甜橙果实膳食纤维代谢机理研究
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摘要
柑橘果实中的膳食纤维(DF)、特别是对人体更加有益的可溶性膳食纤维(SDF)的含量十分丰富,因此开发和利用柑橘中的DF已成为当前研究的热点问题之一。本试验以红肉脐橙(Citrus sinensis Osbeck cv.Cara cara)、纽荷尔脐橙(Citrus sinensisOsbeck cv.Newhall)和塔罗科血橙(Citrus sinensis Osbeck cv.Tarocco Sangnine)为试材,研究了果实发育过程中DF各成分的变化规律及其主要调控因子的作用模式,探讨了不同贮藏条件和Ca、B等矿质元素处理对甜橙果实DF的影响,以期了解甜橙果实DF的代谢规律,为调控柑橘果实DF成分和功能产品的开发提供理论依据。主要研究结果如下:
(1)甜橙果实发育过程中DF及相关水解酶活性的变化规律。红肉脐橙、纽荷尔脐橙和塔罗科血橙果实发育过程中总膳食纤维(TDF)、SDF、不溶性膳食纤维(IDF)、总果胶(TP)、原果胶(Protopectin)、水溶性果胶(WSP)、纤维素(CEL)、半纤维素(HC)和木质素(lignin)等的含量以及多聚半乳糖醛酸酶(PG)、纤维素酶(Cx)、果胶酯酶(PE)和β-半乳糖苷酶(β-Gal)等的活性的测定。结果表明:3品种果实发育过程中TDF含量变化趋势基本一致,随着果实的成熟其含量逐渐减少;果肉中,塔罗科血橙TDF含量最少,纽荷尔次之,红肉脐橙最多:IDF含量变化趋势与TDF基本一致,而SDF与TDF相反;果实发育过程中果胶含量呈下降趋势,果肉中表现较果皮明显;WSP含量随着果实成熟不断增加;随着果实的发育,木质素和HC含量急剧下降,且果肉中木质素和HC含量与Cx活性呈显著负相关;PG活性在果实发育前期较低,随着果实的成熟迅速增加,在果实转色期其酶活性达到最大值后急剧下降;PE酶活性在果实发育前期的果肉中呈下降趋势,果实成熟前酶活性显著升高,果皮中呈下降趋势;β-Gal在果肉中随着果实发育酶活性逐渐降低,果皮中成熟前后差异不显著。
(2)不同贮藏条件下红肉脐橙果实DF及相关水解酶活性的变化规律。室内贮藏、留树贮藏条件下不同贮藏期的红肉脐橙果肉硬度、DF各成分的含量以及相关水解酶PG、Cx、PE和β-Gal等的活性的分析。结果表明:留树贮藏能够显著降低红肉脐橙果实TDF、IDF以及HC和木质素等的含量,提高SDF含量,留树贮藏后作为细胞壁主要成分的HC、木质素等不断降解,原果胶继续转化为WSP;果实贮藏期间Cx酶活性与HC含量呈显著负相关,留树贮藏Cx酶活性与木质素含量呈显著负相关;果肉中PE、β-Gal酶活性在贮藏期间基本维持恒定,留树贮藏与室内贮藏没有显著差异,而PG酶活性在留树贮藏果实中有个明显的升高过程。
(3) Ca、B处理对甜橙果实DF及相关水解酶活性的影响。不同Ca、B处理对红肉脐橙果实成熟后果肉DF各成分含量以及PG、Cx、PE和βGal等酶活性的影响测定。结果表明:叶面喷施Ca、B可以不同程度的改变果肉中Ca、B含量;降低PG、PE和β-Gal酶的活性,减少果胶和CEL等的降解,显著提高果肉中的TDF、IDF、CEL和原果胶等成分的含量,降低SDF和WSP的含量。叶面喷施Ca、B可作为调控柑橘果实DF含量以及相关水解酶活性的有效方法。
(4)水解酶基因的克隆、表达与亚细胞定位。以红肉脐橙、纽荷尔脐橙和塔罗科血橙为试材,克隆果实扩展蛋白(Exp)、PG、Cx、PE和β-Gal基因全长,进行基因的亚细胞定位与实时定量表达。结果表明:转化了pC1302-Exp-GFP、pC1302-PG-GFP和pC1302-Cx-GFP的质粒定位于细胞核中,而转化了pC1302-PE-GFP和pC1302-Gal-GFP的质粒绿色荧光则主要集中在细胞壁上;Exp随着果实的发育基因表达上调,PG基因的表达与果胶物质的降解显著相关,PE、β-Gal基因在果实发育前期存在转录水平较高的阶段,果实成熟前都有下降的过程,成熟后又显著升高;Cx基因在果实发育初期,果皮中的转录水平较高,果肉中则在果实成熟前有一个基因上调表达过程;留树贮藏期间,PG基因的上调表达最为明显;果实叶面喷施Ca、B可显著抑制PG、PE和β-Gal基因的表达。
(5)甜橙果实细胞超微结构变化。随着红肉脐橙果实的发育成熟,囊衣细胞超微结构发生了显著变化。果实膨大初期,细胞呈椭圆形,胞内细胞器结构完整,有明显的细胞核,细胞原生质膜与细胞壁结合紧密,初生细胞壁明显且非常厚,中胶层薄且未出现明显熔融状态。果实发育到膨大后期,细胞开始出现质壁分离,细胞内容物出现降解痕迹,初生壁和中胶层与果实膨大初期相比没有明显变化。转色期,囊衣细胞超微结构发生了显著的变化,细胞质壁分离明显,内容物消失,初生细胞壁开始降解、变薄,中胶层出现熔融状态。果实成熟前,细胞超微结构变化更为显著,初生细胞壁不断降解变得更薄,中胶层熔融状态明显,细胞壁在外界挤压作用下不能维持细胞原来的形状而变形,细胞内容挤压在一起。果实完全成熟后,中胶层完全呈熔融状态,初生壁更薄,细胞器空泡化,细胞完全变形,相互挤压在一起。果实叶面喷施Ca、B对红肉脐橙囊衣细胞结构的影响基本一致,与对照果实相比,初生细胞壁变厚,中胶层熔融不明显,细胞基本维持原来的形状。
