Abstract
Polygalacturonase (PG) plays a significant role in pectin solubilization and depolymerization in vivo and is involved in numerous plant developmental processes. In this study, a polygalacturonase gene (CitPG, EF185420) was isolated from Citrus sinensis. It is 1,686 bp with a putative open reading frame of 1,338 bp encoding 445 amino acids. Phylogenetic analysis showed that CitPG belongs to clade B which includes PGs expressed in fruits or dehiscence zones. CitPG expression profiles during fruit ripening were compared between two pairs of varieties which differ in their mastication traits: C. sinensis cv. Fengjiewancheng (FJWC) vs. C. sinensis cv. Fengjie 72-1(FJ72-1) and Citrus reticulata cv. Kinokuni (NM) vs. C. reticulata cv. Miguang (MG), in which the mastication trait of “FJWC” and “NM” are inferior to their respective partner cultivars. Results indicated that the CitPG transcript level was significantly lower in the inferior mastication variety at the late ripening stage or at all ripening stages. Calcium or boron treatment resulted in a significant reduction in CitPG transcription level in fruit pulp at harvest time (235 days after anthesis). This was accompanied by an increase in protopectin content. In addition, the mRNA level of CitPG in the fruit peel and pulp increased during the fruit's rapid cell enlargement stage and was inversely correlated with protopectin levels. These results suggest that CitPG is associated with the favorable enhancement of the fruit mastication trait and is involved in dissolving the protopectin during cell enlargement.
Similar content being viewed by others
Abbreviations
- B:
-
Boron
- Cara Cara:
-
Citrus sinensis cv.Cara Cara
- Ca:
-
Calcium
- CitPG :
-
Citrus polygalacturonase gene
- DAA:
-
Days after anthesis
- FJ72-1:
-
C. sinensis cv. Fengjie 72-1
- FJWC:
-
C. sinensis cv. Fengjiewancheng
- MG:
-
C. reticulate cv. Miguang
- NM:
-
C. reticulate cv. Kinokuni
- PG:
-
Polygalacturonase
- RACE:
-
Rapid amplification of cDNA ends
- TDF:
-
Transcript-derived fragment
- WSP:
-
Water-soluble pectins
References
Altschul SF, Wootton JC, Gertz EM et al (2005) Protein database searches using compositionally adjusted substitution matrices. Febs Journal 272:5101–5109
Asif MH, Nath P (2005) Expression of multiple forms of polygalacturonase gene during ripening in banana fruit. Plant Physiol Biochem 43:177–184
Atkinson RG, Bolitho KM, Wright MA et al (1998) Apple ACC-oxidase and polygalacturonase: ripening-specific gene expression and promoter analysis in transgenic tomato. Plant Mol Biol 38:449–460
Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Mol Biol 49:481–500
Braddock RJ (1995) By-products of citrus fruits. Food Technol 49:74–77
Callahan AM, Scorza R, Bassett C et al (2004) Deletions in an endopolygalacturonase gene cluster correlate with non-melting flesh texture in peach. Funct Plant Biol 31:159–168
Chaiprasart P, Handsawasdi C, Pipattanawong N (2006) The effect of chitosan coating and calcium chloride treatment on postharvest qualities of strawberry fruit (Fragaria × ananassa). Acta Horticulturae 708:337–342
Deng XX (2008) Citrus cultivars in China. China agricultural press, Beijing
Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Mol Biol 52:725–749
Gonzalez-Carranza ZH, Whitelaw CA, Swarup R et al (2002) Temporal and spatial expression of a polygalacturonase during leaf and flower abscission in oilseed rape and Arabidopsis. Plant Physiol 128:534–543
Gorguet B, Schipper D, van Lammeren A et al (2009) ps-2, the gene responsible for functional sterility in tomato, due to non-dehiscent anthers, is the result of a mutation in a novel polygalacturonase gene. Theor Appl Genet 118:1199–1209
Goulao LF, Oliveira CM (2008) Cell wall modifications during fruit ripening: when a fruit is not the fruit. Trends in Food Sci Technol 19:4–25
Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337–343
Ham BK, Park JM, Lee SB et al (2006) Tobacco Tsip1, a DnaJ-type Zn finger protein, is recruited to and potentiates Tsi1-mediated transcriptional activation. Plant Cell 18:2005–2020
Hiwasa K, Kinugasa Y, Amano S et al (2003) Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit. J Exp Bot 54:771–779
Iglesias-Fernández R, Matilla AJ, Rodríguez-Gacio MC et al (2007) The polygalacturonase gene PdPG1 is developmentally regulated in reproductive organs of Prunus domestica L. subsp. insititia. Plant Sci 172:763–772
Jiang CZ, Lu F, Imsabai W et al (2008) Silencing polygalacturonase expression inhibits tomato petiole abscission. J Exp Bot 59:973–979
Kutsunai SY, Lin AC, Percival FW et al (1993) Ripening-related polygalacturonase cDNA from avocado. Plant Physiol 103:289–290
