Skip to main content
Log in

Sequential actions of pectinases and cellulases during secretory cavity formation in Citrus fruits

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Pectinase and cellulase activities are involved in a number of intercellular space-forming processes in plants. In this study, we combined cytochemistry with ultrastructural analysis to investigate the ontogeny of secretory cavity in fruits of Citrus medica L. var. sarcodactylis (Noot.) Swingle, Citrus reticulata Blanco and Citrus limon (L.) Burm. f. Pectinase activity was first detectable at the initial stage of cavity formation, peaked at the intercellular space-forming stage, and diminished at the following stages. In comparison, no cellulase activity was detected until the early lumen-expanding stage. The cellulase activity increased at the late lumen-expanding stage and culminated at the near-mature stage. In the fruit of C. medica var. sarcodactylis, the distribution of pectinase and cellulase reaction products was restricted to the endoplasmic reticulum (ER), the vesicles derived from ER and the cell wall. We also observed that multivesicular structure containing the pectinase reaction product at the initial stage of cavity formation. Our results suggest that pectinase and cellulase are synthesized on ER and secreted directly into the cell wall through exocytosis of ER-derived vesicles. Our observations are consistent with the notion that the secretory cavity in Citrus fruits is formed through a schizolysigenous process in which pectinase activity is involved in the degradation of the middle lamella, whereas cellulase activity is responsible for the degradation of the cell wall.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

References

  • Allen RD, Nessler CR (1984) Cytochemical localization of pectinase activity in laticifers of Nerium oleander L. Protoplasma 119:74–78. doi:10.1007/BF01287819

    Article  CAS  Google Scholar 

  • Atkinson RG, Schröder R, Hallett IC, Cohen D, MacRae EA (2002) Overexpression of polygalacturonase in transgenic apple trees leads to a range of novel phenotypes involving changes in cell adhesion. Plant Physiol 129:122–133. doi:10.1104/pp. 010986

    Article  PubMed  CAS  Google Scholar 

  • Bal AK (1974) Cellulase. In: Hayat MA (ed) Electron microscopy of enzymes, vol 3. Van Nostrand Reinhold, New York, pp 68–76

    Google Scholar 

  • Bal AK, Verma DPS, Byrne H, Maclachlan GA (1976) Subcellular localization of cellulase in auxin-treated pea. J Cell Biol 69:97–105. doi:10.1083/jcb.69.1.97

    Article  PubMed  CAS  Google Scholar 

  • Bamonieri A, Safaei-Ghomi J, Asadi H, Batooli H, Masoudi S, Rustaiyan A (2006) Essential oils from leaves, stems, flowers and fruits of Haplophyllum robustum Bge (Rutaceae) grown in Iran. J Essent Oil Res 18(4):379–380

    CAS  Google Scholar 

  • Bennici A, Tani C (2004) Anatomical and ultrastructural study of the secretory cavity development of Citrus sinensis and C. limon: evaluation of schizolysigenous ontogeny. Flora 199:464–475

    Google Scholar 

  • Bosabalidis A, Tsekos I (1982a) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. I. Early stages of the gland cells differentiation. Protoplasma 112:55–62. doi:10.1007/BF01280215

    Article  Google Scholar 

  • Bosabalidis A, Tsekos I (1982b) Ultrastructural studies on the secretory cavities of Citrus deliciosa Ten. II. Development of the essential oil-accumulating space of the gland and process of active secretion. Protoplasma 112:63–70. doi:10.1007/BF01280216

    Article  Google Scholar 

  • Brummell DA, Catala C, Lashbrook CC, Bennett AB (1997) A menbrane-anchored E-type endo-1,4-glucanase is localized on Golgi and plasma membranes of higher plants. Proc Natl Acad Sci USA 94:4794–4799. doi:10.1073/pnas.94.9.4794

    Article  PubMed  CAS  Google Scholar 

  • Buvat R (1989) Ontogeny, cell differentiation and structure of vascular plants. Springer, Berlin

