Different Activities of Pectin-degrading Enzymes Affecting the Growth of Asian Pears

Yun-Ju Baek; Sang Wook Park; Bok-Rye Lee; Ung Yang; Sol Han; Seung Gon Wi; Sang-Hyun Lee

doi:10.7235/HORT.20230046

All Issue

2023 Vol.41, Issue 5 Preview Page Next Page

Research Article

Different Activities of Pectin-degrading Enzymes Affecting the Growth of Asian Pears

31 October 2023. pp. 537-548

PDF XML

Abstract

Fruit size is determined by the number and size of cells resulting from cell division and expansion, which are correlated with changes in the cell wall content. The pivotal roles of pectin-methylesterase (PME) and polygalacturonase (PG) have been well documented with regard to fruit ripening. Therefore, this study analyzed fruit growth and pectin contents for three consecutive years (from 2019 to 2021) until 180 days after full bloom (DAFB) at 15-day intervals to examine how pectin in the cell wall components affects fruit growth and development. Although there were no differences in the fruit size at harvest for these three years, the absolute fruit growth rate (AGR) peaked most rapidly in 2020, reaching the maximum fruit size earlier compared to the other two years. The pectin content of fruits in 2020, which showed the fastest growth, remained at a low level early in the growing season compared to those in the other years. The change in the pattern of the gradual increase in the PG activity with a decrease in the PME activity resulted in correspondingly different intersecting points over the three years. We found that the intersection of PME and PG activities observed in the order of 2020, 2021, and 2019 was identical to the order when the fruits reached their final weight. Interestingly, this timeline coincided with the point in time when the AGR increased rapidly over these three years. Differences in fruit volume increases, pectin contents, and pectin-degrading enzyme activities observed during fruit growth over three years suggest that the intersection of PME and PG activities is one of the key factors influencing cell expansion activation. Taken together, these results indicate that the intersection of PME and PG activities may affect the pectin content during fruit growth and development, which in turn affects the fruit growth rate in Asian pears.

Keywords

absolute fruit growth rate

intersection point

pectin methylesterase

polygalacturonase

Pyrus pyrifolia Nakai cv. Niitaka

References

Abu-Sarra A, Abu-Goukh A (1992) Changes in pectinesterase, polygalacturonase and cellulase activity during mango fruit ripening. J Hortic Sci 67:561-568. doi:10.1080/00221589.1992.11516284 10.1080/00221589.1992.11516284

Adams S, Cockshull K, Cave C (2001) Effect of temperature on the growth and development of tomato fruits. Ann Bot 88:869-877. doi:10.1006/anbo.2001.1524 10.1006/anbo.2001.1524

Ahmed DM, Yousef AR, Hassan H (2010) Relationship between electrical conductivity, softening and color of Fuerte avocado fruits during ripening. Agr Biol J N Am 1:878-885. doi:10.5251/abjna.2010.1.5.878.885 10.5251/abjna.2010.1.5.878.885

Brahem M, Renard CM, Gouble B, Bureau S, Le Bourvellec C (2017) Characterization of tissue specific differences in cell wall polysaccharides of ripe and overripe pear fruit. Carbohydr Polym 156:152-164 10.1016/j.carbpol.2016.09.01927842809

Brummell DA (2006) Cell wall disassembly in ripening fruit. Funct Plant Biol 33:103-119. doi:10.1016/j.carbpol.2016.09.019 10.1016/j.carbpol.2016.09.01927842809

Brummell DA, Dal Cin V, Crisosto CH, Labavitch JM (2004) Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot 55:2029-2039. doi:10.1093/jxb/erh227 10.1093/jxb/erh22715286150

Byeon SE, Park GH, Lee J, Lwin HP, Su'udi M, Kim J, Lee J (2022) Alteration of Fruit Quality Attributes and Cell Wall-Degrading Enzymatic Activities in Cluster Tomatoes After Combination Treatment with 1-methylcyclopropene and Modified Atmosphere Packaging During Cold Storage. Hortic Sci Technol 40:307-323. doi:10.7235/HORT.20220029 10.7235/HORT.20220029

Chen H, Cao S, Fang X, Mu H, Yang H, Wang X, Xu Q, Gao H (2015) Changes in fruit firmness, cell wall composition and cell wall degrading enzymes in postharvest blueberries during storage. Sci Hortic 188:44-48. doi:10.1016/j.scienta.2015.03.018 10.1016/j.scienta.2015.03.018

