Nomenclature of Miscanthus xgiganteus (Poaceae) Kew Bull. 2001;56:759. doi: 10.2307/4117709. DOI

Dohleman F.G., Long S.P. More productive than maize in the Midwest: How does miscanthus do it? PLANT Physiol. 2009;150:2104–2115. doi: 10.1104/pp.109.139162. PubMed DOI PMC

Christian D.G., Riche A.B., Yates N.E. Growth, yield and mineral content of Miscanthus×giganteus grown as a biofuel for 14 successive harvests. Ind. Crops Prod. 2008;28:320–327. doi: 10.1016/j.indcrop.2008.02.009. DOI

Devrije T. Pretreatment of Miscanthus for hydrogen production by Thermotoga elfii. Int. J. Hydrogen Energy. 2002;27:1381–1390. doi: 10.1016/S0360-3199(02)00124-6. DOI

Lewandowski I., Clifton-Brown J.C., Scurlock J.M.O., Huisman W. Miscanthus: European experience with a novel energy crop. Biomass and Bioenergy. 2000;19:209–227. doi: 10.1016/S0961-9534(00)00032-5. DOI

Wanat N., Austruy A., Joussein E., Soubrand M., Hitmi A., Gauthier-Moussard C., Lenain J.-F., Vernay P., Munch J.C., Pichon M. Potentials of Miscanthus×giganteus grown on highly contaminated Technosols. J. Geochemical Explor. 2013;126–127:78–84. doi: 10.1016/j.gexplo.2013.01.001. DOI

Pogrzeba M., Rusinowski S., Sitko K., Krzyżak J., Skalska A., Małkowski E., Ciszek D., Werle S., McCalmont J.P., Mos M., et al. Relationships between soil parameters and physiological status of Miscanthus x giganteus cultivated on soil contaminated with trace elements under NPK fertilisation vs. microbial inoculation. Environ. Pollut. 2017;225:163–174. doi: 10.1016/j.envpol.2017.03.058. PubMed DOI

Nsanganwimana F., Pourrut B., Mench M., Douay F. Suitability of Miscanthus species for managing inorganic and organic contaminated land and restoring ecosystem services. A review. J. Environ. Manage. 2014;143:123–134. doi: 10.1016/j.jenvman.2014.04.027. PubMed DOI

Pidlisnyuk V., Erickson L., Kharchenko S., Stefanovska T. Sustainable land management: Growing Miscanthus in soils contaminated with heavy metals. J. Environ. Prot. (Irvine,. Calif) 2014;05:723–730. doi: 10.4236/jep.2014.58073. DOI

Rusinowski S., Krzyżak J., Sitko K., Kalaji H.M., Jensen E., Pogrzeba M. Cultivation of C4 perennial energy grasses on heavy metal contaminated arable land: Impact on soil, biomass, and photosynthetic traits. Environ. Pollut. 2019;250:300–311. doi: 10.1016/j.envpol.2019.04.048. PubMed DOI

Beale C.V., Long S.P. Can perennial C4 grasses attain high efficiencies of radiant energy conversion in cool climates? Plant, Cell Environ. 1995;18:641–650. doi: 10.1111/j.1365-3040.1995.tb00565.x. DOI

Dohleman F.G., Heaton E.A., Leakey A.D.B., Long S.P. Does greater leaf-level photosynthesis explain the larger solar energy conversion efficiency of Miscanthus relative to switchgrass? Plant. Cell Environ. 2009;32:1525–1537. doi: 10.1111/j.1365-3040.2009.02017.x. PubMed DOI

Jiao X., Kørup K., Andersen M.N., Sacks E.J., Zhu X.-G., Laerke P.E., Jørgensen U. Can miscanthus C 4 photosynthesis compete with festulolium C 3 photosynthesis in a temperate climate? GCB Bioenergy. 2017;9:18–30. doi: 10.1111/gcbb.12342. DOI

Stavridou E., Webster R.J., Robson P.R.H. Novel Miscanthus genotypes selected for different drought tolerance phenotypes show enhanced tolerance across combinations of salinity and drought treatments. Ann. Bot. 2019;124:653–674. doi: 10.1093/aob/mcz009. PubMed DOI PMC

Lewandowski I., Clifton-Brown J., Trindade L.M., Van Der Linden G.C., Schwarz K.U., Müller-Sämann K., Anisimov A., Chen C.L., Dolstra O., Donnison I.S., et al. Progress on optimizing miscanthus biomass production for the european bioeconomy: Results of the EU FP7 project OPTIMISC. Front. Plant Sci. 2016;7 doi: 10.3389/fpls.2016.01620. PubMed DOI PMC

