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Ginseng root water-extracted pectic polysaccharides originate from secretory cavities

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Abstract

A range of molecular probes for cell wall polysaccharides has been used to explore the structure and location of water-extracted pectic polysaccharides occurring in fractions isolated from ginseng roots. The LM19 homogalacturonan (HG) epitope was abundant in an HG fraction and analysis of LM19 binding to a rhamnogalacturonan-I (RG-I) rich-fraction indicated that the LM19 epitope is sensitive to acetylation. A specific RG-I epitope (LM16), four arabinogalactan-protein (AGP) epitopes (LM2, LM14, JIM16, MAC207) and an extensin epitope (JIM20) were found to be abundant and co-located in several isolated polysaccharide fractions including an arabinogalactan fraction and two RG-I fractions. Detection of the RG-I, AGP and extensin epitopes identified in isolated polysaccharide fractions in sections of ginseng roots indicated that they were most abundant in secretory cavities found in the cortical regions of ginseng roots. In addition, the immunocytochemical study indicated that polysaccharide epitope masking is a widespread phenomenon in the primary cell walls of ginseng roots.

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Abbreviations

AGP:

Arabinogalactan-protein

CBM:

Carbohydrate-binding module

ELISA:

Enzyme-linked immunosorbent assay

FITC:

Fluorescein isothiocyanate

HG:

Homogalacturonan

MP:

Milk protein

PBS:

Phosphate-buffered saline

PG:

Endo-polygalacturonase

RG-I:

Rhamnogalacturonan-I

TBO:

Toluidine blue O

TFA:

Trifluoroacetic acid

References

  • Blake AW, McCartney L, Flint JE, Bolam DN, Boraston AB, Gilbert HJ, Knox JP (2006) Understanding the biological rationale for the diversity of cellulose-directed carbohydrate-binding modules in prokaryotic enzymes. J Biol Chem 281:29321–29329

    Article  PubMed  CAS  Google Scholar 

  • Buettner C, Yeh GY, Phillips RS, Mittleman MA, Kaptchuk TJ (2006) Systematic review of the effects of ginseng on cardiovascular risk factors. Ann Pharmacother 40:83–95

    PubMed  CAS  Google Scholar 

  • Caffall KH, Mohnen D (2009) The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr Res 344:879–900

    Article  Google Scholar 

  • Cheng H, Li S, Fan Y, Gao X, Hao M, Wang J, Zhang X, Tai G, Zhou Y (2010) Comparative studies of the antiproliferative effects of ginseng polysaccharides on HT-29 human colon cancer cells. Med Oncol 28:175–181

    Article  PubMed  Google Scholar 

  • Clausen MH, Willats WGT, Knox JP (2003) Synthetic methyl hexagalacturonate hapten inhibitors of anti-homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydr Res 338:1797–1800

    Article  PubMed  CAS  Google Scholar 

  • Clausen MH, Ralet MC, Willats WGT, McCartney L, Marcus SE, Thibault JF, Knox JP (2004) A monoclonal antibody to feruloylated-(1 → 4)-β-d-galactan. Planta 219:1036–1041

    Article  PubMed  CAS  Google Scholar 

  • Evert RF (2006) Xylem: cell types and developmental aspects. In: Evert RF (ed) Esau’s plant anatomy: meristems, cells and tissues of the plant body—their structure, function, and development, 3rd edn. Wiley, New York, pp 255–283

    Chapter  Google Scholar 

  • Fan Y, Cheng H, Li S, Wang J, Liu D, Hao M, Gao X, Fan E, Tai G, Zhou Y (2010) Relationship of the inhibition of cell migration with the structure of ginseng pectic polysaccharides. Carbohydr Polym 81:340–347

    Article  CAS  Google Scholar 

  • Gleeson PA, Clarke AE (1979) Structural studies on the major component of Gladiolus style mucilage, an arabinogalactan-protein. Biochem J 181:607–621

    PubMed  CAS  Google Scholar 

  • Golovchenko VV, Ovodova RG, Shashkov AS, Ovodov YS (2002) Structural studies of the pectic polysaccharide from duckweed Lemna minor L. Phytochemistry 60:89–97

    Article  PubMed  CAS  Google Scholar 

  • Hu SY (1976) The genus Panax (ginseng) in Chinese medicine. Econ Bot 30:11–28

    Article  Google Scholar 

  • Immerzeel P, Eppink MM, de Vries SC, Schols HA, Voragen AGJ (2006) Carrot arabinogalactan proteins are interlinked with pectins. Physiol Plant 128:18–28

    Article  CAS  Google Scholar 

  • Jones L, Seymour GB, Knox JP (1997) Localization of pectic galactan in tomato cell walls using a monoclonal antibody specific to (1 → 4)-β-d-galactan. Plant Physiol 113:1405–1412

