Abscisic acid stimulates anthocyanin accumulation in ‘Jersey’ highbush blueberry fruits during ripening

doi:10.1016/j.foodchem.2017.10.051

Food Chemistry

Volume 244, 1 April 2018, Pages 403-407

https://doi.org/10.1016/j.foodchem.2017.10.051 Get rights and content

Highlights

•
Exogenous ABA temporarily increased the level of ABA in ‘Jersey’ fruits.
•
Exogenous ABA had no obvious effect on fruit growth.
•
Exogenous ABA promoted fruit colouration during ripening.
•
Exogenous ABA accelerated the accumulation of anthocyanins.
•
Malvidin, delphinidin and petunidin glycosides were found to be major anthocyanins.

Abstract

Non-climacteric blueberry (Vaccinium spp.) fruits accumulate high levels of anthocyanins during ripening, which are a good source of dietary antioxidants. This study examined the effects of exogenous abscisic acid (ABA) application on fruit characteristics and anthocyanin accumulation in a northern highbush blueberry (V. corymbosum ‘Jersey’) during development. Fruits on shrubs were treated with 1 g L⁻¹ ABA before the initiation of fruit colouration. Application of ABA temporarily increased the level of ABA in the fruits during development. Exogenous ABA had no obvious effect on fruit growth, but stimulated fruit colouration by accelerating the accumulation of individual anthocyanins, mainly malvidin, delphinidin and petunidin glycosides. This is the first report to show that ABA promotes the accumulation of anthocyanins in blueberry fruits. However, exogenous ABA also promoted fruit softening, which is undesirable during harvest and shelf life.

Introduction

Fruits are classified as climacteric or non-climacteric according to their ripening characteristics. Climacteric fruits, such as apple, peach and banana, generate a burst of ethylene followed by an increase in respiration rate at the onset of ripening (Giovannoni, 2001). These changes act as a signal for the initiation of ripening in all climacteric fruits. However, the hormonal control of ripening in non-climacteric fruits remains largely unknown. Non-climacteric fruits exhibit no dramatic changes in ethylene production or respiration (Frenkel, 1972), and ripening cannot be triggered by application of exogenous ethylene (Janes, Chin, & Frenkel, 1978).

Abscisic acid (ABA) may be important in the ripening of some non-climacteric fruits, such as grape (Berli et al., 2011, Jeong et al., 2004, Peppi et al., 2008, Sandhu et al., 2011), strawberry (Jia et al., 2011, Li et al., 2011) and sweet cherry (Shen et al., 2014). Acceleration of fruit softening by exogenous ABA has been observed in many grape (Peppi et al., 2006, Peppi et al., 2007, Roberto et al., 2012) and strawberry (Li et al., 2014) cultivars. Fruit colouration is also promoted by exogenous ABA in grape (Jeong et al., 2004, Koyama et al., 2010, Koyama et al., 2014, Yamamoto et al., 2015), strawberry (Jia et al., 2011, Li et al., 2014) and sweet cherry (Shen et al., 2014). Shen et al. (2014) reported that silencing NCED, a gene encoding a key enzyme in the ABA biosynthesis pathway, resulted in a colourless phenotype in sweet cherry. These findings suggest that exogenous ABA up-regulates genes related to ripening, including those associated with cell wall modification and anthocyanin biosynthesis (Giribaldi et al., 2010, Koyama et al., 2010). However, it is unclear whether these properties are shared by all non-climacteric fruits, since some reports suggest that exogenous ABA has no effect on anthocyanin accumulation in southern highbush blueberry (Vaccinium darrowii; Buran et al., 2012) or lowbush blueberry (V. angustifolium; Percival & MacKenzie, 2007).

