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Journal of Integrative Agriculture  2023, Vol. 22 Issue (9): 2705-2718    DOI: 10.1016/j.jia.2023.07.019
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Comparison of cell wall changes of two different types of apple cultivars during fruit development and ripening

LI Xiang-lu1, SU Qiu-fang1, JIA Rong-jian1, WANG Zi-dun1, FU Jiang-hong1, GUO Jian-hua1, YANG Hui-juan1, 2#, ZHAO Zheng-yang1, 2#

1 College of Horticulture, Northwest A&F University, Yangling 712100, P.R.China
2 Apple Engineering and Technology Research Center of Shaanxi Province, Yangling 712100, P.R.China 
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摘要  

果实的发育和成熟是一个复杂的过程(Malus×domestica Borkh.)许多因素都可以影响该过程,如细胞结构、细胞壁成分和细胞壁水解酶等。本文研究了硬脆和松脆两种不同类型苹果品种果实发育过程中果实硬度、细胞壁形态和成分、细胞壁水解酶活性及相关基因表达模式的变化,旨在找出不同类型品种间质地变化的原因。细胞壁物质(CWMs)、半纤维素和纤维素含量与果实硬度的变化密切相关。4个品种的水溶性果胶(WSP)和共价结合型果胶(CSP)含量逐渐升高,而离子型果胶(ISP)含量变化趋势不一致。4个品种的多聚半乳糖醛酸酶(PG)、β-半乳糖苷酶(β-gal)、纤维素酶(CEL)和果胶裂解酶(PL)活性逐渐升高。随着果实发育,‘富士’和‘蜜脆’果实中PGβ-galCEL的活性较高,而‘富士’和‘蜜脆’果实中PL的活性低于‘爱妃’和‘魔笛’。随着果实的发育,四个品种的果实细胞逐渐变大,细胞排列更松散,细胞间隙更大。qRT-PCR结果显示MdACO1Mdβ-gal的相对表达量明显升高。研究表明,两种不同类型的苹果品种在ISP和半纤维素含量、PL活性和Mdβ-gal相对表达量上存在较大差异,这些差异可能是造成4个品种质地差异的原因。



Abstract  

Fruit development and ripening is a complex procedure (Malus×domestica Borkh.) and can be caused by various factors such as cell structure, cell wall components, and cell wall hydrolytic enzymes.  In our study, we focused on the variations in fruit firmness, cell wall morphology and components, the activity of cell wall hydrolytic enzymes and the expression patterns of associated genes during fruit development in two different types of apple cultivars, the hard-crisp cultivar and the loose-crisp cultivar.  In this paper, the aim was to find out the causes of the texture variations between the different type cultivars.  Cell wall materials (CWMs), hemicellulose and cellulose content were strongly associated with variations in fruit firmness during the fruit development.  The content of water soluble pectin (WSP) and chelator soluble pectin (CSP) gradually increased, while the content of ionic soluble pectin (ISP) showed inconsistent trends in the four cultivars.  The activities of polygalacturonase (PG), β-galactosidase (β-gal), cellulase (CEL), and pectate lyase (PL) gradually increased in four cultivars.  And the activities of PG, β-gal, and CEL were higher in ‘Fuji’ and ‘Honeycrisp’ fruit with the fruit development, while the activity of PL of ‘Fuji’ and ‘Honeycrisp’ was lower than that of ‘ENVY’ and ‘Modi’.  Both four cultivars of fruit cells progressively became bigger as the fruit expanded, with looser cell arrangements and larger cell gaps.  According to the qRT-PCR, the relative expression levels of MdACO and Mdβ-gal were notably enhanced.  Our study showed that there were large differences in the content of ISP and hemicellulose, the activity of PL and the relative expression of Mdβ-gal between two different types of apple cultivars, and these differences might be responsible for the variations in the texture of the four cultivars.

Keywords:  apple (Malus×domestica Borkh.)        fruit softening        cell wall        firmness  
Received: 16 March 2023   Accepted: 25 June 2023
Fund: 

This work was supported by the earmarked fund for the China Agriculture Research System (CARS-27).

