The Medicago SymCEP7 hormone increases nodule number via shoots without compromising lateral root number.


Journal

Plant physiology
ISSN: 1532-2548
Titre abrégé: Plant Physiol
Pays: United States
ID NLM: 0401224

Informations de publication

Date de publication:
17 03 2023
Historique:
received: 18 11 2022
accepted: 02 12 2022
pubmed: 19 1 2023
medline: 22 3 2023
entrez: 18 1 2023
Statut: ppublish

Résumé

Legumes acquire soil nutrients through nitrogen-fixing root nodules and lateral roots. To balance the costs and benefits of nodulation, legumes negatively control root nodule number by autoregulatory and hormonal pathways. How legumes simultaneously coordinate root nodule and lateral root development to procure nutrients remains poorly understood. In Medicago (Medicago truncatula), a subset of mature C-TERMINALLY ENCODED PEPTIDE (CEP) hormones can systemically promote nodule number, but all CEP hormones tested to date negatively regulate lateral root number. Here we showed that Medicago CEP7 produces a mature peptide, SymCEP7, that promotes nodulation from the shoot without compromising lateral root number. Rhizobial inoculation induced CEP7 in the susceptible root nodulation zone in a Nod factor-dependent manner, and, in contrast to other CEP genes, its transcription level was elevated in the ethylene signaling mutant sickle. Using mass spectrometry, fluorescence microscopy and expression analysis, we demonstrated that SymCEP7 activity requires the COMPACT ROOT ARCHITECTURE 2 receptor and activates the shoot-to-root systemic effector, miR2111. Shoot-applied SymCEP7 rapidly promoted nodule number in the pM to nM range at concentrations up to five orders of magnitude lower than effects mediated by root-applied SymCEP7. Shoot-applied SymCEP7 also promoted nodule number in White Clover (Trifolium repens) and Lotus (Lotus japonicus), which suggests that this biological function may be evolutionarily conserved. We propose that SymCEP7 acts in the Medicago shoot to counter balance the autoregulation pathways induced rapidly by rhizobia to enable nodulation without compromising lateral root growth, thus promoting the acquisition of nutrients other than nitrogen to support their growth.

Identifiants

pubmed: 36653329
pii: 6991717
doi: 10.1093/plphys/kiad012
pmc: PMC10022606
doi:

Substances chimiques

Peptides 0
Hormones 0
Nitrogen N762921K75
Plant Proteins 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

2012-2026

Informations de copyright

© American Society of Plant Biologists 2023. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.

Déclaration de conflit d'intérêts

Conflict of interest statement. None declared.

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Auteurs

Ariel Ivanovici (A)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.

Carole Laffont (C)

University of Paris-Saclay, CNRS, INRAE, University Paris-Cité, Univ. d'Evry, Gif-sur-Yvette, France.

Estíbaliz Larrainzar (E)

Sciences Department, Institute for Multidisciplinary Research in Applied Biology (IMAB), Universidad Pública de Navarra, Pamplona 31006, Spain.

Neha Patel (N)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.

Courtney S Winning (CS)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.

Han-Chung Lee (HC)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.

Nijat Imin (N)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.
School of Science, Western Sydney University, Penrith, New South Wales 2751, Australia.
School of Biological Sciences, Faculty of Science, The University of Auckland, Auckland, New Zealand.

Florian Frugier (F)

University of Paris-Saclay, CNRS, INRAE, University Paris-Cité, Univ. d'Evry, Gif-sur-Yvette, France.

Michael A Djordjevic (MA)

Division of Plant Sciences, Research School of Biology, The Australian National University, Canberra, Australian Capital Territory 2601, Australia.

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Classifications MeSH