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SF-Assemblin Genes in Paramecium Nabi et al. Cilia (2019) 8:2 https://doi.org/10.1186/s13630-019-0062-y Cilia RESEARCH Open Access SF-Assemblin genes in Paramecium: phylogeny and phenotypes of RNAi silencing on the ciliary-striated rootlets and surface organization Ashikun Nabi1,4, Junji Yano1, Megan S. Valentine2, Tyler Picariello3 and Judith L. Van Houten1* Abstract Background: Cilia emanate from basal bodies just underneath the cell membrane. Basal bodies must withstand torque from the ciliary beat and be appropriately spaced for cilia to beat in metachronal waves. Basal body rootlets provide stability for motile cilia. Paramecium has three. Our focus is on the largest one, the striated rootlet (SR). Para- mecium basal bodies align in straight rows. Previously we found a potential role for the SR in this alignment. Here we present a phylogeny of the Paramecium homologs of the SF-Assemblin gene of the SR of Chlamydomonas, and the organization of these genes. We describe the phenotypes from RNA interference (RNAi) silencing of genes and gene groups. Methods: Phenotypes of the RNAi depletions were characterized by immunofuorescence (IF), electron microscopy, and mass spectrometry. Results: We found 30 genes for Paramecium SF-Assemblin homologs (SFA) organized into 13 Paralog Groups (further categorized in fve Structural Groups). Representatives of Paralog Groups were found in the SRs. Silencing the tran- scripts of any of the Structural Groups correlates with misaligned rows of basal bodies, SRs, and cortical units. The silencing of Structural Groups was key and gave us the ability to systematically disrupt SR structures and cell surface organization. Conclusions: Silencing of SFA genes and Paralog Groups shows no efects on the SR or the cell surface organization. Silencing of the larger Structural Groups has an enormous impact on rows of basal bodies, SRs and cortical units, and SR striations, and length. Misaligned basal bodies have cilia causing the cells to swim in abnormal paths. Keywords: Cilia, Basal body, Striated rootlet, RNAi Background reinhardtii, can be used as a model system for cilia devel- Cilia are the slender organelles that project from the sur- opment [3, 4]. Similarly, Paramecium tetraurelia, long face of eukaryotic cells, found in all extant eukaryotes studied for its ciliary structure, beat, and electrical con- [1]. We focus here on motile cilia, which allow cells like trol of this beating, serves as a model system for motile Paramecium to swim in their watery environment of a cilia including those of multiciliated cells [5, 6]. pond or stream and also to sense and respond to their At the base of each cilium is the basal body, a modifed environment [2]. Tese cilia share many proteins across centriole, with its associated rootlets [7]. While there can phyla, which is why the green algae, Chlamydomonas be microtubule-based appendages at the basal body, there usually is at least one striated rootlet (SR) composed of proteins unrelated to tubulin. Tis SR (also known as a *Correspondence: [email protected] kinetodesmal fber, KF in protists) links the cilium to the 1 University of Vermont, Burlington, VT 05405, USA Full list of author information is available at the end of the article cell body. Tis rootlet has been found to be important for © The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat iveco mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Nabi et al. Cilia (2019) 8:2 Page 2 of 21 basal body cohesion, anchoring of the basal body, mecha- the SR of the basal body meandered under the surface nosensation, and chemosensation of sensory neurons of [16]. A contemporaneous study of Tetrahymena showed Drosophila [8, 9]; long-term stability of photoreceptors that the SR and associated proteins secure the basal body by modulating the successful delivery of cargo through to the cell surface to resist hydrodynamic forces as the IFT particles to the cilium of Caenorhabditis elegans cilia beat [12, 13]. A breakdown in this resistance led to [10]; prevention of degeneration of the photoreceptors in meandering rows of basal bodies and disrupted surface. mouse and Drosophila through physically protecting the Tese discoveries encouraged us to investigate the Para- thin bridge between the cell body and large light-sensing mecium SR further for maintaining the organization of organelle [11]; and securing the Tetrahymena basal body basal bodies and cortical units in rows. to resist hydrodynamic forces as the cilia beat [12, 13]. In Paramecium, the SR projects from the basal body Te Paramecium surface with a thousand or more cilia toward the anterior of the cell past several more ante- is organized into roughly rectangular units bounded by rior basal bodies. Te