Skip to main content
SpringerLink
Log in

Changes in the abundance of cell wall apiogalacturonan and xylogalacturonan and conservation of rhamnogalacturonan II structure during the diversification of the Lemnoideae

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

The diversification of the Lemnoideae was accompanied by a reduction in the abundance of cell wall apiogalacturonan and an increase in xylogalacturonan whereas rhamnogalacturonan II structure and cross-linking are conserved.

The subfamily Lemnoideae is comprised of five genera and 38 species of small, fast-growing aquatic monocots. Lemna minor and Spirodela polyrhiza belong to this subfamily and have primary cell walls that contain large amounts of apiogalacturonan and thus are distinct from the primary walls of most other flowering plants. However, the pectins in the cell walls of other members of the Lemnoideae have not been investigated. Here, we show that apiogalacturonan decreased substantially as the Lemnoideae diversified since Wolffiella and Wolffia walls contain between 63 and 88% less apiose than Spirodela, Landoltia, and Lemna walls. In Wolffia, the most derived genus, xylogalacturonan is far more abundant than apiogalacturonan, whereas in Wolffiella pectic polysaccharides have a high arabinose content, which may arise from arabinan sidechains of RG I. The apiose-containing pectin rhamnogalacturonan II (RG-II) exists in Lemnoideae walls as a borate cross-linked dimer and has a glycosyl sequence similar to RG-II from terrestrial plants. Nevertheless, species-dependent variations in the extent of methyl-etherification of RG-II sidechain A and arabinosylation of sidechain B are discernible. Immunocytochemical studies revealed that pectin methyl-esterification is higher in developing daughter frond walls than in mother frond walls, indicating that methyl-esterification is associated with expanding cells. Our data support the notion that a functional cell wall requires conservation of RG-II structure and cross-linking but can accommodate structural changes in other pectins. The Lemnoideae provide a model system to study the mechanisms by which wall structure and composition has changed in closely related plants with similar growth habits.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12

Similar content being viewed by others

Abbreviations

AIR:

Alcohol insoluble residue

Apif :

Apiofuranosyl

ApiGalA:

Apiogalacturonan

EPG:

Endopolygalacturonase

HPAEC-PAD:

High-performance anion-exchange chromatography with pulsed amperometric detection

mAb:

Monoclonal antibody

RG-I:

Rhamnogalacturonan I

RG-II:

Rhamnogalacturonan II

SEC:

Size-exclusion chromatography

XylGalA:

Xylogalacturonan

References

  • Albersheim P, Darvill A, Roberts K, Sederoff R, Staehelin A (2010) Plant cell walls. From chemistry to biology. Garland Science, New York

    Google Scholar 

  • Anderson CT (2016) We be jammin’: an update on pectin biosynthesis, trafficking and dynamics. J Exp Bot 67:495–502

    Article  CAS  PubMed  Google Scholar 

  • Atmodjo MA, Hao Z, Mohnen D (2013) Evolving views of pectin biosynthesis. Annu Rev Plant Biol 64:747–779

    Article  CAS  PubMed  Google Scholar 

  • Avci U, Pattathil S, Hahn MG (2012) Immunological approaches to plant cell wall and biomass characterization: Immunolocalization of glycan epitopes. In: Himmell ME (ed) Biomass conversion: methods and protocols, vol 908. Humana Press, New York, pp 73–82

    Chapter  Google Scholar 

  • Bar-Peled M, O’Neill MA (2011) Plant nucleotide sugar formation, interconversion, and salvage by sugar recycling. Annu Rev Plant Biol 62:127–155

    Article  CAS  PubMed  Google Scholar 

  • Bar-Peled M, Urbanowicz BR, O’Neill MA (2012) The synthesis and origin of the pectic polysaccharide rhamnogalacturonan II—insights from nucleotide sugar formation and diversity. Front Plant Sci 3:92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell D, Isherwood F, Hardwick NE (1954) D(+)-Apiose from the monocotyledon, Posidonia australis. J Chem Soc (resumed), 3702–3706

  • Blumenkrantz N, Asboe-Hansen G (1973) New method for quantitative determination of uronic acids. Anal Biochem 54:484–489

    Article  CAS  PubMed  Google Scholar 

  • Bouveng H (1965) Polysaccharides in pollen II. The xylogalacturonan from mountain pine (Pinus mugo Turra) pollen. Acta Chem Scand 19:953–963

