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Isolation of a Polygalacturonase Gene from Citrus sinensis Fruit and Its Expression Relative to Fruit Mastication Trait, Fruit Development, and Calcium or Boron Treatments

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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.

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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

    Article  CAS  PubMed  Google Scholar 

  • Asif MH, Nath P (2005) Expression of multiple forms of polygalacturonase gene during ripening in banana fruit. Plant Physiol Biochem 43:177–184

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Blevins DG, Lukaszewski KM (1998) Boron in plant structure and function. Annu Rev Plant Physiol Mol Biol 49:481–500

    Article  CAS  Google Scholar 

  • Braddock RJ (1995) By-products of citrus fruits. Food Technol 49:74–77

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Deng XX (2008) Citrus cultivars in China. China agricultural press, Beijing

    Google Scholar 

  • Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annu Rev Plant Physiol Mol Biol 52:725–749

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Hadfield KA, Bennett AB (1998) Polygalacturonases: many genes in search of a function. Plant Physiol 117:337–343

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Jiang CZ, Lu F, Imsabai W et al (2008) Silencing polygalacturonase expression inhibits tomato petiole abscission. J Exp Bot 59:973–979

    Article  CAS  PubMed  Google Scholar 

  • Kutsunai SY, Lin AC, Percival FW et al (1993) Ripening-related polygalacturonase cDNA from avocado. Plant Physiol 103:289–290

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • Marin-Rodriguez MC, Orchard J, Seymour GB (2002) Pectate lyases, cell wall degradation and fruit softening. J Exp Bot 53:2115–2119

    Article  CAS  PubMed  Google Scholar 

  • Markovic O, Janecek S (2001) Pectin degrading glycoside hydrolases of family 28: sequence-structural features, specificities and evolution. Protein Eng 14:615–631

    Article  CAS  PubMed  Google Scholar 

  • Maurice D, Claudine M, Michel T (1984) Calcium and the cell wall. Plant Cell Environ 7:441–448

    Article  Google Scholar 

  • Nunan K, Davies C, Robinson S et al (2001) Expression patterns of cell wall-modifying enzymes during grape berry development. Planta 214:257–264

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Ovodov Y (2009) Current views on pectin substances. Russ J Bioorgan Chem 35:269–284

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Payasi A, Mishra N, Chaves A et al (2009) Biochemistry of fruit softening: an overview. Physiol Mol Biol Plants 15:103–113

    Article  CAS  Google Scholar 

  • Prasanna V, Prabha TN, Tharanathan RN (2007) Fruit ripening phenomena—an overview. Crit Rev Food Sci Nutr 47:1–19

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Reuther W, Bachelor LD, Webber HJ (1968) The citrus industry. University of California, USA

    Google Scholar 

  • Sakai T, Sakamoto T, Hallaert J et al (1993) Pectin, pectinase and protopectinase: production, properties, and applications. Adv Appl Microbiol 39:213–294

    Article  CAS  PubMed  Google Scholar 

  • Sitrit Y, Hadfield KA, Bennett AB et al (1999) Expression of a polygalacturonase associated with tomato seed germination. Plant Physiol 121:419–428

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tebbutt SJ, Rogers HJ, Lonsdale DM (1994) Characterization of a tobacco gene encoding a pollen-specific polygalacturonase. Plant Mol Biol 25:283–297

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Waldron KW, Parker ML, Smith AC (2003) Plant cell walls and food quality. Comprehensive Reviews in Food Science and Food Safety 2:101–119

    Article  CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

Download references

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.

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Correspondence to Xiu-Xin Deng.

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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

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