skip to main content

Explore Research Products in the NSF-PAR

Title: Expanding the Junction: New Insights into Non-Occluding Roles for Septate Junction Proteins during Development
The septate junction (SJ) provides an occluding function for epithelial tissues in invertebrate organisms. This ability to seal the paracellular route between cells allows internal tissues to create unique compartments for organ function and endows the epidermis with a barrier function to restrict the passage of pathogens. Over the past twenty-five years, numerous investigators have identified more than 30 proteins that are required for the formation or maintenance of the SJs in Drosophila melanogaster, and have determined many of the steps involved in the biogenesis of the junction. Along the way, it has become clear that SJ proteins are also required for a number of developmental events that occur throughout the life of the organism. Many of these developmental events occur prior to the formation of the occluding junction, suggesting that SJ proteins possess non-occluding functions. In this review, we will describe the composition of SJs, taking note of which proteins are core components of the junction versus resident or accessory proteins, and the steps involved in the biogenesis of the junction. We will then elaborate on the functions that core SJ proteins likely play outside of their role in forming the occluding junction and describe studies that provide some cell biological perspectives that are beginning to provide mechanistic understanding of how these proteins function in developmental contexts.  more » « less
Award ID(s):
2111069
NSF-PAR ID:
10315257
Author(s) / Creator(s):
; ; ; ;
Date Published:
Journal Name:
Journal of Developmental Biology
Volume:
9
Issue:
1
ISSN:
2221-3759
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ( , G3 Genes|Genomes|Genetics)
    Reed, B H (Ed.)
    Abstract Protein components of the invertebrate occluding junction—known as the septate junction (SJ)—are required for morphogenetic developmental events during embryogenesis in Drosophila melanogaster. In order to determine whether SJ proteins are similarly required for morphogenesis during other developmental stages, we investigated the localization and requirement of four representative SJ proteins during oogenesis: Contactin, Macroglobulin complement-related, Neurexin IV, and Coracle. A number of morphogenetic processes occur during oogenesis, including egg elongation, formation of dorsal appendages, and border cell (BC) migration. We found that all four SJ proteins are expressed in egg chambers throughout oogenesis, with the highest and the most sustained levels in the follicular epithelium (FE). In the FE, SJ proteins localize along the lateral membrane during early and mid-oogenesis, but become enriched in an apical-lateral domain (the presumptive SJ) by stage 11. SJ protein relocalization requires the expression of other SJ proteins, as well as Rab5 and Rab11 like SJ biogenesis in the embryo. Knocking down the expression of these SJ proteins in follicle cells throughout oogenesis results in egg elongation defects and abnormal dorsal appendages. Similarly, reducing the expression of SJ genes in the BC cluster results in BC migration defects. Together, these results demonstrate an essential requirement for SJ genes in morphogenesis during oogenesis, and suggest that SJ proteins may have conserved functions in epithelial morphogenesis across developmental stages. 
    more » « less
  2. ; ; ; ; ( , Frontiers in Cell and Developmental Biology)
    Septate junctions (SJs) serve as occluding barriers in invertebrate epithelia. In Drosophila , at least 30 genes are required for the formation or maintenance of SJs. Interestingly, loss-of-function mutations in core SJ components are embryonic lethal, with defects in developmental events such as head involution and dorsal closure (DC) that occur prior to the formation of a mature SJ, indicating a role for these proteins in mid-embryogenesis independent of their occluding function. To understand this novel function in development, we examined loss-of-function mutations in three core SJ proteins during the process of DC. DC occurs during mid-embryogenesis to seal a dorsal gap in the epidermis following germ band retraction. Closure is driven by contraction of the extraembryonic amnioserosa cells that temporarily cover the dorsal surface and by cell shape changes (elongation) of lateral epidermal cells that bring the contralateral sheets together at the dorsal midline. Using live imaging and examination of fixed tissues, we show that early events in DC occur normally in SJ mutant embryos, but during later closure, coracle , Macroglobulin complement-related and Neurexin-IV mutant embryos exhibit slower rates of closure and display aberrant cells shapes in the dorsolateral epidermis, including dorsoventral length and apical surface area. SJ mutant embryos also show mild defects in actomyosin structures along the leading edge, but laser cutting experiments suggest similar tension and viscoelastic properties in SJ mutant versus wild type epidermis. In a high percentage of SJ mutant embryos, the epidermis tears free from the amnioserosa near the end of DC and live imaging and immunostaining reveal reduced levels of E-cadherin, suggesting that defective adhesion may be responsible for these tears. Supporting this notion, reducing E-cadherin by half significantly enhances the penetrance of DC defects in coracle mutant embryos. 
    more » « less
  3. ; ; ; ; ( , Plant and Cell Physiology)
    Abstract