Citrus fruits are rich in dietary fibre (DF), especially soluble dietary fibre (SDF) which is of value for human health. Thus, it has been focused to open out and utilize the DF of citrus. In this study, the concentration and composition of DF in the peel and pulp were comparatively analyzed among 'Cara cara' (Citrus sinensis Osbeck cv.), 'Newhall'(Citrus sinensis Osbeck cv.) and 'Tarocco Sanguine'(Citrus sinensis Osbeck cv.) orange during fruit development and maturation. Meanwhile, cell ultrastructure, mRNA transcript levels, subcellular localization and enzyme activity of hydrolases were analyzed. In addition, we have studied the effect of storage methods and pre-harvest foliar application of Ca, B on DF, to identify the relationship between gene expression of hydrolases and DF changes. Molecular, biochemical and ultrastructure characterization of the orange may provide new insights into the mechanism of DF metabolism. The main contents and results in the present study are as follows:
(1) Changes of DF and hydrolases activities in development sweet orange fruit
Total dietary fiber (TDF), insoluble dietary fiber (IDF), SDF, cellulose (CEL), hemicellulose (HC), totale pectin (TP), protopectin, water soluble pectin (WSP) and polygalacturonase (PG), pectinesterase (PE), cellulase (Cx),β-galactosidase (β-Gdl) enzymes activities were determined in the peel and pulp of 'Cara cara', 'Newhall' navel orange and 'Tarocco Sanguine' at different developmental stages. The results showed that TDF contents in the peel and pulp of three sweet orange decreased gradually during the whole developmental period and the change tendency were identical in three varieties. 'Tarocco Sanguine' orange TDF contents throughout were least, 'Newhall' were next, 'Cara cara' most. The change tendency of IDF contents was accord with TDF, but against with SDF. Pectin contents decreased in fruit especially in pulp. WSP contents increased slighty during the later stage. Following growth of the fruit, the lignin and HC decreased rapidly. Lignin and HC contents were opposite correlation with Cx activities markedly. PG activities were lower in the fruit growth earlier period, along with the fruit mature increased quickly, and decreased rapidiy after the maximizing at the beginning of November. PE activities decreased in fruit especially in pulp, increased before fruit mature, and decreased along the fruit development in peel. The change tendency ofβ-Gal activities in pulp was accord with PE in peel, but there were no significant difference between green and mature fruit aboutβ-Gal activities in peel.