Lester DR, Speirs J, Orr G et al (1994) Peach (Prunus persica) endopolygalacturonase cDNA isolation and mRNA analysis in melting and nonmelting peach cultivars. Plant Physiol 105:225–231
Lieten P (2002) Boron deficiency of strawberries grown in substrate culture. Acta Horticulturae 2
Liu YZ, Baig M, Fan R et al (2009a) Identification and expression pattern of a novel NAM, ATAF, and CUC-like gene from Citrus sinensis Osbeck. Plant Mol Biol Rep 27:292–297
Liu YZ, Zhu AD, Lei Y et al (2009b) Identifying differently expressed transcripts between a novel late-ripening Citrus sinensis mutant and its wild variety during fruit ripening using cDNA–AFLP. In: Tennant P, Benkeblia N (Eds) Citrus III. Tree and Forestry Science and Biotechnology 3:5–11
Marin-Rodriguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119
Markovic O, Janecek S (2001) Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng 14:615–631
Maurice D, Claudine M, Michel T (1984) Calcium and the cell wall. Plant Cell Environ 7:441–448
Nunan K, Davies C, Robinson S et al (2001) Expression patterns of cell wall-modifying enzymes during grape berry development. Planta 214:257–264
Ogawa M, Kay P, Wilson S et al (2009) Arabidopsis dehiscence zone polygalacturonase1 (ADPG1), ADPG2, and QUARTET2 are polygalacturonases required for cell separation during reproductive development in Arabidopsis. Plant Cell 21:216–233
Ovodov Y (2009) Current views on pectin substances. Russ J Bioorgan Chem 35:269–284
Park KC, Kwon SJ, Kim PH et al (2008) Gene structure dynamics and divergence of the polygalacturonase gene family of plants and fungus. Genome 51:30–40
Payasi A, Mishra N, Chaves A et al (2009) Biochemistry of fruit softening: an overview. Physiol Mol Biol Plants 15:103–113
Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena—an overview. Crit Rev Food Sci Nutr 47:1–19
Redondo-Nevado J, Moyano E, Medina-Escobar N et al (2001) A fruit-specific and developmentally regulated endopolygalacturonase gene from strawberry (Fragaria × ananassa cv. Chandler). J Exp Bot 52:1941–1945
Reuther W, Bachelor LD, Webber HJ (1968) The citrus industry. University of California, USA
Sakai T, Sakamoto T, Hallaert J et al (1993) Pectin, pectinase and protopectinase: production, properties, and applications. Adv Appl Microbiol 39:213–294
Sitrit Y, Hadfield KA, Bennett AB et al (1999) Expression of a polygalacturonase associated with tomato seed germination. Plant Physiol 121:419–428
Sun X, Collins R (2004) A comparison of attitudes among purchasers of imported fruit in Guangzhou and Urumqi, China. Food Qual Prefer 15:229–237
Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tebbutt SJ, Rogers HJ, Lonsdale DM (1994) Characterization of a tobacco gene encoding a pollen-specific polygalacturonase. Plant Mol Biol 25:283–297
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680
Torki M, Mandaron P, Mache R et al (2000) Characterization of a ubiquitous expressed gene family encoding polygalacturonase in Arabidopsis thaliana. Gene 242:427–436
Van Buggenhout S, Sila DN, Duvetter T et al (2009) Pectins in processed fruits and vegetables: part III—texture engineering. Comprehensive Reviews in Food Science and Food Safety 8:105–117
Villarreal NM, Rosli HG, Martinez GA et al (2008) Polygalacturonase activity and expression of related genes during ripening of strawberry cultivars with contrasting fruit firmness. Postharvest Biol Technol 47:141–150
Waldron KW, Parker ML, Smith AC (2003) Plant cell walls and food quality. Comprehensive Reviews in Food Science and Food Safety 2:101–119
Wang YW, Xu WY (1987) A ration analytical process for hemicellulose, cellulose and lignin in the solid substrata fermentation of lignocellulose. Chin Bull Microbiol 14:81–84
Wang ZY, MacRae EA, Wright MA et al (2000) Polygalacturonase gene expression in kiwifruit: relationship to fruit softening and ethylene production. Plant Mol Biol 42:317–328
Zhang Q, Huang L, Liu T et al (2008) Functional analysis of a pollen-expressed polygalacturonase gene BcMF6 in Chinese cabbage (Brassica campestris L. ssp. chinensis Makino). Plant Cell Rep 27:1207–1215
Acknowledgements
The National Natural Science Foundation of China (No. 30700551 and 30760145) supported this work. In addition, we would like to acknowledge Avi Sadka (senior scientist in Israeli Agricultural Research Organization) in helping improve the quality of this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Liu, YZ., Dong, T., Lei, Y. et al. Isolation of a Polygalacturonase Gene from Citrus sinensis Fruit and Its Expression Relative to Fruit Mastication Trait, Fruit Development, and Calcium or Boron Treatments. Plant Mol Biol Rep 29, 51–59 (2011). https://doi.org/10.1007/s11105-010-0206-0
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-010-0206-0