Cybulska J, Zdunek A, Konstankiewicz K (2011) Calcium effect on mechanical properties of model cell walls and apple tissue. J Food Eng 102:217-223. doi:10.1016/j.jfoodeng.2010.08.01 10.1016/j.jfoodeng.2010.08.019

Dai S, Li P, Chen P, Li Q, Pei Y, He S, Sun Y, Wang Y, Kai W, et al. (2014) Transcriptional regulation of genes encoding ABA metabolism enzymes during the fruit development and dehydration stress of pear 'Gold Nijisseiki'. Plant Physiol Biochem 82:299-308. doi:10.1016/j.plaphy.2014.06.013 10.1016/j.plaphy.2014.06.01325038474

Gao Y, Guo Y, Su Z, Yu Y, Zhu Z, Gao P, Wang X (2020) Transcriptome analysis of genes related to fruit texture in watermelon. Sci Hortic 262:109075. doi:10.1016/j.scienta.2019.109075 10.1016/j.scienta.2019.109075

Goulao LF, Oliveira CM (2008) Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends Food Sci Technol 19:4-25. doi:10.1016/j.tifs.2007.07.002 10.1016/j.tifs.2007.07.002

Grierson D, Tucker GA (1983) Timing of ethylene and polygalacturonase synthesis in relation to the control of tomato fruit ripening. Planta 157:174-179. doi:10.1007/BF00393652 10.1007/BF0039365224264072

Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337-343. doi:10.1104/pp.117.2.337 10.1104/pp.117.2.3379625687PMC1539180

Hiwasa K, Nakano R, Hashimoto A, Matsuzaki M, Murayama H, Inaba A, Kubo Y (2004) European, Chinese and Japanese pear fruits exhibit differential softening characteristics during ripening. J Exp Bot 55:2281-2290. doi:10.1093/jxb/erh250 10.1093/jxb/erh25015333646

Karim SKA, Allan AC, Schaffer RJ, David KM (2022) Cell division controls final fruit size in three apple (Malus x domestica) cultivars. Horticulturae 8:657. doi:10.3390/horticulturae8070657 10.3390/horticulturae8070657

Kozioł A, Cybulska J, Pieczywek PM, Zdunek A (2017) Changes of pectin nanostructure and cell wall stiffness induced in vitro by pectinase. Carbohydr Polym 161:197-207. doi:10.1016/j.carbpol.2017.01.014 10.1016/j.carbpol.2017.01.01428189229

Kwon JG, Yoo J, Win NM, Naing AH, Cho YJ, Jung HY, Kang IK (2022) Minimization of 1-methylcyclopropene concentration to regulate cell wall metabolism of 'Arisoo'and 'Picnic'apples in cold storage. Hortic Sci Technol 40:410-419. doi:10.7235/HORT.20220037 10.7235/HORT.20220037

Lahaye M, Tabi W, Le Bot L, Delaire M, Orsel M, Campoy JA, Garcia JQ, Le Gall S (2021) Comparison of cell wall chemical evolution during the development of fruits of two contrasting quality from two members of the Rosaceae family: Apple and sweet cherry. Plant Physiol Biochem 168:93-104. doi:10.1016/j.plaphy.2021.10.002 10.1016/j.plaphy.2021.10.00234627026

Leboeuf E, Thoiron S, Lahaye M (2004) Physico-chemical characteristics of cell walls from Arabidopsis thaliana microcalli showing different adhesion strengths. J Exp Bot 55:2087-2097. doi:10.1093/jxb/erh225 10.1093/jxb/erh22515286149

Lee BR, Baek YJ, Wi SG, Yang U, Lee SH (2022) ROS-mediated Lignin Biosynthesis is Associated with Cell Wall Expansion in Asian Pear (Pyrus pyrifolia Nakai) During Fruit Development and Ripening. Hortic Sci Technol 40:349-360. doi:10.7235/HORT.20220032 10.7235/HORT.20220032

Li J, Dai X, Li Q, Jiang F, Xu X, Guo T, Zhang H (2023) Low temperatures inhibit the pectin degradation of 'Docteur Jules Guyot'pear (Pyrus communis L.). Int J Biol Macromol 124719. doi:10.1016/j.ijbiomac.2023.124719 10.1016/j.ijbiomac.2023.12471937150373

