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1589168784 145 20.Pdf Plant Physiology and Biochemistry 136 (2019) 188–195 Contents lists available at ScienceDirect Plant Physiology and Biochemistry journal homepage: www.elsevier.com/locate/plaphy Research article Exogenous γ-aminobutyric acid treatment improves the cold tolerance of zucchini fruit during postharvest storage T ∗ Francisco Palmaa, ,1, Fátima Carvajala,b,1, Raquel Jiménez-Muñoza, Amada Pulidoa, Manuel Jamilenac, Dolores Garridoa a Department of Plant Physiology, Facultad de Ciencias, University of Granada, Fuentenueva s/n, 18071, Granada, Spain b Plant Breeding, Wageningen University and Research, Droevendaalsesteeg 1, 6708PB, Wageningen, Netherlands c Department of Biology and Geology, Agrifood Campus of International Excellence (CeiA3), CIAIMBITAL, University of Almería, La Cañada de San Urbano s/n, 04120, Almería, Spain ARTICLE INFO ABSTRACT Keywords: This work examines the effect of a treatment with 1 mM of γ-aminobutyric acid (GABA) on zucchini fruit during Chilling postharvest cold storage. Specifically, the effect of GABA on postharvest quality was measured, as well as its Zucchini implication in the GABA shunt and other related metabolic pathways. The treatments were performed in Sinatra, γ -aminobutyric acid a variety of zucchini highly sensitive to low-temperature storage. The application of GABA improved the quality Putrescine of zucchini fruit stored at 4 °C, with a reduction of chilling-injury index, weight loss, and cell death, as well as a GABA shunt lower rate of electrolyte leakage. GABA content was significantly higher in the treated fruit than in the control ATP NADH fruit at all times analyzed. At the end of the storage period, GABA-treated fruit had higher contents of both proline and putrescine. The catabolism of this polyamine was not affected by exogenous GABA. Also, over the long term, the treatment induced the GABA shunt by increasing the activities of the enzymes GABA transaminase (GABA-T) and glutamate decarboxylase (GAD). GABA-treated fruit contained higher levels of fumarate and malate than did non-treated fruit, as well as higher ATP and NADH contents. These results imply that the GABA shunt is involved in providing metabolites to produce energy, reduce power, and help the fruit to cope with cold stress over the long term. 1. Introduction endogenous GABA content in fruit during cold storage along with an induction of the GABA-shunt pathway for long-term storage (Palma γ-aminobutyric acid (GABA), a non-proteinogenic amino acid, has et al., 2014). The GABA shunt is the conversion of glutamate to GABA different functions in plant growth and development (Li et al., 2018). Its and its catabolism to succinate by three enzymatic reactions (Shelp accumulation has been described under several abiotic stress conditions et al., 1999). First, glutamate is α-decarboxylated to form GABA by the such as heat and cold, salinity, drought, hypoxia, and mechanical da- cytosolic enzyme glutamate decarboxylase (GAD). GABA is then mage (Kinnersley and Turano, 2000; Ramesh et al., 2015; Shelp et al., transported to the mitochondria and converted to succinic semi- 1999). Under cold storage, an accumulation of GABA correlates with a aldehyde via transamination by GABA transaminase (GABA-T). Finally, higher capacity to cope with adverse postharvest conditions in several the oxidation of succinic semialdehyde to succinate coupled with the crops such as loquat (Cao et al., 2012), banana (Wang et al., 2016), and production of NADH is catalyzed by succinic semialdehyde dehy- bamboo shoot (Wang et al., 2017). GABA acts as an inhibitor of mal- drogenase (SSADH). Succinate produced by this short pathway can ondialdehyde formation during lipid peroxidation (Deng et al., 2010), enter the tricarboxylic acid (TCA) cycle. maintains membrane integrity (Aghdam et al., 2015), increases anti- Zucchini fruit is highly sensitive to cold storage, developing damage oxidant metabolism and GABA-shunt pathway (Aghdam et al., 2016; Li on the exocarp surface and suffering a weight and firmness loss when et al., 2016; Malekzadeh et al., 2017), and helps to maintain osmotic kept at temperatures below 8-10 °C. Sensitivity to cold storage in zuc- adjustment (Li et al., 2016). In the case of zucchini (Cucurbita pepo L. chini is variety dependent (Carvajal et al., 2011; Megías et al., 2016) morphotype Zucchini), we have previously reported a decrease of with Sinatra being among the most chilling-sensitive varieties analyzed ∗ Corresponding author. E-mail address: [email protected] (F. Palma). 