Abstract
Fruit cell wall modification is the main factor affecting fruit softening. β-Galactosidase (EC 3.2.1.23) is one of the cell wall modifying enzymes that are involved in fruit ripening. Although β-galactosidase genes have been characterized in multiple fruits, the relationship between β-galactosidase genes and persimmon (Diospyros kaki) ripening remains unknown. In this study, four persimmon β-galactosidase genes, designated DkGAL1 to DkGAL4, were isolated from ‘Fupingjianshi’ persimmon fruit. Transcriptional profiles of DkGAL genes during fruit development and in response to ethylene were investigated. β-Galactosidase activity increased during postharvest ripening and was considerably induced by propylene. The accumulation of DkGAL1 was relatively low during fruit growth but significantly increased throughout fruit ripening. In contrast, DkGAL2 mRNA levels were the highest at the early phase of fruit growth and decreased towards fruit maturity. DkGAL3 and DkGAL4 exhibited very low levels of expression in both growing fruit and postharvest fruit but were predominantly expressed in the leaf and stem. The expression pattern of DkGAL1 was positively regulated by ethylene, up-regulated under propylene treatment and suppressed by 1-MCP treatment. Ethylene appears to have little effect on the transcription of DkGAL2, DkGAL3 and DkGAL4. These results demonstrate that multiple β-galactosidase genes have differential transcript and hormonal regulation characteristics in ripening persimmon fruit. The functions of DkGAL3 and DkGAL4 are limited in fruit. However, DkGAL2 may play a crucial role in fruit development. Furthermore, DkGAL1 is a predominant β-galactosidase gene that is involved in persimmon fruit softening and regulated by ethylene.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn YO, Zheng M, Bevan DR, Esen A, Shiu SH, Benson J, Peng HP, Miller JT, Cheng CL, Poulton JE, Shih MC (2007) Functional genomic analysis of Arabidopsis thaliana glycoside hydrolase family 35. Phytochemistry 68:1510–1520
Bakshi A, Shemansky JM, Chang C, Binder BM (2015) History of research on the plant hormone ethylene. J Plant Growth Regul, pp 1–19
Balasubramaniam S, Lee HC, Lazan H, Othman R, Ali ZM (2005) Purification and properties of a β-galactosidase from carambola fruit with significant activity towards cell wall polysaccharides. Phytochemistry 66:153–163
Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P (2010) Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnol Adv 28:94–107
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. In: Plant Cell Walls. Springer, Berlin, pp 311–340
Carrington CS, Pressey R (1996) ß-Galactosidase II activity in relation to changes in cell wall galactosyl composition during tomato ripening. J Am Soc Hort Sci 121:132–136
Esteban R, Dopico B, Munoz FJ, Romo S, Martin I, Labrador E (2003) Cloning of a Cicer arietinum beta-galactosidase with pectin-degrading function. Plant Cell Physiol 44:718–725
Fu X, Feng C, Wang C, Yin X, Lu P, Grierson D, Xu C, Chen K (2014) Involvement of multiple phytoene synthase genes in tissue- and cultivar-specific accumulation of carotenoids in loquat. J Exp Bot 65:4679–4689
Gantulga D, Turan Y, Bevan DR, Esen A (2008) The Arabidopsis At1g45130 and At3g52840 genes encode beta-galactosidases with activity toward cell wall polysaccharides. Phytochemistry 69:1661–1670
Gapper NE, McQuinn RP, Giovannoni JJ (2013) Molecular and genetic regulation of fruit ripening. Plant Mol Biol 82:575–591
Gerardi C, Blando F, Santino A (2012) Purification and chemical characterisation of a cell wall-associated beta-galactosidase from mature sweet cherry (Prunus avium L.) fruit. Plant Physiol Biochem 61:123–130
Henrissat B, Teeri T, Warren R (1998) A scheme for designating enzymes that hydrolyse the polysaccharides in the cell walls of plants. FEBS Lett 425:352–354
Kang I-K, Suh S-G, Gross KC, Byun J-K (1994) N-terminal amino acid sequence of persimmon fruit [beta]-galactosidase. Plant Physiol 105:975–979
Kotake T, Dina S, Konishi T, Kaneko S, Igarashi K, Samejima M, Watanabe Y, Kimura K, Tsumuraya Y (2005) Molecular cloning of a β-galactosidase from radish that specifically hydrolyzes β-(1 → 3)-and β-(1 → 6)-galactosyl residues of arabinogalactan protein. Plant Physiol 138:1563–1576
Lazan H, Ng S-Y, Goh L-Y, Ali ZM (2004) Papaya β-galactosidase/galactanase isoforms in differential cell wall hydrolysis and fruit softening during ripening. Plant Physiol Biochem 42:847–853
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2 − ΔΔCT method. Methods 25(4):402–408
