PROGETTO E PIANO DELLE ATTIVITÀ
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1 PROGETTO E PIANO DELLE ATTIVITÀ! TITOLO DEL PROGETTO DI RICERCA: "Mitochondrial activity in germ line development"! TUTOR PROPONENTE: Liliana Milani! ELENCO DEI PARTECIPANTI (incluso non strutturati) Cognome e nome Ruolo nel progetto SSD Impegno previsto (mesi/uomo) Milani Liliana PI Bio06 6 annui (Tot: 12) Franceschini Valeria Supervisore Bio06 3 annui (Tot: 6) Ghiselli Fabrizio Collaboratore Bio05 6 annui (Tot: 12)! BASE DI PARTENZA SCIENTIFICA ed OBIETTIVI (max 500 parole) Following the endosymbiotic event that originated mitochondria, the vast majority of genes from the protomitochondrion has been transferred to the nucleus or lost. So, although mitochondria play multiple roles in eukaryotes, the information stored in their DNA is limited to replication and expression of mitochondrial DNA (mtdna), and oxidative phosphorylation (OXPHOS). Why did mitochondria retain a small core of genes, and why is this core extremely conserved among metazoans? According to the co-location for redox regulation hypothesis [1], mitochondria retained genes whose expression needs to be under direct regulation of the redox state of their products, or of electron carriers with which their products interact, allowing an autonomous regulation of gene expression. Thanks to this, the eukaryotic cell acquired the capacity of an increased and fine-tuned energy production that permitted a release from genome size constraints, making mitochondria a prerequisite to eukaryote complexity and multicellular life [2,3]. The retention of a genome in mitochondria entails two major problems: 1) OXPHOS is accompanied by the generation of mutagenic reactive oxygen species (ROS) [4], so mtdna is located in a potentially hostile environment which can compromise the integrity of its genetic information; 2) mitochondrial and nuclear elements interact to carry out their function, so the two genomes need to coevolve despite their quite different evolutionary dynamics. According to several theories, these problems were solved by the evolution of uniparental inheritance of cytoplasmic organelles, which entailed anisogamy and thus the establishment of two sexes, making mitochondria also responsible for the evolution of sex in eukaryotes [3]. In all eukaryotes, uniparental inheritance shows a high degree of homoplasy, yet, it is not clear whether the trait is under selection itself, or it is the outcome of selection for other aspects of reproduction [5]. If uniparental inheritance is adaptive, what caused the selective pressure on the trait? Was it the preservation of egg mitochondria from ROS damage in order to assure a viable transmission of mtdna information across generations? Was it the avoidance of heteroplasmy in order to favour mito-nuclear coadaptation? In this project we propose to exploit an organism with an unusual mitochondrial inheritance system (doubly uniparental inheritance, DUI) [6] to test some basic assumptions that cannot be tested in organisms with strictly maternal inheritance (SMI). Most of the working hypotheses associated with the above mentioned topics still need to be tested, and the new comparative data generated by this project will represent a relevant step forward. The outcome will be a deeper knowledge of mitochondrial functions and their evolution, particularly in
2 relation with energy production, germ line development, and ultimately with the origin of anisogamy and sex. References: 1. Allen JF Phil Trans R Soc Lond B 358: Lane N & Martin W Nature 467: Lane N Bioessays 33: Chance B et al Physiol Rev 59: Birky CW Jr Proc Natl Acad Sci USA 92: Zouros E Evol Biol 40:1 31! ARTICOLAZIONE DEL PROGETTO E TEMPI DI REALIZZAZIONE (MAX 1000 PAROLE) The goal of this project is to address two major topics of mitochondrial biology: 1) How is a faithful transmission of mitochondrial genetic information achieved? 