Non-climacteric highbush blueberry (V. corymbosum) fruits accumulate high levels of anthocyanins during ripening, leading to a highly noticeable colouration process (Frenkel, 1972, Janes et al., 1978, Zifkin et al., 2012). This development-related colouration makes highbush blueberries suitable for studies of ripening. The present study was conducted to characterise the effects of exogenous ABA application on morphological and physiological characteristics, especially anthocyanin accumulation, during fruit development in ‘Jersey’ northern highbush blueberry.

Section snippets

Plant materials and ABA treatments

Ten-year-old northern highbush blueberry (V. corymbosum ‘Jersey’) shrubs were grown at the experimental orchard of Seoul National University, Suwon, Republic of Korea.

Six weeks after full bloom, fruit clusters were dipped into 1 g L⁻¹ (±)-ABA (Sigma–Aldrich, St. Louis, MO, USA) solution for 1 min, according to the methods of Jeong et al. (2004) and Zhang, Yuan, and Leng (2009). The ABA concentration was chosen from our preliminary experiment. This study was in a randomised complete block design

Effects of exogenous ABA on fruit ABA concentration

Before exogenous ABA application, ABA concentrations in ‘Jersey’ highbush blueberry fruits were maintained below 2 µg g⁻¹ dry weight (DW) (data not shown). In untreated fruits, ABA concentration steadily increased and reached a maximum concentration of 9.6 µg g⁻¹ DW during the 12-day observation period (Fig. 1). Similar patterns were observed in ‘Rubel’ highbush blueberry (Zifkin et al., 2012), grape (Owen et al., 2009, Sun et al., 2010) and strawberry (Jia et al., 2011). However, exogenous ABA

Conclusion

Application of exogenous ABA temporarily increased the level of ABA in ‘Jersey’ northern highbush blueberry fruits during development. Exogenous ABA had no obvious effect on fruit growth, but stimulated non-climacteric fruit colouration by accelerating the accumulation of anthocyanins. The main anthocyanins identified were malvidin, delphinidin and petunidin glycosides. This is the first report to show that ABA has a positive effect on anthocyanin accumulation in blueberries. However, exogenous

Acknowledgements

This work was supported by the Basic Science Research Program of the National Research Foundation of Korea, funded by the Ministry of Education (2017R1D1A1B03028749).

References (36)

T.J. Buran et al.
Effects of exogenous abscisic acid on fruit quality, antioxidant capacities and phytochemical contents of southern highbush blueberries
Food Chemistry
(2012)
S. Dudonné et al.
Comprehensive analysis of phenolic compounds and abscisic acid profiles of twelve native Canadian berries
Journal of Food Composition and Analysis
(2015)
L. Jaakola
New insights into the regulation of anthocyanin biosynthesis in fruits
Trends in Plant Science
(2013)
S.T. Jeong et al.
Effects of plant hormones and shading on the accumulation of anthocyanins and the expression of anthocyanin biosynthetic genes in grape berry skins
Plant Science
(2004)
D. Li et al.
ABA and UV-C effects on quality, antioxidant capacity and anthocyanin contents of strawberry fruit (Fragaria ananassa Duch.)
Postharvest Biology and Technology
(2014)
S.R. Roberto et al.
Application timing and concentration of abscisic acid improve colour of ‘Benitaka’ table grape
Scientia Horticulturae
(2012)
A.K. Sandhu et al.
Effects of exogenous abscisic acid on antioxidant capacities, anthocyanins and flavonol contents of muscadine grape (Vitis rotundifolia) skins
Food Chemistry
(2011)
L.Y. Yamamoto et al.
Application of abscisic acid (S-ABA) to cv. Isabel grapes (Vitis vinifera × Vitis labrusca) for colour improvement: Effect on colour, phenolic composition and antioxidant capacity of their grape juice
Food Research International
(2015)
F.J. Berli et al.
Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols
Journal of Agricultural and Food Chemistry
(2011)
S.W. Chung et al.
Changes in anthocyanidin and anthocyanin pigments in highbush blueberry (Vaccinium corymbosum cv. Bluecrop) fruits during ripening
Horticulture, Environment and Biotechnology
(2016)