Lindo-García V, Muñoz P, Larrigaudière C, Munné-Bosch S, Giné-Bordonaba J (2020) Interplay between hormones and assimilates during pear development and ripening and its relationship with the fruit postharvest behaviour. Plant Sci 291:110339. doi:10.1016/j.plantsci.2019.110339 10.1016/j.plantsci.2019.11033931928676

Liu J, Zhao Y, Xu H, Zhao X, Tan Y, Li P, Li D, Tao Y, Liu D (2021) Fruit softening correlates with enzymatic activities and compositional changes in fruit cell wall during growing in Lycium barbarum L. Int J Food Sci 56:3044-3054. doi:10.1111/ijfs.14948 10.1111/ijfs.14948

Lötze E, Bergh O (2004) Early prediction of harvest fruit size distribution of an apple and pear cultivar. Sci Hortic 101:281-290. doi:10.1016/j.scienta.2003.11.006 10.1016/j.scienta.2003.11.006

Mauxion JP, Chevalier C, Gonzalez N (2021) Complex cellular and molecular events determining fruit size. Trends Plant Sci 26:1023-1038. doi:10.1016/j.tplants.2021.05.008 10.1016/j.tplants.2021.05.00834158228

McCormick R, Biegert K, Streif J (2021) Occurrence of physiological browning disorders in stored 'Braeburn'apples as influenced by orchard and weather conditions. Postharvest Biol Technol 177:111534. doi:10.1016/j.postharvbio.2021.111534 10.1016/j.postharvbio.2021.111534

Pei MS, Cao SH, Wu L, Wang GM, Xie ZH, Gu C, Zhang SL (2020) Comparative transcriptome analyses of fruit development among pears, peaches, and strawberries provide new insights into single sigmoid patterns. BMC Plant Biol 20:1-15. doi:10.1186/s12870-020-2317-6 10.1186/s12870-020-2317-632143560PMC7060524

Posé S, Paniagua C, Matas AJ, Gunning AP, Morris VJ, Quesada MA, Mercado JA (2019) A nanostructural view of the cell wall disassembly process during fruit ripening and postharvest storage by atomic force microscopy. Trends Food Sci Technol 87:47-58. doi:10.1016/j.tifs.2018.02.011 10.1016/j.tifs.2018.02.011

Ren YY, Sun PP, Wang XX, Zhu ZY (2020) Degradation of cell wall polysaccharides and change of related enzyme activities with fruit softening in Annona squamosa during storage. Postharvest Biol Technol 166:111203. doi:10.1016/j.postharvbio.2020.111203 10.1016/j.postharvbio.2020.111203

Saei H, Sharifani MM, Dehghani A, Seifi E, Akbarpour V (2014) Description of biomechanical forces and physiological parameters of fruit cracking in pomegranate. Sci Hortic 178:224-230. doi:10.1016/j.scienta.2014.09.005 10.1016/j.scienta.2014.09.005

Sakai WS (1973) Simple method for differential staining of paraffin embedded plant material using toluidine blue O. Stain Technology 48:247-249. doi:10.3109/10520297309116632 10.3109/105202973091166324126691

Segonne SM, Bruneau M, Celton JM, Le Gall S, Francin-Allami M, Juchaux M, Laurens F, Orsel M, Renou JP (2014) Multiscale investigation of mealiness in apple: an atypical role for a pectin methylesterase during fruit maturation. BMC Plant Biol 14:1-18. doi:10.1186/s12870-014-0375-3 10.1186/s12870-014-0375-325551767PMC4310206

Sirisomboon P, Tanaka M, Fujita S, Kojima T (2000) Relationship between the texture and pectin constituents of Japanese pear. J Texture Stud 31:679-690. doi:10.1111/j.1745-4603.2000.tb01028.x 10.1111/j.1745-4603.2000.tb01028.x

Srivastava H, Narasimhan P (1967) Physiological studies during the growth and development of different varieties of guavas (Psidium guajava L.). J Hortic Sci 42:97-104. doi:10.1080/00221589.1967.11514197 10.1080/00221589.1967.11514197

Sugiura A, Zheng G, Yonemori K (1991) Growth and ripening of persimmon fruit at controlled temperatures during growth stage III. HortScience 26:574-576. doi:10.21273/HORTSCI.26.5.574 10.21273/HORTSCI.26.5.574