    Article  CAS  PubMed  Google Scholar 

  • Cabrera LI, Salazar GA, Chase MW, Mayo SJ, Bogner J, Dávilla P (2008) Phylogenetic relationships of aroids and duckweeds (Araceae) inferred from coding and noncoding plastid DNA. Am J Bot 95:1153–1165

    Article  CAS  PubMed  Google Scholar 

  • Carpita N, Gibeaut D (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 3:1–30

    Article  CAS  PubMed  Google Scholar 

  • Cheng L, Kindel PK (1997) Detection and homogeneity of cell wall pectic polysaccharides of Lemna minor. Carbohydr Res 301:205–212

    Article  CAS  Google Scholar 

  • Chormova D, Messenger DJ, Fry SC (2014) Boron bridging of rhamnogalacturonan-II, monitored by gel electrophoresis, occurs during polysaccharide synthesis and secretion but not post-secretion. Plant J 77:534–546

    Article  CAS  PubMed  Google Scholar 

  • Dick-Perez M, Wang T, Salazar A, Zabotina O, Hong M (2012) Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magn Reson Chem 50:539–550

    Article  CAS  PubMed  Google Scholar 

  • Duff R (1965) The occurrence of apiose in Lemna (duckweed) and other angiosperms. Biochem J 94:768–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glandon R, McNabb C (1978) The uptake of boron by Lemna minor. Aquat Bot 4:53–64

    Article  CAS  Google Scholar 

  • Gloaguen V, Brudieux V, Closs B, Barbat A, Krausz P, Sainte-Catherine O, Kraemer M, Maes E, Guerardel Y (2010) Structural characterization and cytotoxic properties of an apiose-rich pectic polysaccharide obtained from the cell wall of the marine phanerogam Zostera marina. J Nat Prod 73:1087–1092

    Article  CAS  PubMed  Google Scholar 

  • Glushka JN, Terrell M, York WS, O’Neill MA, Gucwa A, Darvill AG, Albersheim P, Prestegard JH (2003) Primary structure of the 2-O-methyl-α-fucose-containing side chain of the pectic polysaccharide, rhamnogalacturonan II. Carbohydr Res 338:341–352

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Guyett P, Glushka J, Gu X, Bar-Peled M (2009) Real-time NMR monitoring of intermediates and labile products of the bifunctional enzyme UDP-apiose/UDP-xylose synthase. Carbohydr Res 344:1072–1078

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hart DA, Kindel PK (1970a) Isolation and partial characterization of apiogalacturonans from the cell wall of Lemna minor. Biochem J 116:569–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hart D, Kindel PK (1970b) A novel reaction involved in the degradation of apiogalacturonans from Lemna minor and the isolation of apibiose as a product. Biochemistry 9:2190–2196

    Article  CAS  PubMed  Google Scholar 

  • Hsieh YSY, Harris PJ (2009) Xyloglucans of monocotyledons have diverse structures. Mol Plant 2:943–965

    Article  CAS  PubMed  Google Scholar 

  • Huisman M, Fransen C, Kamerling J, Vliegenthart J, Schols HA, Voragen A (2001) The CDTA-soluble pectic substances from soybean meal are composed of rhamnogalacturonan and xylogalacturonan but not homogalacturonan. Biopolymers 58:279–294

    Article  CAS  PubMed  Google Scholar 

  • Jacobs A, Dahlman O (2001) Enhancement of the quality of MALDI mass spectra of highly acidic oligosaccharides by using a Nafion-coated probe. Anal Chem 73:405–410

    Article  CAS  PubMed  Google Scholar 

  • Jensen JK, Sørensen SO, Harholt J, Geshi N, Sakuragi Y, Møller I, Zandleven J, Bernal AJ, Jensen NB, Sørensen C, Pauly M, Beldman G, Willats W, Scheller HV (2008) Identification of a xylogalacturonan xylosyltransferase involved in pectin biosynthesis in Arabidopsis. Plant Cell 20:1289–1302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones L, Seymour G, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kikuchi A, Edashige Y, Ishii T, Satoh S (1996) A xylogalacturonan whose level is dependent on the size of cell clusters is present in the pectin from cultured carrot cells. Planta 200:369–372

