Cited by 55Polysaccharides and Plant Cell WallsPlant Surface Properties and TreatmentsGlycosylation and Glycoproteins Research

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Polymerization of the backbone of the pectic polysaccharide rhamnogalacturonan I

Open access

Published version of a preprint

Abstract

Rhamnogalacturonan I (RG-I) is a major plant cell wall pectic polysaccharide defined by its repeating disaccharide backbone structure of [4)-α-D-GalA-(1,2)-α-L-Rha-(1,]. A family of RG-I:Rhamnosyltransferases (RRT) has previously been identified, but synthesis of the RG-I backbone has not been demonstrated in vitro because the identity of Rhamnogalacturonan I:Galaturonosyltransferase (RG-I:GalAT) was unknown. Here a putative glycosyltransferase, At1g28240/MUCI70, is shown to be an RG-I:GalAT. The name RGGAT1 is proposed to reflect the catalytic activity of this enzyme. When incubated together with the rhamnosyltransferase RRT4, the combined activities of RGGAT1 and RRT4 result in elongation of RG-I acceptors in vitro into a polymeric product. RGGAT1 is a member of a new GT family categorized as GT116, which does not group into existing GT-A clades and is phylogenetically distinct from the GALACTURONOSYLTRANSFERASE (GAUT) family of GalA transferases that synthesize the backbone of the pectin homogalacturonan. RGGAT1 has a predicted GT-A fold structure but employs a metal-independent catalytic mechanism that is rare among glycosyltransferases with this fold type. The identification of RGGAT1 and the 8-member Arabidopsis GT116 family provides a new avenue for studying the mechanism of RG-I synthesis and the function of RG-I in plants.

