A conserved gene regulatory network controls root epidermal cell patterning in superrosid species

Abstract

In superrosid species, root epidermal cells differentiate into root hair cells and non-hair cells. In some superrosids, the root hair cells and non-hair cells are distributed randomly (Type I pattern) and in others, they are arranged in a position-dependent manner (Type III pattern). The model plant Arabidopsis (Arabidopsis thaliana) adopts the Type III pattern, and the gene regulatory network (GRN) that controls this pattern has been defined. However, it is unclear whether the Type III pattern in other species is controlled by a similar GRN as in Arabidopsis, and it is not known how the different patterns evolved. In this study, we analyzed superrosid speciesRhodiola rosea,Boehmeria nivea, andCucumis sativusfor their root epidermal cell patterns. Combining phylogenetics, transcriptomics, and cross-species complementation, we analyzed homologs of the Arabidopsis patterning genes from these species. We identifiedR.roseaandB.niveaas Type III species andC.sativusas Type I species. We discovered substantial similarities in structure, expression, and function of Arabidopsis patterning gene homologs inR.roseaandB.nivea, and major changes inC.sativus. We propose that in superrosids, diverse Type III species inherited the patterning GRN from a common ancestor, whereas Type I species arose by mutations in multiple lineages.

Evolution of gene regulatory network architectures regulating root hair patterning in superrosid species

“…Like Arabidopsis, Rhodiola rosea (R. rosea) and Boehmeria nivea (B. nivea) exhibit the type III pattern (Dolan et al, 1994;Galway et al, 1994;Zhu & Schiefelbein, 2023). Consistent with this, they encode all relevant orthologs of the GRN regulating root hair patterning in Arabidopsis and their transcripts locate in roots (Zhu & Schiefelbein, 2023). Specifically, R. rosea encodes two RDH6like bHLH (RLB) proteins: RrRLB1 and RrRLB2.…”

“…Furthermore, like RHD6-GFP fusion proteins (Menand et al, 2007), the GFP signal of these constructs preferentially accumulates in differentiating hair epidermal cells (Zhu & Schiefelbein, 2023). These species also encode GL2-like-HD-Zip (GLH) proteins (Zhu & Schiefelbein, 2023): RrGLH1 and RrGHL2 in R. rosea and BnGLH in B. nivea. In Arabidopsis, gl2 mutants develop root hairs from essentially every root epidermal cell (Masucci et al, 1996;Hung et al, 1998).…”

“…These results are telling us that these WRL proteins repress root hair formation by inducing GL2 expression. Like WER-GFP fusion proteins (Ryu et al, 2005), the GFP signal of these constructs preferentially accumulates in differentiating hairless epidermal cells (Zhu & Schiefelbein, 2023). The cellular localization of the promoter induction of BnWRLs has been also investigated (Zhu & Schiefelbein, 2023): while that of the BnWRL2 gene overlaps with that of the WER gene in differentiating nonhair cells, the promoter of the BnWRL1 gene, unexpectedly, is induced in future hair cells.…”

“…Like WER-GFP fusion proteins (Ryu et al, 2005), the GFP signal of these constructs preferentially accumulates in differentiating hairless epidermal cells (Zhu & Schiefelbein, 2023). The cellular localization of the promoter induction of BnWRLs has been also investigated (Zhu & Schiefelbein, 2023): while that of the BnWRL2 gene overlaps with that of the WER gene in differentiating nonhair cells, the promoter of the BnWRL1 gene, unexpectedly, is induced in future hair cells. The simplest explanation is that BnWRL1 may be differently regulated when expressed in Arabidopsis (Zhu & Schiefelbein, 2023).…”

“…Rhodiola rosea and B. nivea also encode CPC-like (CPL) MYB proteins (Zhu & Schiefelbein, 2023). Specifically, R. rosea encodes RrCPL1 and RrCPL2 and B. nivea encodes BnCPL1 and BnCPL2, which cluster in a clade with CPC.…”