Lv J, Rao J, Zhu Y, Chang X, Hou Y, Zhu Q (2014) Cloning and expression of lipoxygenase genes and enzyme activity in ripening persimmon fruit in response to GA and ABA treatments. Postharvest Biol Technol 92:54–61
Martin I, Hernandez-Nistal J, Albornos L, Labrador E, Dopico B (2013) betaIII-Gal is involved in galactan reduction during phloem element differentiation in chickpea stems. Plant Cell Physiol 54:960–970
Matas AJ, Gapper NE, Chung M-Y, Giovannoni JJ, Rose JK (2009) Biology and genetic engineering of fruit maturation for enhanced quality and shelf-life. Curr Opin Biotechnol 20:197–203
Moctezuma E, Smith DL, Gross KC (2003a) Antisense suppression of a beta-galactosidase gene (TBG6) in tomato increases fruit cracking. J Exp Bot 54:2025–2033
Moctezuma E, Smith DL, Gross KC (2003b) Effect of ethylene on mRNA abundance of three β-galactosidase genes in wild type and mutant tomato fruit. Postharvest Biol Technol 28:207–217
Mwaniki MW, Mathooko FM, Matsuzaki M, Hiwasa K, Tateishi A, Ushijima K, Nakano R, Inaba A, Kubo Y (2005) Expression characteristics of seven members of the β-galactosidase gene family in ‘La France’ pear (Pyrus communis L.) fruit during growth and their regulation by 1-methylcyclopropene during postharvest ripening. Postharvest Biol Technol 36:253–263
Nakagawa T, Nakatsuka A, Yano K, Yasugahira S, Nakamura R, Sun N, Itai A, Suzuki T, Itamura H (2008) Expressed sequence tags from persimmon at different developmental stages. Plant Cell Rep 27:931–938
Nakamura A, Maeda H, Mizuno M, Koshi Y, Nagamatsu Y (2003) β-Galactosidase and its significance in ripening of “Saijyo” japanese persimmon fruit. Biosci Biotechnol Biochem 67:68–76
Othman R, Chong HL, Choo TS, Ali ZM (2011) Three β-galactosidase cDNA clones related to fruit ripening in papaya (Carica papaya). Acta Physiol Plant 33:2301–2310
Payasi A, Mishra NN, Chaves ALS, Singh R (2009) Biochemistry of fruit softening: an overview. Physiol Mol Biol Plants 15:103–113
Pressey R (1983) β-Galactosidases in ripening tomatoes. Plant Physiol 71:132–135
Roach MJ, Mokshina NY, Badhan A, Snegireva AV, Hobson N, Deyholos MK, Gorshkova TA (2011) Development of cellulosic secondary walls in flax fibers requires beta-galactosidase. Plant Physiol 156:1351–1363
Sampedro J, Gianzo C, Iglesias N, Guitian E, Revilla G, Zarra I (2012) AtBGAL10 is the main xyloglucan beta-galactosidase in Arabidopsis, and its absence results in unusual xyloglucan subunits and growth defects. Plant Physiol 158:1146–1157
Smith DL, Gross KC (2000) A family of at least seven β-galactosidase genes is expressed during tomato fruit development. Plant Physiol 123:1173–1184
Smith DL, Abbott JA, Gross KC (2002) Down-regulation of tomato beta-galactosidase 4 results in decreased fruit softening. Plant Physiol 129:1755–1762
Sozzi G, Camperi S, Cascone O, Fraschina A (1998) Galactosidases in tomato fruit ontogeny: decreased galactosidase activities in antisense ACC synthase fruit during ripening and reversal with exogenous ethylene. Funct Plant Biol 25:237–244
Tateishi A, Inoue H, Shiba H, Yamaki S (2001) Molecular cloning of β-galactosidase from Japanese pear (Pyrus pyrifolia) and its gene expression with fruit ripening. Plant Cell Physiol 42:492–498
Tateishi A, Shiba H, Ogihara J, Isobe K, Nomura K, Watanabe K, Inoue H (2007) Differential expression and ethylene regulation of β-galactosidase genes and isozymes isolated from avocado (Persea americana Mill.) fruit. Postharvest Biol Technol 45:56–65
Trainotti L, Spinello R, Piovan A, Spolaore S, Casadoro G (2001) beta-Galactosidases with a lectin-like domain are expressed in strawberry. J Exp Bot 52:1635–1645
Vicente AR, Saladie M, Rose JK, Labavitch JM (2007) The linkage between cell wall metabolism and fruit softening: looking to the future. J Sci Food Agric 87:1435–1448
Wan C-Y, Wilkins TA (1994) A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.). Anal Biochem 223:7–12
Acknowledgments
The authors thank Zhenying Sun and Xun Sun for their assistance in fruit harvest. This work was supported by the National Major Special Project for “The research on logistics environmental adaptability and quality control mechanism of fresh edible agricultural products” during the Thirteenth Five-year Plan Period.
Author information
Authors and Affiliations
Corresponding author
Additional information
Qiuyan Ban and Ye Han have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Ban, Q., Han, Y., Meng, K. et al. Characterization of β-Galactosidase Genes Involved in Persimmon Growth and Fruit Ripening and in Response to Propylene and 1-Methylcyclopropene. J Plant Growth Regul 35, 1025–1035 (2016). https://doi.org/10.1007/s00344-016-9601-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-016-9601-6