A rapidly evolving actin mediates fertility and developmental tradeoffs in Drosophila
Posted on: 16 October 2020
Preprint posted on 28 September 2020
Fast actin’ : non-canonical, rapidly evolving Arp detrimental to the male germline retained in flies for boost to female fertility
Selected by Hiral Shah, Dey Lab
Categories: cell biology, evolutionary biology, genetics
Introduction/ Background
Actin-related proteins (Arps) constitute an ancient (1,2) superfamily of cytoskeletal proteins with specialized functions in polymerisation of actin structures, dynein motility and chromatin remodeling (3). Arps retain the characteristic actin fold domain (4) but have diverged to incorporate other structural elements. While many Arps are widely conserved, others appear to evolve rapidly, restricted to certain lineages or ‘orphaned’. Interestingly, many of these Arps show sex- and tissue-specific expression, contrary to the ubiquitous presence of actin and canonical Arps (5). It is likely that non-canonical Arps play specialized but important roles in cytoskeletal organization, however, their functions remain largely unknown. Arp53D, for instance, the first non-canonical Arp to be described (6), is conserved across the Drosophila lineage, is absent outside insects and is enriched in the male testis. Arp53D proteins are defined by an unstructured 40 amino acid N-terminal stretch and a fast evolving actin fold domain. Owing to the male germline expression of Arp53D, this preprint set out to understand its function in male fertility using genetic and cytological studies.
Key Findings
Arp53D localized to testis-specific actin structures – such as the fusome and the actin cones. The N-terminal stretch was important for this unique localisation pattern of Arp53D. To identify Arp53D function, Arp53D knock-out (KO) flies were generated, marked with DsRed fluorescent eyes, to facilitate analysis of future crosses. Based on the tissue-specific localization and conservation across Drosophila, the authors expected the KO to show a decline in male fertility. Intriguingly, the loss of Arp53 led to an increase in male fertility, producing a higher number of progeny. Independent of the method, KO or RNAi, the Arp53D deficient flies consistently produced more progeny. What could be the possible advantage of retaining a gene that has detrimental effects on male fertility? Could the gene provide a benefit in competition between males? To address this, the authors attempted crosses with Arp53 KO males in isolation and in presence of Wild type (WT) competitors. Once again, irrespective of the competition, the Arp53 KO males outdid the WT counterparts. One possible explanation for selection of a gene with negative effects, the authors reasoned, would be an advantageous effect on some other traits. Which other traits could this gene affect?
All the authors’ observations thus far related to KO males. What would happen in reciprocal crosses? Interestingly, when Arp53D KO females were crossed with WT or KO males the fitness advantage conferred by Arp53 KO males was lost (Fig. 1). This opened up two possibilities: either Arp53D affected zygotic development or female fertility. The lower number of progeny in crosses with KO females and WT males pointed in the direction of reduced maternal effects. A further reduction in progeny number when both parents lacked Arp53D suggested additional defects in zygotic development or viability, with KO females making the larger contribution. What was causing this decline in progeny numbers? While there was no difference in egg numbers, it turns out the number of eggs developing into larvae was much smaller.
Thus, despite its negative impact on male fertility, Arp53D was likely retained for advantages conferred on maternal fertility and zygotic fitness. This was only possible if the net outcome of retaining Arp53D was beneficial. Would it be possible to demonstrate this in the lab? Indeed, the authors carried out population cage experiments over multiple generations to study long term changes in frequencies of the WT and KO alleles in a population isogenic for all other loci. At each generation randomly selected individuals were used to set up the subsequent cross and the Arp53D status of the remaining progeny was determined based on DsRed fluorescence. The Arp53D WT allele increased significantly within 20 generations, rising from less than one-third to almost two thirds of the fly population.
Questions
Does lack of the N-terminal stretch affect progeny size, male or female fertility?
What is the evolutionary history of this fitness tradeoff? In other words, would it be possible to reconstruct ancestral Arp53D variants and evaluate their impact on fitness? Alternatively, since this might be difficult for such a fast-evolving protein, would swapping Arp53D between species alter progeny numbers or female fertility? How would these different versions compete in population cage experiments?
