First published online June 12, 2003; 10.1104/pp.103.021766
Plant Physiology 132:1362-1369 (2003)
© 2003 American Society of Plant Biologists
BIOCHEMICAL PROCESSES AND MACROMOLECULAR STRUCTURES
Glycosylation Motifs That Direct Arabinogalactan Addition to Arabinogalactan-Proteins1
Li Tan,
Joseph F. Leykam and
Marcia J. Kieliszewski*
Department of Chemistry and Biochemistry, Ohio University, Athens, Ohio
45701 (L.T., M.J.K.); and Biochemistry Department, Michigan State University,
East Lansing, Michigan 48824 (J.F.L.)
Hydroxyproline (Hyp)-rich glycoproteins (HRGPs) participate in all aspects
of plant growth and development. HRGPs are generally highly
O-glycosylated through the Hyp residues, which means carbohydrates
help define the interactive molecular surface and, hence, HRGP function. The
Hyp contiguity hypothesis predicts that contiguous Hyp residues are sites of
HRGP arabinosylation, whereas clustered noncontiguous Hyp residues are sites
of galactosylation, giving rise to the arabinogalactan heteropolysaccharides
that characterize the arabinogalactan-proteins. Early tests of the hypothesis
using synthetic genes encoding only clustered noncontiguous Hyp in the
sequence (serine [Ser]-Hyp-Ser-Hyp)n or contiguous Hyp in the
series (Ser-Hyp-Hyp)n and (Ser-Hyp-Hyp-Hyp-Hyp)n
confirmed that arabinogalactan polysaccharide was added only to noncontiguous
Hyp, whereas arabinosylation occurred on contiguous Hyp. Here, we extended our
tests of the codes that direct arabinogalactan polysaccharide addition to Hyp
by building genes encoding the repetitive sequences (alanine [Ala]-proline
[Pro]-Ala-Pro)n, (threonine [Thr]-Pro-Thr-Pro)n, and
(valine [Val]-Pro-Val-Pro)n, and expressing them in tobacco
(Nicotiana tabacum) Bright-Yellow 2 cells as fusion proteins with
green fluorescent protein. All of the Pro residues in the
(Ala-Pro-Ala-Pro)n fusion protein were hydroxylated and consistent
with the hypothesis that every Hyp residue was glycosylated with
arabinogalactan polysaccharide. In contrast, 20% to 30% of Pro residues
remained non-hydroxylated in the (Thr-Pro-Thr-Pro)n, and
(Val-Pro-Val-Pro)n fusion proteins. Furthermore, although 50% to
60% of the Hyp residues were glycosylated with arabinogalactan polysaccharide,
some remained non-glycosylated or were arabinosylated. These results suggest
that the amino acid side chains of flanking residues influence the extent of
Pro hydroxylation and Hyp glycosylation and may explain why isolated
noncontiguous Hyp in extensins do not acquire an arabinogalactan
polysaccharide but are arabinosylated or remain non-glycosylated.
Article, publication date, and citation information can be found at
www.plantphysiol.org/cgi/doi/10.1104/pp.103.021766.
1 This work was supported by the National Science Foundation (grant no.
MCB–9874744), by Ohio University (Molecular and Cellular Biology Program
grants), and in part by the National Institutes of Health (grant no.
2–P41–RR05351–06 awarded to the Complex Carbohydrate
Research Center).
*
Corresponding author; e-mail
kielisze{at}helios.phy.ohiou.edu;
fax 740–597–1772.
Received March 12, 2003;
returned for revision April 2, 2003;
accepted April 2, 2003.
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