(2) Effects of different storage method on DF and hydrolases activities of Cara cara navel orange fruit
'Cara cara' fruit were stored in room as control. Pulp firmness, TDF, IDF, SDF, CEL, HC, TP, protopectin, WSP and PG, Cx, PE,β-Gal enzymes activities were determined in the peel and pulp of 'Cara cara' fruit stored on tree and in room at different storage stages. The results showed that contents of TDF, IDF, HC and CEL were diminished because of keeping fruits on tree, but WSP contents increased. As cell wall principal component HC, CEL hydrolyzed continuously and protopectin translated to WSP during storing on tree. It was negative correlation between Cx enzyme activity with CEL contents of stored 'Cara cara' fruit, Cx enzyme activity and the lignin contents of fruit storing on tree were negative correlation, too. There was no significant difference between fruit stored in room and on tree about PE andβ-Gal activities.
(3) Effects of Ca, B on DF and hydrolases activities of Cara cara navel orange fruit
In the present study, specific activities of PG, Cx, PE,β-Gal were determined in order to identify the effect of pre-harvest application of Ca and B alone or in combination on DF of 'Cara cara' navel orange fruit. The results showed that the enzyme activities of PG, PE andβ-Gal were significantly reduced by pre-harvest application of Ca, B alone or in combination. Such treatments increased contents of TDF, IDF, CEL and protopectin, decreased SDF and WSP. Our study indicated that pre-harvest foliar application of Ca, B is useful for regulating the content of DF on 'Cara cara' navel orange.
(4) Cloning, expression and subcellular localization of hydrolases gene in sweet orange
Expansin (Exp), PG, Cx, PE andβ-Gal were cloned from sweet arange, gene expression levels and subcellular localization of hydrolases were determined. The results showed that onion cells expressing the pC1302-Exp-GFP, pC1302-PE-GFP and pC1302-Gal-GFP showed cell wall GFP localization, when onion peels expressing pC1302-PE-GFP and pC1302-Gal-GFP were incubated on MS agar plates the pattern of fluorescence appeared different, they were located on the outer surface of the primary cell wall. The transcript levels of Exp increased following the fruit development. PG was largely responsible for pectin depolymerization and solubilization. The expression pattern of PE,β-Gal was similar in orange fruit, which showed a high level in the early stage of fruit development and decreased in the stage of fruit color turning, reaching a high level at the stage of fruit maturation. The transcript levels of Cx in orange fruit peel remained high in the green fruit stage and increased before fruit maturation in pulp. The results showed that the mRNA expression levels of PG increased significantly in the fruits of ST. Expression levels of PG, PE andβ-Gal were significantly reduced by pre-harvest application of Ca, B alone or in combination.
(5) Changes of cell ultrastructure in the sweet orange fruit
Changes of cell ultrastructure in the 'Cara cara' navel orange fruit segment membrane during maturation were assessed. The cells of early stage of fruit expansion were full and intact with different size of organelles and an obvious cell nucleus. The primary cell wall was very thick, and the cell middle lamella slightly apparent. At the late stage of fruit expansion, segment membrane cell were slightly different from those at the early stage. The middle lamella became distinct, and within cells, the cytoplasm was denser with a slight plasmolysis. At the early stage of fruit color turning, cell middle lamella became slightly thick and protoplasts in the cells became sparse. The cell plasmolysis was more apparent and cell organelles became faint with broken or uneven cell membranes. More significant changes in the cell ultrastructure occurred after the early stage of fruit color turning. The cell plasmalemma could not maintain a stable structure. The cell had large lumen, and the plasmalemma separated from the cell wall and shrank inwards. The middle lamella became distinct extremely and the primary cell wall became very thin. Following fruit maturation, the cell could not undergo the pressure, tortuosity and transmutation. Pre-harvest application of Ca, B had significant effect on the cross-linked polymer network of fruit segment membrane, the primary cell wall was very thick, the cell middle lamella was slightly apparent, and cell plasmalemma could maintain a stable structure.