About author:  LI Xiang-lu, E-mail: xiangluLi@nwsuaf.edu.cn; #Correspondence YANG Hui-juan, E-mail: huijuanyang@nwsuaf.edu.cn; ZHAO Zheng-yang, E-mail: zhaozy@nwsuaf.edu.cn

Cite this article: 

LI Xiang-lu, SU Qiu-fang, JIA Rong-jian, WANG Zi-dun, FU Jiang-hong, GUO Jian-hua, YANG Hui-juan, ZHAO Zheng-yang. 2023. Comparison of cell wall changes of two different types of apple cultivars during fruit development and ripening. Journal of Integrative Agriculture, 22(9): 2705-2718.

Atkinson R G, Schröder R, Hallett I C, Cohen D, MacRae E A. 2002. Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiology129, 122–133.

Bennett A B, Labavitch J M. 2008. Ethylene and ripening-regulated expression and function of fruit cell wall modifying proteins. Plant Sciences175, 130–136.

Bowen A J, Blake A, Tureček J, Amyotte B. 2019. External preference mapping: A guide for a consumer-driven approach to apple breeding. Journal of Sensory Studies34, e12472.

Brummell D A. 2006. Cell wall disassembly in ripening fruit. Functional Plant Biology33, 103–119.

Brummell D A, Harpster M H. 2001. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology47, 311–339.

Cheng G P, Duan X W, Jiang Y M, Sun J, Yang S Y, Yang B, He S G, Liang H, Luo Y B. 2009. Modification of hemicellulose polysaccharides during ripening of postharvest banana fruit. Food Chemistry115, 43–47.

Costa F, Peace C P, Stella S, Musacchi S, Bazzani M, Sansavini S, Van de Weg W E. 2010. QTL dynamics for fruit firmness and softening around an ethylene-dependent polygalacturonase gene in apple (Malus×domestica Borkh.). Journal of Experimental Botany61, 3029–3039.

Dheilly E, Gall S L, Guillou M C, Renou J P, Bonnin E, Orsel M, Lahaye M. 2016. Cell wall dynamics during apple development and storage involves hemicellulose modifications and related expressed genes. BMC Plant Biology16, 1–20.

Dong Y, Zhang S, Wang Y. 2018. Compositional changes in cell wall polyuronides and enzyme activities associated with melting/mealy textural property during ripening following long-term storage of ‘Comice’ and ‘d’Anjou’ pears. Postharvest Biology and Technology135, 131–140.

Fischer R L, Bennett A B. 1991. Role of cell wall hydrolases in fruit ripening. Annual Review of Plant Biology42, 675–703.

Ge Y, Duan B, Li C, Wei M, Chen Y, Li X, Tang Q. 2019. Application of sodium silicate retards apple softening by suppressing the activity of enzymes related to cell wall degradation. Journal of the Science of Food and Agriculture99, 1828–1833.

Ghiani A, Onelli E, Aina R, Cocucci M, Citterio S. 2011. A comparative study of melting and non-melting flesh peach cultivars reveals that during fruit ripening endo-polygalacturonase (endo-PG) is mainly involved in pericarp textural changes, not in firmness reduction. Journal of Experimental Botany62, 4043–4054.

Giongo L, Poncetta P, Loretti P, Costa F. 2013. Texture profiling of blueberries (Vaccinium spp.) during fruit development, ripening and storage. Postharvest Biology and Biotechnology76, 34–39.

Giovannoni J J. 2004. Genetic regulation of fruit development and ripening. The Plant Cell16, S170–S180.

Goulao L F, Oliveira C M. 2008. Cell wall modifications during fruit ripening: When a fruit is not the fruit. Trends in Food Science & Technology19, 4–25.

Gross B L, Olsen K M. 2010. Genetic perspectives on crop domestication. Trends in Plant Science15, 529–537.

Hampson C, Quamme H, Hall J, MacDonald R, King M, Cliff M. 2000. Sensory evaluation as a selection tool in apple breeding. Euphytica111, 79–90.

Han Y, Ban Q, Li H, Hou Y, Jin M, Han S, Rao J. 2016. DkXTH8, a novel xyloglucan endotransglucosylase/hydrolase in persimmon, alters cell wall structure and promotes leaf senescence and fruit postharvest softening. Scientific Reports6, 39155.

