averof lab

Evolution of development and morphology


Research / training fellowships (click here)



Interests

Research on model organisms has shown that some aspects of development are conserved in animals as diverse as insects and vertebrates, and depend on homologous sets of regulatory genes. We are interested in comparing developmental processes and gene functions among diverse animals, to answer three types of broad questions: (a) how far we can extrapolate from model organisms? (to what extent are developmental processes really conserved?) (b) can gene expression patterns and functions tell us something about the origin of key evolutionary innovations, such as the insects' wings and tracheal systems? and (c) can we discover specific genetic changes that lie behind evolutionary changes in morphology? We focus on segmentation, segment specialization, tracheal and appendage development in arthropods, because the genetic basis of these processes is among the best understood (primarily from studies in flies), and their evolution poses intriguing questions.


Research projects

Axis elongation and segmentation: Unlike Drosophila, the majority of arthropods generate their segments sequentially from a posteriorly located growth zone, a process known as 'short-germ' development. Parallels to this can be found in vertebrates, where somites are generated sequentially from a posteriorly located pre-somitic zone. The mechanisms underlying this process are poorly understood. We are developing genetics and imaging approaches to study this process in two short-germ arthropods, a crustacean (Artemia) and an insect (Tribolium).

Hox genes and the evolution of segmental specialization: All arthropods share the same set of Hox genes, although their bodies display strikingly diverse patterns of segmental specialization. Differences in these patterns probably depend on changes in the expression of Hox genes, and in the way these genes are able to regulate their targets. We are developing transgenesis tools that will allow us to explore these changes, by mis-expressing Hox genes and by comparing the activity of their target cis-regulatory elements across species.

Origin of key evolutionary novelties (wings and tracheae) in the evolution of insects: Our work has suggested that insect wings and tracheal systems evolved from the gills of ancestral aquatic arthropods. The book lungs, tracheae and spinnerets of spiders appear to have evolved independently from related ancestral structures. We are currently investigating the origin of respiratory organs (tracheae) in other groups of terrestrial arthropods, and looking for the actual molecular-developmental changes that were associated with the evolution of these structures.

Transgenesis tools and RNAi for functional studies in emerging model arthropods: Until recently, functional genetic studies were limited to a small number of model organisms. We are establishing RNAi and transgenesis tools that will allow us to study developmental processes and gene functions in new species of interest. We have used the Minos transposable element to establish transgenesis in the crustacean Parhyale hawaiensis. We are currently developing tools for marking specific populations of cells and for mis-expressing genes in this species (reporter constructs, enhancer traps, heat-inducible and GAL4/UAS mis-expression systems). We are also generating tools for mosaic analysis and live imaging in the beetle Tribolium castaneum.


Publications

Pavlopoulos A, Kontarakis Z, Liubicich D, Serano J, Akam M, Patel NH and Averof M (2009) Probing the evolution of appendage specialization by Hox gene mis-expression in an emerging model crustacean. PNAS 106: 13897-13902. PDF download  PubMed link

Liubicich D, Serano J, Pavlopoulos A, Kontarakis Z, Protas ME, Kwan E, Chattergee S, Tran KD, Averof M and Patel NH (2009) Knockdown of Parhyale Ultrabithorax recapitulates evolutionary changes in crustacean appendage morphology. PNAS 106: 12892-12896. PDF download  PubMed link

Franch-Marro X, Martin N, Averof M and Casanova J (2006) Association of tracheal placodes with leg primordia in Drosophila and implications for the origin of insect tracheal systems. Development 133, 785-790. PDF download  PubMed link

Copf T, Rabet N and Averof M (2006) Knockdown of spalt function by RNAi causes de-repression of Hox genes and homeotic transformations in the crustacean Artemia franciscana. Dev Biol 298, 87-94. PDF download  PubMed link

Kontarakis Z, Copf T and Averof M (2006) Expression of hunchback during trunk segmentation in the branchiopod crustacean Artemia franciscana . Dev Genes Evol 216, 89-93. PDF download  PubMed link

Pavlopoulos A and Averof M (2005) Establishing genetic transformation for comparative developmental studies in the crustacean Parhyale hawaiensis. PNAS 102: 7888-7893.  PDF download  PubMed link

Copf T, Schroder R and Averof M (2004) Ancestral role of caudal genes in axis elongation and segmentation. PNAS 101, 17711-17715.  PDF download  PubMed link

Pavlopoulos A, Berghammer AJ, Averof M and Klingler M (2004) Efficient transformation of the beetle Tribolium castaneum using the Minos transposable element: quantitative and qualitative analysis of genomic integration events. Genetics 167, 737-746.  PDF download  PubMed link

Copf T, Rabet N, Celniker SE and Averof M (2003) Posterior patterning genes and the identification of a unique body region in the brine shrimp Artemia franciscana. Development 130, 5915-5927.  PDF download  PubMed link

