Three RLKs integrate SHR-SCR and gibberellins to regulate root ground tissue patterning in Arabidopsis thaliana

Curr Biol. 2024 Oct 25:S0960-9822(24)01342-3. doi: 10.1016/j.cub.2024.09.074. Online ahead of print.

Abstract

Precise regulation of cell division is essential for proper tissue patterning in multicellular organisms. In Arabidopsis, the ground tissue (GT) comprises cortex and endodermis in the early stages of root development. During GT maturation, additional periclinal cell divisions (PCDs) occasionally occur of the endodermis, generating a middle cortex (MC) layer between the cortex and endodermis. Although several regulatory proteins and phytohormones were identified to mediate GT patterning, such as SHORT-ROOT (SHR), SCARECROW (SCR), CYCLIND6;1 (CYCD6;1), and gibberellins (GAs), the interrelationship among these factors is not elucidated. Here, we report that three closely related receptor-like kinases (RLKs), ARH1, FEI1, and FEI2, play crucial roles in mediating a signal transduction pathway from the SHR-SCR module to GA to regulate GT patterning. Two independent triple mutants of these RLKs (tri-1 and tri-2) exhibit increased MC formation compared with wild type. Genetic analysis indicated that all three RLKs regulate MC formation mainly in a cell-autonomous manner. The transcription levels of these RLKs are negatively controlled by SHR and SCR. The altered GT patterns in shr and scr can be partially complemented by tri-1. GA biosynthesis is significantly reduced in the roots of tri-1. The excessive MC formation in tri-1 can be greatly suppressed by the exogenous application of GA3 or by the mutation of CYCD6;1. Our results demonstrate a signaling pathway involving SHR/SCR-ARH1/FEI1/FEI2-GA-CYCD6;1 to govern GT patterning in Arabidopsis thaliana.

Keywords: ARH1; FEI1; FEI2; gibberellin; ground tissue; middle cortex; periclinal cell division; receptor-like kinase.