Distinct mechanisms orchestrate the contra-polarity of IRK and KOIN, two LRR-receptor-kinases controlling root cell division

Abstract

In plants, cell polarity plays key roles in coordinating developmental processes. Despite the characterization of several polarly localized plasma membrane proteins, the mechanisms connecting protein dynamics with cellular functions often remain unclear. Here, we introduce a polarized receptor, KOIN, that restricts cell divisions in the Arabidopsis root meristem. In the endodermis, KOIN polarity is opposite to IRK, a receptor that represses endodermal cell divisions. Their contra-polar localization facilitates dissection of polarity mechanisms and the links between polarity and function. We find that IRK and KOIN are recognized, sorted, and secreted through distinct pathways. IRK extracellular domains determine its polarity and partially rescue the mutant phenotype, whereas KOIN’s extracellular domains are insufficient for polar sorting and function. Endodermal expression of an IRK/KOIN chimera generates non-cell-autonomous misregulation of root cell divisions that impacts patterning. Altogether, we reveal two contrasting mechanisms determining these receptors’ polarity and link their polarity to cell divisions in root tissue patterning.

Asymmetric cell division in plant development

“…Two LRR‐RLK pseudo‐kinases, KOIN and INFLORESCENCE AND ROOT APICES RECEPTOR KINASE (IRK), show contrasting polar localization in the Arabidopsis root meristem (Campos et al, 2020; Rodriguez‐Furlan et al, 2022). In the endodermis, IRK localizes to the outer domain, while KOIN accumulates in the inner domain of the plasma membrane (Rodriguez‐Furlan et al, 2022). In irk or koin mutants, excessive cell divisions are produced in the ground tissue stem cells and endodermis, implying that IRK and KOIN perceive bi‐directional cues to repress specific cell division and to coordinate patterning across the entire root meristem (Rodriguez‐Furlan et al, 2022).…”

The sorting of cargo proteins in the plant trans-Golgi network

“…These different de novo pathways have also been demonstrated using BFA and Endosidin16 in combination with or without the protein synthesis inhibitor cycloheximide. Trafficking of IRK is compromised with BFA but not Endosidin16, whereas that of KOIN is sensitive to Endosidin16 but not BFA ( Rodriguez-Furlan et al, 2022 ). Interestingly, the PM targeting of both IRK and KOIN is also compromised with Endosidin2 ( Rodriguez-Furlan et al, 2022 ).…”

“…Trafficking of IRK is compromised with BFA but not Endosidin16, whereas that of KOIN is sensitive to Endosidin16 but not BFA ( Rodriguez-Furlan et al, 2022 ). Interestingly, the PM targeting of both IRK and KOIN is also compromised with Endosidin2 ( Rodriguez-Furlan et al, 2022 ). Endosidin2 inhibits exocytosis by binding the EXOCYST subunit EXO70A1 that plays important roles in targeted secretion and tethering at the PM ( Zhang et al, 2016 ).…”

Mechanical forces in extendable tissue matrix orient cell divisions via microtubule stabilization inArabidopsis

“…The copyright holder for this preprint this version posted January 16, 2023. ; https://doi.org/10.1101/2023.01.16.524206 doi: bioRxiv preprint Willemsen et al, 2008;van Damme et al, 2011;De Rybel et al, 2013;Yoshida et al, 2014;Rodriguez-Furlan et al, 2022). However, such developmental cues only mildly affect the division plane switch after cell ablation (Marhava et al, 2019), suggesting a greater importance of alternative factors driving division plane selection in the root.…”

“…Developmental cues may override the division plane selection through gene expression or localisation of polarity-defining proteins, e.g. during formative divisions in stem cells and throughout embryo development (Helariutta et al, 2000;Heidstra, Welch and Scheres, 2004;Willemsen et al, 2008;van Damme et al, 2011;De Rybel et al, 2013;Yoshida et al, 2014;Rodriguez-Furlan et al, 2022). However, such developmental cues only mildly affect the division plane switch after cell ablation (Marhava et al, 2019), suggesting a greater importance of alternative factors driving division plane selection in the root.…”