    PubMed  CAS  Google Scholar 

  • Kieliszewski M, Lamport DTA (1994) Extensin: repetitive motifs, functional sites, posttranslational codes, and phylogeny. Plant J 5:157–172

    Article  PubMed  CAS  Google Scholar 

  • Kieliszewski MJ, Kamyab A, Leykam JF, Lamport DTA (1992) A histidine-rich extensin from Zea mays is an arabinogalactan protein. Plant Physiol 99:538–547

    Article  PubMed  CAS  Google Scholar 

  • Knox JP, Linstead PJ, Peart J, Cooper C, Roberts K (1991) Developmentally-regulated epitopes of cell surface arabinogalactan-proteins and their relation to root tissue pattern formation. Plant J 1:317–326

    Google Scholar 

  • Li F (2002) The anatomy of China ginseng. In: Li F (ed) China ginseng and American ginseng. China Agricultural Science and Technology Press, Beijing, pp 38–64

    Google Scholar 

  • Mahady GB, Gyllenhaal C, Fong HHS, Farnsworth NR (2000) Ginsengs: a review of safety and efficacy. Nutr Clin Care 3:90–101

    Article  Google Scholar 

  • Marcus SE, Verhertbruggen Y, Hervé C, Ordaz-Ortiz JJ, Farkas V, Pedersen HL, Willats WGT, Knox JP (2008) Pectic homogalacturonan masks abundant sets of xyloglucan epitopes in plant cell walls. BMC Plant Biol 8:60

    Article  PubMed  Google Scholar 

  • Marcus SE, Blake AW, Benians TAS, Lee KJD, Poyser C, Donaldson L, Leroux O, Rogowski A, Petersen HL, Boraston A, Gilbert HJ, Willats WGT, Knox PJ (2010) Restricted access of proteins to mannan polysaccharides in intact plant cell walls. Plant J 64:191–203

    Article  PubMed  CAS  Google Scholar 

  • McCartney L, Steele-King CG, Jordan E, Knox JP (2003) Cell wall pectic (1 → 4)-β-d-galactan marks the acceleration of cell elongation in the Arabidopsis seedling root meristem. Plant J 33:447–454

    Article  PubMed  CAS  Google Scholar 

  • McCartney L, Marcus SE, Knox JP (2005) Monoclonal antibodies to plant cell wall xylans and arabinoxylans. J Histochem Cytochem 53:543–546

    Article  PubMed  CAS  Google Scholar 

  • Moller I, Marcus SE, Haeger A, Verhertbruggen Y, Verhoef R, Schols H, Mikklesen JD, Knox JP, Willats WGT (2008) High-throughput screening of monoclonal antibodies against plant cell wall glycans by hierarchial clustering of their carbohydrate microarray binding profiles. Glycoconj J 25:37–48

    Article  PubMed  CAS  Google Scholar 

  • Nah SY, Kim DH, Rhim H (2007) Ginsenosides: are any of them candidates for drugs acting on the central nervous system? CNS 13:381–404

    CAS  Google Scholar 

  • O’Brien TP, Feder N, Mc-Cully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:367–373

    Google Scholar 

  • Parker AJP, Haskins EF, Deyrup-Olsen I (1982) Toluidine blue: a simple, effective stain for plant tissues. Am Biol Teach 44:487–489

    Google Scholar 

  • Pennell RI, Knox JP, Scofield GN, Selvendran RR, Roberts K (1989) A family of abundant plasma membrane-associated glycoproteins related to the arabinogalactan proteins is unique to flowering plants. J Cell Biol 108:1967–1977

    Article  PubMed  CAS  Google Scholar 

  • Radad K, Gille G, Irausch WD (2004) Use of ginseng in medicine: perspectives on CNS disorders. Iranian J Pharmacol Therapeut 3:30–40

    Google Scholar 

  • Ridley BL, O’Neill MA, Mohnen D (2001) Pectins: structure, biosynthesis, and oligogalacturonide-related signalling. Phytochemistry 57:929–967

    Article  PubMed  CAS  Google Scholar 

  • Round AN, Rigby NM, MacDougall AJ, Morris VJ (2010) A new view of pectin structure revealed by acid hydrolysis and atomic force microscopy. Carbohydr Polym 345:487–497

    CAS  Google Scholar 

  • Seifert GJ, Roberts K (2007) The biology of arabinogalactan proteins. Annu Rev Plant Biol 58:137–161

    Article  PubMed  CAS  Google Scholar 

  • Showalter AM (2001) Arabinogalactan-proteins: structure, expression and function. Cell Mol Life Sci 58:1399–1417

    Article  PubMed  CAS  Google Scholar 

  • Smallwood M, Beven A, Donovan N, Neill SJ, Peart J, Roberts K, Knox JP (1994) Localization of cell wall proteins in relation to the developmental anatomy of the carrot root apex. Plant J 5:237–246