    Tudor-SN is involved in a myriad of transcriptional and post-transcriptional processes due to its modular structure consisting of 4 tandem SN domains (4SN module) and C-terminal Tsn module consisting of Tudor-partial SN domains. We had previously demonstrated that OsTudor-SN is a key player for transporting storage protein mRNAs to specific ER subdomains in developing rice endosperm. Here, we provide genetic evidence that this multifunctional RBP is required for storage protein expression, seed development and protein body formation. The rice EM1084 line, possessing a nonsynonymous mutation in the 4SN module (SN3 domain), exhibited a strong reduction in grain weight and storage protein accumulation, while a mutation in the Tudor domain (47M) or the loss of the Tsn module (43M) had much smaller effects. Immunoelectron microscopic analysis showed the presence of a new protein body type containing glutelin and prolamine inclusions in EM1084, while 43M and 47M exhibited structurally modified prolamine and glutelin protein bodies. Transcriptome analysis indicates that OsTudor-SN also functions in regulating gene expression of transcriptional factors and genes involved in developmental processes and stress responses as well as for storage proteins. Normal protein body formation, grain weight and expression of many genes were partially restored in EM1084 transgenic line complemented with wild-type OsTudor-SN gene. Overall, our study showed that OsTudor-SN possesses multiple functional properties in rice storage protein expression and seed development and that the 4SN and Tsn modules have unique roles in these processes.

     
    more » « less
  4. ; ; ; ; ( , mSystems)
    Rappe, Michael S. (Ed.)
    ABSTRACT For the abundant marine Alphaproteobacterium Pelagibacter (SAR11), and other bacteria, phages are powerful forces of mortality. However, little is known about the most abundant Pelagiphages in nature, such as the widespread HTVC023P-type, which is currently represented by two cultured phages. Using viral metagenomic data sets and fluorescence-activated cell sorting, we recovered 80 complete, undescribed Podoviridae genomes that form 10 phylogenomically distinct clades (herein, named Clades I to X) related to the HTVC023P-type. These expanded the HTVC023P-type pan-genome by 15-fold and revealed 41 previously unknown auxiliary metabolic genes (AMGs) in this viral lineage. Numerous instances of partner-AMGs (colocated and involved in related functions) were observed, including partners in nucleotide metabolism, DNA hypermodification, and Curli biogenesis. The Type VIII secretion system (T8SS) responsible for Curli biogenesis was identified in nine genomes and expanded the repertoire of T8SS proteins reported thus far in viruses. Additionally, the identified T8SS gene cluster contained an iron-dependent regulator (FecR), as well as a histidine kinase and adenylate cyclase that can be implicated in T8SS function but are not within T8SS operons in bacteria. While T8SS are lacking in known Pelagibacter , they contribute to aggregation and biofilm formation in other bacteria. Phylogenetic reconstructions of partner-AMGs indicate derivation from cellular lineages with a more recent transfer between viral families. For example, homologs of all T8SS genes are present in syntenic regions of distant Myoviridae Pelagiphages, and they appear to have alphaproteobacterial origins with a later transfer between viral families. The results point to an unprecedented multipartner-AMG transfer between marine Myoviridae and Podoviridae. Together with the expansion of known metabolic functions, our studies provide new prospects for understanding the ecology and evolution of marine phages and their hosts. IMPORTANCE One of the most abundant and diverse marine bacterial groups is Pelagibacter . Phages have roles in shaping Pelagibacter ecology; however, several Pelagiphage lineages are represented by only a few genomes. This paucity of data from even the most widespread lineages has imposed limits on the understanding of the diversity of Pelagiphages and their impacts on hosts. Here, we report 80 complete genomes, assembled directly from environmental data, which are from undescribed Pelagiphages and render new insights into the manipulation of host metabolism during infection. Notably, the viruses have functionally related partner genes that appear to be transferred between distant viruses, including a suite that encode a secretion system which both brings a new functional capability to the host and is abundant in phages across the ocean. Together, these functions have important implications for phage evolution and for how Pelagiphage infection influences host biology in manners extending beyond canonical viral lysis and mortality. 
    more » « less
  5. ; ; ; ( , Frontiers in Plant Science)
    Chloroplasts are endosymbiotic organelles derived from cyanobacteria. They have a double envelope membrane, including the outer envelope and the inner envelope. A complex membrane system, thylakoids, exists inside the chloroplast. It is the site of the light-dependent reactions of photosynthesis. The stroma is the main site of the carbon fixation reactions. Although photosynthesis is a very complicated process with many proteins involved, there are many other important processes that occur in chloroplasts, including the regulation of photosynthesis, the biogenesis and maintenance of the structures, carbohydrate, lipid, tetrapyrrole, amino acid, and isoprenoid metabolism, production of some phytohormones, production of specialized metabolites, regulation of redox, and interactions with other parts of the cell (Sabater, 2018). During evolution, most of the cyanobacterial genes were lost and many of them were transferred into the nuclear genome. A majority of chloroplast proteins are nuclear-encoded and possess an N-terminal transit peptide which helps the protein to be targeted into chloroplasts. Chloroplasts have their own highly reduced genome which works coordinately with the nuclear genome for the biogenesis and function of chloroplasts (Liebers et al., 2022). This Research Topic presents studies covering different aspects of chloroplast function, including photosynthesis, biogenesis, structure, and maintenance. These works push the frontiers of chloroplast research further in the field of plant biology. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email