Abstract
Xyloglucan oligosaccharides (XGOs), derived from the hydrolysis of plant cell wall xyloglucan, are a novel class of biostimulants that exert positive effects on plant growth and morphology and can enhance plant stress tolerance. The aim of this study was to determine the influence of the application of exogenous Tamarindus indica L. cell wall-derived XGOs on Nicotiana tabacum L. tolerance to salt stress by evaluating morphology, physiological, and metabolic changes. N. tabacum plants were grown in agar-gelled media for 2 mo under salt stress with 100 mM of sodium chloride (NaCl) ± 0.1 μM XGOs. The germination percentage (GP), number of leaves (NL), foliar area (FA), primary root length (PRL), and density of lateral roots (DLR) were measured. In addition, unaffected 21-d-old N. tabacum plants were treated with a salt shock (100 mM NaCl) ± 0.1 μM XGOs. Proline, total chlorophyll, and total carbonyl levels, in addition to lipid peroxidation degree and activities of four enzymes related to oxidative stress, were quantified. The results indicated that XGOs significantly improved N. tabacum plants development after exposure to salt stress. XGOs caused a significant increase in NL and PRL, promoted lateral root formation, and produced an increase in proline and total chlorophyll contents, while reducing protein oxidation and lipid peroxidation. Although the XGOs modulated the activity of the enzymes analyzed, they were not statistically different from the salt control. It was concluded that XGOs may act as metabolic inducers that trigger the physiological responses that counteract the negative effects of oxidative stress under saline conditions.
Similar content being viewed by others
References
Abrol IP, Yadav JSP, Massoud FI (1988) Salt-affected soils and their management. vol n.° 39. Food and Agriculture Organization of the United Nations
Acosta A (2006) Estudio del efecto de dos oligosacarinas sintéticas sobre el cultivo del tabaco (Nicotiana tabacum L.). Máster en Ciencias en Biología Vegetal, Universidad de la Habana
Aebi H (1984) Catalase in vitro. In: methods in enzymology, vol volume 105. Academic press, pp 121-126
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066
Cabrera JC et al (2012) Practical use of oligosaccharins in agriculture. Acta Hort 1009:195–212
Carillo P, Gibon Y (2011) PROTOCOL: extraction and determination of proline. PrometheusWiki. Accessed 2017-07-10 20:08:33 UTC 2017
Carlberg I, Mannervik B (1985) Glutathione reductase. Meth Enzymol 113:484–490
Chen S et al (2016) Effects of uneven vertical distribution of soil salinity under a buried straw layer on the growth, fruit yield, and fruit quality of tomato plants. Sci Hort 203:131–142
Conover WJ (1999) Practical nonparametric statistics. Wiley series in probability and statistics, Third edn. Wiley, New York
Cutillas-Iturralde A, Peña MJ, Zarra I, Lorences EP (1998) A xyloglucan from persimmon fruit cell walls. Phytochem 48:607–610
de Azevedo Neto AD, Prisco JT, Enéas-Filho J, Abreu CEB, Gomes-Filho E (2006) Effect of salt stress on antioxidative enzymes and lipid peroxidation in leaves and roots of salt-tolerant and salt-sensitive maize genotypes. Environ Exp Bot 56:87–94
Di Rienzo J, Casanoves F, Balzarini M, Gonzalez L, Tablada M, Robledo C (2011) InfoStat versión 2015. Universidad Nacional de Córdoba, Argentina, FCA
du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hort 196:3–14
Dubrovsky JG, Gambetta GA, Hernandez-Barrera A, Shishkova S, Gonzalez I (2006) Lateral root initiation in Arabidopsis: developmental window, spatial patterning, density and predictability. Ann Bot 97:903–915
Fry SC (1994) Oligosaccharins as plant growth regulators. Biochem Soc Symp 60:5–14
Fry SC, Aldington S, Hetherington PR, Aitken J (1993a) Oligosaccharides as signals and substrates in the plant cell wall. Plant Physiol 103:1–5
Fry SC et al (1993b) An unambiguous nomenclature for xyloglucan-derived oligosaccharides. Physiol Plant 89:1–3
Garcı́a-Limones C, Hervás A, Navas-Cortés JA, Jiménez-Daı́z RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp.ciceris. Physiol Mol Plant Path 61:325–337
González-Pérez L et al (2012) Oligosaccharins and Pectimorf® stimulate root elongation and shorten the cell cycle in higher plants. Plant Growth Regul 68:211–221
Gonzalez-Perez L et al (2014) In tobacco BY-2 cells xyloglucan oligosaccharides alter the expression of genes involved in cell wall metabolism, signalling, stress responses, cell division and transcriptional control. Mol Biol Rep 41:6803–6816
