RALF1-FERONIA complex affects splicing dynamics to modulate stress responses and growth in plants

Abstract

The environmentally responsive signaling pathways that link global transcriptomic changes through alternative splicing (AS) to plant fitness remain unclear. Here, we found that the interaction of the extracellular rapid alkalinization FACTOR 1 (RALF1) peptide with its receptor FERONIA (FER) triggered a rapid and massive RNA AS response by interacting with and phosphorylating glycine-rich RNA binding protein7 (GRP7) to elevate GRP7 nuclear accumulation in Arabidopsis thaliana. FER-dependent GRP7 phosphorylation enhanced its mRNA binding ability and its association with the spliceosome component U1-70K to enable splice site selection, modulating dynamic AS. Genetic reversal of a RALF1-FER–dependent splicing target partly rescued mutants deficient in GRP7. AS of GRP7 itself induced nonsense-mediated decay feedback to the RALF1-FER-GRP7 module, fine-tuning stress responses, and cell growth. The RALF1-FER-GRP7 module provides a paradigm for regulatory mechanisms of RNA splicing in response to external stimuli.

Protein kinases in plant responses to drought, salt, and cold stress

“…Type 2C protein phosphatases indirectly inhibit OST1 activity via the dephosphorylation of its activation loop (Umezawa et al, 2009; Vlad et al, 2009) and ABA or osmotic stress activates SnRK2s. However, OST1 activity cannot be detected in higher‐order pp2c mutants under normal conditions (Brandt et al, 2015; Wang et al, 2018b), suggesting that OST1 activation requires additional proteins. An early study in the moss P. patens indicated that the ABA and abiotic stress‐responsive Raf‐like kinase (ARK), which belongs to the B3 group of Raf‐like MAPKKKs, participates in ABA and hyperosmotic stress signaling by regulating the activity of SnRK2s (Saruhashi et al, 2015).…”

RALF–FERONIA Signaling: Linking Plant Immune Response with Cell Growth

“…Recently, the roles of Cr RLK1L proteins in regulating agronomic traits have begun to be appreciated in crop species ( Table 1 ). In general, Cr RLK1L proteins play versatile roles in plant growth and development, reproduction, hormone signaling, stress responses, immunity ( Escobar-Restrepo et al., 2007 ; Guo et al., 2009 , 2018 ; Duan et al., 2010 , 2014 ; Yu et al., 2012 , 2014 ; Haruta et al., 2014 ; Li et al., 2015 , 2016a ; Mao et al., 2015 ; Chen et al., 2016 ; Du et al., 2016 ; Ge et al., 2017 , 2019 ; Mecchia et al., 2017 ; Stegmann et al., 2017 ; Chakravorty et al., 2018 ; Feng et al., 2018 ; Franck et al., 2018 ; Gonneau et al., 2018 ; Hansen et al., 2019 ; Wang et al., 2020a ; Zhou and Zhang, 2020 ), energy production and RNA metabolism ( Xu et al., 2019 ; Zhu et al., 2020a ; Wang et al., 2020b ).…”

“…In the cytoplasm, the RALF1–FER complex also uses the small G-protein pathway to regulate auxin responses and root hair growth ( Duan et al., 2010 ) as well as abscisic acid (ABA) responses ( Yu et al., 2012 ; Chen et al., 2016 ). FER also monitors the carbon/nitrogen (C/N) balance by interacting with ATL6 ( Xu et al., 2019 ), regulates mRNA alternative splicing by phosphorylating the RNA-binding protein glycine-rich protein 7 (GRP7) to modulate plant fitness and flowering time ( Wang et al., 2020a , 2020b ) and promotes protein synthesis and polar cell growth by phosphorylating eIF4E1 ( Zhu et al., 2020a ). The RALF1–FER complex uses a “shortcut” mechanism to directly regulate gene expression by phosphorylating a DNA-binding protein, namely ErbB3-binding protein 1 (EBP1) ( Li et al., 2018 ).…”

Versatile Roles of the Receptor-Like Kinase Feronia in Plant Growth, Development and Host-Pathogen Interaction

“…Recently, it was demonstrated that the interaction of FER with RALF1 resulted in the phosphorylation of the GLYCINE-RICH RNA-BINDING PROTEIN 7 (GRP7) to promote GRP7 nuclear accumulation, thus triggering a rapid and massive RNA alternative splicing response. GRP7 phosphorylation enhanced its mRNA binding ability and its association with the spliceosome component U1-70K, which depends on FER [ 68 ].…”