Photosynthetic performance of young maize (Zea mays L.) plants exposed to chilling stress can be improved by the application of protein hydrolysates

Rositsa Cholakova-Bimbalova, Veselin Petrov, Andon Vassilev

Abstract


Biostimulants offer a novel approach for the regulation of crucial physiological processes in plants. Recently, it has been observed that the application of biostimulants on both seeds and plants may ameliorate to some extent the negative effects of abiotic stresses such as drought, heat, salinity, and others. In the climate conditions of Bulgaria, the early developmental stages of warm climate crops, like maize, often occur under suboptimal temperatures. Although the mitigation of abiotic stress is perhaps the most frequently cited benefit of biostimulant formulations, little is known about their influence on chilling-stressed plants. The aim of our study was to evaluate the effects of a biostimulant from the group of protein hydrolysates on both the growth and the photosynthetic performance of chilling-exposed young maize plants grown in controlled environment. Here, we report that application of a protein hydrolysate increased the performance of chilled maize plants, as demonstrated by leaf gas exchange, photosynthetic pigment content, and chlorophyll fluorescence, but did not affect their growth. Nevertheless, based on the better preserved photosynthetic performance of the biostimulant-treated maize plants exposed to chilling, we assume that under subsequent favorable conditions their growth would recover more quickly as compared to the untreated ones.

Keywords


stress; Zea mays L.; chilling; biostimulants; photosynthesis

Full Text:

PDF

References


Sharma HSS, Fleming C, Selby C, Rao JR, Martin T. Plant biostimulants: a review on the processing of macroalgae and use of extracts for crop management to reduce abiotic and biotic stresses. J Appl Phycol. 2014;26:465–490. https://doi.org/10.1007/s10811-013-0101-9

Du Jardin P. Plantbiostimulants: definition, concept, main categories and regulation. Sci Hortic (Amsterdam). 2015;196:3–14. https://doi.org/10.1016/j.scienta.2015.09.021

Yakhin OI, Lubyanov AA, Yakhin IA. Biostimulants in agrotechnologies: problems, solutions, outlook. Agrochemical Herald. 2016;1:15–21.

European Biostimulants Industry Council [Internet]. 2019 [cited 2019 Jun 19]. Available from: http://www.biostimulants.eu/

Ertani A, Francioso O, Tugnoli V, Righi V, Nardi S. Effect of commercial Lignosulfonate-Humate on Zea mays L. metabolism. J Agric Food Chem. 2011;59:11940–11948. https://doi.org/10.1021/jf202473e

Jannin L, Arkoun M, Ourry A, Laîné P, Goux D, Garnica M, et al. Microarray analysis of humic acid effects on Brassica napus growth: involvement of N, C and S metabolisms. Plant Soil. 2012;359:297–319. https://doi.org/10.1007/s11104-012-1191-x

Craigie JS. Seaweed extract stimuli in plant science and agriculture. J Appl Phycol. 2011;23:371–393. https://doi.org/10.1007/s10811-010-9560-4

Ertani A, Pizzeghello D, Francioso O, Sambo P, Sanchez-Cortes S, Nardi S. Capsicum chinensis L. growth and nutraceutical properties are enhanced by biostimulants in a long-term period: chemical and metabolomic approaches. Front Plant Sci. 2014;5:375. https://doi.org/10.3389/fpls.2014.00375

Colla G, Rouphael Y, Canaguier R, Svecova E, Cardarelli M. The biostimulant action of a plant-derived protein hydrolysate produced through enzymatic hydrolysis. Front Plant Sci. 2014;5:448. https://doi.org/10.3389/fpls.2014.00448

Ertani A, Schiavon M, Muscolo A, Nardi S. Alfalfa plant-derived biostimulant stimulate short-term growth of salt stressed Zea mays L. plants. Plant Soil. 2013;364:145–158. https://doi.org/10.1007/s11104-012-1335-z

Rodríguez-Morgado B, Gómez I, Parrado J, Tejada M. Behaviour of oxyfluorfen in soils amended with edaphic biostimulants/biofertilizers obtained from sewage sludge and chicken feathers. Effects on soil biological properties. Environ Sci Pollut Res Int. 2014;21:11027–11035. https://doi.org/10.1007/s11356-014-3040-3

Rouphael Y, de Micco V, Arena C, Raimondi G, Colla G, de Pascale S. Effect of Ecklonia maxima sea weed extract on yield, mineral composition, gas exchange and leaf anatomy of zucchini squash grown under saline conditions. J Appl Phycol. 2017;29:459–470. https://doi.org/10.1007/s10811-016-0937-x

Colla G, Nardi S, Cardarelli M, Ertani A, Lucini L, Canaguier R, et al. Protein hydrolysates as biostimulants in horticulture. Sci Hortic (Amsterdam). 2015;96:28–38. https://doi.org/10.1016/j.scienta.2015.08.037

Nardi S, Pizzeghello D, Schiavon M, Ertani A. Plant biostimulants: physiological responses induced by protein hydrolyzed-based products and humic substances in plant metabolism. Sci Agric. 2016;73:18–23. https://doi.org/10.1590/0103-9016-2015-0006

Brown P, Saa S. Biostimulants in agriculture. Front Plant Sci. 2015;6:671. https://doi.org/10.3389/fpls.2015.00671

Schaafsma G. Safety of protein hydrolysates, fractions thereof and bioactive peptides in human nutrition. Eur J Clin Nutr. 2009;63:1161–1168. https://doi.org/10.1038/ejcn.2009.56

Grabowska A, Kunicki E, Sękara A, Kalisz A, Wojciechowska R. The effect of cultivar and biostimulant treatment on the carrot yield and its quality. Vegetable Crops Research Bulletin. 2012;77:37–48. https://doi.org/10.2478/v10032-012-0014-1

Cavani L, Halle AT, Richard C, Ciavatta C. Photosensitizing properties of protein hydrolysate-based fertilizers. J Agric Food Chem. 2006;54:9160–9167. https://doi.org/10.1021/jf0624953

Schiavon M, Ertani A, Nardi S. Effects of an alfalfa protein hydrolysate on the gene expression and activity of enzymes of TCA cycle and N metabolism in Zea mays L. J Agric Food Chem. 2008;56:11800–11808. https://doi.org/10.1021/jf802362g

de Lucia B, Vecchietti L. Type of bio-stimulant and application method effects on stem quality and root system growth in L.A. Lily. Eur J Hortic Sci. 2012;77:10–15.