(1)甜橙果实发育过程中DF及相关水解酶活性的变化规律。红肉脐橙、纽荷尔脐橙和塔罗科血橙果实发育过程中总膳食纤维(TDF)、SDF、不溶性膳食纤维(IDF)、总果胶(TP)、原果胶(Protopectin)、水溶性果胶(WSP)、纤维素(CEL)、半纤维素(HC)和木质素(lignin)等的含量以及多聚半乳糖醛酸酶(PG)、纤维素酶(Cx)、果胶酯酶(PE)和β-半乳糖苷酶(β-Gal)等的活性的测定。结果表明:3品种果实发育过程中TDF含量变化趋势基本一致,随着果实的成熟其含量逐渐减少;果肉中,塔罗科血橙TDF含量最少,纽荷尔次之,红肉脐橙最多:IDF含量变化趋势与TDF基本一致,而SDF与TDF相反;果实发育过程中果胶含量呈下降趋势,果肉中表现较果皮明显;WSP含量随着果实成熟不断增加;随着果实的发育,木质素和HC含量急剧下降,且果肉中木质素和HC含量与Cx活性呈显著负相关;PG活性在果实发育前期较低,随着果实的成熟迅速增加,在果实转色期其酶活性达到最大值后急剧下降;PE酶活性在果实发育前期的果肉中呈下降趋势,果实成熟前酶活性显著升高,果皮中呈下降趋势;β-Gal在果肉中随着果实发育酶活性逐渐降低,果皮中成熟前后差异不显著。
(2)不同贮藏条件下红肉脐橙果实DF及相关水解酶活性的变化规律。室内贮藏、留树贮藏条件下不同贮藏期的红肉脐橙果肉硬度、DF各成分的含量以及相关水解酶PG、Cx、PE和β-Gal等的活性的分析。结果表明:留树贮藏能够显著降低红肉脐橙果实TDF、IDF以及HC和木质素等的含量,提高SDF含量,留树贮藏后作为细胞壁主要成分的HC、木质素等不断降解,原果胶继续转化为WSP;果实贮藏期间Cx酶活性与HC含量呈显著负相关,留树贮藏Cx酶活性与木质素含量呈显著负相关;果肉中PE、β-Gal酶活性在贮藏期间基本维持恒定,留树贮藏与室内贮藏没有显著差异,而PG酶活性在留树贮藏果实中有个明显的升高过程。
(3) Ca、B处理对甜橙果实DF及相关水解酶活性的影响。不同Ca、B处理对红肉脐橙果实成熟后果肉DF各成分含量以及PG、Cx、PE和βGal等酶活性的影响测定。结果表明:叶面喷施Ca、B可以不同程度的改变果肉中Ca、B含量;降低PG、PE和β-Gal酶的活性,减少果胶和CEL等的降解,显著提高果肉中的TDF、IDF、CEL和原果胶等成分的含量,降低SDF和WSP的含量。叶面喷施Ca、B可作为调控柑橘果实DF含量以及相关水解酶活性的有效方法。
(4)水解酶基因的克隆、表达与亚细胞定位。以红肉脐橙、纽荷尔脐橙和塔罗科血橙为试材,克隆果实扩展蛋白(Exp)、PG、Cx、PE和β-Gal基因全长,进行基因的亚细胞定位与实时定量表达。结果表明:转化了pC1302-Exp-GFP、pC1302-PG-GFP和pC1302-Cx-GFP的质粒定位于细胞核中,而转化了pC1302-PE-GFP和pC1302-Gal-GFP的质粒绿色荧光则主要集中在细胞壁上;Exp随着果实的发育基因表达上调,PG基因的表达与果胶物质的降解显著相关,PE、β-Gal基因在果实发育前期存在转录水平较高的阶段,果实成熟前都有下降的过程,成熟后又显著升高;Cx基因在果实发育初期,果皮中的转录水平较高,果肉中则在果实成熟前有一个基因上调表达过程;留树贮藏期间,PG基因的上调表达最为明显;果实叶面喷施Ca、B可显著抑制PG、PE和β-Gal基因的表达。
(5)甜橙果实细胞超微结构变化。随着红肉脐橙果实的发育成熟,囊衣细胞超微结构发生了显著变化。果实膨大初期,细胞呈椭圆形,胞内细胞器结构完整,有明显的细胞核,细胞原生质膜与细胞壁结合紧密,初生细胞壁明显且非常厚,中胶层薄且未出现明显熔融状态。果实发育到膨大后期,细胞开始出现质壁分离,细胞内容物出现降解痕迹,初生壁和中胶层与果实膨大初期相比没有明显变化。转色期,囊衣细胞超微结构发生了显著的变化,细胞质壁分离明显,内容物消失,初生细胞壁开始降解、变薄,中胶层出现熔融状态。果实成熟前,细胞超微结构变化更为显著,初生细胞壁不断降解变得更薄,中胶层熔融状态明显,细胞壁在外界挤压作用下不能维持细胞原来的形状而变形,细胞内容挤压在一起。果实完全成熟后,中胶层完全呈熔融状态,初生壁更薄,细胞器空泡化,细胞完全变形,相互挤压在一起。果实叶面喷施Ca、B对红肉脐橙囊衣细胞结构的影响基本一致,与对照果实相比,初生细胞壁变厚,中胶层熔融不明显,细胞基本维持原来的形状。
Citrus fruits are rich in dietary fibre (DF), especially soluble dietary fibre (SDF) which is of value for human health. Thus, it has been focused to open out and utilize the DF of citrus. In this study, the concentration and composition of DF in the peel and pulp were comparatively analyzed among 'Cara cara' (Citrus sinensis Osbeck cv.), 'Newhall'(Citrus sinensis Osbeck