DEVELOPMENT AND EVOLUTION
Eldon Ball Laboratory - CMGD Canberra
Telephone: +61 2 6125 4496
Facsimile: + 61 2 6125 8294
are characterising the genome of the coral, Acropora millepora, and studying
the molecular control of its development. Our work provides fundamental knowledge
about the evolution of genomes and developmental pathways as well as having
potential practical value for regulating coral settlement and combating environmental
stressors such as environmental pollution and rising temperatures.
Collaborators & Linkages
- Dr. David Miller and associates, Comparative Genomics Centre, Molecular
Sciences Building, James Cook University, Townsville, QLD
- Prof Sue Wilson, Dr. Conrad Burden, Dr. Sylvain Foret, Mr John Maindonald,
Centre for Bioinformation Science, Australian National University, Canberra,
- Dr. Stephen Rudd, Centre for Biotechnology, Turku, Finland
- Prof. Michel Anctil, Department of Biological Sciences, University of Montreal,
- Dr. Joan Hooper, Dept of Cell and Developmental Biology, University of Colorado,
Health Sciences Center, Aurora, USA
- ARC/NHMRC Research Network in Genes and Environment in Development (NGED)
Coral Genomics and Development:
EST and microarray Studies
Lauretta Grasso, David Hayward, Bryony Fahey, Eldon Ball, Robert Saint in collaboration
with David Miller (James Cook University), Stephen Rudd (Turku University, Finland),
and John Maindonald (CBIS, ANU)
The comparative approach has proven to be invaluable when considering the evolution
of gene families and genomes. The coral Acropora millepora is of particular
interest in this context, as it is a member of the Phylum Cnidaria, an ancient
group of animals which separated from more complex animals at least 540 million
years ago. Genes and developmental pathways shared between the Cnidaria and
the higher animals are therefore considered to be ancient while those present
only in higher animals may be newly evolved.
In this project we addressed two questions: firstly, what genes are present
in coral? and secondly, how are these genes deployed to regulate development?
Expressed sequence tags (ESTs) provide us with a way of answering both questions.
As we are particularly interested in how gene expression changes during the
course of development we have taken ESTs from a number of different life stages
of Acropora including eggs (1000 ESTs), a pre-gastrulation stage known as the
prawn chip (3300 ESTs), the post-gastrulation planula larva (3700 ESTs), the
single polyp stage formed immediately post-settlement (3200 ESTs), and the bleached
adult colony (4800 ESTs).
Genomics Our research has yielded several unexpected results.
First, the complexity of the A. millepora genome has proven to be surprising,
considering the relatively simple cellular organisation of these animals. We
now estimate that there are at least 20,000 genes in the coral genome, many
more than we would have guessed when we started the project. Second, many genes
previously thought to be vertebrate specific, because they were missing from
Drosophila and Caenorhabditis, are present in the genome of A. millepora. This
finding indicates that gene loss has played a major role in the evolution of
a number of genomes. In addition there often appears to be a greater similarity
between the genes of corals and humans, than between coral and the first model
invertebrates, Drosophila and Caenorhabditis. Third, Acropora contains a substantial
number of "non-metazoan genes" in its genome. Because in many cases
these genes contain introns, are clearly incorporated into the coral DNA and
occur in scattered other organisms from throughout the animal kingdom, we argue
that these are ancient metazoan genes which have been lost in many animals.
Microarray Lauretta Grasso is currently analyzing the first large
scale microarray experiment in which a slide containing 13,000 ESTs (3000-4000
from each of prawn chip, planula, and polyp, was probed with RNA from those
stages plus adult. The ESTs have then been clustered by their stage of preferential
expression. We are now in the process of analyzing the results for groups of
interacting genes and trying to understand how the changes in gene expression
relate to processes such as gastrulation and settlement. A larger array, including
ESTs from the bleached adult colony, has recently been completed and will be
used for analyzing changes in gene expression under various environmental stresses.
Molecular control of metamophosis
in the coral Acropora millepora
David Hayward, Suzannah Hetherington, David Miller, Eldon Ball
During the life cycle of the coral Acropora, the planktonic planula larva settles
on the substratum, first forming a single polyp which then eventually grows
into the familiar colony. The processes of settlement and metamorphosis are
poorly understood at both the cellular and molecular level, but are of profound
importance to the sustainability of coral reefs. In order to understand the
genetic control of events underlying settlement and metamorphosis we are isolating
genes whose levels of expression differ before and after settlement using the
Clontech PCR Select System.
Research Outcomes: Over 270 differentially expressed genes have been identified.
Full length cDNA clones corresponding to genes which are candidates for involvement
in processes such as calcification, reception and transduction of settlement
cues, and nervous system function have been isolated and their temporal and
spatial expression characterized using virtual northern blots and in situ hybridization.