    Google Scholar 

  • Cheng KC, Nie SW, Chen SW, Jian LC, Sun LH, Sun DL (1987) Studies on the secondary formation of plasmodesmata between the pollen mother cells of lily before cytomixis. Acta Biol Exp Sin 20:1–11

    Google Scholar 

  • Crookes PR, Grierson D (1983) Ultrastructure of tomato fruit ripening and the role of polygalacturonase isoenzymes in cell wall degradation. Plant Physiol 72:1088–1093

    Article  PubMed  CAS  Google Scholar 

  • Degan FD, Child R, Svendsen I, Ulvskov P (2001) The cleavable N-terminal domain of plant endopolygalacturonases from clade B may be involved in a regulated secretion mechanism. J Biol Chem 276:35297–35304. doi:10.1074/jbc.M102136200

    Article  PubMed  CAS  Google Scholar 

  • Esau K (1965) Plant anatomy, 2nd edn. Wiley, New York

    Google Scholar 

  • Fahn A (1979) Secretory tissue in Plants. Academic Press, London

    Google Scholar 

  • Fahn A, Benayoun J (1976) Ultrastructure of resin ducts in Pinus halepensis development, possible sites of resin synthesis, and mode of its elimination from the protoplast. Ann Bot (Lond) 40:857–863

    Google Scholar 

  • Roberts JA, Gonzalez-Carranza (2007) Plant cell separation and adhesion. Blackwell Publishing Ltd., Oxford, pp 174

  • Heinrich G (1966) Licht-und elektronenmikroskopische Untersuchungen zur Genese der Exkrete in den lysigenen Exkreträumen von Citrus medica. Flora 156A:451–456

    Google Scholar 

  • Hu ZH, Yu G (1993) Studies on the structure and development of secretory cavities in Poncirus trifoliate. Acta Bot Sin 35:447–452 (in Chinese with English abstract)

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde–glutaraldehyde fixation of high osmolality for use in electron microscopy. J Cell Biol 27:137

    Google Scholar 

  • Knight TG, Klieber A, Sedgley M (2001) The relationship between oil gland and fruit development in Washington Navel Orange (Citrus sinensis L. Osbeck). Ann Bot (Lond) 88:1039–1047. doi:10.1006/anbo.2001.1546

    Article  Google Scholar 

  • Knight TG, Klieber A, Sedgley M (2002) Structural basis of the rind disorder oleocellosis in Washington Navel Orange (Citrus sinensis L. Osbeck). Ann Bot (Lond) 90:765–773. doi:10.1093/aob/mcf258

    Article  CAS  Google Scholar 

  • Li AM, Wang YR, Wu H (2004) Cytochemical localization of pectinase: the cytochemical evidence for resin ducts formed by schizogeny in Pinus massoniana. Acta Bot Sin 46(4):443–450

    CAS  Google Scholar 

  • Liang SJ, Wu H, Lun X, Lu DW (2006) Secretory cavity development and its relationship with the accumulation of essential oil in fruits of Citrus medica L. var. sarcodactylis (Noot.) Swingle. J Integr Plant Biol 48(5):573–583. doi:10.1111/j.1744-7909.2006.00230.x

    Article  CAS  Google Scholar 

  • Nakashima J, Endo S, Fukuda H (2004) Immunocytochemical localization of polygalacturonase during tracheary element differentiation in Zinnia elegans. Planta 218:729–739. doi:10.1007/s00425-003-1167-4

    Article  PubMed  CAS  Google Scholar 

  • Neelam A, Sexton R (1995) Cellulase (endo-1, 4-glucanase) and cell wall breakdown during anther development in the sweet pea (Lathyrus odoratus L.): isolation and characterization of partial cDNA clones. J Plant Physiol 146:622–628

    CAS  Google Scholar 

  • Nessler CL, Mahlberg PG (1981) Cytochemical localization of cellulase activity in articulated, anastomosing laticifers of Papaver somniferum L. (Papaveraceae). Am J Bot 68:730–732. doi:10.2307/2442800