cv.) and 'Tarocco Sanguine'(Citrus sinensis Osbeck cv.) orange during fruit development and maturation. Meanwhile, cell ultrastructure, mRNA transcript levels, subcellular localization and enzyme activity of hydrolases were analyzed. In addition, we have studied the effect of storage methods and pre-harvest foliar application of Ca, B on DF, to identify the relationship between gene expression of hydrolases and DF changes. Molecular, biochemical and ultrastructure characterization of the orange may provide new insights into the mechanism of DF metabolism. The main contents and results in the present study are as follows:
(1) Changes of DF and hydrolases activities in development sweet orange fruit
Total dietary fiber (TDF), insoluble dietary fiber (IDF), SDF, cellulose (CEL), hemicellulose (HC), totale pectin (TP), protopectin, water soluble pectin (WSP) and polygalacturonase (PG), pectinesterase (PE), cellulase (Cx),β-galactosidase (β-Gdl) enzymes activities were determined in the peel and pulp of 'Cara cara', 'Newhall' navel orange and 'Tarocco Sanguine' at different developmental stages. The results showed that TDF contents in the peel and pulp of three sweet orange decreased gradually during the whole developmental period and the change tendency were identical in three varieties. 'Tarocco Sanguine' orange TDF contents throughout were least, 'Newhall' were next, 'Cara cara' most. The change tendency of IDF contents was accord with TDF, but against with SDF. Pectin contents decreased in fruit especially in pulp. WSP contents increased slighty during the later stage. Following growth of the fruit, the lignin and HC decreased rapidly. Lignin and HC contents were opposite correlation with Cx activities markedly. PG activities were lower in the fruit growth earlier period, along with the fruit mature increased quickly, and decreased rapidiy after the maximizing at the beginning of November. PE activities decreased in fruit especially in pulp, increased before fruit mature, and decreased along the fruit development in peel. The change tendency ofβ-Gal activities in pulp was accord with PE in peel, but there were no significant difference between green and mature fruit aboutβ-Gal activities in peel.
