Global Analysis of Proline-Rich Tandem Repeat Proteins Reveals Broad Phylogenetic Diversity in Plant Secretomes

Newman, Aaron M.; Cooper, J. B.

doi:10.1371/journal.pone.0023167

Cited by 16 publications

(14 citation statements)

References 59 publications

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“…The viscoelastic properties of mucus, slimes, and other viscous biofluids are determined in large part by the formation of extended and entangled structures by mucins such as the SCPP mucin 7 (Supplementary Table S4, http:// dx.doi.org/10.3168/jds.2013-6831; Schenkels et al, 1995;Thornton et al, 2008;Senapati et al, 2010). Likewise, P,Q-rich proteins readily form gels; for example, the seed storage prolamins wheat gliadin and barley hordein (Shewry and Halford, 2002) or the plant cell wall extensins (Newman and Cooper, 2011). Extended hydrated structures and low sequence specificity both point to a predominance of main-chain interactions mediated by direct H-bonding or through bridging water molecules.…”

Section: Quaternary Structures and The Hydrophobic Effectmentioning

confidence: 99%

Invited review: Caseins and the casein micelle: Their biological functions, structures, and behavior in foods

Holt

Carver

Ecroyd

et al. 2013

Journal of Dairy Science

394

240

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A typical casein micelle contains thousands of casein molecules, most of which form thermodynamically stable complexes with nanoclusters of amorphous calcium phosphate. Like many other unfolded proteins, caseins have an actual or potential tendency to assemble into toxic amyloid fibrils, particularly at the high concentrations found in milk. Fibrils do not form in milk because an alternative aggregation pathway is followed that results in formation of the casein micelle. As a result of forming micelles, nutritious milk can be secreted and stored without causing either pathological calcification or amyloidosis of the mother's mammary tissue. The ability to sequester nanoclusters of amorphous calcium phosphate in a stable complex is not unique to caseins. It has been demonstrated using a number of noncasein secreted phosphoproteins and may be of general physiological importance in preventing calcification of other biofluids and soft tissues. Thus, competent noncasein phosphoproteins have similar patterns of phosphorylation and the same type of flexible, unfolded conformation as caseins. The ability to suppress amyloid fibril formation by forming an alternative amorphous aggregate is also not unique to caseins and underlies the action of molecular chaperones such as the small heat-shock proteins. The open structure of the protein matrix of casein micelles is fragile and easily perturbed by changes in its environment. Perturbations can cause the polypeptide chains to segregate into regions of greater and lesser density. As a result, the reliable determination of the native structure of casein micelles continues to be extremely challenging. The biological functions of caseins, such as their chaperone activity, are determined by their composition and flexible conformation and by how the casein polypeptide chains interact with each other. These same properties determine how caseins behave in the manufacture of many dairy products and how they can be used as functional ingredients in other foods. aBStraCtA typical casein micelle contains thousands of casein molecules, most of which form thermodynamically stable complexes with nanoclusters of amorphous calcium phosphate. Like many other unfolded proteins, caseins have an actual or potential tendency to assemble into toxic amyloid fibrils, particularly at the high concentrations found in milk. Fibrils do not form in milk because an alternative aggregation pathway is followed that results in formation of the casein micelle. As a result of forming micelles, nutritious milk can be secreted and stored without causing either pathological calcification or amyloidosis of the mother's mammary tissue. The ability to sequester nanoclusters of amorphous calcium phosphate in a stable complex is not unique to caseins. It has been demonstrated using a number of noncasein secreted phosphoproteins and may be of general physiological importance in preventing calcification of other biofluids and soft tissues. Thus, competent noncasein phosphoproteins have similar patterns of phosp...

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Section: Quaternary Structures and The Hydrophobic Effectmentioning

confidence: 99%

Invited review: Caseins and the casein micelle: Their biological functions, structures, and behavior in foods

Holt

Carver

Ecroyd

et al. 2013

Journal of Dairy Science

394

240

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“…Showalter et al [2 and unpublished data] conducted the identification of the HRGP superfamily in Arabidopsis thaliana and Populus trichocarpa in which 59 and 60 EXTs were identified, respectively. In addition, Newman and Cooper [ 27 ] identified numerous proline-rich tandem repeat proteins (TRPs) including EXTs through a bioinformatics approach using EST and NCBI Non-Redundant protein sequence data of a number of plant species, but the search criteria for TRPs were not tailored for identifying EXTs. Nonetheless, knowledge about the number and distribution of EXTs in plant kingdom is still lacking.…”

