AtJAC1 Regulates Nuclear Accumulation of GRP7, Influencing RNA Processing of FLC Antisense Transcripts and Flowering Time in Arabidopsis

Abstract

Lectins selectively recognize sugars or glycans for defense in living cells, but less is known about their roles in the development process and the functional network with other factors. Here, we show that Arabidopsis (Arabidopsis thaliana) JACALIN-LECTIN LIKE1 (AtJAC1) functions in flowering time control. Loss of function of AtJAC1 leads to precocious flowering, whereas overexpression of AtJAC1 causes delayed flowering. AtJAC1 influences flowering through regulation of the key flowering repressor gene FLOWERING LOCUS C (FLC). Genetic analysis revealed that AtJAC1's function is mostly dependent on GLYCINE-RICH RNA-BINDING PROTEIN7 (GRP7), an upstream regulator of FLC. Biochemical and cell biological data indicated that AtJAC1 interacted physically with GRP7 specifically in the cytoplasm. AtJAC1 influences the nucleocytoplasmic distribution of GRP7, with predominant nuclear localization of GRP7 when AtJAC1 function is lost but retention of GRP7 in the cytoplasm when AtJAC1 is overexpressed. A temporal inducible assay suggested that AtJAC1's regulation of flowering could be compromised by the nuclear accumulation of GRP7. In addition, GRP7 binds to the antisense precursor messenger RNA of FLC through a conserved RNA motif. Loss of GRP7 function leads to the elevation of total FLC antisense transcripts and reduced proximal-distal polyadenylation ratio, as well as histone methylation changes in the FLC gene body region and increased total functional sense FLC transcript. Attenuating the direct binding of GRP7 with competing artificial RNAs leads to changes of FLC antisense precursor messenger RNA processing and flowering transition. Taken together, our study indicates that AtJAC1 coordinates with GRP7 in shaping plant development through the regulation of RNA processing in Arabidopsis.

Genome‐Wide Screening for Lectin Motifs in Arabidopsis thaliana

“…The jacalin homolog AtJAC1 (AT3G16470) plays a role in controlling the flowering time of A. thaliana . AtJAC1 regulates the expression of the repressor gene flowering locus C through interaction with glycine‐rich RNA‐binding protein 7 and as such influences the flowering time (Xiao et al, 2015). The jacalin homolog–restricted tobacco etch potyvirus movement 1 (RTM1, AT1G05760) restricts the long‐distance movement of tobacco etch potyvirus in the phloem by acting together with the nonlectin proteins RTM2 and RTM3.…”

Overexpression of a flower‐specific aerolysin‐like protein from the dioecious plant Rumex acetosa alters flower development and induces male sterility in transgenic tobacco

“…A lectin receptor-like kinase (lectin RLK) in which the lectin domain is coupled with a serine/threonine kinase domain has been found to play a critical role in Arabidopsis pollen development (Wan et al, 2008). Jacalin-Lectin-like proteins are mainly involved in jasmonic acid-mediated defence responses (Xiang et al, 2011), but it was recently found that Arabidopsis JACALIN-LECTIN LIKE1 (AtJAC1) regulates flowering time (Xiao et al, 2015), as previously demonstrated for the wheat JACALIN-like lectin VER2 (Yong et al, 2003).…”

RNA Splicing of FLC Modulates the Transition to Flowering

“…As a result, this proximal polyadenylation inhibits the transcription of FLC through triggering H3K4me2 demethylation in the FLC locus (Marquardt et al, 2014). A few 3′-end processing factors containing RNA-recognition motifs, such as flowering control locus a (FCA) and FPA, glycine-rich rna-binding protein7 (GRP7), cleavage stimulation factor 64 (CstF64), CstF77, and nuclear speckle RNA binding protein a (NSRa), affect the splice site selection and polyadenylation site usage of COOLAIR transcripts, leading to an altered ratio of proximal-distal spliced variants (Liu et al, 2007;Streitner et al, 2008;Liu et al, 2010;Hornyik et al, 2010;Streitner et al, 2012;Xiao et al, 2015;Bazin et al, 2018). Loss-of-function mutations in these factors decrease or increase the usage of COOLAIR proximal polyadenylation site, leading to upregulated or downregulated FLC transcription.…”

“…Two classes of COOLAIR transcripts bind to FCA and recruit PRC2 complex to FLC locus (Tian et al, 2019). The class I variants with proximal polyadenylation and the proximal-distal ratio of COOLAIR transcripts effect the histone methylation of H3K4me2, H3K36me3 and H3K27me3 (Marquardt et al, 2014;Berry and Dean, 2015;Xiao et al, 2015;Rosa et al, 2016). The class II COOLAIR transcripts with distal polyadenylation influence the degree of capping of the FLC nascent transcripts (Li et al, 2015).…”