(2) Effects of different storage method on DF and hydrolases activities of Cara cara navel orange fruit
'Cara cara' fruit were stored in room as control. Pulp firmness, TDF, IDF, SDF, CEL, HC, TP, protopectin, WSP and PG, Cx, PE,β-Gal enzymes activities were determined in the peel and pulp of 'Cara cara' fruit stored on tree and in room at different storage stages. The results showed that contents of TDF, IDF, HC and CEL were diminished because of keeping fruits on tree, but WSP contents increased. As cell wall principal component HC, CEL hydrolyzed continuously and protopectin translated to WSP during storing on tree. It was negative correlation between Cx enzyme activity with CEL contents of stored 'Cara cara' fruit, Cx enzyme activity and the lignin contents of fruit storing on tree were negative correlation, too. There was no significant difference between fruit stored in room and on tree about PE andβ-Gal activities.
(3) Effects of Ca, B on DF and hydrolases activities of Cara cara navel orange fruit
In the present study, specific activities of PG, Cx, PE,β-Gal were determined in order to identify the effect of pre-harvest application of Ca and B alone or in combination on DF of 'Cara cara' navel orange fruit. The results showed that the enzyme activities of PG, PE andβ-Gal were significantly reduced by pre-harvest application of Ca, B alone or in combination. Such treatments increased contents of TDF, IDF, CEL and protopectin, decreased SDF and WSP. Our study indicated that pre-harvest foliar application of Ca, B is useful for regulating the content of DF on 'Cara cara' navel orange.
(4) Cloning, expression and subcellular localization of hydrolases gene in sweet orange
Expansin (Exp), PG, Cx, PE andβ-Gal were cloned from sweet arange, gene expression levels and subcellular localization of hydrolases were determined. The results showed that onion cells expressing the pC1302-Exp-GFP, pC1302-PE-GFP and pC1302-Gal-GFP showed cell wall GFP localization, when onion peels expressing pC1302-PE-GFP and pC1302-Gal-GFP were incubated on MS agar plates the pattern of fluorescence appeared different, they were located on the outer surface of the primary cell wall. The transcript levels of Exp increased following the fruit development. PG was largely responsible for pectin depolymerization and solubilization. The expression pattern of PE,β-Gal was similar in orange fruit, which showed a high level in the early stage of fruit development and decreased in the stage of fruit color turning, reaching a high level at the stage of fruit maturation. The transcript levels of Cx in orange fruit peel remained high in the green fruit stage and increased before fruit maturation in pulp. The results showed that the mRNA expression levels of PG increased significantly in the fruits of ST. Expression levels of PG, PE andβ-Gal were significantly reduced by pre-harvest application of Ca, B alone or in combination.
(5) Changes of cell ultrastructure in the sweet orange fruit
Changes of cell ultrastructure in the 'Cara cara' navel orange fruit segment membrane during maturation were assessed. The cells of early stage of fruit expansion were full and intact with different size of organelles and an obvious cell nucleus. The primary cell wall was very thick, and the cell middle lamella slightly apparent. At the late stage of fruit expansion, segment membrane cell were slightly different from those at the early stage. The middle lamella became distinct, and within cells, the cytoplasm was denser with a slight plasmolysis. At the early stage of fruit color turning, cell middle lamella became slightly thick and protoplasts in the cells became sparse. The cell plasmolysis was more apparent and cell organelles became faint with broken or uneven cell membranes. More significant changes in the cell ultrastructure occurred after the early stage of fruit color turning. The cell plasmalemma could not maintain a stable structure. The cell had large lumen, and the plasmalemma separated from the cell wall and shrank inwards. The middle lamella became distinct extremely and the primary cell wall became very thin. Following fruit maturation, the cell could not undergo the pressure, tortuosity and transmutation. Pre-harvest application of Ca, B had significant effect on the cross-linked polymer network of fruit segment membrane, the primary cell wall was very thick, the cell middle lamella was slightly apparent, and cell plasmalemma could maintain a stable structure.
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