Overview

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1038/s41477-022-01270-3

Cites

1 of 1 references verified0 citation errors · 0 not checkable

Statistics

Verification

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Citations

Cites

Flagged first, then by citations

Research works printed but not linked: 63

  1. Atmodjo, M. A., Hao, Z. & Mohnen, D. Evolving views of pectin biosynthesis. Annu. Rev. Plant Biol. 64, 747–779 (2013). · DOI · Paper page
  2. Biswal, A. K. et al. Sugar release and growth of biofuel crops are improved by downregulation of pectin biosynthesis. Nat. Biotechnol. 36, 249–257 (2018). · DOI
  3. Wu, D. et al. Dietary pectic substances enhance gut health by its polycomponent: a review. Compr. Rev. Food Sci. Food Saf. 20, 2015–2039 (2021). · DOI
  4. Bonnin, E., Garnier, C. & Ralet, M. C. Pectin-modifying enzymes and pectin-derived materials: applications and impacts. Appl. Microbiol. Biotechnol. 98, 519–532 (2014). · DOI
  5. Atmodjo, M. A. et al. Galacturonosyltransferase (GAUT)1 and GAUT7 are the core of a plant cell wall pectin biosynthetic homogalacturonan:galacturonosyltransferase complex. Proc. Natl Acad. Sci. USA 108, 20225–20230 (2011). · DOI
  6. Amos, R. A. et al. A two-phase model for the non-processive biosynthesis of homogalacturonan polysaccharides by the GAUT1:GAUT7 complex. J. Biol. Chem. 293, 19047–19063 (2018). · DOI
  7. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, D490–D495 (2014). · DOI
  8. Engle, K. A. et al. Multiple Arabidopsis galacturonosyltransferases synthesize polymeric homogalacturonan by oligosaccharide acceptor-dependent or de novo synthesis. Plant J. https://doi.org/10.1111/tpj.15640 (2021). · DOI
  9. Kaczmarska, A., Pieczywek, P. M., Cybulska, J. & Zdunek, A. Structure and functionality of rhamnogalacturonan I in the cell wall and in solution: a review. Carbohydr. Polym. 278, 118909 (2022). · DOI
  10. Pena, M. J. & Carpita, N. C. Loss of highly branched arabinans and debranching of rhamnogalacturonan I accompany loss of firm texture and cell separation during prolonged storage of apple. Plant Physiol. 135, 1305–1313 (2004). · DOI
  11. Molina-Hidalgo, F. J. et al. The strawberry (Fragaria×ananassa) fruit-specific rhamnogalacturonate lyase 1 (FaRGLyase1) gene encodes an enzyme involved in the degradation of cell-wall middle lamellae. J. Exp. Bot. 64, 1471–1483 (2013). · DOI
  12. Yapo, B. M., Lerouge, P., Thibault, J.-F. & Ralet, M.-C. Pectins from citrus peel cell walls contain homogalacturonans homogenous with respect to molar mass, rhamnogalacturonan I and rhamnogalacturonan II. Carbohydr. Polym. 69, 426–435 (2007). · DOI
  13. Arsovski, A. A., Haughn, G. W. & Western, T. L. Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signal. Behav. 5, 796–801 (2010). · DOI
  14. Haughn, G. W. & Western, T. L. Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front. Plant Sci. 3, 64 (2012). · DOI
  15. Macquet, A., Ralet, M. C., Kronenberger, J., Marion-Poll, A. & North, H. M. In situ, chemical and macromolecular study of the composition of Arabidopsis thaliana seed coat mucilage. Plant Cell Physiol. 48, 984–999 (2007). · DOI
  16. Takenaka, Y. et al. Pectin RG-I rhamnosyltransferases represent a novel plant-specific glycosyltransferase family. Nat. Plants 4, 669–676 (2018). · DOI
  17. Wachananawat, B. et al. Diversity of pectin rhamnogalacturonan I rhamnosyltransferases in glycosyltransferase family 106. Front. Plant Sci. 11, 997 (2020). · DOI
  18. Liwanag, A. J. et al. Pectin biosynthesis: GALS1 in Arabidopsis thaliana is a β-1,4-galactan β-1,4-galactosyltransferase. Plant Cell 24, 5024–5036 (2012). · DOI
  19. Ebert, B. et al. The three members of the Arabidopsis glycosyltransferase family 92 are functional β-1,4-galactan synthases. Plant Cell Physiol. 59, 2624–2636 (2018). · DOI
  20. Voiniciuc, C. et al. Identification of key enzymes for pectin synthesis in seed mucilage. Plant Physiol. 178, 1045–1064 (2018). · DOI
  21. Mistry, J. et al. Pfam: the protein families database in 2021. Nucleic Acids Res. 49, D412–D419 (2021). · DOI · Paper page