2) How does heteroplasmy affect mito-nuclear coevolution? We will perform comparative genomics and transcriptomics between the DUI species Ruditapes philippinarum and other SMI species (Danio rerio and Drosophila melanogaster). DUI is the only known evolutionary stable exception to SMI, and characterizes ~100 species of bivalve molluscs in which two mitochondrial lineages are inherited, one through eggs (F-type), the other through sperm (M-type) [1]. Females are homoplasmic for F, while males are heteroplasmic in their soma and homoplasmic for M in sperm. Since eggs do not transmit M, in DUI male germ line, mitochondria are apportioned from the four mitochondria of the fertilizing spermatozoon [2]. Thanks to its features, DUI provides a useful system that will help elucidating general processes of mitochondrial biology and evolution. TOPIC 1 Mitochondrial respiratory activity generates ROS that are known to damage DNA. How can germ line mitochondria avoid ROS damage? Motility of at least one gamete is needed for fertilization, and it requires ATP. It was proposed that male gametes maximize energy for motility by sacrificing mtdna to OXPHOS, while the non-motile female gametes repress respiratory activity, preserving their mtdna from ROS. Accordingly, because of maternal inheritance, male gametes make no contribution to the mitochondrial genome of the embryo. Such "division of labour" between male and female with respect to mitochondrial function is consistent with data from some metazoans [3], but not with what observed in DUI species, in which sperm mitochondria appear to perform OXPHOS while maintaining a viable genetic information [3]. In this project, ROS scavenging processes, the presence of antioxidant defense mechanisms, as well as the activity of pathways for ATP production other than OXPHOS and mechanisms of mtdna protection and repair, will be investigated. TOPIC 2 Mito-nuclear mismatches result in low ATP production and high free-radical leak, compromising fertility, embryo development and adult survival [4,5]. The DUI male represents a valuable experimental system because it is naturally heteroplasmic, differently from cybrids or inbred animals commonly used to study heteroplasmy. We will test the presence of differential mitochondrial activity between sexes and across different tissues, the potential silencing/downregulation of one mtdna type in heteroplasmic tissues, the presence of splice variants and/or genetic polymorphism associated with each mtdna type. Answering to these
3 questions will greatly improve our knowledge about mito-nuclear coevolution and about the effects of heteroplasmy. BACKGROUND In the last couple of years, my Collaborators and I obtained a large amount of genomic and transcriptomic data (~690 Gigabases) on R. philippinarum (see table). Library Type of Tissue Sex # of samples 1) RNA-Seq Ripe gonad, adductor Males + 150PE reads, 500bp (mrna) muscle, mantle Females insert, 2 lanes. 2) High depth mtdna 3) Whole genome 4) Whole genome 150PE reads, 500bp insert, 2 lanes. 250PE reads, 500bp bp inserts, 2 lanes. PacBio RSII P6-C4, 54 SMRT cells, 12-50Kb size selected. Whole body, ripe gonad, adductor muscle, sperm, sperm after 1h swimming Males + Females Sequenced bases Gb Gb Mantle 1 Male Gb Mantle 1 Male 1 37 Gb Such data will be integrated with data from D. melanogaster and D. rerio provided by our Collaborators, and data obtained from public databases. A few months ago we assembled a high-quality genome of R. philippinarum, and we are in the process of annotating it. This will be an important resource for this project. FIRST YEAR The first year of the project will be characterized by the following tasks (the numbers in brackets indicate the table column describing the data involved in the process): a) quality check and filtering (1,2); b) de novo assembly of transcriptomes and mtdna deep- (1,2); c) genome-guided de novo assembly of transcriptomes (1); d) mapping and variant discovery: SNPs, CNV (1,2); e) alternative splicing (1,3,4); f) annotation (1,2,3,4); g) differential transcription (1,3,4). All these tasks require a large amount of time because of their complexity and computation time required. SECOND YEAR The second year will be devoted to the comparative analyses. In the last few years we developed some data analysis pipelines optimized for operating inside a comparative framework, and we will apply such methods to our data, to the data provided from our Collaborators, and to the data obtained from the public databases.
