Zooming in on cells reveals patterns on their outer surfaces. These patterns are actually a collection of distinct areas of the cell surface, each containing specific combinations of molecules. The outer layers of pollen grains consist of a cell wall, and a softer cell membrane that sits underneath. As a pollen grain develops, it recruits certain fats and proteins to specific areas of the cell membrane, known as ‘aperture domains’. The composition of these domains blocks the cell wall from forming over them, leading to gaps in the wall called ‘pollen apertures’. Pollen apertures can open and close, aiding reproduction and protecting pollen grains from dehydration. The number, location, and shape of pollen apertures vary between different plant species, but are consistent within the same species. In the plant species Arabidopsis thaliana , pollen normally develops three long and narrow, equally spaced apertures, but it remains unclear how pollen grains control the number and location of aperture domains. Zhou et al. found that mutations in two closely related A. thaliana proteins – ELMOD_A and MCR – alter the number and positions of pollen apertures. When A. thaliana plants were genetically modified so that they would produce different levels of ELMOD_A and MCR, Zhou et al. observed that when more of these proteins were present in a pollen grain, more apertures were generated on the pollen surface. This finding suggests that the levels of these proteins must be tightly regulated to control pollen aperture numbers. Further tests revealed that another related protein, called ELMOD_E, also has a role in domain formation. When artificially produced in developing pollen grains, it interfered with the activity of ELMOD_A and MCR, changing pollen aperture shape, number, and location. Zhou et al. identified a group of proteins that help control the formation of domains in the cell membranes of A. thaliana pollen grains. Further research will be required to determine what exactly these proteins do to promote formation of aperture domains and whether similar proteins control domain development in other organisms.
more »
« less
Molecular mechanisms of pollen aperture formation in Arabidopsis and rice
Abstract Apertures are specialized regions on the pollen surface that receive little to no exine deposition, forming distinct structures important for pollen function. Aperture number, shape, and positions vary widely across species, resulting in diverse, species-specific patterns that make apertures fascinating from both cell biological and evolutionary perspectives. Aperture formation requires developing pollen to establish polarity and define specific regions of the plasma membrane as aperture domains. In the decade or so since the discovery of the first aperture factor, INAPERTURATE POLLEN1 (INP1), pollen apertures have become a powerful model for investigating how cells form distinct plasma membrane domains. Recent studies in Arabidopsis and rice, two species with contrasting aperture patterns, have identified key molecular players that regulate aperture domain specification and development. In this review, we summarize these advances and discuss directions for future studies on the molecular mechanisms controlling aperture formation.
more »
« less
- Award ID(s):
- 2240972
- PAR ID:
- 10655932
- Editor(s):
- Melzer, Rainer
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 76
- Issue:
- 22
- ISSN:
- 0022-0957
- Page Range / eLocation ID:
- 6674 to 6682
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Dobritsa, Anna (Ed.)Abstract In plant cells, linkage between the cytoskeleton, plasma membrane, and cell wall is crucial for maintaining cell shape. In highly polarized pollen tubes, this coordination is especially important to allow rapid tip growth and successful fertilization. Class I formins contain cytoplasmic actin-nucleating formin homology domains as well as a proline-rich extracellular domain and are candidate coordination factors. Here, using Arabidopsis, we investigated the functional significance of the extracellular domain of two pollen-expressed class I formins: AtFH3, which does not have a polar localization, and AtFH5, which is limited to the growing tip region. We show that the extracellular domain of both is necessary for their function, and identify distinct O-glycans attached to these sequences, AtFH5 being hydroxyproline-arabinosylated and AtFH3 carrying arabinogalactan chains. Loss of hydroxyproline arabinosylation altered the plasma membrane localization of AtFH5 and disrupted actin cytoskeleton organization. Moreover, we show that O-glycans differentially affect lateral mobility in the plasma membrane. Together, our results support a model of protein sub-functionalization in which AtFH5 and AtFH3, restricted to specific plasma membrane domains by their extracellular domains and the glycans attached to them, organize distinct subarrays of actin during pollen tube elongation.more » « less
-
null (Ed.)Pollen grains show an enormous variety of aperture systems. What genes are involved in the aperture formation pathway and how conserved this pathway is in angiosperms remains largely unknown. INAPERTURATE POLLEN1 ( INP1 ) encodes a protein of unknown function, essential for aperture formation in Arabidopsis, rice and maize. Yet, because INP1 sequences are quite divergent, it is unclear if their function is conserved across angiosperms. Here, we conducted a functional study of the INP1 ortholog from the basal eudicot Eschscholzia californica ( EcINP1 ) using expression analyses, virus-induced gene silencing, pollen germination assay, and transcriptomics. We found that EcINP1 expression peaks at the tetrad stage of pollen development, consistent with its role in aperture formation, which occurs at that stage, and showed, via gene silencing, that the role of INP1 as an important aperture factor extends to basal eudicots. Using germination assays, we demonstrated that, in Eschscholzia , apertures are dispensable for pollen germination. Our comparative transcriptome analysis of wild-type and silenced plants identified over 900 differentially expressed genes, many of them potential candidates for the aperture pathway. Our study substantiates the importance of INP1 homologs for aperture formation across angiosperms and opens up new avenues for functional studies of other aperture candidate genes.more » « less
-
Abstract Cellular membranes provide a unique platform for interactions that drive emergent behaviors in protein dynamics and cellular signaling, distinct from those observed in solution. We investigated the proline‐rich region (PRR) and Src Homology 3 (SH3) domains of Bruton's tyrosine kinase (Btk) and its phase separation driven by the weak interactions of regulatory domains at membrane surfaces. Using supported lipid bilayers (SLBs) and giant unilamellar vesicles (GUVs), we demonstrate that membrane localization amplifies weak PRR‐SH3 interactions, enabling the formation of higher‐order assemblies and phase‐separated condensates. These assemblies, previously undescribed by solution‐state studies, are supported by reductions in the lateral diffusion of membrane‐bound Btk molecules and the stabilization of reversible condensates at the membrane surface. Constructs containing the native PRR and SH3 domains reliably formed membrane‐associated clusters, while mutation or deletion of these domains lessened changes in diffusion and impaired condensate formation. Our findings establish the membrane as an essential mediator of PRR‐SH3‐driven phase separation in Btk, thereby advancing our understanding of membrane‐specific regulation in signaling protein dynamics.more » « less
-
ABSTRACT Specialized membrane and cortical protein regions are common features of cells and are utilized to isolate differential cellular functions. In Drosophila photoreceptors, the apical membrane domain is defined by two distinct morphological membranes: the rhabdomere microvilli and the stalk membrane. To define the apical cortical protein complexes, we performed proximity labeling screens utilizing the rhabdomeric-specific protein PIP82 as bait. We found that the PIP82 interactome is enriched in actin-binding and cytoskeleton proteins, as well as proteins for cellular trafficking. Analysis of one target, Bifocal, with PIP82 revealed two independent pathways for localization to the rhabdomeric membrane and an additional mechanism of crosstalk between the protein complexes of the rhabdomeric and stalk membranes. The loss of Bifocal, and enhancement in the PIP82, bifocal double mutant, resulted in the additional distribution of Crumbs, an apical stalk membrane protein, to the lateral basal photoreceptor membrane. This phenotype was recapitulated by the knockdown of the catalytic subunit of Protein phosphatase 1, a known interactor with Bifocal. Taken together, these results expand our understanding of the molecular mechanisms underlying the generation of the two distinct photoreceptor apical domains.more » « less
An official website of the United States government