What do you suspect is the exact nature of the molecular or cellular defects in female fertility and zygote development?
References
- Akıl C., Kitaoku Y., Tran L.T., Liebl D., Choe H., Muengsaen D., Suginta W., Schulte A. & Robinson R.C. 2021. Mythical origins of the actin cytoskeleton. Curr. Opin. Cell Biol. 68:55-63. doi: 10.1016/j.ceb.2020.08.011
- Izoré, T., Kureisaite-Ciziene, D., McLaughlin, S.H. & Löwe, J. 2016. Crenactin forms actin-like double helical filaments regulated by arcadin-2. eLife 5:e21600 doi: 10.7554/eLife.21600
- Schafer, D.A. & Schroer, T.A. 1999. Actin-related proteins. Annu. Rev. Cell Dev. 15:341-363.
- Dominguez, R. & Holmes, K.C. 2011. Actin structure and function. Annu. Rev. Biophys. 40, 169-86. doi: 10.1146/annurev-biophys-042910-155359
- Schroeder, C.M., Valenzuela, J.R., Natividad, I.M., Hocky, G.M. & Malik, H.S. 2019. A burst of genetic innovation in Drosophila actin-related proteins for testis-specific function. Mol. Biol. Evol. 37(3):757-772. doi: 10.1093/molbev/msz262
- Fyrberg C, Ryan L, Kenton M, Fyrberg E. 1994. Genes encoding actin-related proteins of Drosophila melanogaster. J. Mol. Biol. 241(3):498-503.
doi: https://doi.org/10.1242/prelights.25213
Read preprint
(No Ratings Yet)Sign up to customise the site to your preferences and to receive alerts
Register hereAlso in the cell biology category:
Motor Clustering Enhances Kinesin-driven Vesicle Transport
Sharvari Pitke
Cellular signalling protrusions enable dynamic distant contacts in spinal cord neurogenesis
Ankita Walvekar
Green synthesized silver nanoparticles from Moringa: Potential for preventative treatment of SARS-CoV-2 contaminated water
Safieh Shah, Benjamin Dominik Maier
Also in the evolutionary biology category:
Enhancer-driven cell type comparison reveals similarities between the mammalian and bird pallium
Rodrigo Senovilla-Ganzo
Modular control of time and space during vertebrate axis segmentation
AND
Natural genetic variation quantitatively regulates heart rate and dimension
Girish Kale, Jennifer Ann Black
Fetal brain response to maternal inflammation requires microglia
Manuel Lessi
Also in the genetics category:
Intracellular diffusion in the cytoplasm increases with cell size in fission yeast
Leeba Ann Chacko, Sameer Thukral
HIF1A contributes to the survival of aneuploid and mosaic pre-implantation embryos
Anchel De Jaime Soguero
Significantly reduced, but balanced, rates of mitochondrial fission and fusion are sufficient to maintain the integrity of yeast mitochondrial DNA
Leeba Ann Chacko
preLists in the cell biology category:
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
preLights peer support – preprints of interest
This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.
| List by | preLights peer support |
The Society for Developmental Biology 82nd Annual Meeting
This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.
| List by | Joyce Yu, Katherine Brown |
CSHL 87th Symposium: Stem Cells
Preprints mentioned by speakers at the #CSHLsymp23
| List by | Alex Eve |
Journal of Cell Science meeting ‘Imaging Cell Dynamics’
This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.
| List by | Helen Zenner |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
CellBio 2022 – An ASCB/EMBO Meeting
This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.
| List by | Nadja Hümpfer et al. |
Fibroblasts
The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!
| List by | Osvaldo Contreras |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
FENS 2020
A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020
| List by | Ana Dorrego-Rivas |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
BioMalPar XVI: Biology and Pathology of the Malaria Parasite
[under construction] Preprints presented at the (fully virtual) EMBL BioMalPar XVI, 17-18 May 2020 #emblmalaria
| List by | Dey Lab, Samantha Seah |
1
Cell Polarity
Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.
| List by | Yamini Ravichandran |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
3D Gastruloids
A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.
