Genome-wide annotation and characterization of CLAVATA/ESR (CLE) peptide hormones of soybean (Glycine max) and common bean (Phaseolus vulgaris), and their orthologues ofArabidopsis thaliana

Hastwell, April H.; Gresshoff, Peter M.; Ferguson, Brett J.

doi:10.1093/jxb/erv351

Cited by 48 publications

(88 citation statements)

References 85 publications

(164 reference statements)

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“…Our ITC data of the TDIF mutants suggests, TDIF-H1 contributes most to the binding of the N-terminal anchoring site, while TDIF-E2 plays a marginal role in this interaction. H1 is conserved in TDIF, CLE42, and CLE46 (S1 Fig), which have been classified into the same group [11, 37, 38]. Changing E2 to G in CLE42 does not influence the binding significantly, while E2K, V3H, I10T and S11G substitutions in CLE46 render it unable to bind TDR (Fig 3).…”

Section: Resultsmentioning

confidence: 99%

Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions

Chakraborty

2017

PLoS ONE

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Tracheary Element Differentiation Inhibitory Factor (TDIF) belongs to the family of post-translationally modified CLE (CLAVATA3/embryo surrounding region (ESR)-related) peptide hormones that control root growth and define the delicate balance between stem cell proliferation and differentiation in SAM (shoot apical meristem) or RAM (root apical meristem). In Arabidopsis, Tracheary Element Differentiation Inhibitory Factor Receptor (TDR) and its ligand TDIF signaling pathway is involved in the regulation of procambial cell proliferation and inhibiting its differentiation into xylem cells. Here we present the crystal structures of the extracellular domains (ECD) of TDR alone and in complex with its ligand TDIF resolved at 2.65 Ǻ and 2.75 Ǻ respectively. These structures provide insights about the ligand perception and specific interactions between the CLE peptides and their cognate receptors. Our in vitro biochemical studies indicate that the interactions between the ligands and the receptors at the C-terminal anchoring site provide conserved binding. While the binding interactions occurring at the N-terminal anchoring site dictate differential binding specificities between different ligands and receptors. Our studies will open different unknown avenues of TDR-TDIF signaling pathways that will enhance our knowledge in this field highlighting the receptor ligand interaction, receptor activation, signaling network, modes of action and will serve as a structure function relationship model between the ligand and the receptor for various similar leucine-rich repeat receptor-like kinases (LRR-RLKs).

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Section: Resultsmentioning

confidence: 99%

Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions

Chakraborty

2017

PLoS ONE

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“…japonicus , Phaseolus vulgaris , and A . thaliana (Alves‐Carvalho et al, ;Cock & McCormick, ; Hastwell et al, , ). The search yielded 40 unique CLE peptide‐encoding gene candidates of pea (Figure , Table S1) and a further eight sequences with unclear gene structures and/or analogous CLE peptide domains (Table S2).…”

Section: Resultsmentioning

confidence: 99%

“…CLE peptide‐encoding genes in P . sativum were identified using BLAST searches of known legume genes identified in Hastwell, de Bang, Gresshoff, and Ferguson () and Hastwell, Gresshoff, and Ferguson () as well as those from Arabidopsis thaliana (Cock & McCormick, ) with E value = 1 (Altschul et al, ; Altschul et al, ). The searches were conducted in The Pea RNA‐Seq gene atlas (http://bios.dijon.inra.fr/FATAL/cgi/pscam.cgi; Alves‐Carvalho et al, ).…”

Section: Methodsmentioning

confidence: 99%

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Triarabinosylation is required for nodulation‐suppressive CLE peptides to systemically inhibit nodulation in Pisum sativum

Hastwell

Corcilius

Williams

et al. 2018

Plant Cell & Environment

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Legumes form root nodules to house beneficial nitrogen-fixing rhizobia bacteria. However, nodulation is resource demanding; hence, legumes evolved a systemic signalling mechanism called autoregulation of nodulation (AON) to control nodule numbers. AON begins with the production of CLE peptides in the root, which are predicted to be glycosylated, transported to the shoot, and perceived. We synthesized variants of nodulation-suppressing CLE peptides to test their activity using petiole feeding to introduce CLE peptides into the shoot. Hydroxylated, monoarabinosylated, and triarabinosylated variants of soybean GmRIC1a and GmRIC2a were chemically synthesized and fed into recipient Pisum sativum (pea) plants, which were used due to the availability of key AON pathway mutants unavailable in soybean. Triarabinosylated GmRIC1a and GmRIC2a suppressed nodulation of wild-type pea, whereas no other peptide variant tested had this ability. Suppression also occurred in the supernodulating hydroxyproline O-arabinosyltransferase mutant, Psnod3, but not in the supernodulating receptor mutants, Pssym29, and to some extent, Pssym28. During our study, bioinformatic resources for pea became available and our analyses identified 40 CLE peptide-encoding genes, including orthologues of nodulation-suppressive CLE peptides. Collectively, we demonstrated that soybean nodulation-suppressive CLE peptides can function interspecifically in the AON pathway of pea and require arabinosylation for their activity.

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“…1,8,9 The CLE genes have been found in many plant species, whereas the roles of most identified CLE genes remained to be elucidated. 2,[10][11][12][13][14][15] As the 2 most known members of CLE peptide family, AtCLV3 and AtCLE40 are key regulators in coordinating stem cell homeostasis in the SAM (Shoot Apical Meristem) and RAM (Root Apical Meristem), respectively. 1 Other than their functions in stem cell fate, it has been also revealed that the CLE peptides are important players in modulating various plant growth and developmental processes such as nodulation, [16][17][18] protoxylem formation, 19 embryogenesis and endosperm development, 20 phloem formation, 21 pollen growth, 22 and lateral root expansion.…”

Section: Introductionmentioning

confidence: 99%

The CLE gene family in Populus trichocarpa

Liu

Yang

et al. 2016

Plant Signaling & Behavior

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Genome-wide annotation and characterization of CLAVATA/ESR (CLE) peptide hormones of soybean (Glycine max) and common bean (Phaseolus vulgaris), and their orthologues ofArabidopsis thaliana

Abstract: HighlightUsing a genome-wide approach, the complete CLE peptide-encoding gene families of soybean and common bean were identified, characterized, and compared with those of Arabidopsis.

Cited by 48 publications

References 85 publications

Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions

Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions

Triarabinosylation is required for nodulation‐suppressive CLE peptides to systemically inhibit nodulation in Pisum sativum

The CLE gene family in Populus trichocarpa

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