Dual regulation of the receptor-like kinase BIR1 involves site-directed transcript cleavage and 5’-leader-mediated translational control
5 affiliations
- 1Centro de Investigaciones Biológicas Margarita Salas. Consejo Superior de Investigaciones Científicas, Ramiro de Maeztu, Madrid, Spain
- 2Doctorado en Biotecnología y Recursos Genéticos de Plantas y Microorganismos Asociados, Universidad Politécnica de Madrid, Madrid, Spain
- 3Department of Plant Molecular Genetics. Centro Nacional de Biotecnología, Consejo Superior de Investigaciones Científicas, Darwin, Madrid, Spain
- 4State Key Laboratory of Hybrid Rice, Hubei Provincial Research Center for Basic Biological Sciences, Hubei Hongshan Laboratory, RNA Institute, Institute for Advanced Studies (IAS), Wuhan University, Wuhan, Hubei, China
- 5Instituto de Hortofruticultura Subtropical y Mediterránea La Mayora (IHSM-UMA-CSIC), Boulevard Louis Pasteur, Málaga, Spain
Abstract
In Arabidopsis, BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE 1 (BAK1)-INTERACTING RECEPTOR-LIKE KINASE 1 (BIR1) is a negative regulator of plant immunity and cell death. BIR1 was earlier described as a target of epigenetic and post-transcriptional degradation. During virus infections, degradome analysis of BIR1 transcripts mapped predominant mRNA cleavage sites at the 5’-untranslated leader region (site A) and the protein-coding sequence (sites B and C). Here, we identified another virus-associated cleavage site (D) within the BIR1 coding region and investigated the contribution of site-directed mRNA cleavage to BIR1 regulation. Mutations at B, C, and D sites enhanced mRNA stability by impairing transcript cleavage, resulting in increased BIR1 mRNA and protein accumulation. This regulation is disrupted in RNA silencing mutants, supporting a model of cis-directed small interfering RNA (siRNA)-mediated degradation. We next demonstrate that virus infection reduces BIR1 translation in Arabidopsis. Furthermore, our data reveal a repressive role for the 5’-leader in regulating BIR1 translation, potentially mediated by upstream open reading frames (uORFs) and a virus-responsive long non-coding RNA (lncRNA) derived from the natural antisense At4g39838 locus. Together, these findings reveal a multilayered regulatory mechanism that integrates sRNA-mediated cleavage with translational control, with broader implications for the fine-tuning of stress-responsive gene expression during infection. Author summary: Plants must tightly control immune responses to ensure effective defense while avoiding immune-associated self-damage. In Arabidopsis thaliana, the receptor-like kinase BIR1 functions as a negative regulator of multiple immune resistance pathways. Previous reports have shown that misregulation of BIR1 leads to cell-death-like phenotypes, underscoring the need for precise control of its expression. However, the mechanisms governing BIR1 expression have remained largely unexplored. Here, we show that BIR1 transcripts are subject to post-transcriptional gene silencing and, through mutational analysis, identify the precise cleavage sites involved. In addition, we demonstrate that virus infection compromises BIR1 translation efficiency and reveal a previously uncharacterized translational control mechanism mediated by the BIR1 5’- leader, involving the combined action of multiple upstream open reading frames and a virus-responsive long non-coding RNA derived from the antisense At4g39838 locus. These findings reveal an unexpected and sophisticated regulatory architecture controlling BIR1 expression, with potential relevance for the broader BIR receptor family and plant immune signaling networks.
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BibTeX
@article{guzmanbenito2026dual,
title = {{Dual regulation of the receptor-like kinase BIR1 involves site-directed transcript cleavage and 5’-leader-mediated translational control}},
author = {Irene Guzmán-Benito and Carmen Robinson and Livia Donaire and Lourdes Fernández-Calvino and José Manuel Franco-Zorrilla and Ruixia Niu and Guoyong Xu and Catharina Merchante and César Llave},
journal = {PLOS Pathogens},
year = {2026},
month = sep,
doi = {10.1371/journal.ppat.1014571},
url = {https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014571},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Dual regulation of the receptor-like kinase BIR1 involves site-directed transcript cleavage and 5’-leader-mediated translational control
AU - Irene Guzmán-Benito
AU - Carmen Robinson
AU - Livia Donaire
AU - Lourdes Fernández-Calvino
AU - José Manuel Franco-Zorrilla
AU - Ruixia Niu
AU - Guoyong Xu
AU - Catharina Merchante
AU - César Llave
PY - 2026
DA - 2026/09/15
JO - PLOS Pathogens
DO - 10.1371/journal.ppat.1014571
UR - https://journals.plos.org/plospathogens/article?id=10.1371/journal.ppat.1014571
AB - In Arabidopsis, BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE 1 (BAK1)-INTERACTING RECEPTOR-LIKE KINASE 1 (BIR1) is a negative regulator of plant immunity and cell death. BIR1 was earlier described as a target of epigenetic and post-transcriptional degradation. During virus infections, degradome analysis of BIR1 transcripts mapped predominant mRNA cleavage sites at the 5’-untranslated leader region (site A) and the protein-coding sequence (sites B and C). Here, we identified another virus-associated cleavage site (D) within the BIR1 coding region and investigated the contribution of site-directed mRNA cleavage to BIR1 regulation. Mutations at B, C, and D sites enhanced mRNA stability by impairing transcript cleavage, resulting in increased BIR1 mRNA and protein accumulation. This regulation is disrupted in RNA silencing mutants, supporting a model of cis-directed small interfering RNA (siRNA)-mediated degradation. We next demonstrate that virus infection reduces BIR1 translation in Arabidopsis. Furthermore, our data reveal a repressive role for the 5’-leader in regulating BIR1 translation, potentially mediated by upstream open reading frames (uORFs) and a virus-responsive long non-coding RNA (lncRNA) derived from the natural antisense At4g39838 locus. Together, these findings reveal a multilayered regulatory mechanism that integrates sRNA-mediated cleavage with translational control, with broader implications for the fine-tuning of stress-responsive gene expression during infection. Author summary: Plants must tightly control immune responses to ensure effective defense while avoiding immune-associated self-damage. In Arabidopsis thaliana, the receptor-like kinase BIR1 functions as a negative regulator of multiple immune resistance pathways. Previous reports have shown that misregulation of BIR1 leads to cell-death-like phenotypes, underscoring the need for precise control of its expression. However, the mechanisms governing BIR1 expression have remained largely unexplored. Here, we show that BIR1 transcripts are subject to post-transcriptional gene silencing and, through mutational analysis, identify the precise cleavage sites involved. In addition, we demonstrate that virus infection compromises BIR1 translation efficiency and reveal a previously uncharacterized translational control mechanism mediated by the BIR1 5’- leader, involving the combined action of multiple upstream open reading frames and a virus-responsive long non-coding RNA derived from the antisense At4g39838 locus. These findings reveal an unexpected and sophisticated regulatory architecture controlling BIR1 expression, with potential relevance for the broader BIR receptor family and plant immune signaling networks.
SN - 1553-7374
ER -