Hydroxyproline O‐arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens

MacAlister, Cora A.; Ortiz‐Ramírez, Carlos; Becker, Jörg; Feijó, José A.; Lippman, Zachary B.

doi:10.1111/tpj.13079

Cited by 41 publications

(54 citation statements)

References 83 publications

(116 reference statements)

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“…These mutant phenotypes indicate that sequential arabinosylation of CLE peptides by three enzymes is crucial to CLV signaling in tomato. The situation in Arabidopsis, however, is less clear, since null mutants for HPAT genes do not have a clv phenotype (MacAlister et al, 2016). It should also be noted that, although arabinosylation may increase the potency of some CLE peptides, other CLE peptides that are able to control meristem size have serine or alanine residues instead of the hydroxyproline at position 7 and presumably are not modified, suggesting that arabinosylation is not essential for CLE function, unless the first hydroxyproline at position 4 can be modified (Ohyama et al, 2009).…”

Section: Introductionmentioning

confidence: 97%

CLAVATA-WUSCHEL signaling in the shoot meristem

2016

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Shoot meristems are maintained by pluripotent stem cells that are controlled by CLAVATA-WUSCHEL feedback signaling. This pathway, which coordinates stem cell proliferation with differentiation, was first identified in Arabidopsis, but appears to be conserved in diverse higher plant species. In this Review, we highlight the commonalities and differences between CLAVATA-WUSCHEL pathways in different species, with an emphasis on Arabidopsis, maize, rice and tomato. We focus on stem cell control in shoot meristems, but also briefly discuss the role of these signaling components in root meristems.

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Section: Introductionmentioning

confidence: 97%

CLAVATA-WUSCHEL signaling in the shoot meristem

2016

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“…Cross-linking of EXTs into the wall is proposed to result in the cessation of cell expansion, and yet, some EXTs are important for cell elongation in root hairs (Velasquez et al, 2011(Velasquez et al, , 2015. The importance of glycosylation on EXT-like motifs in the moss Physcomitrella patens was shown recently through mutants in Hyp O-arabinosyltransferases (MacAlister et al, 2016). Reduced levels of cell wallassociated Hyp arabinosides (as found in EXTs) in P. patens resulted in increased elongation of protonemal tip cells.…”

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confidence: 99%

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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“…These observations are consistent with prior in vitro and in vivo analyses supporting physiological functions of dual CLV3 peptides identified in calli and liquid medium of seedlings overexpression the Arabidopsis CLV3 transgene (Kondo et al, 2006; Kondo et al, 2008; Ohyama et al, 2009; Song et al, 2012; Song et al, 2013). Moreover, a recent study of the Arabidopsis loss-of-function mutants of three HPATs without overt SAM defect supports the likely physiological role of the 12-amino-acid MCLV3p in shoot stem cell signaling when the 13-amino-acid [Ara 3 ]CVL3p cannot be generated (MacAlister et al, 2016). Indeed, since the arbinosylated modification of the 12-amino acid CLE2 peptide was almost disappeared even in the hpat3 single mutant (Ogawa-Ohnishi et al, 2013), the arabinosylation of CLV3p is not functionally indispensable in the Arabidopsis shoot stem cell signaling as previously suggested (Ohyama et al, 2009; Shinohara and Matsubayashi, 2013; Shinohara and Matsubayashi, 2015).…”

Section: Discussionmentioning

confidence: 81%

“…Three studies spanning the past decade have led to unresolved puzzles regarding the physiological function of arabinosylation in the Arabidopsis CLV3 peptides (Kondo et al, 2008; Song et al, 2012; Song et al, 2013; MacAlister et al, 2016). Alanine-scan analyses were conducted using synthetic MCLV3 peptide variants in bioassays and in vitro competitive binding with the CLV1 ectodomain (Kondo et al, 2008), or using in vivo complementation of the SAM size and WUS expression in clv3-2 transgenic plants expressing MCLV3 peptide variants from CLV3 transgenes (Song et al, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…These systematic analyses of peptide mutants in vitro and in vivo failed to support a critical biological role of the 7 th hydroxyproline residue, where three arabinoses are covalently attached (Kondo et al, 2008; Ohyama et al, 2009; Song et al, 2012; Shinohara and Matsubayashi, 2013). Although recent findings on hydroxyproline O-arabinosyltransferases (HPATs), responsible for the arabinosylation of proteins or peptides, have confirmed the importance of peptide arabinosylation in tomato plants (Xu et al, 2015), the thorough genetic and phenotypic analyses of the single, double and triple Arabidopsis hpat1,2,3 mutants do not support a role of HPATs in stem cell signaling in the SAM (MacAlister et al, 2016). …”

Section: Introductionmentioning

confidence: 99%

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Dual CLAVATA3 peptides in Arabidopsis shoot stem cell signaling

Kim

et al. 2017

J. Plant Biol.

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Plant shoot stem cell pool is constantly maintained by a negative feedback loop through peptide-receptor mediated signaling pathway. CLAVATA3 (CLV3) encode a 96 amino-acid protein which is processed to 12-amino-acid or arabinosylated 13-amino-acid peptides, acting as a ligand signal to regulate stem cell homeostasis in the shoot apical meristem (SAM). Although arabinosylated 13-amino-acid CLV3 peptide (CLV3p) shows more significant binding affinity to its receptors and biological activities in the SAM, the physiological function of two mature forms of CLV3p remained an unresolved puzzle in the past decade due to the technical difficulties of arabinosylation modification in the peptide synthesis. Here, we analyzed the role of two mature CLV3 peptides with newly synthesized arabinosylated peptide. Beside shoot meristem phenotypes, arabinosylated CLV3p showed the conventional trait of CLV2-dependent root growth inhibition. Moreover, both 12-amino-acid and arabinosylated 13-amino-acid CLV3 peptides have analogous activities in shoot stem cell signaling. Notably, we demonstrated that non-arabinosylated 12-amino acid CLV3p can affect shoot stem cell signaling at the physiological level unlike previously suggested (Ohyama et al., 2009; Shinohara and Matsubayashi, 2013; Shinohara and Matsubayashi, 2015). Therefore, these results support the physiological role of the 12-amino-acid CLV3p in shoot stem cell signaling in the deficient condition of arabinosylated 13-amino-acid CLV3p in Arabidopsis thaliana.

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Hydroxyproline O‐arabinosyltransferase mutants oppositely alter tip growth in Arabidopsis thaliana and Physcomitrella patens

Cited by 41 publications

References 83 publications

CLAVATA-WUSCHEL signaling in the shoot meristem

CLAVATA-WUSCHEL signaling in the shoot meristem

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

Dual CLAVATA3 peptides in Arabidopsis shoot stem cell signaling

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