  22. Nikolovski, N. et al. Putative glycosyltransferases and other plant Golgi apparatus proteins are revealed by LOPIT proteomics. Plant Physiol. 160, 1037–1051 (2012). · DOI
  23. Sterling, J. D. et al. Functional identification of an Arabidopsis pectin biosynthetic homogalacturonan galacturonosyltransferase. Proc. Natl Acad. Sci. USA 103, 5236–5241 (2006). · DOI
  24. Fabrissin, I. et al. Natural variation reveals a key role for rhamnogalacturonan I in seed outer mucilage and underlying genes. Plant Physiol. 181, 1498–1518 (2019). · DOI
  25. Moremen, K. W. et al. Expression system for structural and functional studies of human glycosylation enzymes. Nat. Chem. Biol. 14, 156–162 (2018). · DOI
  26. Urbanowicz, B. R., Pena, M. J., Moniz, H. A., Moremen, K. W. & York, W. S. Two Arabidopsis proteins synthesize acetylated xylan in vitro. Plant J. 80, 197–206 (2014). · DOI
  27. Urbanowicz, B. R. et al. Structural, mutagenic and in silico studies of xyloglucan fucosylation in Arabidopsis thaliana suggest a water-mediated mechanism. Plant J. 91, 931–949 (2017). · DOI
  28. Soto, M. J. et al. AtFUT4 and AtFUT6 are arabinofuranose-specific fucosyltransferases. Front. Plant Sci. 12, 589518 (2021). · DOI
  29. Kofod, L. V. et al. Cloning and characterization of two structurally and functionally divergent rhamnogalacturonases from Aspergillus aculeatus. J. Biol. Chem. 269, 29182–29189 (1994). · DOI
  30. Azadi, P., O’Neill, M. A., Bergmann, C., Darvill, A. G. & Albersheim, P. The backbone of the pectic polysaccharide rhamnogalacturonan I is cleaved by an endohydrolase and an endolyase. Glycobiology 5, 783–789 (1995). · DOI
  31. Ishii, T., Ichita, J., Matsue, H., Ono, H. & Maeda, I. Fluorescent labeling of pectic oligosaccharides with 2-aminobenzamide and enzyme assay for pectin. Carbohydr. Res. 337, 1023–1032 (2002). · DOI
  32. Scheller, H. V., Doong, R. L., Ridley, B. L. & Mohnen, D. Pectin biosynthesis: a solubilized α1,4-galacturonosyltransferase from tobacco catalyzes the transfer of galacturonic acid from UDP-galacturonic acid onto the non-reducing end of homogalacturonan. Planta 207, 512–517 (1999). · DOI
  33. Moremen, K. W. & Haltiwanger, R. S. Emerging structural insights into glycosyltransferase-mediated synthesis of glycans. Nat. Chem. Biol. 15, 853–864 (2019). · DOI
  34. Drula, E. et al. The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res. https://doi.org/10.1093/nar/gkab1045 (2021). · DOI · Paper page
  35. Taujale, R. et al. Deep evolutionary analysis reveals the design principles of fold A glycosyltransferases. eLife https://doi.org/10.7554/eLife.54532 (2020). · DOI
  36. Taujale, R. et al. Mapping the glycosyltransferase fold landscape using interpretable deep learning. Nat. Commun. 12, 5656 (2021). · DOI
  37. Kadirvelraj, R. et al. Comparison of human poly-N-acetyl-lactosamine synthase structure with GT-A fold glycosyltransferases supports a modular assembly of catalytic subsites. J. Biol. Chem. 296, 100110 (2021). · DOI
  38. Klepikova, A. V., Kasianov, A. S., Gerasimov, E. S., Logacheva, M. D. & Penin, A. A. A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J. 88, 1058–1070 (2016). · DOI
  39. Round, A. N., Rigby, N. M., MacDougall, A. J. & Morris, V. J. A new view of pectin structure revealed by acid hydrolysis and atomic force microscopy. Carbohydr. Res. 345, 487–497 (2010). · DOI
  40. Zdunek, A., Pieczywek, P. M. & Cybulska, J. The primary, secondary, and structures of higher levels of pectin polysaccharides. Compr. Rev. Food Sci. Food Saf. 20, 1101–1117 (2021). · DOI
  41. Amos, R. A. & Mohnen, D. Critical review of plant cell wall matrix polysaccharide glycosyltransferase activities verified by heterologous protein expression. Front. Plant Sci. 10, 915 (2019). · DOI
  42. Meinke, D. W. Genome-wide identification of EMBRYO-DEFECTIVE (EMB) genes required for growth and development in Arabidopsis. New Phytol. 226, 306–325 (2020). · DOI
  43. Tzafrir, I. et al. Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 135, 1206–1220 (2004). · DOI
  44. Chen, L. Y. et al. The Arabidopsis alkaline ceramidase TOD1 is a key turgor pressure regulator in plant cells. Nat. Commun. 6, 6030 (2015). · DOI
