Elsevier

Journal of Plant Physiology

Volume 189, 15 September 2015, Pages 97-104
Journal of Plant Physiology

Physiology
The effects of cold stress on the phenolic compounds and antioxidant capacity of grapevine (Vitis vinifera L.) leaves

https://doi.org/10.1016/j.jplph.2015.10.002Get rights and content

Abstract

According to some estimates, a 70% increase in crop yield could be achieved if the environmental conditions were close to the optimum ones for a given plant, which is why the identification and control of adverse environmental effects is a top priority in many countries worldwide. This paper contains a discussion of the changes in selected elements of the secondary metabolism in the leaves of two grapevine varieties (Vitis vinifera L.) with a different degree of tolerance to cold stress during prolonged and constant low temperature stress. The analyses have shown that the more-tolerant variety was characterized by a higher content of phenolic compounds, better radical-scavenging capacity and stronger reducing power. However, the cold stress caused a decrease in the concentration of the phenolics and decreased the scavenging capacity in the leaves of both varieties. Four phenolic acids have been identified in the extracts from the leaves of both grapevines: caffeic acid, p-coumaric acid, ferulic acid and a caffeic acid derivative. Caffeic acid appeared in the highest concentrations in all the leaf extracts. Additionally, it has been noted that in the leaves of the varieties susceptible and tolerant to cold stress, the prolonged exposure to low temperature caused a considerable reduction of the content of all identified phenolic acids. The results of the analyses have demonstrated large differences in the functioning of the secondary metabolism in response to the same stressor.

Introduction

Low temperature is one of the major factors limiting the geographical distribution of plants. Stress factors have a negative influence on the growth and development of plants. Cold is also the main reason why crop plantations are geographically limited; additionally, it is responsible for lower volumes and decreased quality of yields (Passioura, 2007, Cattivelli et al., 2008, Farooq et al., 2009). In the course of evolution, many plant species growing in our climate have acquired tolerance to periodically occurring low temperatures (Nayyer et al., 2007). In contrast, plants from warmer climates, such as grapevines, are more sensitive to cold. However, there are many grapevine varieties that show a wide range of tolerance to low temperatures. The most resistant is Vitis amurensis, which can survive at temperatures falling to -40 °C (Ma et al., 2010). Low temperatures induce secondary oxidative stress, which causes metabolic changes in cells (Bohenert et al., 1995, Kranner et al., 2010). Cold stress reduced the water uptake by plants, which leads to changes in the structure of cellular membranes and distorts the selective transport carried out by these membranes (Larcher, 1995, Bray, 2009). Subsequently, destabilization of nucleic acid structure and alteration of enzyme activity may be observed (Lee et al., 2009, Dumont et al., 2011). Low temperature also reduces the rate of photosynthesis and disturbs the redox homeostasis in cells (Asada, 1999), which in turn may lead to secondary oxidative stress and production of reactive oxygen species (ROS) (Asada, 2006). ROS function as signal molecules, but their excessive accumulation in cells causes disruptions of electron transport in mitochondria and chloroplasts. This disruption can lead to considerable damage to key cellular components, such as proteins, nucleic acids and lipids located in cellular membranes (Aroca et al., 2003, Imlay, 2003, Murata et al., 2012). Consequently, alterations in the cellular genetic programme occur. The synthesis of compounds will help reinstate homeostasis (Gilmour et al., 2000). Secondary metabolic products, which are intensively synthesized under stress, act as antioxidants (Nascimento and Fett-Neto, 2010). This group of compounds protects cells against the negative effects of ROS, as well as against lipid peroxidation, protein denaturation and DNA damage (Kranner et al., 2002, Mittler, 2002, Allakhverdiev et al., 2008). Phenolic acids are metabolites endowed with a considerable antioxidant and radical scavenging potential. Phenolic acids are a large group of organic compounds (Gumul et al., 2007) that are widely distributed in plants (Javanmardi et al., 2003). Environmental stresses may either increase or decrease the synthesis of phenolic compounds in cells. Phenolic compounds are able to scavenge ROS, form complexes with metals and raise the activity of oxidative enzymes (Amarowicz et al., 2004, Negro et al., 2003, Caillet et al., 2006, Amarowicz and Weidner, 2009, Elavarthi and Martin, 2010). An increased activity of antioxidant enzymes improves the resistance of plants to stressors (Hayat et al., 2010). Phenols constitute a large group of compounds that may be divided into five subgroups: coumarins, lignins, flavonoids, phenolic acids and tannins (Gumul et al., 2007). Precursors for the synthesis of phenolic compounds are formed in the shikimic acid and chorismic acid pathways. The metabolism of chorismic acid leads to l-phenylalanine and l-tyrosine. Tyrosine biosynthesis leads to the production of p-coumaric acid and L-phenylalanine synthesis leads to the generation of cinnamic acid. As a result of the methylation, hydration and dehydration of cinnamic acid, phenolic acids are produced, which are an element of the response of plants to abiotic stresses (Dixon and Paiva, 1995). Some phenolic compounds, such as phenolic acids or flavonoids, are well known and present in most plant species (Jwa et al., 2006). Recently, more attention has been paid to natural antioxidants. Phenolic acids are biologically active substances (Dueñas et al., 2009); in addition to playing a significant role in processes that constitute the self-protection strategy of plants, phenolic acids have a beneficial influence on people and animals (Franca et al., 2001, Amarowicz and Weidner, 2009).

