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Abstract Oriented cell divisions establish plant tissue and organ patterning and produce different cell types; this is particularly true of the highly organized Arabidopsis (Arabidopsis thaliana) root meristem. Mutant alleles of INFLORESCENCE AND ROOT APICES RECEPTOR KINASE (IRK) exhibit excess cell divisions in the root endodermis. IRK is a transmembrane receptor kinase that localizes to the outer polar domain of these cells, suggesting that directional signal perception is necessary to repress endodermal cell division. Here, a detailed examination revealed many of the excess endodermal divisions in irk have division planes that specifically skew toward the outer lateral side. Therefore, we termed them “outward askew” divisions. Expression of an IRK truncation lacking the kinase domain retains polar localization and prevents outward askew divisions in irk; however, the roots exhibit excess periclinal endodermal divisions. Using cell identity markers, we show that the daughters of outward askew divisions transition from endodermal to cortical identity similar to those of periclinal divisions. These results extend the requirement for IRK beyond repression of cell division activity to include cell division plane positioning. Based on its polarity, we propose that IRK at the outer lateral endodermal cell face participates in division plane positioning to ensure normal root ground tissue patterning.
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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.
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- Award ID(s):
- 1751385
- PAR ID:
- 10378952
- Publisher / Repository:
- Nature Publishing Group
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 13
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Polarity of plasma membrane proteins is essential for cell morphogenesis and control of cell division and, thus, influences organ and whole plant development. In Arabidopsis (Arabidopsis thaliana) root endodermal cells, 2 transmembrane kinases, INFLORESCENCE AND ROOT APICES RECEPTOR KINASE (IRK) and KINASE ON THE INSIDE (KOIN), accumulate at opposite lateral domains. Their polarization is tightly linked to their activities regulating cell division and ground tissue patterning. The polarization of IRK and KOIN relies solely on the secretion of newly synthesized protein. However, the secretion machinery by which their opposite, lateral polarity is achieved remains largely unknown. Here, we show that different sets of ADP-ribosylation factor (ARF)-guanine-nucleotide exchange factors (ARF-GEFs) mediate their secretion. ARF-GEF GNOM-like-1 (GNL1) regulates KOIN secretion to the inner polar domain, thereby directing KOIN sorting early in the secretion pathway. For IRK, combined chemical and genetic analyses showed that the ARG-GEF GNL1, GNOM, and the BREFELDIN A-INHIBITED-GUANINE NUCLEOTIDE-EXCHANGE FACTORs 1 to 4 (BIG1-BIG4) collectively regulate its polar secretion. The ARF-GEF-dependent mechanisms guiding IRK or KOIN lateral polarity were active across different root cell types and functioned regardless of the protein's inner/outer polarity in those cells. Therefore, we propose that specific polar trafficking of IRK and KOIN occurs via distinct mechanisms that are not constrained by cell identity or polar axis and likely rely on individual protein recognition.more » « less
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