    Article  CAS  Google Scholar 

  • Kim I (2013) Cellular features of the fronds and turions in Spirodela polyrhiza. Korean Soc Microscop 43:140–145

    Google Scholar 

  • Kis P, Potocká E, Mastihuba V, Mastihubová M (2016) Efficient chemoenzymatic synthesis of 4-nitrophenyl β-d-apiofuranoside and its use in screening of β-d-apiofuranosidases. Carbohydr Res 430:48–53

    Article  CAS  PubMed  Google Scholar 

  • Koller A, O’Neill M, Darvill A, Albersheim P (1991) A comparison of the polysaccharides extracted from dried and non-dried walls of suspension-cultured sycamore cells. Phytochemistry 30:3903–3908

    Article  CAS  Google Scholar 

  • Konishi T, Takeda T, Miyazaki Y, Ohnishi-Kameyama M, Hayashi T, O’Neill MA, Ishii T (2007) A plant mutase that interconverts UDP-arabinofuranose and UDP-arabinopyranose. Glycobiology 17:345–352

    Article  CAS  PubMed  Google Scholar 

  • Landolt E (1986) Biosystematic investigation in the family of duckweeds (Lemnaceae), vol. 2: the family of “Lemnaceae”: a monographic study. Veröffentlichungen des Geobotanischen Institutes der ETH, Zürich, Switzerland, No 71

  • Lemon GD, Posluszny U (2000) Comparative shoot development and evolution in the Lemnaceae. Int J Plant Sci 161:733–748

    Article  Google Scholar 

  • Levesque-Tremblay G, Pelloux J, Braybrook SA, Müller K (2015) Tuning of pectin methylesterification: consequences for cell wall biomechanics and development. Planta 242:791–811

    Article  CAS  PubMed  Google Scholar 

  • Longland JM, Fry SC, Trewavas AJ (1989) Developmental control of apiogalacturonan biosynthesis and UDP-apiose production in a duckweed. Plant Physiol 90:972–978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matoh T, Kawaguchi S, Kobayashi M (1996) Ubiquity of a borate-rhamnogalacturonan II complex in the cell walls of higher plants. Plant Cell Physiol 37:636–644

    Article  CAS  Google Scholar 

  • Matsunaga T, Ishii T, Matsumoto S, Higuchi M, Darvill A, Albersheim P, O’Neill MA (2004) Occurrence of the primary cell wall polysaccharide rhamnogalacturonan II in pteridophytes, lycophytes, and bryophytes. Implications for the evolution of vascular plants. Plant Physiol 134:339–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mølhøj M, Verma R, Reiter WD (2003) The biosynthesis of the branched-chain sugar d-apiose in plants: functional cloning and characterization of a UDP α-d-apiose/UDP-d-xylose synthase from Arabidopsis. Plant J 35:693–703

    Article  PubMed  Google Scholar 

  • Mort A, Zheng Y, Qiu F, Nimtz M, Bell-Eunice G (2008) Structure of xylogalacturonan fragments from watermelon cell-wall pectin. Endopolygalacturonase can accommodate a xylosyl residue on the galacturonic acid just following the hydrolysis site. Carbohydr Res 343:1212–1221

    Article  CAS  PubMed  Google Scholar 

  • Muszyński A, O’Neill MA, Ramasamy E, Pattathil S, Avci U, Peña MJ, Libault M, Hossain MS, Brechenmacher L, York WS, Barbosa R, Hahn M, Stacey G, Carlson R (2015) Xyloglucan, galactomannan, glucuronoxylan, and rhamnogalacturonan I do not have identical structures in soybean root and root hair cell walls. Planta 242:1123–1138

    Article  PubMed  Google Scholar 

  • Nauheimer L, Metzler D, Renner S (2012) Global history of the ancient monocot family Araceae inferred with models accounting for past continental positions and previous ranges based on fossils. New Phytol 195:938–950

    Article  PubMed  Google Scholar 

  • Ndeh D, Rogowski A, Cartmell A, Luis A, Baslé A, Gray J, Venditto I, Briggs J, Zhang X, Labourel A, Terrapon N, Buffetto F, Nepogodiev S, Xiao Y, Field R, Zhu Y, O’Neill M, Urbanowicz B, York W, Davies G, Abbott W, Ralet M-C, Martens E, Henrissat B, Gilbert H (2017) Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature 544:65–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Neill MA, Warrenfeltz D, Kates K, Pellerin P, Doco T, Darvill AG, Albersheim P (1996) Rhamnogalacturonan-II, a pectic polysaccharide in the walls of growing plant cells, forms a dimer that is covalently cross-linked by a borate ester. J Biol Chem 271:22923–22931