  45. Pham, T. T. et al. Structures of complexes of a metal-independent glycosyltransferase GT6 from Bacteroides ovatus with UDP-N-acetylgalactosamine (UDP-GalNAc) and its hydrolysis products. J. Biol. Chem. 289, 8041–8050 (2014). · DOI
  46. Wu, D. et al. Rethinking the impact of RG-I mainly from fruits and vegetables on dietary health. Crit. Rev. Food Sci. Nutr. 60, 2938–2960 (2020). · DOI
  47. Naqash, F., Masoodi, F. A., Rather, S. A., Wani, S. M. & Gani, A. Emerging concepts in the nutraceutical and functional properties of pectin—a review. Carbohydr. Polym. 168, 227–239 (2017). · DOI
  48. Singh, R. P. et al. Generation of structurally diverse pectin oligosaccharides having prebiotic attributes. Food Hydrocoll. 108, 105988 (2020). · DOI
  49. Cui, J. et al. Dietary fibers from fruits and vegetables and their health benefits via modulation of gut microbiota. Compr. Rev. Food Sci. Food Saf. 18, 1514–1532 (2019). · DOI
  50. Micoli, F. et al. Glycoconjugate vaccines: current approaches towards faster vaccine design. Expert Rev. Vaccines 18, 881–895 (2019). · DOI
  51. Barnes, W. J. et al. Protocols for isolating and characterizing polysaccharides from plant cell walls: a case study using rhamnogalacturonan-II. Biotechnol. Biofuels 14, 142 (2021). · DOI
  52. Klausen, M. S. et al. NetSurfP-2.0: improved prediction of protein structural features by integrated deep learning. Proteins 87, 520–527 (2019). · DOI
  53. Rohl, C. A., Strauss, C. E., Misura, K. M. & Baker, D. Protein structure prediction using Rosetta. Methods Enzymol. 383, 66–93 (2004). · DOI
  54. Osawa, T. et al. Crystal structure of chondroitin polymerase from Escherichia coli K4. Biochem. Biophys. Res. Commun. 378, 10–14 (2009). · DOI
  55. Neuwald, A. F. Rapid detection, classification and accurate alignment of up to a million or more related protein sequences. Bioinformatics 25, 1869–1875 (2009). · DOI
  56. Goodstein, D. M. et al. Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res. 40, D1178–D1186 (2012). · DOI
  57. Tamura, K., Stecher, G. & Kumar, S. MEGA11: molecular evolutionary genetics analysis version 11. Mol. Biol. Evol. 38, 3022–3027 (2021). · DOI
  58. Hall, B. G. Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 30, 1229–1235 (2013). · DOI
  59. Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293–W296 (2021). · DOI
  60. Morris, G. M. et al. AutoDock4 and AutoDockTools4: automated docking with selective receptor flexibility. J. Comput. Chem. 30, 2785–2791 (2009). · DOI
  61. Nivedha, A. K., Thieker, D. F., Makeneni, S., Hu, H. & Woods, R. J. Vina-Carb: improving glycosidic angles during carbohydrate docking. J. Chem. Theory Comput. 12, 892–901 (2016). · DOI
  62. Neelamegham, S. et al. Updates to the symbol nomenclature for glycans guidelines. Glycobiology 29, 620–624 (2019). · DOI
  63. Krissinel, E. & Henrick, K. Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions. Acta Crystallogr. D 60, 2256–2268 (2004). · DOI

Metadata

Authors
Amos, R. A., Atmodjo, M. A., Huang, C., Gao, Z., Venkat, A., Taujale, R., Kannan, N., Moremen, K. W., & Mohnen, D.
Affiliations
University of Georgia (US)
Corresponding author
Mohnen, Debra
Venue
Nature Plants
Published
2022-11-10
Volume
8
Issue
11
Pages
1289-1303
ISSN
  • 2055-026X (ISSN-L)
  • 2055-0278
OpenAlex
W4308695747
Cited by
55
References
1
Citations by year
2026: 19 · 2025: 14 · 2024: 14 · 2023: 8
FWCI
4.96
Type
journal article
Language
en
Open access
Locations
  • Nature Plants (publishedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
Funders
  • U.S. Department of Health & Human Services | National Institutes of Health (R35 GM139656, P41GM103390, R01GM130915)
  • U.S. Department of Energy (DE-SC0015662, AC05-000R22725)
Topics
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Polysaccharides and Plant Cell Walls
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Surface Properties and Treatments
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
Keywords
rhamnogalacturonan I, pectin, rhamnosyltransferase, Arabidopsis thaliana, homogalacturonan
MeSH terms
Pectins, Polysaccharides, Glycosyltransferases, Arabidopsis, Polymerization

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review