Huber D J. 1983. The role of cell wall hydrolases in fruit softening. Horticultural Reviews5, 169–219.

Jarvis M, Briggs S, Knox J. 2003. Intercellular adhesion and cell separation in plants. PlantCell & Environment26, 977–989.

Jarvis M C. 2011. Plant cell walls: Supramolecular assemblies. Food Hydrocolloids25, 257–262.

Ke X, Wang H, Li Y, Zhu B, Zang Y, He Y, Cao J, Zhu Z, Yu Y. 2018. Genome-wide identification and analysis of polygalacturonase genes in Solanum lycopersicumInternational Journal of Molecular Sciences19, 2290.

Kou X, Feng Y, Yuan S, Zhao X, Wu C, Wang C, Xue Z. 2021. Different regulatory mechanisms of plant hormones in the ripening of climacteric and non-climacteric fruits: A review. Plant Molecular Biology107, 1–21.

Li M, Zhang Y, Zhang Z, Ji X, Zhang R, Liu D, Gao L, Zhang J, Wang B, Wu Y, Wu S, Chen X, Feng S, Chen X. 2013. Hypersensitive ethylene signaling and ZMdPG1 expression lead to fruit softening and dehiscence. PLoS ONE8, e58745.

Li Y, He H, Hou Y, Kelimu A, Wu F, Zhao Y, Shi L, Zhu X. 2022. Salicylic acid treatment delays apricot (Prunus armeniaca L.) fruit softening by inhibiting ethylene biosynthesis and cell wall degradation. Scientia Horticulturae300, 111061.

Liu X, Hao N, Feng R, Meng Z, Li Y, Zhao Z. 2021. Transcriptome and metabolite profiling analyses provide insight into volatile compounds of the apple cultivar ‘Ruixue’ and its parents during fruit development. BMC Plant Biology21, 1–16.

Marín-Rodríguez M, Smith D, Manning K, Orchard J, Seymour G. 2003. Pectate lyase gene expression and enzyme activity in ripening banana fruit. Plant Molecular Biology51, 851–857.

Melton L D, Smith B G. 2001. Isolation of plant cell walls and fractionation of cell wall polysaccharides. Current Protocols in Food Analytical Chemistry, (01), 697–719.

Moya-León M A, Mattus-Araya E, Herrera R. 2019. Molecular events occurring during softening of strawberry fruit. Frontiers in Plant Science10, 615.

Muñoz-Bertomeu J, Miedes E, Lorences E. 2013. Expression of xyloglucan endotransglucosylase/hydrolase (XTH) genes and XET activity in ethylene treated apple and tomato fruits. Journal of Plant Physiology170, 1194–1201.

Ng J K, Schröder R, Brummell D A, Sutherland P W, Hallett I C, Smith B G, Melton L D, Johnston J W. 2015. Lower cell wall pectin solubilisation and galactose loss during early fruit development in apple (Malus×domestica) cultivar ‘Scifresh’ are associated with slower softening rate. Journal of Plant Physiology176, 129–137.

Oraguzie N, Iwanami H, Soejima J, Harada T, Hall A. 2004. Inheritance of the Md-ACS1 gene and its relationship to fruit softening in apple (Malus×domestica Borkh.). Theoretical and Applied Genetics108, 1526–1533.

Payasi A, Misra P C, Sanwal G G. 2004. Effect of phytohormones on pectate lyase activity in ripening Musa acuminataPlant Physiology and Biochemistry42, 861–865.

Quesada M A, Blanco-Portales R, Posé S, García-Gago J A, Jiménez-Bermúdez S, Muñoz-Serrano A, Caballero J L, Pliego-Alfaro F, Mercado J A, Muñoz-Blanco J. 2009. Antisense down-regulation of the FaPG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiology150, 1022–1032.

Redgwell R J, MacRae E, Hallett I, Fischer M, Perry J, Harker R. 1997. In vivo and in vitro swelling of cell walls during fruit ripening. Planta203, 162–173.

