Regulation of Arabidopsis root development by small signaling peptides

Delay, Christina; Imin, Nijat; Djordjevic, Michael A.

doi:10.3389/fpls.2013.00352

Cited by 49 publications

(35 citation statements)

References 51 publications

(70 reference statements)

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“…3). Previous studies connecting nutrient acquisition and SSP function in M. truncatula have focused largely on the roles of CLE and CEP genes in N status-dependent root development and nodulation (Mortier et al, 2010;Delay et al, 2013a;Imin et al, 2013;Okamoto et al, 2013;Araya et al, 2014;Huault et al, 2014;Tabata et al, 2014;Mohd-Radzman et al, 2016;Ohkubo et al, 2017). Demonstrating the validity of our data sets, we could confirm these previous reports of CLE and CEP regulation (Supplemental Table S7).…”

Section: Hundreds Of Ssps Are Regulated During Nodulation and By Macrsupporting

confidence: 81%

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

et al. 2017

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Growing evidence indicates that small, secreted peptides (SSPs) play critical roles in legume growth and development, yet the annotation of SSP-coding genes is far from complete. Systematic reannotation of the Medicago truncatula genome identified 1,970 homologs of established SSP gene families and an additional 2,455 genes that are potentially novel SSPs, previously unreported in the literature. The expression patterns of known and putative SSP genes based on 144 RNA sequencing data sets covering various stages of macronutrient deficiencies and symbiotic interactions with rhizobia and mycorrhiza were investigated. Focusing on those known or suspected to act via receptor-mediated signaling, 240 nutrient-responsive and 365 nodulation-responsive Signaling-SSPs were identified, greatly expanding the number of SSP gene families potentially involved in acclimation to nutrient deficiencies and nodulation. Synthetic peptide applications were shown to alter root growth and nodulation phenotypes, revealing additional regulators of legume nutrient acquisition. Our results constitute a powerful resource enabling further investigations of specific SSP functions via peptide treatment and reverse genetics.

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Section: Hundreds Of Ssps Are Regulated During Nodulation and By Macrsupporting

confidence: 81%

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

et al. 2017

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“…To balance the carbon cost to the host with the benefits of N‐fixation, nodule number and activity is carefully regulated by systemic mechanisms that involve the long‐distance root‐to‐shoot movement of peptide hormones. Specific members of the CLE peptide family negatively regulate nodule number by a process called autoregulation of nodulation (AON) (Ferguson et al ., ; Mortier et al ., ; Reid et al ., ; Suzaki et al ., ; Djordjevic et al ., ; Shabala et al ., ; Kassaw et al ., ) and C ‐TERMINALLY ENCODED PEPTIDE (CEP) family members positively control nodule number (Delay et al ., ; Imin et al ., ; Mohd‐Radzman et al ., , ). In CLE‐dependent AON, the descending shoot‐derived AON signal and the mechanism by which it restricts nodulation have not been conclusively identified.…”

Section: Introductionmentioning

confidence: 99%

CLE peptide tri‐arabinosylation and peptide domain sequence composition are essential for SUNN‐dependent autoregulation of nodulation in Medicago truncatula

et al. 2018

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MtCLE12 and MtCLE13 encode CLAVATA3/EMBRYO-SURROUNDING REGION RELATED (CLE) peptides which regulate autoregulation of nodulation (AON) in Medicago through the shoot receptor, SUNN (SUPER NUMERIC NODULES). Genetics suggests RDN1 (ROOT-DETERMINED NODULATION 1) arabinosylates MtCLE12 to enable SUNN perception. The functional structures of MtCLE12 and MtCLE13 peptides, however, remain elusive. We combined genetic and chemical synthesis approaches to determine if glyco-modifications of three nodule-expressed CLE peptides are essential for AON. We also examined how root and shoot applied AON-CLEs inhibit nodulation. MtCLE12, MtCLE13 and MtCLE42 peptides were synthesized with hydroxylation, mono-arabinosylation or tri-arabinosylation (TaP) at proline 7. Only MtCLE12-TaP and MtCLE13-TaP peptides induced AON in wild-type (WT) and rdn1-1, but not in sunn-4. The application of MtCLE13-TaP to cotyledons 1 d before rhizobial inoculation completely inhibited both rhizobial infection and nodulation. By contrast, MtCLE12-TaP induced significant AON without abolishing rhizobial infection. The results indicate that key CLE domain amino acids and TaP modifications to MtCLE12 and MtCLE13 are essential for SUNN-dependent AON. We also show evidence that RDN1 does not tri-arabinosylate MtCLE13. Finally, MtCLE13-TaP can induce a strong AON response in shoots that inhibits the entire symbiotic processes in roots. We present a new model for AON in Medicago.