Damen WGM, Saridaki T and Averof M (2002) Diverse adaptations of an ancestral gill: A common evolutionary origin for wings, breathing organs and spinnerets. Current Biology 12, 1711-1716.  PDF download  PubMed link

Averof M (2002) Arthropod Hox genes: insights on the evolutionary forces that shape gene functions. Curr Op Genetics and Development 12, 386-392 (review).  PDF download  PubMed link

Pavlopoulos A and Averof M (2002)  Developmental evolution: Hox proteins ring the changes. Current Biology 12: R291-293 (review).  PDF download  PubMed link

Ligoxygakis P, Strigini M and Averof M (2001) Specification of left-right asymmetry in the embryonic gut of Drosophila. Development 128, 1171-1174. PDF download  PubMed link

Averof M, Rokas A, Wolfe KH and Sharp PM (2000) Evidence for a high frequenvy of simultaneous double-nucleotide substitutions. Science 287, 1283-1286. PDF download  PubMed link

Averof M and Patel NH (1997) Crustacean appendage evolution associated with changes in Hox gene expression. Nature 388, 682-686.  PDF download  PubMed link

Averof M and Cohen SM (1997) Evolutionary origin of insect wings from ancestral gills. Nature 385, 627-630.  PDF download  PubMed link

Averof M and Akam M (1995) Hox genes and the diversification of insect and crustacean body plans. Nature 376, 420-423.  PDF download  PubMed link

Averof M and Akam M (1995) Insect-crustacean relationships: Insights from comparative developmental and molecular studies. Phil Trans R Soc B 347, 293-303.  PDF download


Current lab members


Meriem Takarli (takarli@imbb.forth.gr)
Origin of tracheal systems in diverse terrestrial arthropods

Andrew Peel (apeel@imbb.forth.gr)
Evolution of patterning mechanisms in insects

Claudia Roedel (roedel@imbb.forth.gr)
Evolution of caudal translational repression in insects

Haris Kontarakis (kontar@imbb.forth.gr)
Genetic approaches for comparative developmental studies in crustaceans

Nikos Konstandinidis (nkonst@imbb.forth.gr)
Genetic approaches for comparative developmental studies in crustaceans

Vassilis Douris (vdouris@imbb.forth.gr)
Gene trapping in the amphipod Parhyale hawaiensis

Andrés Sarrazin (sarrazin@imbb.forth.gr)
Live imaging in the beetle Tribolium castaneum

Past lab members

Petros Ligoxygakis (1999, currently has his own group in Oxford)

Maurijn van der Zee (2000-01, currently in Paul Brakefield's lab, Leiden)

Valia Stamataki (2001-03, currently in Pat Simpson's lab, Cambridge)

Tassos Pavlopoulos (2000-04, currently in Michael Akam's lab, Cambridge)

Theodora Saridaki (2001-04, currently in Fabrizio Chiti's lab, Florence)

Tijana Copf (2000-05, currently in Wes Grueber's lab, New York)

Alexandros Kiupakis (2006-08)

Visitors

Eduardo Moreno (1999 EMBO short-term from Morata lab, Madrid)

Cassandra Extavour (2001 EMBO short-term from Akam lab, Cambridge)


Lab environment and facilities

Our lab is located at the Institute of Molecular Biology and Biotechnology (IMBB), a few kilometers from the city of Iraklio, in Crete. The Institute provides an excellent environment and infrastructure for molecular biology, microscopy (transmission/Nomarski, fluorescence, laser scanning and spinning disc confocals), and  insect transgenesis, with expertise on microinjection and transgenesis in diverse species.

The IMBB participates in a joint graduate programme with the Departments of Biology and Medicine of the University of Crete (both located nearby). Although the majority of students are Greek, our labs also attract a significant number of PhD students and post-docs from abroad. All seminars and group meetings are conducted in English.

We share our lab with the group of Christos Delidakis (working on Drosophila neurogenesis), sharing many reagents, ideas, group meetings and coffee breaks.


Funding

EMBO Young Investigators' Award (2000-03)

EPAN programme "Establishing transgenic technology for functional genomic studies in a model crustacean" (2003-05)

EPAN programme "Establishing transgenic technology for functional genomic studies in a model crustacean" (2006-08)

Marie Curie Early Stage Training FAMED "Functional analysis of microRNAs during early development" (2005-2008)

Marie Curie Research Training Network ZOONET "Development and evolution of animal form: training modern comparative zoologists" (2005-08) 

Marie Curie Transfer of Knowledge CELLIMAGE "Advanced cell imaging approaches in developmental biology " (2007-2010) 



Michalis Averof

Institute of Molecular Biology and Biotechnology (IMBB)
711 10 Iraklio Crete, Greece

Tel.: +30-2810-391158 (office), +30-2810-391148 (lab)
Fax: +30-2810-391104
Email: averof@imbb.forth.gr

 


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