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Plant Physiol. 2017 Jun;174(2):904-921. doi: 10.1104/pp.17.00295. Epub 2017 Apr 26.

Insights into the Evolution of Hydroxyproline-Rich Glycoproteins from 1000 Plant Transcriptomes.

Johnson KL1,2,3,4,5,6,7,8,9,10,11,12,13, Cassin AM1,2,3,4,5,6,7,8,9,10,11,12,13, Lonsdale A1,2,3,4,5,6,7,8,9,10,11,12,13, Wong GK1,2,3,4,5,6,7,8,9,10,11,12,13, Soltis DE1,2,3,4,5,6,7,8,9,10,11,12,13, Miles NW1,2,3,4,5,6,7,8,9,10,11,12,13, Melkonian M1,2,3,4,5,6,7,8,9,10,11,12,13, Melkonian B1,2,3,4,5,6,7,8,9,10,11,12,13, Deyholos MK1,2,3,4,5,6,7,8,9,10,11,12,13, Leebens-Mack J1,2,3,4,5,6,7,8,9,10,11,12,13, Rothfels CJ1,2,3,4,5,6,7,8,9,10,11,12,13, Stevenson DW1,2,3,4,5,6,7,8,9,10,11,12,13, Graham SW1,2,3,4,5,6,7,8,9,10,11,12,13, Wang X1,2,3,4,5,6,7,8,9,10,11,12,13, Wu S1,2,3,4,5,6,7,8,9,10,11,12,13, Pires JC1,2,3,4,5,6,7,8,9,10,11,12,13, Edger PP1,2,3,4,5,6,7,8,9,10,11,12,13, Carpenter EJ1,2,3,4,5,6,7,8,9,10,11,12,13, Bacic A1,2,3,4,5,6,7,8,9,10,11,12,13, Doblin MS1,2,3,4,5,6,7,8,9,10,11,12,13, Schultz CJ14,15,16,17,18,19,20,21,22,23,24,25,26.

Author information

1
Australian Research Council Centre of Excellence in Plant Cell Walls, School of BioSciences, University of Melbourne, Parkville, Victoria 3010, Australia (K.L.J., A.M.C., A.L., A.B., M.S.D.).
2
Departments of Biological Sciences and Medicine, University of Alberta, Edmonton, Alberta, Canada, and BGI-Shenzhen, Bei Shan Industrial Zone, Yantian District, Shenzhen, China (G.K.-S.W., E.J.C.).
3
Florida Museum of Natural History, Department of Biology, University of Florida, Gainsville, Florida 32611 (D.E.S., N.W.M.).
4
Botanical Institute, Cologne Biocenter, University of Cologne, D50674 Cologne, Germany (M.M., B.M.).
5
Department of Biology, University of British Columbia, Kelowna, British Columbia V1V 1V7, Canada (M.K.D.).
6
Department of Plant Biology, University of Georgia, Athens, Georgia 3062 (J.L.-M.).
7
University Herbarium and Department of Integrative Biology, University of California, Berkeley, California 94720 (C.J.R.).
8
New York Botanical Garden, Bronx, New York 10458 (D.W.S.).
9
Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada (S.W.G.).
10
Key Laboratory of Genome Science and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China (X.W., S.W.).
11
Division of Biological Sciences and Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211 (J.C.P.).
12
Department of Horticulture, Michigan State University, East Lansing, Michigan 48823 (P.P.E.); and.
13
School of Agriculture, Food, and Wine, University of Adelaide, Waite Research Institute, Glen Osmond, South Australia 5064, Australia (C.J.S.).
14
Australian Research Council Centre of Excellence in Plant Cell Walls, School of BioSciences, University of Melbourne, Parkville, Victoria 3010, Australia (K.L.J., A.M.C., A.L., A.B., M.S.D.); carolyn.schultz@adelaide.edu.au.
15
Departments of Biological Sciences and Medicine, University of Alberta, Edmonton, Alberta, Canada, and BGI-Shenzhen, Bei Shan Industrial Zone, Yantian District, Shenzhen, China (G.K.-S.W., E.J.C.); carolyn.schultz@adelaide.edu.au.
16
Florida Museum of Natural History, Department of Biology, University of Florida, Gainsville, Florida 32611 (D.E.S., N.W.M.); carolyn.schultz@adelaide.edu.au.
17
Botanical Institute, Cologne Biocenter, University of Cologne, D50674 Cologne, Germany (M.M., B.M.); carolyn.schultz@adelaide.edu.au.
18
Department of Biology, University of British Columbia, Kelowna, British Columbia V1V 1V7, Canada (M.K.D.) carolyn.schultz@adelaide.edu.au.
19
Department of Plant Biology, University of Georgia, Athens, Georgia 3062 (J.L.-M.); carolyn.schultz@adelaide.edu.au.
20
University Herbarium and Department of Integrative Biology, University of California, Berkeley, California 94720 (C.J.R.); carolyn.schultz@adelaide.edu.au.
21
New York Botanical Garden, Bronx, New York 10458 (D.W.S.); carolyn.schultz@adelaide.edu.au.
22
Department of Botany, University of British Columbia, Vancouver, British Columbia V6T 1Z4, Canada (S.W.G.); carolyn.schultz@adelaide.edu.au.
23
Key Laboratory of Genome Science and Information, Beijing Institute of Genomics, Chinese Academy of Sciences, Beijing 100101, China (X.W., S.W.); carolyn.schultz@adelaide.edu.au.
24
Division of Biological Sciences and Bond Life Sciences Center, University of Missouri, Columbia, Missouri 65211 (J.C.P.); carolyn.schultz@adelaide.edu.au.
25
Department of Horticulture, Michigan State University, East Lansing, Michigan 48823 (P.P.E.); and carolyn.schultz@adelaide.edu.au.
26
School of Agriculture, Food, and Wine, University of Adelaide, Waite Research Institute, Glen Osmond, South Australia 5064, Australia (C.J.S.) carolyn.schultz@adelaide.edu.au.

Abstract

The carbohydrate-rich cell walls of land plants and algae have been the focus of much interest given the value of cell wall-based products to our current and future economies. Hydroxyproline-rich glycoproteins (HRGPs), a major group of wall glycoproteins, play important roles in plant growth and development, yet little is known about how they have evolved in parallel with the polysaccharide components of walls. We investigate the origins and evolution of the HRGP superfamily, which is commonly divided into three major multigene families: the arabinogalactan proteins (AGPs), extensins (EXTs), and proline-rich proteins. Using motif and amino acid bias, a newly developed bioinformatics pipeline, we identified HRGPs in sequences from the 1000 Plants transcriptome project (www.onekp.com). Our analyses provide new insights into the evolution of HRGPs across major evolutionary milestones, including the transition to land and the early radiation of angiosperms. Significantly, data mining reveals the origin of glycosylphosphatidylinositol (GPI)-anchored AGPs in green algae and a 3- to 4-fold increase in GPI-AGPs in liverworts and mosses. The first detection of cross-linking (CL)-EXTs is observed in bryophytes, which suggests that CL-EXTs arose though the juxtaposition of preexisting SPn EXT glycomotifs with refined Y-based motifs. We also detected the loss of CL-EXT in a few lineages, including the grass family (Poaceae), that have a cell wall composition distinct from other monocots and eudicots. A key challenge in HRGP research is tracking individual HRGPs throughout evolution. Using the 1000 Plants output, we were able to find putative orthologs of Arabidopsis pollen-specific GPI-AGPs in basal eudicots.

PMID:
28446636
PMCID:
PMC5462033
DOI:
10.1104/pp.17.00295
[Indexed for MEDLINE]
Free PMC Article

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