González-Pérez L et al (2018) Application of exogenous xyloglucan oligosaccharides affects molecular responses to salt stress in Arabidopsis thaliana seedlings. J Soil Sci Plant Nut 18:1187–1205
Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A (2012) Role of proline under changing environments: a review. Plant Signal Behav 7:1456–1466
Huang Z, Zhao L, Chen D, Liang M, Liu Z, Shao H, Long X (2013) Salt stress encourages proline accumulation by regulating proline biosynthesis and degradation in Jerusalem artichoke plantlets. PLoS One 8:e62085
Jolliffe I (2002) Principal component analysis. Springer series in statistics, 2nd edn. Springer-Verlag, New York
Kakkar P, Das B, Viswanathan PN (1984) A modified spectrophotometric assay of superoxide dismutase. Indian J Biochem Biophys 21:130–132
Larskaya IA, Gorshkova TA (2015) Plant oligosaccharides - outsiders among elicitors? Biochem Mosc 80:881–900
Levine RL et al (1990) Determination of carbonyl content in oxidatively modified proteins. In: Meth Enzymol, vol 186. Academic press, pp 464–478
Lucini L, Rouphael Y, Cardarelli M, Canaguier R, Kumar P, Colla G (2015) The effect of a plant-derived biostimulant on metabolic profiling and crop performance of lettuce grown under saline conditions. Sci Hort 182:124–133
Misaki A, Sekiya K, Yamatoya K (1997) Agent for inducing phytoalexin and method for inducing phytoalexin. United Stated Patent No. USO05602111A.
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358
O'Neill RA, Albersheim P, Darvill AG (1989) Purification and characterization of a xyloglucan oligosaccharide-specific xylosidase from pea seedlings. J Biol Chem 264:20430–20437
Park YB, Cosgrove DJ (2015) Xyloglucan and its interactions with other components of the growing cell wall. Plant Cell Physiol 56:180–194
Pilz J, Meineke I, Gleiter CH (2000) Measurement of free and bound malondialdehyde in plasma by high-performance liquid chromatography as the 2,4-dinitrophenylhydrazine derivative. Journal of Chromatography B: Biomed Sci App 742:315–325
Porra RJ (2002) The chequered history of the development and use of simultaneous equations for the accurate determination of chlorophylls a and b. Photosynth Res 73:149–156
Roy SJ, Negrao S, Tester M (2014) Salt resistant crop plants. Curr Opin Biotechnol 26:115–124
Santos CV (2004) Regulation of chlorophyll biosynthesis and degradation by salt stress in sunflower leaves. Sci Hort 103:93–99
Schluter D, Whitlock M (2015) The analysis of biological data. Second edn, Macmillan Learning
Stratistics M (2017) Biostimulants - Global Market Outlook (2017–2023). Stratistics MRC, USA
Vahdati K, Lotfi N (2013) Abiotic stress tolerance in plants with emphasizing on drought and salinity stresses in walnut. In: Vahdati K, Leslie C (eds) Abiotic stress - plant responses and applications in agriculture. InTech, Rijeka p Ch. 10
Vargas-Rechia C, Reicher F, Rita Sierakowski M, Heyraud A, Driguez H, Linart Y (1998) Xyloglucan octasaccharide XXLGol derived from the seeds of hymenaea courbaril acts as a signaling molecule. Plant Physiol 116:1013–1021
Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645
Yang C, Liu J, Dong X, Cai Z, Tian W, Wang X (2014) Short-term and continuing stresses differentially interplay with multiple hormones to regulate plant survival and growth. Mol Plant 7:841–855
Zhang X, Li K, Liu S, Zou P, Xing R, Yu H, Chen X, Qin Y, Li P (2017) Relationship between the degree of polymerization of chitooligomers and their activity affecting the growth of wheat seedlings under salt stress. J Agric Food Chem 65:501–509
Zhang X, Schmidt R (1999) Biostimulating turfgrasses. Grounds Maintenance 34:14–15
Zou P, Li K, Liu S, He X, Zhang X, Xing R, Li P (2016) Effect of sulfated Chitooligosaccharides on wheat seedlings (Triticum aestivum L.) under salt stress. J Agric Food Chem 64:2815–2821
Funding
This study was supported by Universidad de Las Américas (UDLA), Quito, Ecuador.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest. All authors have read and approved the submitted manuscript.
Additional information
Editor: Bin Tian
Rights and permissions
About this article
Cite this article
Páez-Watson, T., Álvarez-Suárez, J.M., Rivas-Romero, F. et al. Increased salinity stress tolerance of Nicotiana tabacum L. in vitro plants with the addition of xyloglucan oligosaccharides to the culture medium. In Vitro Cell.Dev.Biol.-Plant 56, 325–334 (2020). https://doi.org/10.1007/s11627-019-10048-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11627-019-10048-w