Torun H, Uluisik S (2022) Postharvest application of hydrogen peroxide affects physicochemical characteristics of tomato fruits during storage. Hortic Environ Biotechnol 63:391-401. doi:10.1007/s13580-021-00403-5 10.1007/s13580-021-00403-5

van der Knaap E, Østergaard L (2018) Shaping a fruit: developmental pathways that impact growth patterns. Semin Cell Dev Biol, Vol 79. Elsevier, pp 27-36. doi:10.1016/j.semcdb.2017.10.028 10.1016/j.semcdb.2017.10.02829092788

Vicente AR, Costa ML, Martínez GA, Chaves AR, Civello PM (2005) Effect of heat treatments on cell wall degradation and softening in strawberry fruit. Postharvest Biol Technol 38:213-222. doi:10.1016/j.postharvbio.2005.06.005 10.1016/j.postharvbio.2005.06.005

Wang G, Gao X, Wang X, Liu P, Guan SL, Qi K, Zhang S, Gu C (2022) Transcriptome analysis reveals gene associated with fruit size during fruit development in pear. Scientia Horticulturae 305:111367. doi:10.1016/j.scienta.2022.111367 10.1016/j.scienta.2022.111367

Willats WG, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. Plant Mol Biol 47:9-27. doi:10.1023/A:1010662911148 10.1023/A:101066291114811554482

Wormit A, Usadel B (2018) The multifaceted role of pectin methylesterase inhibitors (PMEIs). Int J Mol Sci 19:2878. doi:10.3390/ijms19102878 10.3390/ijms1910287830248977PMC6213510

Yadav S, Yadav PK, Yadav D, Yadav KDS (2009) Pectin lyase: a review. Process Biochem 44:1-10. doi:10.1016/j.procbio.2008.09.012 10.1016/j.procbio.2008.09.012

Yamaki S, Machida Y, Kakiuchi N (1979) Changes in cell wall polysaccharides and monosaccharides during development and ripening of Japanese pear fruit. Plant Cell Physiol 20:311-321. doi:10.1093/oxfordjournals.pcp.a075815 10.1093/oxfordjournals.pcp.a075815

Zdunek A, Kozioł A, Pieczywek PM, Cybulska J (2014) Evaluation of the nanostructure of pectin, hemicellulose and cellulose in the cell walls of pears of different texture and firmness. Food Bioproc Tech 7:3525-3535. doi:10.1007/s11947-014-1365-z 10.1007/s11947-014-1365-z

Zhang Q, Zhou BB, Li MJ, Wei QP, Han ZH (2018) Multivariate analysis between meteorological factor and fruit quality of Fuji apple at different locations in China. J Integr Agric 17:1338-1347. doi:10.1016/S2095-3119(17)61826-4 10.1016/S2095-3119(17)61826-4

Zhang W, Guo M, Yang W, Liu Y, Wang Y, Chen G (2022) The Role of Cell Wall Polysaccharides Disassembly and Enzyme Activity Changes in the Softening Process of Hami Melon (Cucumis melo L.). Foods 11:841. doi:10.3390/foods11060841 10.3390/foods1106084135327264PMC8954864

Zhang WW, Zhao SQ, Zhang LC, Xing Y, Jia WS (2020) Changes in the cell wall during fruit development and ripening in Fragaria vesca. Plant Physiol Biochem 154:54-65. doi:10.1016/j.plaphy.2020.05.028 10.1016/j.plaphy.2020.05.02832526611

Zhang X, Lu M, Ludlow RA, Ma W, An H (2021) Transcriptome analysis reveals candidate genes for dietary fiber metabolism in Rosa roxburghii fruit grown under different light intensities. Hortic Environ Biotechnol 62:751-764. doi:10.1007/s13580-021-00359-6 10.1007/s13580-021-00359-6

Zibordi M, Domingos S, Corelli Grappadelli L (2009) Thinning apples via shading: an appraisal under field conditions. J Hortic Sci Biotechnol 84:138-144. doi:10.1080/14620316.2009.11512611 10.1080/14620316.2009.11512611

Information

Publisher :KOREAN SOCIETY FOR HORTICULTURAL SCIENCE
Publisher(Ko) :한국원예학회
Journal Title :Horticultural Science and Technology
Journal Title(Ko) :원예과학기술지
Volume : 41
No :5
Pages :537-548
Received Date : 2023-05-22
Revised Date : 2023-07-03
Accepted Date : 2023-07-13
DOI :https://doi.org/10.7235/HORT.20230046

Horticultural Science and Technology 원예과학기술지 ISSN:1226-8763(Print) 2465-8588(Online)

All Issue