S. Forcat et al.

A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress

Plant Methods

(2008)

C. Frenkel

Involvement of peroxidase and indole-3-acetic acid oxidase isozyme from pear, tomato and blueberry fruits in ripening

Plant Physiology

(1972)

V. Gavrilova et al.

Separation, characterisation and quantification of phenolic compounds in blueberries and red and black currants by HPLC-DAD-ESI-MSⁿ

Journal of Agricultural and Food Chemistry

(2011)

J. Giovannoni

Molecular biology of fruit maturation and ripening

Annual Review of Plant Physiology and Plant Molecular Biology

(2001)

M. Giribaldi et al.

Proteomic analysis of the effects of ABA treatments on ripening Vitis vinifera berries

Journal of Experimental Botany

(2010)

P. Hugueney et al.

A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine

Plant Physiology

(2009)

R.S. Hunter et al.

The measurement of appearance

(1987)

H.W. Janes et al.

Respiratory upsurge in blueberries and strawberries as influenced by ethylene and acetaldehyde

Botanical Gazette

(1978)

Cited by (63)

Regulation of carotenoid metabolism and ABA biosynthesis during blueberry fruit ripening
2024, Plant Physiology and Biochemistry
Carotenoids and their derivates play critical physiologic roles in plants. However, these substrates and their metabolism have not been elucidated in fruit of blueberry (Vaccinium corymbosum). In this study, carotenoids and ABA were investigated by LC-MS and their biosynthesis were subject to proteomic analysis during fruit ripening. Activity of CCD1 and NCED1/3 were studied in vivo or in vitro. Also, effects of ethephon and 1-MCP on biosynthesis of carotenoid and ABA were investigated through the expression of corresponding genes using qPCR. As a result, carotenoid biosynthesis was prominently mitigated whereas its metabolism was enhanced during fruit ripening, which resulted in a decrease in the carotenoids. VcCCD1 could both cleave β-carotene, zeaxanthin and lutein at positions of 9, 10 (9′, 10′), which was mainly responsible for the degradation of these carotenoids. Interestingly, in the situation of mitigation of carotenoid biosynthesis, ABA still rapidly accumulated, which was mainly attributed to the upregulated expression of VcNCED1/3. Notably, VcNCED1/3 also showed a cleavage activity of all-trans-zeaxanthin and a stereospecific cleavage activity of 9-cis-carotene to generate C15-carotenal. The C15-carotenal could be potentially converted to ABA through ZEP-independent ABA biosynthetic pathway during blueberry fruit ripening. Similar to a nature natural maturation, ethylene accelerated the carotenoid degradation and ABA biosynthesis trough downregulating the expression of genes in carotenoid biosynthesis and upregulating the expression of genes in ABA biosynthesis. These information help understand the regulation of carotenoids and ABA, and effects of ethylene on the regulation during blueberry fruit ripening.
Hormonal regulation of anthocyanin biosynthesis for improved stress tolerance in plants
2023, Plant Physiology and Biochemistry
Due to unprecedented climate change, rapid industrialization and increasing use of agrochemicals, abiotic stress, such as drought, low temperature, high salinity and heavy metal pollution, has become an increasingly serious problem in global agriculture. Anthocyanins, an important plant pigment, are synthesized through the phenylpropanoid pathway and have a variety of physiological and ecological functions, providing multifunctional and effective protection for plants under stress. Foliar anthocyanin accumulation often occurs under abiotic stress including high light, cold, drought, salinity, nutrient deficiency and heavy metal stress, causing leaf reddening or purpling in many plant species. Anthocyanins are used as sunscreens and antioxidants to scavenge reactive oxygen species (ROS), as metal(loid) chelators to mitigate heavy metal stress, and as crucial molecules with a role in delaying leaf senescence. In addition to environmental factors, anthocyanin synthesis is affected by various endogenous factors. Plant hormones such as abscisic acid, jasmonic acid, ethylene and gibberellin have been shown to be involved in regulating anthocyanin synthesis either positively or negatively. Particularly when plants are under abiotic stress, several plant hormones can induce foliar anthocyanin synthesis to enhance plant stress resistance. In this review, we revisit the role of plant hormones in anthocyanin biosynthesis and the mechanism of plant hormone-mediated anthocyanin accumulation and abiotic stress tolerance. We conclude that enhancing anthocyanin content with plant hormones could be a prospective management strategy for improving plant stress resistance, but extensive further research is essentially needed to provide future guidance for practical crop production.
Ethylene promotes ABA biosynthesis by repressing the expression of miR161 in postharvest strawberry fruit
2023, Postharvest Biology and Technology
