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Peer-reviewedCC BY-NC-ND 4.0Proceedings of the National Academy of Sciences of the United States of America

HAR1 receptor kinase links nodule autoregulation with repression of auxin signaling and lateral root development

  1. 1London Research and Development Centre, Agriculture and Agri-Food Canada, London, ON N5V 4T3, Canada
  2. 2Department of Biology, University of Western Ontario, London, ON N6A 5B7, Canada
  3. 3Department of Molecular Biology and Genetics, Aarhus University, Aarhus C DK-8000, Denmark

Abstract

Nitrogen-fixing root nodules develop as lateral organs on legume roots and their formation is restricted by autoregulation of nodulation (AON), a systemic mechanism with unclear evolutionary origins. We identify Lotus japonicus NUCLEAR FACTOR Y subunit A4 (NF-YA4) gene as a central target of the leucine-rich repeat receptor kinase HAR1, which controls both AON and root system architecture. Under nonsymbiotic conditions, HAR1 suppresses expression of NF-YA4 and its close paralog NF-YA1, at least in part through a miR169-dependent mechanism, mirroring the Arabidopsis CLAVATA1/2-miR169-NF-YA module. Loss of HAR1 leads to NF-YA4 overexpression, broad transcriptional reprogramming, and induction of LATERAL ORGAN BOUNDARIES DOMAIN, STYLISH, and YUCCA auxin biosynthesis genes, enhancing auxin signaling and lateral root development. Grafting experiments show that HAR1 constrains NF-YA4-mediated branching both locally in roots and systemically from shoots. Because NF-YA4 functions partly redundantly with NF-YA1 to mediate nodule emergence, our results suggest a model in which duplication and neofunctionalization of an ancestral NF-YA-dependent pathway controlling lateral root development facilitated its recruitment to the nodulation program. They also raise the possibility that AON could have evolved, at least in part, through the co-option of a LRR-RK/miR169/NF-YA regulatory module that limited lateral root development.

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BibTeX
@article{therrien2026har1,
  title = {{HAR1 receptor kinase links nodule autoregulation with repression of auxin signaling and lateral root development}},
  author = {Jasmine A. Therrien and Terry Huebert and Preetam Janakirama and Emine Kaplanoglu and Lavinia I. Fechete and Susanne Kohalmi and Stig U. Andersen and Jens Stougaard and Loretta Ross and Krzysztof Szczyglowski},
  journal = {Proceedings of the National Academy of Sciences of the United States of America},
  year = {2026},
  month = oct,
  doi = {10.1073/pnas.2619141123},
  url = {https://doi.org/10.1073/pnas.2619141123},
  note = {CC BY-NC-ND 4.0},
}
RIS
TY  - JOUR
TI  - HAR1 receptor kinase links nodule autoregulation with repression of auxin signaling and lateral root development
AU  - Jasmine A. Therrien
AU  - Terry Huebert
AU  - Preetam Janakirama
AU  - Emine Kaplanoglu
AU  - Lavinia I. Fechete
AU  - Susanne Kohalmi
AU  - Stig U. Andersen
AU  - Jens Stougaard
AU  - Loretta Ross
AU  - Krzysztof Szczyglowski
PY  - 2026
DA  - 2026/10/30
JO  - Proceedings of the National Academy of Sciences of the United States of America
DO  - 10.1073/pnas.2619141123
UR  - https://doi.org/10.1073/pnas.2619141123
AB  - Nitrogen-fixing root nodules develop as lateral organs on legume roots and their formation is restricted by autoregulation of nodulation (AON), a systemic mechanism with unclear evolutionary origins. We identify Lotus japonicus NUCLEAR FACTOR Y subunit A4 (NF-YA4) gene as a central target of the leucine-rich repeat receptor kinase HAR1, which controls both AON and root system architecture. Under nonsymbiotic conditions, HAR1 suppresses expression of NF-YA4 and its close paralog NF-YA1, at least in part through a miR169-dependent mechanism, mirroring the Arabidopsis CLAVATA1/2-miR169-NF-YA module. Loss of HAR1 leads to NF-YA4 overexpression, broad transcriptional reprogramming, and induction of LATERAL ORGAN BOUNDARIES DOMAIN, STYLISH, and YUCCA auxin biosynthesis genes, enhancing auxin signaling and lateral root development. Grafting experiments show that HAR1 constrains NF-YA4-mediated branching both locally in roots and systemically from shoots. Because NF-YA4 functions partly redundantly with NF-YA1 to mediate nodule emergence, our results suggest a model in which duplication and neofunctionalization of an ancestral NF-YA-dependent pathway controlling lateral root development facilitated its recruitment to the nodulation program. They also raise the possibility that AON could have evolved, at least in part, through the co-option of a LRR-RK/miR169/NF-YA regulatory module that limited lateral root development.
SN  - 0027-8424
SN  - 1091-6490
ER  -