    Article  PubMed  Google Scholar 

  • O’Neill MA, Eberhard S, Albersheim P, Darvill AG (2001) Requirement of borate cross-linking of cell wall rhamnogalacturonan II for Arabidopsis growth. Science 294:846–849

    Article  PubMed  Google Scholar 

  • O’Neill MA, Ishii T, Albersheim P, Darvill AG (2004) Rhamnogalacturonan II: structure and function of a borate cross-linked cell wall pectic polysaccharide. Annu Rev Plant Biol 55:109–139

    Article  PubMed  Google Scholar 

  • Ovodov YS, Ovodova R, Bondarenko O, Krasikova I (1971) The pectic substances of Zosteraceae: part IV. Pectinase digestion of zosterine. Carbohydr Res 18:311–318

    Article  CAS  Google Scholar 

  • Ovodova R, Golovchenko V, Shashkov A, Popov S, Ovodov YS (2000) Structural studies and physiological activity of lemnan, a pectin from Lemna minor L. Russ J Bioorg Chem 26:669–676

    Article  CAS  Google Scholar 

  • Pabst M, Fischl RM, Brecker L, Morelle W, Fauland A, Köfeler H, Altmann F, Léonard R (2013) Rhamnogalacturonan II structure shows variation in the side chains monosaccharide composition and methylation status within and across different plant species. Plant J 76:61–72

    CAS  PubMed  Google Scholar 

  • Parre E, Geitmann A (2005) Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220:582–592

    Article  CAS  PubMed  Google Scholar 

  • Pattathil S, Avci U, Baldwin D, Swennes A, McGill J, Popper Z, Bootten T, Albert A, Davis R, Chennareddy C, Dong R, O’Shea B, Rossi R, Leoff C, Freshour G, Narra R, O’Neil M, York W, Hahn M (2010) A comprehensive toolkit of plant cell wall glycan-directed monoclonal antibodies. Plant Physiol 153:514–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peaucelle A, Braybrook SA, Le Guillou L, Bron E, Kuhlemeier C, Höfte H (2011) Pectin-induced changes in cell wall mechanics underlie organ initiation in Arabidopsis. Curr Biol 21:1720–1726

    Article  CAS  PubMed  Google Scholar 

  • Popper ZA, Michel G, Hervé C, Domozych DS, Willats WGT, Tuohy MG, Kloareg B, Stengel DB (2011) Evolution and diversity of plant cell walls: from algae to flowering plants. Annu Rev Plant Biol 62:567–590

    Article  CAS  PubMed  Google Scholar 

  • Reuhs BL, Glenn J, Stephens SB, Kim JS, Christie DB, Glushka JG, Zablackis E, Albersheim P, Darvill AG, O’Neill MA (2004) l-Galactose replaces l-fucose in the pectic polysaccharide rhamnogalacturonan II synthesized by the l-fucose-deficient mur1 Arabidopsis mutant. Planta 219:147–157

    Article  CAS  PubMed  Google Scholar 

  • Schols H, Bakx E, Schipper D, Voragen A (1995) A xylogalacturonan subunit present in the modified hairy regions of apple pectin. Carbohydr Res 279:265–279

    Article  CAS  Google Scholar 

  • Selvendran RR, March JF, Ring SG (1979) Determination of aldoses and uronic acid content of vegetable fiber. Anal Biochem 96:282–292

    Article  CAS  PubMed  Google Scholar 

  • Smith JA, Yang Y, Levy S, Adelusi OO, Hahn MG, O’Neill MA, Bar-Peled M (2016) Functional characterization of UDP-apiose synthases from bryophytes and green algae provides insight into the appearance of apiose-containing glycans during plant evolution. J Biol Chem 291:21434–21447

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sørensen I, Domozych D, Willats WGT (2010) How have plant cell walls evolved? Plant Physiol 153:366–372

    Article  PubMed  PubMed Central  Google Scholar 

  • Tippery N, Les D, Crawford D (2015) Evaluation of phylogenetic relationships in Lemnaceae using nuclear ribosomal data. Plant Biol 17:50–58