Wagner M., Mangold A., Lask J., Petig E., Kiesel A., Lewandowski I. Economic and environmental performance of miscanthus cultivated on marginal land for biogas production. GCB Bioenergy. 2019;11:34–49. doi: 10.1111/gcbb.12567. DOI

Nebeská D., Pidlisnyuk V., Stefanovska T., Trögl J., Shapoval P., Popelka J., Černý J., Medkow A., Kvak V., Malinská H. Impact of plant growth regulators and soil properties on Miscanthus x giganteus biomass parameters and uptake of metals in military soils. Rev. Environ. Health. 2019;34:283–291. doi: 10.1515/reveh-2018-0088. PubMed DOI

Ponomarenko S.P., Terek O.I., Grytsaenko Z.M., Babayants O.V., Moiseeva T.V., Wenxiu H., Eakin D. Bioregulation of growth and development of plants: Plant growth regulators in crop science. In: Ponomarenko S.P., Iutynska H.O., editors. Bioregulyatsiya mikrobnorastitel’nykh system [Bioregulation of microbial-plant systems] Nichlava; Kiev, Ukraine: 2010. pp. 251–291. [in Russian]

Baker N.R. A possible role for photosystem II in environmental perturbations of photosynthesis. Physiol. Plant. 1991;81:563–570. doi: 10.1111/j.1399-3054.1991.tb05101.x. DOI

Shulaev V., Cortes D., Miller G., Mittler R. Metabolomics for plant stress response. Physiol. Plant. 2008;132:199–208. doi: 10.1111/j.1399-3054.2007.01025.x. PubMed DOI

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

Barton L., Hemming B.C. Iron chelation in plants and soil microorganisms. Academic Press; Cambridge, MA, USA: 1993.

Lichtenthaler H.K. Vegetation stress: An introduction to the stress concept in plants. J. Plant Physiol. 1996;148:4–14. doi: 10.1016/S0176-1617(96)80287-2. DOI

Lichtenthaler H.K., Rinderle U. The role of chlorophyll fluorescence in the detection of stress conditions in plants. CRC Crit. Rev. Anal. Chem. 1988;19:S29–S85. doi: 10.1080/15476510.1988.10401466. DOI

Murchie E.H., Lawson T. Chlorophyll fluorescence analysis: A guide to good practice and understanding some new applications. J. Exp. Bot. 2013;64:3983–3998. doi: 10.1093/jxb/ert208. PubMed DOI

Krause G.H., Weis E. Chlorophyll fluorescence and photosynthesis: The basics. Annu. Rev. Plant Physiol. Plant Mol. Biol. 1991;42:313–349. doi: 10.1146/annurev.pp.42.060191.001525. DOI

Kalaji H.M., Jajoo A., Oukarroum A., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Łukasik I., Goltsev V., Ladle R.J. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol. Plant. 2016;38:102. doi: 10.1007/s11738-016-2113-y. DOI

Lazár D. Chlorophyll a fluorescence induction. Biochim. Biophys. Acta - Bioenerg. 1999;1412:1–28. doi: 10.1016/S0005-2728(99)00047-X. PubMed DOI

Butler W.L. Energy Distribution in the Photochemical Apparatus of Photosynthesis. Annu. Rev. Plant Physiol. 1978;29:345–378. doi: 10.1146/annurev.pp.29.060178.002021. DOI

Strasser R.J., Srivastava A.G. Polyphasic chlorophyll a fluorescence transient in plants and cyanobacteriatle. Photochem. Photobiol. 1995;61:32–42. doi: 10.1111/j.1751-1097.1995.tb09240.x. DOI

Strasser R.J., Greppin H. Primary reactions of photochemistry in higher plants. In: Akoyunoglou G., editor. Photosynthesis III. Balaban International Science Services; Philadelphia, PA, USA: 1981. pp. 717–726.

Strasser R.J., Tsimilli-Michael M., Srivastava A. Analysis of the Chlorophyll a Fluorescence Transient. In: Papageorgiou G.C., Govindjee , editors. Chlorophyll a Fluorescence. Springer; Dordrecht, the Netherlands: 2004. pp. 321–362.