This project is supported by ARC Discovery Grant DP0344483 Differential expression
and functional analysis of genes controlling metamorphosis and early neurogenesis
of a model lower animal, the coral Acropora.
Conserved developmental pathways
Eldon Ball, Lauretta Grasso, David Hayward, David Miller
The "higher Metazoa" are classically separated from the "lower
Metazoa" on the basis of two characteristics: being bilaterally, rather
than radially, symmetrical, and being triploblastic (i.e. having three body
layers) rather than diploblastic (having two). In vertebrates mesoderm formation
and formation of the dorsal/ventral axis are linked through the function of
"the organizer", a small group of cells associated with the blastopore
within which a number of interacting developmental pathways intersect.
We decided to examine the validity of the diploblast/triploblast separation
at the molecular level, by using the expression patterns of appropriate genes
as they have become available through our EST studies. By comparing these gene
expression patterns to those of their bilaterian orthologs we should gain insights
into the evolution of the organizer.
Research Outcomes: Genes which we have characterized in connection with this
study include orthologs of the Drosophila genes snail, orthodenticle, forkhead,
decapentaplegic, brachyenteron(Brachyury), and Goosecoid. The expression pattern
of greatest interest in relation to the diploblast-triploblast dichotomy is
that of Acropora snail, which is expressed in tissue invaginating to form endoderm
in a pattern suggestive of its expression in invaginating mesoderm at gastrulation
in Drosophila. Thus, at the molecular level this dichotomy is blurred. The expression
patterns of Acropora BMP2/4 (decapentaplegic) and goosecoid are both consistent
with the hypothesis that Acropora is bilateral, in contrast to the usual textbook
Genes studied in this project have come from research supported by the CMGD,
by ARC Discovery Grant DP0344483 Differential expression and functional analysis
of genes controlling metamorphosis and early neurogenesis of a model lower animal,
the coral Acropora and by internal funding from the Research School of Biological
Sciences, Australian National University.
Hayward, D.C., Trueman, J.W.H., Bastiani, M.J., Ball, E.E. (2005) The structure
of the USP/RXR of Xenos pecki indicates that Strepsiptera are not closely related
to Diptera. Development, Genes and Evolution 215: 213-9
Hislop, N.R., de Jong, D., Hayward, D.C., Ball, E.E., Miller, D.J. (2005). Tandem
organization of independently duplicated homeobox genes in the basal cnidarian
Acropora millepora. Development, Genes and Evolution 215: 268-273
Miller, D.J., Ball E.E. (2005) Animal Evolution: The enigmatic phylum placozoa
revisited. Current Biology 1: R26-R28
Miller, D.J., Ball, E.E., Technau, U. (2005) Cnidarians and ancestral genetic
complexity in the animal kingdom. TRENDS in Genetics 21: 536-9.
Ball, E.E., Hayward, D.C., Saint, R., Miller, D.J. (2004) A simple plan - cnidarians
and the origins of developmental mechanisms. Nature Reviews Genetics 5: 567-77
Hayward, D.C., Miller, d.J., Ball, E.E. (2004) snail expression during embryonic
development of the coral Acropora: blurring the diploblast/trploblast divide?
Development, Genes and Evolution 214: 257-60
Hayward D.C., Dhadialla, T.S., Zhou, S., Kuiper, M.J., Ball, E.E., Wyatt, G.R.,
Walker, V.K. (2003) Ligand specificity and developmental expression of RXR and
ecdysone receptor in the migratory locust. Journal of Insect Physiology 49:
Miller, S.W., Hayward, D.C., Bunch, T.A., Miller, D.J., Ball, E.E., Bardwell,
V.J., Zarkower, D., Brower, D.L. (2003) A DM domain protein from a coral, Acropora
millepora, homologous to proteins important for sex determination. Evolution
& Development 5: 251-8
Ball, E.E., Hayward, D.C., Reece-Hoyes, J.S., Hislop, N.R., Samuel, G., Saint,
R., Harrison, P.L., Miller, D.J. (2002) Coral development: from classical embryology
to molecular control. International Journal of Developmental Biology 46: 671-8
Hayward, D.C., Samuel, G., Pontynen, P.C., Catmull, J., Saint, R., Miller, D.J.,
Ball, E.E. (2002) Localized expression of a dpp/BMP2/4 ortholog in a coral embryo.
Proceedings of the National Academy of Sciences USA 99:8106-11
Kayserili, H., Cox, T.C., Cox, L.L., Basaran, S., Kylyc, G., Ballabio, A., Yüksel-Apak,
M. (2001) Molecular characterization of a new case of Microphthalmia with Linear
Skin defects (MLS): implications for the molecular and clinical classification
of the syndrome. Journal of Medical Genetics 38, 411-417