Both ethylene and abscisic acid (ABA) are identified to be crucial phytohormones that positively regulate strawberry fruit (Fragaria × ananassa Duch.) ripening. In this work, the interplay between ethylene and ABA involved in the ripening of strawberry fruit was explored. Results suggested that ethylene promoted ABA biosynthesis via repressing miR161 expression. Meanwhile, miR161 silencing (STTM161) verified that miR161 negatively regulated ABA biosynthesis via suppressing FaNCED1 expression. In addition, dual-luciferase reporter demonstrated the suppression of miR161 on the promoter of FaNCED1. These results illuminated a potential molecular mechanism of the collaboration between ethylene and ABA in postharvest strawberry fruit through miR161.
Integrated transcriptomics-proteomics analysis reveals the regulatory network of ethanol vapor on softening of postharvest blueberry
2023, LWT
Fruit firmness is an important trait of postharvest blueberry, and ethanol vapor treatment has been shown to can retard blueberry softening by inhibiting the degradation of cell wall polysaccharides in our previous work. However, fruit softening is a complex process regulated by many factors. Here, the regulation mechanism of ethanol mediated delaying blueberry softening at the levels of mRNA and protein were explored with integrated transcriptomics-proteomics analysis. Results revealed that, 9158 differentially expressed genes (DEGs) and 1223 differentially expressed proteins (DEPs) were identified in the ethanol vapor-treated blueberry (E20) compared with the control (C20) at the 20th day of cold storage, 351 correlation molecules (DEG/DEP) were obtained through correlation analysis. Ethanol treatment reduced the overall metabolism level of blueberry, downregulated the gene expression of polygalacturonase, glucan-1,3-β-glucosidase and endoglucanase in carbohydrate metabolism pathway, and slowed down the degradation of cell wall polysaccharides such as pectin and cellulose; downregulated the gene expression of ACC oxidase, the key enzyme for ethylene synthesis, reduced the production of ethylene, reducing the ripening and softening effect of ethylene on the fruit, and then delayed the softening process of blueberry fruit. Collectively, ethanol vapor is a promising technology for retarding the softening of fruit and vegetables.
Advances of anthocyanin synthesis regulated by plant growth regulators in fruit trees
2023, Scientia Horticulturae
Citation Excerpt :
The most important thing is that ABA treatment does not affect grape firmness (Lurie et al., 2009; Ferrara et al., 2013). However, for other non-climacteric fruits like highbush blueberry and strawberry, ABA also accelerates softening while promoting pigmentation, which is undesirable during harvest and shelf life (Jiang and Joyce, 2003; Oh et al., 2018). Taken together, ABA is superior to ethephon as a color enhancer to some extent.
Fruit color is an important indicator of fruit quality, which is mainly determined by anthocyanin accumulation. Therefore, increasing anthocyanin content is an important way to improve the nutritional and commodity value of fruits. Anthocyanin synthesis is not only regulated by internal genetic factors but also affected by external factors such as light, temperature and nutritional levels, etc. In addition, plant growth regulators also play an important role in the regulation of anthocyanin synthesis. They mainly affect anthocyanin synthesis by affecting physiological and biochemical metabolism, the expression of structural genes and the activity of MBW complex. In the production of fruit, the application of plant growth regulators is an important means of promoting coloration. But there are still many problems during application, such as incorrect application time, inappropriate application concentration and so on. This paper reviews the physiological and molecular mechanism of anthocyanin synthesis regulated by plant growth regulators. It concludes that exogenous application of abscisic acid, jasmonate and brassinosteroid can promote the accumulation of anthocyanin. By contrast, ethylene, auxin, cytokinin and gibberellin have dual effects on anthocyanin synthesis. This review provides a theoretical basis for further study on the molecular mechanism of plant growth regulators regulating anthocyanin accumulation and theoretical guidance for scientific and efficient application of plant growth regulators in fruit production.
Recovering high value-added anthocyanins from blueberry pomace with ultrasound-assisted extraction
2022, Food Chemistry: X
Food waste is a potential source to replace fresh materials for obtaining functional ingredients. Blueberry pomace contains considerable amounts of anthocyanins. In this study, we investigated ultrasonic-assisted extraction (UAE) of anthocyanins from blueberry pomace. We used a Box-Behnken design (BBD) to screen and optimize the important factors influencing yield. The optimum extraction conditions were a temperature of 40 °C, an ultrasonic power of 400 W and an extraction time of 40 min. The optimum yield was 108.23 mg/100 g DW. In addition, we used a cation column to separate anthocyanins, and optimized the chromatographic conditions of HPLC to analyze and identify the main anthocyanins. Thirteen anthocyanins were found in blueberry pomace, of which Malvidin-3-Galactoside (22.65 %) was the highest. These findings provide a theoretical basis and optimized process parameters for the recovery of high value-added anthocyanins from blueberry pomace with ultrasound-assisted extraction, thus facilitating the comprehensive utilization of blueberry pomace.