Butler W.L., Strasser R.J. Tripartite model for the photochemical apparatus of green plant photosynthesis. Proc. Natl. Acad. Sci. USA. 1977;74:3382–3385. doi: 10.1073/pnas.74.8.3382. PubMed DOI PMC

Krause G.H., Weis E. Chlorophyll fluorescence as a tool in plant physiology. Photosynth. Res. 1984;5:139–157. doi: 10.1007/BF00028527. PubMed DOI

Stirbet A., Lazár D., Kromdijk J. Govindjee Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynthetica. 2018;56:86–104. doi: 10.1007/s11099-018-0770-3. DOI

Jiang C.-D., Wang X., Gao H.-Y., Shi L., Chow W.S. Systemic regulation of leaf anatomical structure, photosynthetic performance, and high-light tolerance in sorghum. Plant Physiol. 2011;155:1416–1424. doi: 10.1104/pp.111.172213. PubMed DOI PMC

Lopez F.B., Barclay G.F. Plant Anatomy and Physiology. In: Badal S., Delgoda R., editors. Pharmacognosy. Elsevier; Amsterdam, the Netherlands: 2017. pp. 45–60.

Bilska-Kos A., Panek P., Szulc-Głaz A., Ochodzki P., Cisło A., Zebrowski J. Chilling-induced physiological, anatomical and biochemical responses in the leaves of Miscanthus × giganteus and maize (Zea mays L.) J. Plant Physiol. 2018;228:178–188. doi: 10.1016/j.jplph.2018.05.012. PubMed DOI

Brestic M., Zivcak M. PSII fluorescence techniques for measurement of drought and high temperature stress signal in crop plants: Protocols and applications. In: Rout G., Das A., editors. Molecular Stress Physiology of Plants. Springer; New Delhi, India: 2013. pp. 87–131.

DSTU . DSTU ISO 11464-2001: Soil quality. Preliminary preparation of samples for physicalchemical analysis. DSTU; Kyiv, Ukraine: 2001.

Zbíral J., Čižmárová E., Elena O., Rychlý M., Vilamová V., Srnková J., Žalmanová A. Jednotné pracovní postupy: Analýza půd I. Central Institute for Supervising and Testing in Agriculture; Brno, Czech Republic: 2016. [in Czech]

Zbíral J., Malý S., Váňa M., Čuhel J., Fojtlová E., Čižmár D., Žalmanová A., Srnková J., Obdržálková E. Jednotné pracovní postupy: Analýza půd III. Central Institute for Supervising and Testing in Agriculture; Brno, Czech Republic: 2011. [in Czech]

Research Institute for Soil and Water Conservation eKatalog BPEJ. [(accessed on 30 March 2019)]; Available online: https://bpej.vumop.cz.

Trögl J., Jirková I., Zemánková P., Pilařová V., Dáňová P., Pavlorková J., Kuráň P., Popelka J., Křiklavová L. Estimation of the quantity of bacteria encapsulated in Lentikats Biocatalyst via phospholipid fatty acids content: A preliminary study. Folia Microbiol. (Praha.) 2013;58:135–140. doi: 10.1007/s12223-012-0189-3. PubMed DOI

Kuráň P., Trögl J., Nováková J., Pilařová V., Dáňová P., Pavlorková J., Kozler J., Novák F., Popelka J. Biodegradation of spilled diesel fuel in agricultural soil: Effect of humates, zeolite, and bioaugmentation. Sci. World J. 2014;2014:1–8. doi: 10.1155/2014/642427. PubMed DOI PMC

Kaur A., Chaudhary A., Kaur A., Choudhary R., Kaushik R. Phospholipid fatty acid – A bioindicator of environment monitoring and assessment in soil ecosystem. Curr. Sci. 2005 doi: 10.2307/24110962. DOI

Oukarroum A., Saïd S., Madidi E., Schansker G., Strasser R.J., El Madidi S., Schansker G. Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ. Exp. Bot. 2007;60:438–446. doi: 10.1016/j.envexpbot.2007.01.002. DOI

Kruskal W.H., Wallis W.A. Use of ranks in one-criterion variance analysis. J. Am. Stat. Assoc. 1952;47:583–621. doi: 10.1080/01621459.1952.10483441. DOI

Porter M.M., Niksiar P. Multidimensional mechanics: Performance mapping of natural biological systems using permutated radar charts. PLoS ONE. 2018;13:e0204309. doi: 10.1371/journal.pone.0204309. PubMed DOI PMC

Strašil Z., Weger J., Hutla P., Kára J. Biopaliva z pohledu energetiky a vlivu na životní prostředí. eAGRI Ministerstvo zemědělství; Prague, Czech Republic: 2015. The cultivation of Miscanthus determined for energy use (a summary of long-term monitoring) pp. 29–41. [in Czech]

Cadoux S., Riche A.B., Yates N.E., Machet J.-M. Nutrient requirements of Miscanthus x giganteus: Conclusions from a review of published studies. Biomass Bioenergy. 2012;38:14–22. doi: 10.1016/j.biombioe.2011.01.015. DOI