1 These authors have contributed equally to this work. https://doi.org/10.1016/j.plaphy.2019.01.023 Received 31 October 2018; Received in revised form 21 December 2018; Accepted 21 January 2019 Available online 22 January 2019 0981-9428/ © 2019 Elsevier Masson SAS. All rights reserved. F. Palma et al. Plant Physiology and Biochemistry 136 (2019) 188–195 for this crop (Carvajal et al., 2018). Over the long term, a greater in- derivatized with dansyl chloride following the method of Flores and duction of the GABA shunt has been detected in cold-tolerant varieties Galston (1982). Dansylputrescine was measured by HPLC (Agilent 1260 of this species, and also in cold-sensitive fruit after treatments that Infinity) with a 4.6 mm × 250 mm C18 column and a fluorometer improve chilling tolerance during fruit postharvest, such as a pre- (excitation/emission wavelengths 415/510 nm). Dansylputrescine was − conditioning treatment at moderate temperature before cold storage or eluted at a flow rate of 1.5 mL min 1 using a elution gradient with an exogenous application of putrescine (Carvajal et al., 2015b; Palma water (A) and acetonitrile (B). The gradient profile, expressed as (t et al., 2015). The induction of the GABA shunt reportedly correlates [min]; %B), was: (0; 70%), (4.5; 70%), (9; 100%), (14; 100%), (15; with greater oxidative deamination of the polyamine putrescine cata- 70%). lyzed by the diamine oxidase (DAO), an enzyme whose end product is a precursor of GABA different from glutamate, 4-aminobutyraldehyde 2.5. Alanine, glutamate, and proline content (Shelp et al., 2012). The aim of this work was in the first place to elucidate the effect of a Alanine, glutamate, and proline were analyzed following Palma GABA treatment on postharvest quality of a chilling sensitive variety of et al. (2015). The amino acids were extracted with ethanol/chloroform/ zucchini, and to study the implications of the GABA-shunt pathway in HCl 0.1 N (12/5/1; v/v/v) at a proportion of 1:7 (w/v). Norvaline and − cold tolerance when exogenous GABA is applied to the fruit. sarcosine (50 nmol mL 1) were used as internal standards. The extract was centrifuged for 10 min at 4 °C and 3500 g, and the supernatant was 2. Materials and methods separated into chloroform and aqueous phases by the addition of HCl 0.1 N and CHCl3. The aqueous phase was filtered and derivatized with 2.1. Postharvest treatment and plant material o-phthalaldehyde (OPA) and fluorenylmethylchlo-roformate (FMOC). These amino acids were measured by HPLC (Agilent 1260 Infinity) with Zucchini fruit (Cucurbita pepo L. morphotype Zucchini) of the a Zorbax Eclipse-AAA4.6 mm × 150 mm column and a fluorometer commercial variety Sinatra (Clause-Tezier) were supplied by La Ñeca using excitation and emission wavelengths of 340 and 450 nm S.L. The fruit were separated randomly into replicates before treatment, (0–15 min) and 266 and 305 nm (15–26 min). Alanine, glutamate, and − and each replicate was treated independently. Three replicates were proline were eluted at a flow rate of 2 mL min 1 using an elution gra- prepared per treatment (control and GABA 1 mM), and storage period dient with acetonitrile/methanol/water mix (45/45/10, v/v/v) (A) and (0, 1, 3, 5, 10, 14 days), each consisting of 6 fruits (198 fruits in total). sodium phosphate 40 mM pH 7.8 (B). The gradient profile, expressed as Based on previous studies (Malekzadeh et al., 2012, 2014; Shang et al., (t [min]; %A), was: (0; 0%), (1.9; 0%), (18.1; 57%), (18.6; 100%), 2011), and on a preliminary experiment (data not shown), we selected (22.3; 100%), (23.2; 0%), and (26; 0%). 1 mM GABA as the most suitable concentration. Fruit were submerged during 20 min at 20 °C in 1 mM of γ-aminobutyric acid (GABA) or in the 2.6. GABA content case of the control, distilled water. Each replicate was submerged in a volume of 5 L. Finally, fruit were dried 2 h before being stored in a GABA extraction and quantification was conducted as in Palma controlled environmental chamber in darkness at 4 °C and 85–90% RH et al. (2014). Exocarp tissue was homogenized with ethanol/chloro- during 1, 3, 5, 10, 14 days. After weight loss and chilling-injury index form/HCl 0.1 N (12/5/1; v/v/v) at a proportion of 1:10 (w/v) and were evaluated according to Martínez-Téllez et al. (2002), in each centrifuged at 4 °C and 8000 g for 10 min. The supernatant was sepa- biological replicate the exocarp was separated, frozen in liquid ni- rated into chloroform and aqueous phases by the addition of HCl 0.1 N trogen, pulverized, and stored at −80 °C. and CHCl3. The aqueous phase was filtered and evaporated using a nitrogen flow. Dry residues were resuspended in acetonitrile/methanol 2.2. Electrolyte leakage and cell-death assay (1:4). GABA was separated by Acquity UPLC with a Acquity UPLC BEH C18 1.7 μm, 2.1 mm × 50 mm column and quantified by Xevo TQ-S Electrolyte leakage was determined following Mao et al. (2007). triple quadrupole mass spectrometer in the positive electro-spray ioni- From each treatment, four replicates were measured, each consisting of zation mode with the following transitions: m/z 103.84 → 62.78 (cone 10 discs excised from exocarp with a cork borer.
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