Section: Introductionmentioning

confidence: 99%

Bioinformatic Identification and Analysis of Extensins in the Plant Kingdom

et al. 2016

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Extensins (EXTs) are a family of plant cell wall hydroxyproline-rich glycoproteins (HRGPs) that are implicated to play important roles in plant growth, development, and defense. Structurally, EXTs are characterized by the repeated occurrence of serine (Ser) followed by three to five prolines (Pro) residues, which are hydroxylated as hydroxyproline (Hyp) and glycosylated. Some EXTs have Tyrosine (Tyr)-X-Tyr (where X can be any amino acid) motifs that are responsible for intramolecular or intermolecular cross-linkings. EXTs can be divided into several classes: classical EXTs, short EXTs, leucine-rich repeat extensins (LRXs), proline-rich extensin-like receptor kinases (PERKs), formin-homolog EXTs (FH EXTs), chimeric EXTs, and long chimeric EXTs. To guide future research on the EXTs and understand evolutionary history of EXTs in the plant kingdom, a bioinformatics study was conducted to identify and classify EXTs from 16 fully sequenced plant genomes, including Ostreococcus lucimarinus, Chlamydomonas reinhardtii, Volvox carteri, Klebsormidium flaccidum, Physcomitrella patens, Selaginella moellendorffii, Pinus taeda, Picea abies, Brachypodium distachyon, Zea mays, Oryza sativa, Glycine max, Medicago truncatula, Brassica rapa, Solanum lycopersicum, and Solanum tuberosum, to supplement data previously obtained from Arabidopsis thaliana and Populus trichocarpa. A total of 758 EXTs were newly identified, including 87 classical EXTs, 97 short EXTs, 61 LRXs, 75 PERKs, 54 FH EXTs, 38 long chimeric EXTs, and 346 other chimeric EXTs. Several notable findings were made: (1) classical EXTs were likely derived after the terrestrialization of plants; (2) LRXs, PERKs, and FHs were derived earlier than classical EXTs; (3) monocots have few classical EXTs; (4) Eudicots have the greatest number of classical EXTs and Tyr-X-Tyr cross-linking motifs are predominantly in classical EXTs; (5) green algae have no classical EXTs but have a number of long chimeric EXTs that are absent in embryophytes. Furthermore, phylogenetic analysis was conducted of LRXs, PERKs and FH EXTs, which shed light on the evolution of three EXT classes.

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“…Another, less biased approach based on a clustering method was used by Newman and Cooper (2011) to search for tandem repeats to identify Pro-rich proteins in plants. While EXTs were able to be identified, this method was poor in detecting AGPs because their diagnostic AP, SP, and TP glycomotifs that direct arabino-3,6-galactan-type glycosylation (Tan et al, 2003) are scattered throughout the protein backbone, rather than being found in tandem (Schultz et al, 2002;Showalter et al, 2010).…”

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confidence: 99%

Pipeline to Identify Hydroxyproline-Rich Glycoproteins

et al. 2017

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Intrinsically disordered proteins (IDPs) are functional proteins that lack a well-defined three-dimensional structure. The study of IDPs is a rapidly growing area as the crucial biological functions of more of these proteins are uncovered. In plants, IDPs are implicated in plant stress responses, signaling, and regulatory processes. A superfamily of cell wall proteins, the hydroxyprolinerich glycoproteins (HRGPs), have characteristic features of IDPs. Their protein backbones are rich in the disordering amino acid proline, they contain repeated sequence motifs and extensive posttranslational modifications (glycosylation), and they have been implicated in many biological functions. HRGPs are evolutionarily ancient, having been isolated from the protein-rich walls of chlorophyte algae to the cellulose-rich walls of embryophytes. Examination of HRGPs in a range of plant species should provide valuable insights into how they have evolved. Commonly divided into the arabinogalactan proteins, extensins, and proline-rich proteins, in reality, a continuum of structures exists within this diverse and heterogenous superfamily. An inability to accurately classify HRGPs leads to inconsistent gene ontologies limiting the identification of HRGP classes in existing and emerging omics data sets. We present a novel and robust motif and amino acid bias (MAAB) bioinformatics pipeline to classify HRGPs into 23 descriptive subclasses. Validation of MAAB was achieved using available genomic resources and then applied to the 1000 Plants transcriptome project (www.onekp.com) data set. Significant improvement in the detection of HRGPs using multiple-kmer transcriptome assembly methodology was observed. The MAAB pipeline is readily adaptable and can be modified to optimize the recovery of IDPs from other organisms.

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Global Analysis of Proline-Rich Tandem Repeat Proteins Reveals Broad Phylogenetic Diversity in Plant Secretomes

Cited by 16 publications

References 59 publications

Invited review: Caseins and the casein micelle: Their biological functions, structures, and behavior in foods

Invited review: Caseins and the casein micelle: Their biological functions, structures, and behavior in foods

Bioinformatic Identification and Analysis of Extensins in the Plant Kingdom

Pipeline to Identify Hydroxyproline-Rich Glycoproteins

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