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Vidal S, Doco T, Williams P, Pellerin P, York WS, O’Neill MA, Glushka J, Darvill AG, Albersheim P (2000) Structural characterization of the pectic polysaccharide rhamnogalacturonan II: evidence for the backbone location of the aceric acid-containing oligoglycosyl side chain. Carbohydr Res 326:277–294

    Article  CAS  PubMed  Google Scholar 

  • Wang T, Park Y, Cosgrove D, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis thaliana primary cell walls: evidence from solid-state NMR. Plant Physiol 168:871–884

    Article  PubMed  PubMed Central  Google Scholar 

  • Webster J, Stone BA (1994) Isolation, structure and monosaccharide composition of the walls of vegetative parts of Heterozostera tasmanica (Martens ex Aschers.) den Hartog. Aquat Bot 47:39–52

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Willats WT, McCartney L, Mackie W, Knox JP (2001) Pectin: cell biology and prospects for functional analysis. In: Carpita NC, Campbell M, Tierney M (eds) Plant cell walls. Springer, The Netherlands, pp 9–27

    Chapter  Google Scholar 

  • Willats W, McCartney L, Steele-King C, Marcus S, Mort A, Huisman M, van Alebeek G-J, Schols H, Voragen A, Le Goff A, Bonnin E, Thibault J-F, Knox J (2004) A xylogalacturonan epitope is specifically associated with plant cell detachment. Planta 218:673–681

    Article  CAS  PubMed  Google Scholar 

  • York WS, Darvill AG, McNeil M, Albersheim P (1985) 3-Deoxy-D-manno-2-octulosonic acid (KDO) is a component of rhamnogalacturonan II, a pectic polysaccharide in the primary cell walls of plants. Carbohydr Res 138:109–126

    Article  CAS  Google Scholar 

  • York WS, Darvill AG, McNeil M, Stevenson TT, Albersheim P (1986) Isolation and characterization of plant cell walls and cell wall components. Method Enzymol 118:3–40

    Article  CAS  Google Scholar 

  • Zablackis E, Huang J, Muller B, Darvill AG, Albersheim P (1995) Characterization of the cell-wall polysaccharides of Arabidopsis thaliana leaves. Plant Physiol 107:1129–1138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandleven J, Beldman G, Bosveld M, Benen J, Voragen A (2005) Mode of action of xylogalacturonan hydrolase towards xylogalacturonan and xylogalacturonan oligosaccharides. Biochem J 387:719–725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zandleven J, Beldman G, Bosveld M, Schols H, Voragen A (2006) Enzymatic degradation studies of xylogalacturonans from apple and potato, using xylogalacturonan hydrolase. Carbohydr Polym 65:495–503

    Article  CAS  Google Scholar 

  • Zandleven J, Sørensen S, Harholt J, Beldman G, Schols H, Scheller H, Voragen A (2007) Xylogalacturonan exists in cell walls from various tissues of Arabidopsis thaliana. Phytochemistry 68:1219–1226

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences of the United States Department of Energy through Grants DE-FG02-12ER16324 and DE-FG02-12ER16326 (to M.A.O and M.J.P.) for funding the structural studies of Lemnoideae cell walls and DE-FG02-96ER20220 for analytical instrumentation support. The generation and use of plant cell wall glycan-directed antibodies were supported by National Science Foundation Plant Genome Grant ISO-0923992.

Author information

Author notes

  1. Utku Avci

    Present address: Faculty of Engineering, Bioengineering Department, Recep Tayyip Erdogan University, 53100, Rize, Turkey

Authors and Affiliations

  1. Complex Carbohydrate Research Center, University of Georgia, Athens, GA, 30602, USA

    Utku Avci, Maria J. Peña & Malcolm A. O’Neill

Authors
  1. Utku Avci
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Maria J. Peña
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Malcolm A. O’Neill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Malcolm A. O’Neill.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Avci, U., Peña, M.J. & O’Neill, M.A. Changes in the abundance of cell wall apiogalacturonan and xylogalacturonan and conservation of rhamnogalacturonan II structure during the diversification of the Lemnoideae. Planta 247, 953–971 (2018). https://doi.org/10.1007/s00425-017-2837-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-017-2837-y

Keywords

Search

Navigation