structure comprises proteins with ridges and with one or two cilia arising from the depres- molecular mass ranging from 30 to 36 kDa, some of sion between the ridges. Figure 1 shows a section from which are phosphoproteins [17, 18]. Tese proteins form an image of a cell that has been deciliated to better visu- the very long, striated structure (SR) that is dynamic (i.e., alize the surface cortical unit pattern. (Te little nubs in changes length during the cell cycle) [19, 20]. Basal bod- some of the units are the stubs of cilia that were broken ies and associated rootlets are embedded into the infra- of by trituration to deciliate the cell.) Tese units align ciliary lattice (ICL), a mesh that sits beneath the plasma in rows running between the posterior and anterior poles membrane of Paramecium. of the cell [14]. Tis organization keeps the motile cilia Among the best characterized SRs are those of Chla- beating with their power stroke toward the posterior for mydomonas reinhardtii [21]. Tis led us to use the gene efcient swimming. Te separation of cilia into cortical for SF-Assemblin, a component of one of the two types units likely is the key to achieving the optimal distance of SRs in Chlamydomonas [22], to search the Parameci- between cilia and orientation of the cilia for metachrony umDB. We began this study by identifying the SF-Assem- [15]. blin (SFA) genes in the Paramecium annotated genome Our initial evidence for implication of SRs in surface and reconstructing a phylogenetic tree [23]. We organ- organization came from RNA interference (RNAi) silenc- ized 30 genes into 13 Paralog Groups and, more impor- ing of the human ciliopathy gene Meckelin (MKS3) in tantly, into fve Structural Groups based on their primary Paramecium that caused the pattern of surface units and and secondary amino acid structures, especially the ciliary orientation to break down. Rows of basal bodies number and location of coiled-coil domains. Te identi- became disoriented, surface units were misshapen and fcation of Structural Groups was the breakthrough that allowed us to use RNAi to reliably and systematically disrupt SRs. Here we describe the phenotypes of these depletions. Materials and methods Stock, culture, and chemicals Cells (stock 51s P. tetraurelia, sensitive to killer) were grown in wheat grass medium (Pines International, Law- rence, KS, USA) inoculated with Aerobacter aerogenes [24]. All chemicals were purchased from Sigma-Aldrich (St Louis, MO, USA) unless otherwise noted. SFAs sequence analysis We used the SF-Assemblin protein sequence from Chlamydomonas reinhardtii (Accession number: Fig. 1 Section of a scanning electron micrograph of a deciliated P. EDP05674.1) to search for homologous SF-Assemblin tetraurelia cell showing the cortical units that cover the cell surface. protein sequences in the Paramecium annotated genome Rows of cortical units run between the anterior and posterior poles. in the dedicated database ParameciumDB (http://param One or two basal bodies are in each unit but cannot be seen here. ecium .cgm.cnrs-gif.fr/). All possible protein sequences The small structures (arrow) in some of the units are stubs of cilia, were checked in the NCBI conserved domain search and which break of at the transition zone during deciliation. Anterior is to the left. Scale bar is 4 μm the Pfam database (http://pfam.xfam.org/) for the pres- ence of conserved domains of SF-Assemblin protein. Nabi et al. Cilia (2019) 8:2 Page 3 of 21 Coiled-coil domains were identifed by the program SFA12c, SFA13a, SFA13c and SFA13d). Only 24 RNAi SMART [25] and COILS [26]. Finally, the phyloge- constructs for these genes were necessary because some netic relationships among all the SFA genes (nucleotide constructs silenced more than one gene. Constructs were sequence) were analyzed using the MEGA6 software designed from the sequences in the Paramecium anno- [27]. See Table 1 for a summary of the SFA genes. See tated genome using the ParameciumDB database. Gene Additional fle 2: Table S3 for Accession numbers. ID numbers in ParameciumDB and gene nucleotide base We found all 30 individual SFA genes in the Parame- positions for RNAi constructs are available in Additional cium resource for Expressed Sequence Tags (ESTs) in fle 2: Table S1. In order to design specifc constructs, we ParameciumDB. Tey were found to be expressed in veg- carried out of-target analysis for each construct (http:// etative cells but not during cell division. param ecium .cgm.cnrsg if.fr/cgi/align ment/off-targe t.cgi). Specifc oligonucleotide primers (Additional fle 2: RNAi constructs Table S2) were used to amplify the designed sequence by We designed RNAi constructs for 24 of the 30 SFA using Genomic DNA as a template.
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