    Article  CAS  Google Scholar 

  • Smallwood M, Martin H, Knox JP (1995) An epitope of rice threonine- and hydroxyproline-rich glycoprotein is common to cell wall and hydrophobic plasma membrane glycoproteins. Planta 196:510–522

    Article  PubMed  CAS  Google Scholar 

  • Tomoda M, Hirabayashi K, Shimizu N, Gonda R, Ohara N, Takada K (1993) Characterization of two novel polysaccharides having immunological activities from the root of Panax ginseng. Biol Pharm Bull 16:1087–1090

    Article  PubMed  CAS  Google Scholar 

  • Tomoda M, Hirabayashi K, Shimizu N, Gonda R, Ohara N (1994) The core structure of ginseng PA, a phagocytosis-activation polysaccharide from the root of Panax ginseng. Biol Pharm Bull 17:1287–1291

    Article  PubMed  CAS  Google Scholar 

  • Vassilyev AE (2000) Quantitative ultrastructural data of secretory duct epithelial cells in Rhus toxicodendron. Int J Plant Sci 16:615–630

    Article  Google Scholar 

  • Verhertbruggen Y, Marcus SE, Haeger A, Ordaz-Ortiz JJ, Knox JP (2009a) An extended set of monoclonal antibodies to pectic homogalacturonan. Carbohydr Res 344:1858–1862

    Article  PubMed  CAS  Google Scholar 

  • Verhertbruggen Y, Marcus SE, Haeger A, Verhoef R, Schols HA, McCleary BV, Mckee L, Gilbert HJ, Knox JP (2009b) Developmental complexity of arabinan polysaccharides and their processing in plant cell walls. Plant J 59:413–425

    Article  PubMed  CAS  Google Scholar 

  • Vogler BK, Pittler MH, Ernst E (1999) The efficacy of ginseng. A systematic review of randomised clinical trials. Eur J Clin Pharmacol 55:567–575

    Article  PubMed  CAS  Google Scholar 

  • Wang T (2001) Ginseng morphogenesis and anatomy. In: Wang T (ed) China Ginseng. Liaoning Science And Technology Publishing House, Shenyang, pp 132–167

    Google Scholar 

  • Wang J, Li S, Fan Y, Chen Y, Liu D, Cheng H, Gao X, Zhou Y (2010) Anti-fatigue activity of the water-soluble polysaccharides isolated from Panax ginseng C. A. Meyer. J Ethnopharmacol 130:421–423

    Article  PubMed  CAS  Google Scholar 

  • Willats WGT, Marcus SE, Knox JP (1998) Generation of a monoclonal antibody specific to (1 → 5)-α-l-arabinan. Carbohydr Res 308:149–152

    Article  PubMed  CAS  Google Scholar 

  • Willats WGT, McCartney L, Steele-King CG, Marcus SE, Mortm A, Huisman M, van Alebeek GJ, Schols HA, Voragen AGJ, Le Goff A, Bonnin E, Thibault J-F, Knox JP (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681

    Article  PubMed  CAS  Google Scholar 

  • Yates EA, Valdor J-F, Haslam SM, Morris HR, Dell A, Mackie W, Knox JP (1996) Characterization of carbohydrate structural features recognized by anti-arabinogalactan-protein monoclonal antibodies. Glycobiology 6:131–139

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Zhang X, Li S, Liu X, Sun L, Liu H, Iteku J, Zhou Y, Tai G (2009) Rhamnogalacturonan I domains from ginseng pectin. Carbohydr Polym 79:811–817

    Article  Google Scholar 

  • Zhang X, Yu L, Bi H, Li X, Ni W, Han H, Li N, Wang B, Zhou Y, Tai G (2009) Total fractionation and characterization of the water-soluble polysaccharides isolated from Panax ginseng C. A. Meyer. Carbohydr Polym 77:544–552

    Article  CAS  Google Scholar 

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Acknowledgments

We are grateful to the Chinese Scholarship Council for the award of a travel scholarship to Li Yu. We thank Sue Marcus for technical assistance.

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Authors and Affiliations

  1. School of Life Sciences, Northeast Normal University, Changchun, 130024, People’s Republic of China

    Li Yu & Yifa Zhou

  2. Faculty of Biological Sciences, Centre for Plant Sciences, University of Leeds, Leeds, LS2 9JT, UK

    Li Yu & J. Paul Knox

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  1. Li Yu
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  2. Yifa Zhou
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  3. J. Paul Knox
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Correspondence to J. Paul Knox.

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Yu, L., Zhou, Y. & Knox, J.P. Ginseng root water-extracted pectic polysaccharides originate from secretory cavities. Planta 234, 487–499 (2011). https://doi.org/10.1007/s00425-011-1417-9

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