Elsevier

Postharvest Biology and Technology

Volume 97, November 2014, Pages 115-122
Postharvest Biology and Technology

Reduction of postharvest anthracnose and enhancement of disease resistance in ripening mango fruit by nitric oxide treatment

https://doi.org/10.1016/j.postharvbio.2014.06.013Get rights and content

Highlights

  • Nitric oxide (NO) inhibited anthracnose, Colletotrichum gloeosporioides, in mango fruit.

  • NO did not exert direct antifungal activity against C. gloeosporioides in vitro.

  • NO induced defense-related enzymes and inhibited ripening in mango fruit.

  • NO treatment could be a promising strategy for controlling mango anthracnose.

Abstract

Nitric oxide (NO) acts as an important signal molecule with diverse physiological functions in plants. In this study we investigated the effects and possible mechanisms of exogenous NO on anthracnose caused by Colletotrichum gloeosporioides in mango fruit. ‘Guifei’ mango fruit were treated with NO donor (sodium nitroprusside of 0.1 mM) at 25 °C for 5 min, inoculated with spore suspension of C. gloeosporioides after 24 h of NO treatment, and stored at ambient temperature (25 °C). NO treatment effectively suppressed lesion development on mango fruit inoculated with C. gloeosporioides, and lesion diameters at 2 through 8 d in NO-treated fruit averaged 30% lower than those in control fruit. Additionally, NO treatment reduced natural anthracnose incidence and severity of mango fruit ripened at ambient temperature, and the values of both parameters from 4 to 10 d of storage in NO-treated fruit averaged 40 and 45% lower, respectively, than those for control fruit. NO did not exhibit in vitro antifungal activity against C. gloeosporioides. NO treatment enhanced the activities of defense-related enzymes including phenylalanine ammonia-lyase (PAL), cinnamate-hydroxylase (C4H), 4-coumarate: CoA ligase (4CL), peroxidase (POD), β-1,3-glucanase (GLU) and chitinase (CHT). NO treatment also promoted the accumulation of total phenolics, flavonoids and lignin that might contribute to inhibition of the pathogen. In addition to antifungal efficacy, NO treatment delayed flesh softening, yellowing, and changes in soluble solids content (SSC) and titratable acidity (TA), and peaks of respiration rate and ethylene production during ripening. These results suggest that the resistance of NO-treated mango to anthracnose may be attributed to activation of defense responses as well as delay of ripening.

Introduction

Mango (Mangifera indica L.) is considered a functional tropical fruit due to its favorable flavor, superior taste and particular nutritional qualities (Sivakumar et al., 2011). However, the fruit are highly susceptible to various pathogens, leading to quality deterioration and reduced market value. Anthracnose, caused by Colletotrichum gloeosporioides (Penz), is one of the most serious postharvest diseases of mango fruit (Zhang et al., 2013). The pathogen infects immature fruit and remains latent until storage and ripening, when lesions progressively appear (Dodd et al., 1989). Traditionally, control of mango postharvest anthracnose has been performed with fungicides such as benomyl and prochloraz. However, because of issues associated with fungicide toxicity, environmental pollution, development of fungicide resistance in pathogens and potential risks on human health, alternative strategies for reducing postharvest disease have been required (Terry and Joyce, 2004).

Induction of resistance to pathogens by biotic or abiotic factors is becoming a promising approach for controlling postharvest diseases (Terry and Joyce, 2004). Previous studies have shown that application of exogenous chemical elicitors including salicylic acid (SA) (Zeng et al., 2006), acibenzolar-S-methyl (Zhu et al., 2008a), oxalic acid (Zheng et al., 2012), and β-aminobutyric acid (Zhang et al., 2013) suppressed anthracnose in harvested mango fruit.

Nitric oxide (NO), a highly reactive free radical gas, is recognized as a multifunctional signal molecule that participates in diverse physiological processes in phylogenetically distant species (Leshem et al., 1998, Belligni and Lamattina, 2001, Hong et al., 2008, Shi et al., 2012a). Postharvest application of NO, either through direct gas fumigation or by means of NO releasing agents including 3-morpholino sydnonimine, 2,2-(hydroxynitroso-hydrazine)-bisethanamine and sodium nitroprusside (SNP), has been shown to delay fruit ripening and senescence, as well as enhance tolerance to chilling stress in a number of climacteric and non-climacteric fruits (Leshem and Wills, 1998, Wills et al., 2000, Manjunatha et al., 2010, Zhao et al., 2011, Wang et al., 2013, Singh et al., 2013). Recently, the effect of NO on postharvest disease has also received attention. Treatment of tomato fruit with NO or its precursor (l-arginine) resulted in enhanced resistance against Botrytis cinerea and Rhizopus stolonifer, increased activities of defense-related enzymes, and promoted reactive oxyen species (ROS) metabolism (Fan et al., 2008, Lai et al., 2011b, Zheng et al., 2011a). Furthermore, Zheng et al. (2011b) reported that a fungal elicitor isolated from B. cinerea induced disease resistance of tomato fruit in parallel with increased NO and nitric oxide synthase activity. These findings indicate that NO signaling participates in systemic acquired resistance in fruit. However, although mango fruit is prone to pathogen infection and rapidly loses its commercial value after harvest, there is little information available on the inhibitory effects of postharvest NO application against C. gloeosporioides and possible defense mechanisms in mango and other tropical fruit.

The main objective of this study was to investigate the effects of NO on control of anthracnose caused by C. gloeosporioides in mango fruit during ripening at ambient temperature (25 °C). Evaluations addressed the antifungal activity against C. gloeosporioides in vivo and in vitro, the responses of defense-related enzymes and antifungal metabolites, and the influence on ripening.

Section snippets

Plant material

Mature green mango (M. indica L. cv. Guifei) fruit were harvested from a commercial orchard located in Dongfang city, Hainan Province of China. Fruit were packed in cartons and transported to the postharvest laboratory within 6 h. Fruit of uniform size and appearance without visible symptoms of disease and mechanical injury were selected for the experiments.

Pathogen

Isolation of C. gloeosporioides and preparation of spore suspensions (1 × 106 spores per milliliter) were performed as described in Zhang et

Results

In preliminary experiments, we investigated a range of SNP concentrations including 0.02, 0.05, 0.1, 0.2, 0.5, 1, 2 and 4 mM. SNP at 0.1 mM exhibited the best effect inhibiting mango fruit ripening and decay. By contrast, SNP at 1, 2 and 4 mM caused severe phytotoxicity as expressed by skin blackening. SNP at 0.1 mM was used for all experiments. According to reports of Delledonne et al. (1998) and Lai et al. (2011b), 0.1 mM SNP should generate about 0.5 μM NO in water at room temperature.

Discussion

Postharvest decay resulting from anthracnose is a major factor reducing the quality and shelf life of mango fruit. To control disease development of mango fruit, a number of alternatives to fungicides including heat treatment (Jacobi and Giles, 1997), edible coatings (Zhu et al., 2008b), 1-methylcyclopropene treatment in combination with controlled atmosphere storage (Sivakumar et al., 2012), antagonistic microorganisms (Kefialew and Ayalew, 2008), borate treatment (Shi et al., 2011), and

Acknowledgements

This research was supported by the China Postdoctoral Science Foundation (2013M540671), Scientific Foundation for the Returned Overseas Chinese Scholars, MOHRSS, China (2012), and Special Fund for Agro-scientific Research in the Public Interest, China (201203092-2).

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    These authors contributed equally to this work.

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