Robinson Carmen, Guzmán-Benito Irene, Sede Ana Rocío, Elvira-González Laura, Hua Chenlei, Ciska Malgorzata, Nürnberger Thorsten, Heinlein Manfred, Llave César
Centro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas, Ramiro de Maeztu 9, 28040, Madrid, Spain.
Doctorado en Biotecnología y Recursos Genéticos de Plantas y Microorganismos Asociados, Universidad Politécnica de Madrid, 28040, Madrid, Spain.
New Phytol. 2025 Jul;247(2):813-829. doi: 10.1111/nph.70216. Epub 2025 May 23.
BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE 1 (BAK1)-INTERACTING RECEPTOR-LIKE KINASE (BIR) proteins are negative regulators of cell death and defense against microbes in Arabidopsis thaliana. Here, we demonstrate that the members of the BIR family function as negative regulators of antiviral resistance in Arabidopsis. We show that during tobacco rattle virus (TRV) infection, BIR1 and BIR3 gene expression is antagonistically regulated by salicylic acid and jasmonic acid signaling pathways. BIR1 and BIR3 negatively regulate TRV resistance via distinct mechanisms. Our data indicate that BIR1 modulates antiviral defense through mechanisms that include pattern-triggered immune (PTI) gene expression, plasmodesmata callose deposition alongside yet unidentified defense pathways independent of the receptor-like kinases BAK1 and SUPPRESSOR OF BIR1-1 1 (SOBIR1), or the lipase-like PHYTOALEXIN DEFICIENT 4 (PAD4). BIR3 negatively regulates a pathway that involves BAK1 and ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)/PAD4, suggesting that BIR3 disrupts an immune response similar to effector-triggered immunity (ETI) driven by nucleotide-binding leucine-rich intracellular receptors. This response helps control virus proliferation without causing a hypersensitive reaction. Our findings also reveal that BIR2 represses antiviral defense against TRV, highlighting the conserved function of BIR proteins as pivotal modulators in plant-virus interactions. We propose that the induction of BIR proteins during viral infection helps maintain a balance between defense activation and suppression to prevent viral overaccumulation and plant damage.
油菜素类固醇不敏感1相关受体激酶1(BAK1)相互作用的类受体激酶(BIR)蛋白是拟南芥细胞死亡和抗微生物防御的负调控因子。在此,我们证明BIR家族成员在拟南芥中作为抗病毒抗性的负调控因子发挥作用。我们表明,在烟草脆裂病毒(TRV)感染期间,BIR1和BIR3基因表达受水杨酸和茉莉酸信号通路的拮抗调控。BIR1和BIR3通过不同机制负调控TRV抗性。我们的数据表明,BIR1通过包括模式触发免疫(PTI)基因表达、胞间连丝胼胝质沉积以及独立于类受体激酶BAK1和BIR1-1 1抑制因子(SOBIR1)或脂酶样植物抗毒素缺陷4(PAD4)的尚未确定的防御途径等机制来调节抗病毒防御。BIR3负调控一条涉及BAK1和增强的疾病易感性1(EDS1)/PAD4的途径,这表明BIR3破坏了一种类似于由核苷酸结合富含亮氨酸的细胞内受体驱动的效应物触发免疫(ETI)的免疫反应。这种反应有助于控制病毒增殖而不引起超敏反应。我们的研究结果还揭示,BIR2抑制对TRV的抗病毒防御,突出了BIR蛋白作为植物-病毒相互作用中关键调节因子的保守功能。我们提出,病毒感染期间BIR蛋白的诱导有助于维持防御激活与抑制之间的平衡,以防止病毒过度积累和植物损伤。