    Article  Google Scholar 

  • Pressey R (1991) Polygalacturonase in tree pollen. Phytochemistry 30:1753–1755. doi:10.1016/0031-9422(91)85006-L

    Article  CAS  Google Scholar 

  • Pressey R, Reger BJ (1989) Polygalacturonase in pollen from corn and other grasses. Plant Sci 59:57–62. doi:10.1016/0168-9452(89)90008-3

    Article  CAS  Google Scholar 

  • Rose JKC (2003) The plant cell wall. Blackwell Publishing Ltd., Oxford, pp 4–5, 279–285

  • Sexton R, Campillo ED, Duncan D, Lewis LN (1990) The purification of an anther cellulase ((1:4)4-glucan hydrolase) from Lathyrus odoratus L. and its relationship to the similar enzyme found in abscission zones. Plant Sci 67:169–176. doi:10.1016/0168-9452(90)90240-O

    Article  CAS  Google Scholar 

  • Suffredini IB, Paciencia MLB, Varella AD, Younes RN (2006) In vitro prostate cancer cell growth inhibition by Brazilian plant extracts. Pharmazie 61(8):722–724

    PubMed  CAS  Google Scholar 

  • Taylor JE, Tucker GA et al (1990) Polygalacturonases expression during leaf abscission of normal and transgenic tomato plants. Planta 183:133–138

    Google Scholar 

  • Thomson WW, Platt-Aloia K, Endress AG (1976) Ultrastructure of oil gland development in the leaf of Citrus sinensis L. Bot Gaz 137:330–340. doi:10.1086/336880

    Article  Google Scholar 

  • Turner GW (1999) A brief history of the lysigenous gland hypothesis. Bot Rev 65(1):76–88. doi:10.1007/BF02856558

    Article  Google Scholar 

  • Turner GW, Berry AM, Gifford EM (1998) Schizogenous secretory cavities of Citrus limon (L.) Burm. F. and a re-evaluation of the lysigenous gland concept. Int J Plant Sci 159:75–88. doi:10.1086/297523

    Article  Google Scholar 

  • Viljoen AM, Moolla A et al (2006) The biological activity and essential oil composition of 17 Agathosma (Rutaceae) species. J Essent Oil Res 18:2–16

    CAS  Google Scholar 

  • Wang XY, Guo GQ, Nie XW, Zheng GC (1998) Cytochemical localization of cellulase activity in pollen mother cells of David lily during meiotic prophase I and its relation to secondary formation of plasmodesmata. Protoplasma 204:128–138. doi:10.1007/BF01280319

    Article  CAS  Google Scholar 

  • Wilson KJ, Nessler CL, Mahlberg PG (1976) Pectinase in Asclepias latex and its possible role in laticifer growth and development. Am J Bot 63:1140–1144. doi:10.2307/2441659

    Article  CAS  Google Scholar 

  • Wu H, Yang M (2005) Reduction in vacuolar volume in the tapetal cells coincides with conclusion of the tetrad stage in Arabidopsis thaliana. Sex Plant Reprod 18:173–178. doi:10.1007/s00497-005-0010-4

    Article  CAS  Google Scholar 

  • Yu CH, Guo GQ, Nie XW, Zheng GC (2004) Cytochemical localization of pectinase activity in pollen mother cells of Tobacco during meiotic prophase I and its relation to the formation of secondary plasmodesmata and cytoplasmic channels. Acta Bot Sin 46(12):1443–1453

    Google Scholar 

Download references

Acknowledgments

We thank Xuan Lun and Dongwen Lu for assistance with electron microscopy. This work was supported by the National Natural Science Foundation of China (30670119) and Science and Technology Key Program of Guangdong Province (C20605).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hong Wu.

Additional information

Communicated by D. Treutter.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liang, S., Wang, H., Yang, M. et al. Sequential actions of pectinases and cellulases during secretory cavity formation in Citrus fruits. Trees 23, 19–27 (2009). https://doi.org/10.1007/s00468-008-0250-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-008-0250-7

Keywords

Navigation