Evolutionary analysis of theLORELEIgene family in plants reveals regulatory subfunctionalization

Abstract

A signaling complex comprising members of the LORELEI (LRE)-LIKE GPI-anchored protein (LLG) and Catharanthus roseus RECEPTOR-LIKE KINASE 1-LIKE (CrRLK1L) families perceive RAPID ALKALINIZATION FACTOR (RALF) peptides and regulate growth, reproduction, immunity, and stress responses in Arabidopsis (Arabidopsis thaliana). Genes encoding these proteins are members of multi-gene families in most angiosperms and could generate thousands of signaling complex variants. However, the links between expansion of these gene families and the functional diversification of this critical signaling complex as well as the evolutionary factors underlying the maintenance of gene duplicates remain unknown. Here, we investigated LLG gene family evolution by sampling land plant genomes and explored the function and expression of angiosperm LLGs. We found that LLG diversity within major land plant lineages is primarily due to lineage specific duplication events, and that these duplications occurred both early in the history of these lineages and more recently. Our complementation and expression analyses showed that expression divergence (i.e., regulatory subfunctionalization), rather than functional divergence, explains the retention of LLG paralogs. Interestingly, all but one monocot and all eudicot species examined had an LLG copy with preferential expression in male reproductive tissues, while the other duplicate copies showed highest levels of expression in female or vegetative tissues. The single LLG copy in Amborella trichopoda is expressed vastly higher in male compared to in female reproductive or vegetative tissues. We propose that expression divergence plays an important role in retention of LLG duplicates in angiosperms.

A RALF-Brassinosteroid morpho-signaling circuit regulates Arabidopsis hypocotyl cell shape

“…These observations suggest that FER function in regulating hypocotyl cell morphology and BR signaling is primarily achieved by RALF perception and that MalA-mediated pectin sensing has a minor role in this context. To confirm these observations, we analyzed llg1-2 , a loss of function mutant of LORELEI-LIKE GPI-ANCHORED 1 ( LLG1 ) which encodes for the main RALF co-receptor in vegetative tissues (Li et al 2015; Xiao et al 2019; Noble et al 2022). We observed that loss of LLG1 leads to defects in hypocotyl epidermal cell morphology that are reminiscent of fer-4 (Figure S5 A-B).…”

Role of a LORELEI- like gene from Phaseolus vulgaris during a mutualistic interaction with Rhizobium tropici

“…Thus, expression of the LLG1 and LLG2 genes of P. vulgaris and A. thaliana are very similar, indicating similar roles. Differential expression of LLG proteins and their interaction with its tissue-specific ligands have been proposed to determine the wide variety of responses involving CrRLK receptors [24].…”

“…LORELEI (LRE) or LORELEI-like (LLG) proteins act as chaperones and coreceptors for FER [17]. In the Arabidopsis genome, there is one LRE gene (AtLRE1), and three LLG genes (AtLLG1, AtLLG2, and AtLLG3) [22][23][24]. AtLRE1 is expressed only in the synergid, egg, and central cells of the female gametophyte cells [25,26].…”

Rapid alkalinization factor: function, regulation, and potential applications in agriculture

“…Various proteins were found as co-receptors of Cr RLK1Ls, involved in the recognition and binding of RALFs (Ge, et al 2019 ; Stegmann, et al 2017b ; Xiao, et al 2019 ). The protein LRE, and its homolog LLG assist in the structural stabilization and modification of FER, thereby controlling the location and timing of FER transduction signals (Li, et al 2015 ; Liu, et al 2016 ; Noble, et al 2022 ; Xiao, et al 2019 ). The protein LLG1 acts as a co-receptor for FER and assists in transporting FER from the endoplasmic reticulum to the cell membrane surface (Li, et al 2015 ).…”