The metabolism and accumulation of phenolic compounds in grapevine seedlings can be modified during biotic and abiotic stress (Smith and Read, 2008, Webb et al., 2013). Many researchers have studied the adverse effect of low temperature on the growth and development of plants. However, too little attention has been paid to the role of phenolic compounds and their antioxidant properties in a situation of prolonged cold stress affecting young plants, which are the most sensitive to its influence.

The purpose of this study has been to compare changes in the quantities of phenolic compounds and to analyse the fluctuations in the antioxidant activity and reducing power of extracts from the leaves of two varieties of Vitis vinifera, which presented different degrees of tolerance to cold during a prolonged exposure to low temperatures.

Section snippets

Plant material

The material for the study consisted of leaves of two cultivars of the grapevine V. vinifera L. One cultivar was tolerant to chilling stress (Maerchal Foch—MF) and the second cultivars was sensitive to this stress (Kiszmisz Łuczistyj—KL). The seedlings of the grapevine used for testing were purchased from the company “Professional Grapevine Seedlings” in Józefosław (Poland).

Experimental conditions

The seedling were transferred into large pots and grown for the next 8 weeks in a climatic chamber under optimal

Dry matter content

The changes of the percentage of dry matter in the grapevine leaves are illustrated in Fig. 1. The leaves of all grapevine varieties submitted to the long-lasting stress of low temperature had a much higher content of dry matter than the leaves of the grapevine seedlings growing under optimal conditions. The dry matter content in the leaves of the grapevine variety tolerant to cold stress i.e., Maerchal Foch, reached 26.8% in the control (TC) and 30.9% in the sample submitted to cold stress

Discussion

The results of our analyses indicate that the two examined grapevine varieties, which are popular on European plantations, demonstrate substantial differences in their tolerance to long-lasting cold stress. Dry matter determination is one of the most fundamental analytical methods to test the influence of a stressor on a plant. Our observations suggest that the grapevine variety tolerant to low temperature was characterized by much higher dry matter content in the leaves during the stress

Conclusion

The research presented in this paper has demonstrated that the total content of phenolics and phenolic acids, antioxidant activity and reducing power decrease in the grapevine leaves under long-term cold stress. This indicates that some elements of the secondary metabolism in plants slow down during long-term cold stress. Consequently, the plant reduces its energy expenditure until the end of the stressor activity. This is one of the survival strategies deployed under unfavourable environmental

Acknowledgement

The present study was supported by Grant UMO-2013/11/N/NZ9/00099 from National Science Centre in Poland.

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