Cerdán M, Sánchez‐Sánchez A, Jordá JD, Juárez M, Sánchez‐Andreu J. Effect of commercial amino acids on iron nutrition of tomato plants grown under lime-induced iron deficiency. J Plant Nutr Soil Sci. 2013;176:859–866. https://doi.org/10.1002/jpln.201200525

Colla G, Svecová E, Cardarelli M, Rouphael Y, Reynaud H, Canaguier R, et al. Effectiveness of a plant-derived protein hydrolysate to improve crop performances under different growing conditions. Acta Hortic. 2013;1009:175–179. https://doi.org/10.17660/ActaHortic.2013.1009.21

Botta A. Enhancing plant tolerance to temperature stress with amino acids: an approach to their mode of action. Acta Hortic. 2013;1009:29–35. https://doi.org/10.17660/ActaHortic.2013.1009.1

Leipner J, Stamp P. Chilling stress in maize seedlings. In: Bennetzen JL, Hake SC, editors. Handbook of maize: its biology. Heidelberg: Springer; 2009. p. 291–310. https://doi.org/10.1007/978-0-387-79418-1_15

Zaidi PH, Yadav M, Maniselvan P, Khan R, Shadakshari TV, Singh RP, et al. Morpho-physiological traits associated with cold stress tolerance in tropical maize (Zea mays L.). Maydica. 2010;55:201–208.

Stamp P. Chilling tolerance of young plants demonstrated on the example of maize (Zea mays L.). In: Geisler G, editor. Advances in agriculture and crop science. Vol. 7. Berlin: Paul Parey; 1984. p. 1–84.

Lichtenthaler H. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol. 1987;148:350–382. https://doi.org/10.1016/0076-6879(87)48036-1

Genty B, Briantais J, Baker N. The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta. 1989;990:87–92. https://doi.org/10.1016/S0304-4165(89)80016-9

Schreiber U. Pulse amplitude modulation (PAM) fluorometry and saturation pulse method: an overview. In: Papageorgiou GC, editor. Chlorophyll a fluorescence: a signature of photosynthesis Dordrecht: Kluwer Academic; 2004. p. 279–319. https://doi.org/10.1007/978-1-4020-3218-9_11

Haldimann P. Low growth temperature-induced changes to pigment composition and photosynthesis in Zea mays genotypes differing in chilling sensitivity. Plant Cell Environ. 1998;21(2):200–208. https://doi.org/10.1046/j.1365-3040.1998.00260.x

Bolhar-Nordenkampf H, Oquist G. Chlorophyll fluorescence as a tool in photosynthesis research. In: Hall DO, Scurlock JMO, Bolnar-Nordenkampf HR, Leegood RC, Long SP, editors. Photosynthesis and production in a changing environment: a field and laboratory manual. London: Chapman and Hall; 1993. p. 193–205. https://doi.org/10.1007/978-94-011-1566-7_12

Bilska A, Sowiński P. Closure of plasmodesmata in maize (Zea mays) at low temperature: a new mechanism for inhibition of photosynthesis. Ann Bot. 2010;106(5):675–686. https://doi.org/10.1093/aob/mcq169

Cholakova-Bimbalova R, Vassilev A. Influence of biostimulants on growth and photosynthetic performance of young maize (Z. mays L.) plants exposed to chilling stress. Proceedings Conference of Agronomy Students. 2017;10(10):28–37.

Sowinski P, Rudzinska-Langwald A, Adamczyk J, Kubica I, Fronk J. Recovery of maize seedlings growth, development and photosynthetic efficiency after initial growth at low temperature. J Plant Physiol. 2005;162:67–80. https://doi.org/10.1016/j.jplph.2004.03.006

Al-Shoaibi A. Photosynthetic response to the low temperature in elephant grass (Peninsetum purpureum) and Zea mays. Int J Bot. 2008;4(3):309–314. https://doi.org/10.3923/ijb.2008.309.314

Kosová K, Haisel D, Tichá I. Photosynthetic performance of two maize genotypesas affected by chilling stress. Plant Soil Environ. 2005;51:206–212. https://doi.org/10.17221/3575-PSE

Schiavon M, Pizzeghello D, Muscolo A, Vaccaro S, Francioso O, Nardi S. High molecular size humic substances enhance phenylpropanoid metabolism in maize (Zea mays L.). J Chem Ecol. 2010;36:662–669. https://doi.org/10.1007/s10886-010-9790-6

Teixeira, W, Fagan E, Soares L, Umburanas R, Reichardt K, Neto D. Foliar and seed application of amino acids affects the antioxidant metabolism of the soybean crop. Front Plant Sci. 2017;8:327. https://doi.org/10.3389/fpls.2017.00327

Ertani A, Schiavon M, Nardi S. Transcriptome-wide identification of differentially expressed genes in Solanum lycopersicon L. in response to an alfalfa-protein hydrolysate using microarrays. Front Plant Sci. 2017;8:1159. https://doi.org/10.3389/fpls.2017.01159