https://orcid.org/0000-0003-2897-1485
All eukaryotes rely on cell-surface receptors to sense the extracellular environment and transduce stimuli-derived signals into cytosolic responses. In plants, receptor kinases (RKs) represent the largest family of such receptors, which perceive self- or non-self-derived ligands to regulate diverse cellular processes. RKs are divided into numerous families based on the motifs present in their extracellular ligand-binding domains. For example, the Catharanthus roseus RLK1-like (CrRLK1L) family of RKs is characterized by malectin-like extracellular domains, which allow the perception of plant cysteine-rich peptides of the RAPID ALKALINIZATION FACTOR (RALF) family (Zhu et al., 2021).
The model plant Arabidopsis thaliana possesses 17 CrRLK1Ls, the best-studied of which is FERONIA (FER). FER was named for the Etruscan goddess of fertility due to its important role in reproduction (Escobar-Restrepo et al., 2007), and extensive study has since revealed that FER perceives multiple RALFs to regulate numerous processes involved in growth, development, and immunity (Haruta et al., 2014; Xiao et al., 2019). Previous work has generally studied the individual genetic and/or biochemical roles of FER and its ligands in isolation, leaving a knowledge gap in integrated, large-scale datasets.
In the current issue, Ping Wang and colleagues (Wang et al., 2022) deployed an elegant multi-omics approach to study fer mutant plants (see Figure). The authors quantitatively analyzed the transcriptomes and proteomes of wild-type Col-0 and fer mutants using RNAseq and liquid chromatography tandem mass spectrometry. In addition to analyzing protein abundance using tandem mass tag labeling, the authors also identified phosphorylation sites by TiO2 enrichment for phosphopeptides. These efforts achieved excellent coverage of the proteome, with over 8,000 proteins and nearly 12,000 phosphosites identified.
Multi-omics-based analysis of the fer mutant transcriptome and proteome. RNAseq and proteomics were performed on rosettes of adult plants. Transcripts, protein abundance, and phosphosites that were differentially detected in WT versus fer plants are indicated. Adapted from Wang et al. (2022), Figure 1 and Supplemental Figure S2. Figure created with BioRender.com.
In accord with the many striking phenotypes of fer plants, the authors observed massive transcriptional and post-translational reprogramming of fer compared with wild-type plants (see Figure). Using gene ontology term analyses, the multi-omics approach implicated FER in stress responses and hormone signaling, in keeping its known roles (Zhu et al., 2021). Additionally, this approach uncovered potential roles for FER in negatively regulating endoplasmic reticulum body formation and glucosinolate biosynthesis. The multi-omics approach also provided insights into known FER functions, such as its regulation of abscisic acid signaling. Given the strong developmental phenotypes of fer plants, a challenge of such steady-state analyses is the delineation of direct versus indirect effects of FER loss. However, the authors were able to confirm that at least several proteins that were differentially phosphorylated in fer could serve as FER substrates in vitro, suggesting that these may represent bona fide FER targets.
RALF peptides form a large family, and perception of many RALFs is at least partially FER-dependent (Abarca et al., 2021), further underscoring that FER plays a central role in integrating many signaling pathways. Multi-omics fer datasets will provide an excellent foundation for future studies into the functions of this key RK and its ligands, and similar analyses using dynamic ligand treatments and/or in response to different stimuli will be instrumental to clarifying the role of FER in specific signaling pathways.