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“…Previous studies reported that GLV/RGF/CLE-like peptides interplay with auxin to regulate root gravitropism by regulating auxin transport (66,67). Another report showed that ARF7-mediated induction of peptide gene IDA by auxin is involved in the regulation of lateral root initiation (67,68).…”

Section: Discussionmentioning

confidence: 99%

“…Another report showed that ARF7-mediated induction of peptide gene IDA by auxin is involved in the regulation of lateral root initiation (67,68). However, the molecular mechanism underlying auxin-induced IDA expression is unknown.…”

Section: Discussionmentioning

confidence: 99%

Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll

Zhang

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

124

110

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Plants, as sessile organisms, must coordinate various physiological processes to adapt to ever-changing surrounding environments. Stomata, the epidermal pores facilitating gas and water exchange, play important roles in optimizing photosynthetic efficiency and adaptability. Stomatal development is under the control of an intrinsic program mediated by a secretory peptide gene familynamely, EPIDERMAL PATTERNING FACTOR, including positively acting STOMAGEN/EPFL9. The phytohormone brassinosteroids and environment factor light also control stomatal production. However, whether auxin regulates stomatal development and whether peptide signaling is coordinated with auxin signaling in the regulation of stomatal development remain largely unknown. Here we show that auxin negatively regulates stomatal development through MONOPTEROS (also known as ARF5) repression of the mobile peptide gene STOMAGEN in mesophyll. Through physiological, genetic, transgenic, biochemical, and molecular analyses, we demonstrate that auxin inhibits stomatal development through the nuclear receptor TIR1/AFB-mediated signaling, and that MONOPTEROS directly binds to the STOMAGEN promoter to suppress its expression in mesophyll and inhibit stomatal development. Our results provide a paradigm of cross-talk between phytohormone auxin and peptide signaling in the regulation of stomatal production.A uxin is the first identified phytohormone, which exerts multifaceted influences on plant growth and development, such as embryonic root initiation (1, 2), shoot apical meristem function (3), and floral primordia initiation (4). As a "molecular glue," auxin facilitates the formation of its coreceptor complexes comprising F-box proteins (TIR1/AFBs) and AUXIN/INDOLE-3-ACETIC ACID proteins (AUX/IAAs), and subsequent AUX/ IAAs ubiquitination and degradation by 26S proteasome, thus releasing auxin response factors (ARFs) from AUX/IAAs repression to regulate auxin-responsive gene expression by either activation or repression (2, 3, 5-11). Although many physiologic processes are reported to be regulated by auxin (1-4, 6, 12), the full understanding of the functions of this versatile phytohormone has not been reached.Stomata, the pores flanked by a pair of guard cells, mainly constitute the epidermis of plant leaves together with trichomes and neighboring pavement cells that separate stomata to maintain the one-cell spacing rule (13,14). As a gas and water passage between external environment and internal plant tissue, stomata play important roles in photosynthesis and global carbon and water circulation (15). Stomatal generation undergoes several stages, including meristemoid mother cell, meristemoid, guard mother cell, and guard cells, which is modulated by an intrinsic program (14) mainly involving putative peptide ligands [EPI-DERMAL PATTERNING FACTOR (EPF) family] (16-20), membrane proteins (receptor-like protein TMM and receptorlike kinase ERECTA family) (21-23), MAPK cascades (protein kinase YDA, MKK4/5/7/9, and MPK3/6) (24-26), and transcription factors (bHLH...

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Regulation of Arabidopsis root development by small signaling peptides

Cited by 49 publications

References 51 publications

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

CLE peptide tri‐arabinosylation and peptide domain sequence composition are essential for SUNN‐dependent autoregulation of nodulation in Medicago truncatula

Auxin inhibits stomatal development through MONOPTEROS repression of a mobile peptide gene STOMAGEN in mesophyll

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