View all citing articles on Scopus

¹: These authors equally contributed to this work.

View full text

Abscisic acid stimulates anthocyanin accumulation in ‘Jersey’ highbush blueberry fruits during ripening

Highlights

Abstract

Introduction

Section snippets

Plant materials and ABA treatments

Effects of exogenous ABA on fruit ABA concentration

Conclusion

Acknowledgements

Food Chemistry

Journal of Food Composition and Analysis

Trends in Plant Science

Plant Science

Postharvest Biology and Technology

Scientia Horticulturae

Food Chemistry

Food Research International

Solar UV-B and ABA are involved in phenol metabolism of Vitis vinifera L. increasing biosynthesis of berry skin polyphenols

Journal of Agricultural and Food Chemistry

Changes in anthocyanidin and anthocyanin pigments in highbush blueberry (Vaccinium corymbosum cv. Bluecrop) fruits during ripening

Horticulture, Environment and Biotechnology

A rapid and robust method for simultaneously measuring changes in the phytohormones ABA, JA and SA in plants following biotic and abiotic stress

Plant Methods

Involvement of peroxidase and indole-3-acetic acid oxidase isozyme from pear, tomato and blueberry fruits in ripening

Plant Physiology

Separation, characterisation and quantification of phenolic compounds in blueberries and red and black currants by HPLC-DAD-ESI-MSn

Journal of Agricultural and Food Chemistry

Molecular biology of fruit maturation and ripening

Annual Review of Plant Physiology and Plant Molecular Biology

Proteomic analysis of the effects of ABA treatments on ripening Vitis vinifera berries

Journal of Experimental Botany

A novel cation-dependent O-methyltransferase involved in anthocyanin methylation in grapevine

Plant Physiology

The measurement of appearance

Respiratory upsurge in blueberries and strawberries as influenced by ethylene and acetaldehyde

Botanical Gazette

Separation, characterisation and quantification of phenolic compounds in blueberries and red and black currants by HPLC-DAD-ESI-MSⁿ