| List by | Paul Gerald L. Sanchez and Stefano Vianello |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
ASCB EMBO Annual Meeting 2019
A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)
| List by | Madhuja Samaddar et al. |
EMBL Seeing is Believing – Imaging the Molecular Processes of Life
Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019
| List by | Dey Lab |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Lung Disease and Regeneration
This preprint list compiles highlights from the field of lung biology.
| List by | Rob Hynds |
Cellular metabolism
A curated list of preprints related to cellular metabolism at Biorxiv by Pablo Ranea Robles from the Prelights community. Special interest on lipid metabolism, peroxisomes and mitochondria.
| List by | Pablo Ranea Robles |
BSCB/BSDB Annual Meeting 2019
Preprints presented at the BSCB/BSDB Annual Meeting 2019
| List by | Dey Lab |
MitoList
This list of preprints is focused on work expanding our knowledge on mitochondria in any organism, tissue or cell type, from the normal biology to the pathology.
| List by | Sandra Franco Iborra |
Biophysical Society Annual Meeting 2019
Few of the preprints that were discussed in the recent BPS annual meeting at Baltimore, USA
| List by | Joseph Jose Thottacherry |
ASCB/EMBO Annual Meeting 2018
This list relates to preprints that were discussed at the recent ASCB conference.
| List by | Dey Lab, Amanda Haage |
Also in the evolutionary biology category:
‘In preprints’ from Development 2022-2023
A list of the preprints featured in Development's 'In preprints' articles between 2022-2023
| List by | Alex Eve, Katherine Brown |
preLights peer support – preprints of interest
This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.
| List by | preLights peer support |
EMBO | EMBL Symposium: The organism and its environment
This preList contains preprints discussed during the 'EMBO | EMBL Symposium: The organism and its environment', organised at EMBL Heidelberg, Germany (May 2023).
| List by | Girish Kale |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)
A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.
| List by | Alex Eve |
Planar Cell Polarity – PCP
This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.
| List by | Ana Dorrego-Rivas |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
COVID-19 / SARS-CoV-2 preprints
List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic
| List by | Dey Lab, Zhang-He Goh |
1
SDB 78th Annual Meeting 2019
A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.
| List by | Alex Eve |
Pattern formation during development
The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.
| List by | Alexa Sadier |
Also in the genetics category:
BSDB/GenSoc Spring Meeting 2024
A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.
| List by | Joyce Yu, Katherine Brown |
BSCB-Biochemical Society 2024 Cell Migration meeting
This preList features preprints that were discussed and presented during the BSCB-Biochemical Society 2024 Cell Migration meeting in Birmingham, UK in April 2024. Kindly put together by Sara Morais da Silva, Reviews Editor at Journal of Cell Science.
| List by | Reinier Prosee |
9th International Symposium on the Biology of Vertebrate Sex Determination
This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.
| List by | Martin Estermann |
Alumni picks – preLights 5th Birthday
This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.
| List by | Sergio Menchero et al. |
Semmelweis Symposium 2022: 40th anniversary of international medical education at Semmelweis University
This preList contains preprints discussed during the 'Semmelweis Symposium 2022' (7-9 November), organised around the 40th anniversary of international medical education at Semmelweis University covering a wide range of topics.
| List by | Nándor Lipták |
20th “Genetics Workshops in Hungary”, Szeged (25th, September)
In this annual conference, Hungarian geneticists, biochemists and biotechnologists presented their works. Link: http://group.szbk.u-szeged.hu/minikonf/archive/prg2021.pdf
| List by | Nándor Lipták |
2nd Conference of the Visegrád Group Society for Developmental Biology
Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)
| List by | Nándor Lipták |
EMBL Conference: From functional genomics to systems biology
Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020
| List by | Jesus Victorino |
TAGC 2020
Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20
| List by | Maiko Kitaoka et al. |
ECFG15 – Fungal biology
Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome
| List by | Hiral Shah |
Autophagy
Preprints on autophagy and lysosomal degradation and its role in neurodegeneration and disease. Includes molecular mechanisms, upstream signalling and regulation as well as studies on pharmaceutical interventions to upregulate the process.
| List by | Sandra Malmgren Hill |
Zebrafish immunology
A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.
| List by | Shikha Nayar |