CONSTITUTIVE EXPRESSER OF PATHOGENESIS-RELATED GENES 5 is an RNA-binding protein controlling plant immunity via an RNA processing complex

Abstract

Plant innate immunity is capable of combating diverse and ever evolving pathogens. The plasticity of innate immunity could be boosted by RNA processing. Arabidopsis thaliana CONSTITUTIVE EXPRESSER OF PATHOGENESIS-RELATED GENES 5 (CPR5), a key negative immune regulator, is a component of the nuclear pore complex. Here we further identified CPR5 as a component of RNA processing complexes. Through genetic screening, we found that RNA splicing activator NineTeen Complex and RNA polyadenylation factor CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR, coordinately function downstream of CPR5 to activate plant immunity. CPR5 and these two regulators forms a complex that is localized in nuclear speckles, an RNA processing organelle. Intriguingly, we found that CPR5 is an RNA-binding protein belonging to the Transformer 2 (Tra2) subfamily of the serine/arginine-rich family. The RNA recognition motif of CPR5 protein binds the Tra2-targeted RNA sequence in vitro and is functionally replaceable by those of Tra2 subfamily proteins. In planta, it binds RNAs of CPR5-regulated alternatively spliced genes (ASGs) identified by RNA-seq. ARGONAUTE 1 (AGO1) is one of the ASGs and, consistent with this, the ago1 mutant suppresses the cpr5 phenotype. These findings reveal that CPR5 is an RNA-binding protein linking RNA processing with plant immunity.

GBPL3 localizes to the nuclear pore complex and functionally connects the nuclear basket with the nucleoskeleton in plants

“…It was reported that the Arabidopsis ORC nucleoporin Nup85 physically interacts with a key Mediator component MED18, which is required for the expression of abscisic acid- and salt stress-responsive genes [ 66 ]. Recently, the plant-specific transmembrane nucleoporin CPR5 was identified as a novel RNA-binding protein and may work in the pre-mRNA splicing and polyadenylation complex to regulate plant immune induction [ 67 ]. We showed that the NB component GBPL3 recruits chromatin modifiers, core transcription apparatus, and various TFs in vivo.…”

Transcriptional regulation of plant innate immunity

“…Upon ETI, CPR5 releases SIM and SMR1, which activate E2F TFs to induce PCD [ 103 ]. Finally, CPR5 regulates alternative splicing (AS; Figure 1 L) via its RNA-binding activity [ 105 ]. Interestingly, the mRNA of the gene-silencing-related AGO1 and several AS regulators are among its targets, suggesting that apart from its own role in AS, it also indirectly affects gene silencing and AS [ 105 ].…”

“…Finally, CPR5 regulates alternative splicing (AS; Figure 1 L) via its RNA-binding activity [ 105 ]. Interestingly, the mRNA of the gene-silencing-related AGO1 and several AS regulators are among its targets, suggesting that apart from its own role in AS, it also indirectly affects gene silencing and AS [ 105 ]. In addition, Exportin-4 (XPO4) mediates nuclear export of TOPLESS-RELATED1 (TPR1), counteracting the translocation of TPR1 into the nucleus during ETI in the presence of high SA levels, as was studied in the cpr5 background [ 106 ].…”

Function of Nuclear Pore Complexes in Regulation of Plant Defense Signaling

“…Meanwhile, data from the cpr5 RNA-sequencing indicate that CPR5 participates in the regulation of alternative splicing (AS). Hence, CPR5 may act as a component of LLPS [ 68 ] which is involved in the plant immune response [ 69 ]. Collaboratively, NUP54, NUP58, NUP88, and XPO4 cooperate with CPR5 to regulate the disease resistance, highlighting that the integrity of the NPC plays pivotal roles in immune signals.…”