Gordana D., Jelena M., Jela I., Ivana P. Influence of fertilization on Miscanthus × giganteus (Greef et Deu) yield and biomass traits in three experiments in Serbia. Plant Soil Environ. 2017;63:189–193. doi: 10.17221/156/2017-PSE. DOI

Jeżowski S., Mos M., Buckby S., Cerazy-Waliszewska J., Owczarzak W., Mocek A., Kaczmarek Z., McCalmont J.P. Establishment, growth, and yield potential of the perennial grass Miscanthus × giganteus on degraded coal mine soils. Front. Plant Sci. 2017;8 doi: 10.3389/fpls.2017.00726. PubMed DOI PMC

da Costa R.M.F., Simister R., Roberts L.A., Timms-Taravella E., Cambler A.B., Corke F.M.K., Han J., Ward R.J., Buckeridge M.S., Gomez L.D., et al. Nutrient and drought stress: Implications for phenology and biomass quality in miscanthus. Ann. Bot. 2019;124:553–566. doi: 10.1093/aob/mcy155. PubMed DOI PMC

Guha A., Sengupta D., Reddy A.R. Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J. Photochem. Photobiol. B. 2013;119:71–83. doi: 10.1016/j.jphotobiol.2012.12.006. PubMed DOI

Strasser R.J., Stirbet A.D. Heterogeneity of photosystem II probed by the numerically simulated chlorophyll a fluorescence rise (O-J-I-P) Math. Comput. Simul. 1998;48:3–9. doi: 10.1016/S0378-4754(98)00150-5. DOI

Smethurst C.F., Garnett T., Shabala S. Nutritional and chlorophyll fluorescence responses of lucerne (Medicago sativa) to waterlogging and subsequent recovery. Plant Soil. 2005;270:31–45. doi: 10.1007/s11104-004-1082-x. DOI

Kalaji H.M., Oukarroum A., Alexandrov V., Kouzmanova M., Brestic M., Zivcak M., Samborska I.A., Cetner M.D., Allakhverdiev S.I., Goltsev V. Identification of nutrient deficiency in maize and tomato plants by in vivo chlorophyll a fluorescence measurements. Plant Physiol. Biochem. 2014;81:16–25. doi: 10.1016/j.plaphy.2014.03.029. PubMed DOI

Gindel I. Stomata constellation in the leaves of cotton, maize and wheat plants as a function of soil moisture and environment. Physiol. Plant. 1969;22:1143–1151. doi: 10.1111/j.1399-3054.1969.tb09103.x. PubMed DOI

Vaithilingam C.B.M. Effect of potash on sclerenchyma thickness and silica content in rice. Indian Potash J. 1976;1:17–23.

Beaton J.D., Sekhon G.S. Potassium Nutrition of Wheat and Other Small Grains. In: Munson R.D., editor. Potassium in Agriculture. American Society of Agronomy, Crop Science Society of America, Soil Science Society of America; Madison, WI, USA: 1985.

Sharma S.R., Kolte S.J. Effect of soil-applied NPK fertilizers on severity of black spot disease (Alternaria brassicae) and yield of oilseed rape. Plant Soil. 1994;167:313–320. doi: 10.1007/BF00007958. DOI

Pitman W.D., Holt E.C., Conrad B.E., Bashaw E.C. Histological differences in moisture-stressed and nonstressed kleingrass forage. Crop Sci. 1983;23:793. doi: 10.2135/cropsci1983.0011183X002300040046x. DOI

Makbul S., Saruhan Güler N., Durmuş N. Changes in anatomical and physiological parameters of soybean under drought stress. Turk J Bot. 2011;35:369–377. doi: 10.3906/bot-1002-7. DOI

Kharytonov M., Pidlisnyuk V., Stefanovska T., Babenko M., Martynova N., Rula I. The estimation of Miscanthus×giganteus’ adaptive potential for cultivation on the mining and post-mining lands in Ukraine. Environ. Sci. Pollut. Res. 2019;26:2974–2986. doi: 10.1007/s11356-018-3741-0. PubMed DOI

Clifton-Brown J., Schwarz K.-U., Awty-Carroll D., Iurato A., Meyer H., Greef J., Gwyn J., Mos M., Ashman C., Hayes C., et al. Breeding strategies to improve Miscanthus as a sustainable source of biomass for bioenergy and biorenewable products. Agronomy. 2019;9:673. doi: 10.3390/agronomy9110673. DOI

Björkman O., Demmig B. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origins. Planta. 1987;170:489–504. doi: 10.1007/BF00402983. PubMed DOI

Cold plasma treatment influences the physiological parameters of millet