4 During this second year we will finalize the data analysis, discuss the results with our Collaborators, write the manuscripts, and present our findings at international meetings. References: 1. Zouros E Evol Biol 40: Milani L et al J Exp Zool Part B 318: Milani L & Ghiselli F Biol Direct 10:22 4. Lane N Cell 151: Sharpley MS et al Cell 151:333 43! PROGRAMMA FORMATIVO (O PIANO DI ATTIVITÀ) DELL ASSEGNISTA (MAX 1000 PAROLE) The Postdoc will operate in a comparative genomics context, analyzing the obtained data and discussing the results from an evolutionary point of view. To do so, he/she will analyze and compare an unusual biological system (the DUI species R. philippinarum) and two established model systems (the SMI species D. melanogaster, and D. rerio), applying state-of-the-art methodology and analysis tools. The Postdoc will analyze transcriptomic data to investigate topics 1 and 2 using two different approaches in parallel. First, a differential transcription analysis will be used to detect differences across tissues and between sexes. This will allow the identification of genes with the most skewed transcription among different conditions and the recognition of the pathways in which such genes participate. However, this 'classical' approach works best when the signals are strong and neat, namely when phenotypes are caused by differential upregulation/downregulation of one gene or a few genes. In the second approach, the Postdoc will perform a gene co-expression network analysis [1]: based on the idea that genes with similar functions show similar transcription levels in the same conditions, this method transforms coexpression similarities into connection strengths, in order to build networks of genes involved in the same biological process. This analysis isolates clusters of genes showing highly-correlated transcription, and thus likely belonging to the same pathway or group of co-occurring pathways. This will enable a better prediction of gene functions, and the identification of genes showing a high connectivity within networks: such genes likely possess a central role in the processes of interest. Each network will be analyzed to investigate the most representative pathways involved. This second method is more suitable to analyze large regulatory networks where hundreds of genes influence the phenotypic changes each contributing with a small transcriptional variation, which is impossible to detect with the first approach. The Postdoc will also investigate polymorphism and variation at the molecular level, both on DNA (SNPs, CNV) and RNA (SNPs, alternative splicing, RNA editing), and will perform transcriptome annotation using a pipeline we specifically developed for working with nonmodel organisms, classical gene prediction methods [2], and also using a novel gene construction method (i.e.: EvidentialGene, see The integration of all these different methods will generate a robust annotation of R. philippinarum data, which is absolutely necessary in order to be able to perform the comparison with the two model organisms. During this project the Postdoc will work on high performance computation clusters (University of Southern California HPCC, CINECA Galileo) and on the workstations available in our Department, using available bioinformatics software, and writing custom scripts in Unix, R, and Python. He/she will also be part of an ongoing international collaboration with Labs in the USA, Canada, and Russia, having the possibility to interact with a large network of both young and experienced scientists around the world.
5 INTERNATIONAL COLLABORATORS INVOLVED Prof. Sophie Breton (Département de Sciences Biologiques, Université de Montréal, Canada) and her team will collaborate for transcriptomic and genomic analyses in DUI species. Since 2011, we published together 5 papers (plus one pending minor revision) about mitochondrial inheritance. Prof. Sergey Nuzhdin (Department of Biological Sciences, Molecular and Computational Biology, University of Southern California, Los Angeles, USA) and his bioinformatics team will help analyzing data, and will provide data about D. melanogaster. Since 2009, we have collaborated with the Nuzhdin Lab publishing 4 papers so far (plus one under review). Dr. Aleksey Komissarov (Theodosius Dobzhansky Center for Genome Bioinformatics, St. Petersburg State University, Russia) has been one of the main contributors to the de novo assembly of R. philippinarum genome. Our collaboration dates back to March 2015, and we are working on R. philippinarum genome annotation. In the near future our collaboration will move on comparative genomics of bivalves. References 1. van Dam S et al Brief Bioinform doi: /bib/bbw Yandell M & Ence D Nat Rev Genet doi: /nrg3174
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