Santiago-Doménech N, Jiménez-Bemudez S, Matas A J, Rose J K, Munoz-Blanco J, Mercado J A, Quesada M A. 2008. Antisense inhibition of a pectate lyase gene supports a role for pectin depolymerization in strawberry fruit softening. Journal of Experimental Botany59, 2769–2779.

Seymour G B, Manning K, Eriksson E M, Popovich A H, King G J. 2002. Genetic identification and genomic organization of factors affecting fruit texture. Journal of Experimental Botany53, 2065–2071.

Sheehy R E, Kramer M, Hiatt W R. 1988. Reduction of polygalacturonase activity in tomato fruit by antisense RNA. Proceedings of the National Academy of Sciences of the United States of America85, 8805–8809.

Smith C J, Watson C F, Morris P C, Bird C R, Seymour G B, Gray J E, Arnold C, Tucker G A, Schuch W, Harding S. 1990. Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant Molecular Biology14, 369–379.

Su Q, Li X, Wang L, Wang B, Feng Y, Yang H, Zhao Z. 2022. Variation in cell wall metabolism and flesh firmness of four apple cultivars during fruit development. Foods11, 3518.

Trainotti L, Spinello R, Piovan A, Spolaore S, Casadoro G. 2001. β-Galactosidases with a lectin-like domain are expressed in strawberry. Journal of Experimental Botany52, 1635–1645.

Toivonen P M, Brummell D A. 2008. Biochemical bases of appearance and texture changes in fresh-cut fruit and vegetables. Postharvest Biology and Technology48, 1–14.

Uluisik S, Chapman N H, Smith R, Poole M, Adams G, Gillis R B, Besong T M, Sheldon J, Stiegelmeyer S, Perez L, Samsulrizal N, Wang D, Fisk I D, Yang N, Baxter C, Rickett D, Fray R, Blanco-Ulate B, Powell A L, Harding S E, et al. 2016. Genetic improvement of tomato by targeted control of fruit softening. Nature Biotechnology34, 950–952.

Wakasa Y, Kudo H, Ishikawa R, Akada S, Senda M, Niizeki M, Harada T. 2006. Low expression of an endopolygalacturonase gene in apple fruit with long-term storage potential. Postharvest Biology and Technology39, 193–198.

Wang D, Yeats T H, Uluisik S, Rose J K, Seymour G B. 2018. Fruit softening: Revisiting the role of pectin. Trends in Plant Science23, 302–310.

Wei J, Ma F, Shi S, Qi X, Zhu X, Yuan J. 2010. Changes and postharvest regulation of activity and gene expression of enzymes related to cell wall degradation in ripening apple fruit. Postharvest Biology and Technology56, 147–154.

Willats W G, McCartney L, Mackie W, Knox J P. 2001. Pectin: Cell biology and prospects for functional analysis. Plant Molecular Biology47, 9–27.

Witasari L D, Huang F C, Hoffmann T, Rozhon W, Fry S C, Schwab W. 2019. Higher expression of the strawberry xyloglucan endotransglucosylase/hydrolase genes FvXTH9 and FvXTH6 accelerates fruit ripening. Plant Journal100, 1237–1253.

Yang L, Huang W, Xiong F, Xian Z, Su D, Ren M, Li Z. 2017. Silencing of SlPL, which encodes a pectate lyase in tomato, confers enhanced fruit firmness, prolonged shelf-life and reduced susceptibility to grey mould. Plant Biotechnology Journal15, 1544–1555.

Zhang W W, Zhao S Q, Gu S, Cao X Y, Zhang Y, Niu J F, Liu L, Li A R, Jia W S, Qi B X, Xing Y. 2022. FvWRKY48 binds to the pectate lyase FvPLA promoter to control fruit softening in Fragaria vescaPlant Physiology189, 1037–1049.

Zhang W W, Zhao S Q, Zhang L C, Xing Y, Jia W S. 2020. Changes in the cell wall during fruit development and ripening in Fragaria vescaPlant Physiology and Biochemistry154, 54–65.

Zhu Y, Barritt B. 2008. Apple cultivar genotypes for Md-ACS1 and Md-ACO1 ethylene production genes and implications for breeding. Tree Genet Genome4, 555–562.

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