Bioinformatic Identification and Analysis of Extensins in the Plant Kingdom

Liu, Xiao; Wolfe, Richard A.; Welch, Lonnie R.; Domozych, David S.; Popper, Zoë A.; Showalter, Allan M.

doi:10.1371/journal.pone.0150177

Cited by 62 publications

(56 citation statements)

References 94 publications

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“…The value for the Poaceae was at the high end of this range (median, 88.4%; mean, 83.8%), suggesting that the grass transcriptome assemblies are high quality and that CL-EXTs should have been detected if they were present. Our findings also are supported by a recent bioinformatics study of the maize and rice (Oryza sativa) genomes, where no CL-EXTs were identified (Liu et al, 2016).…”

Section: Cl-exts Have Been Lost In Many Grass Speciessupporting

confidence: 87%

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

et al. 2017

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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 SP n 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.Cell walls of plants and algae are widely used for food, textiles, paper, and timber, yet our understanding of their assembly and dynamic remodeling in response to growth, development, and environmental stresses (abiotic and biotic) remains rudimentary (Doblin et al., 2010(Doblin et al., , 2014. There are two contrasting types of walls/extracellular matrices in the green plant lineage, protein-rich walls of some green algae and the cellulose-rich walls of embryophytes (land plants). Recent studies of cell wall evolution suggest that the origins of many wall components occurred in the streptophyte green algae prior to the evolution of embryophytes (Sørensen et al., 2010;Popper et al., 2011;Domozych et al., 2012) with elaboration of a preexisting set of polysaccharides rather than an entirely new polymer framework. Although both the ultrastructure of plant walls and the fine structure of their component polymers vary widely, they all typically constitute a fibrillar network of cellulose microfibrils that is embedded within a gel-like matrix of noncellulosic polysaccharides, pectins, 904

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Section: Cl-exts Have Been Lost In Many Grass Speciessupporting

confidence: 87%

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

et al. 2017

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“…Extensins are one of the major classes of hydroxyproline‐rich glycoproteins (HRGPs) present in plant cell walls (Chen and Varner, ; Lamport, ; Showalter, ). Extensins are characterized by the repeated occurrence of serine followed by proline residues (Kieliszewski and Lamport, ; Liu et al ., ; Memelink et al ., ). Previous studies have demonstrated that extensins are required for normal vegetative growth, male fertility and disease tolerance.…”

Section: Introductionmentioning

confidence: 99%

Ectopic expression of a novel OsExtensin‐like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice

Fan

Liu

et al. 2017

Plant Biotechnology Journal

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SummaryPlant lodging resistance is an important integrative agronomic trait of grain yield and quality in crops. Although extensin proteins are tightly associated with plant cell growth and cell wall construction, little has yet been reported about their impacts on plant lodging resistance. In this study, we isolated a novel extensin‐like (OsEXTL) gene in rice, and selected transgenic rice plants that expressed OsEXTL under driven with two distinct promoters. Despite different OsEXTL expression levels, two‐promoter‐driven OsEXTL‐transgenic plants, compared to a rice cultivar and an empty vector, exhibited significantly reduced cell elongation in stem internodes, leading to relatively shorter plant heights by 7%–10%. Meanwhile, the OsEXTL‐transgenic plants showed remarkably thickened secondary cell walls with higher cellulose levels in the mature plants, resulting in significantly increased detectable mechanical strength (extension and pushing forces) in the mature transgenic plants. Due to reduced plant height and increased plant mechanical strength, the OsEXTL‐transgenic plants were detected with largely enhanced lodging resistances in 3 years field experiments, compared to those of the rice cultivar ZH11. In addition, despite relatively short plant heights, the OsEXTL‐transgenic plants maintain normal grain yields and biomass production, owing to their increased cellulose levels and thickened cell walls. Hence, this study demonstrates a largely improved lodging resistance in the OsEXTL‐transgenic rice plants, and provides insights into novel extensin functions in plant cell growth and development, cell wall network construction and wall structural remodelling.

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“…Thus, Showalter et al (2010Showalter et al ( , 2016) used a combination of both bias and motifs to search for PRPs [45% or greater PVKCYT or 2 or more KKPCPP motifs or 2 or more PPVX(K/T) motifs] in Arabidopsis and P. trichocarpa. With these approaches (Showalter et al, 2010Liu et al, 2016), many HRGP sequences were placed into more than one HRGP family. Therefore, manual curation of BIO OHIO output is required for final classification (Showalter et al, 2010, a task that is not practicable with large data sets and that also has the potential to introduce subjective bias.…”

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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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Bioinformatic Identification and Analysis of Extensins in the Plant Kingdom

Cited by 62 publications

References 94 publications

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

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

Ectopic expression of a novel OsExtensin‐like gene consistently enhances plant lodging resistance by regulating cell elongation and cell wall thickening in rice

Pipeline to Identify Hydroxyproline-Rich Glycoproteins

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