Genetic Toolkits and Multicellularity

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Teleological (July 11, 2010, 20:00:04 PM):
Origins of Multicellularity: All in the Family

ScienceDaily (July 9, 2010) — One of the most pivotal steps in evolution-the transition from unicellular to multicellular organisms-may not have required as much retooling as commonly believed, found a globe-spanning collaboration of scientists led by researchers at the Salk Institute for Biological Studies and the US Department of Energy's Joint Genome Institute

A comparison of the genomes of the multicellular algae Volvox carteri and its closest unicellular relative Chlamydomonas reinhardtii revealed that multicellular organisms may have been able to build their more complex molecular machinery largely from the same list of parts that was already available to their unicellular ancestors.

"If you think of proteins in terms of lego bricks Chlamydomonas already had a great lego set," says James Umen, Ph.D., assistant professor in the Plant Molecular and Cellular Biology Laboratory at the Salk Institute. "Volvox didn't have to buy a new one, and instead could experiment with what it had inherited from its ancestor."

Altogether the findings, published in the journal Science, suggest that very limited protein-coding innovation occurred in the Volvox lineage. "We expected that there would be some major differences in genome size, number of genes, or gene families sizes between Volvox and Chlamydomonas," says Umen. "Mostly that turned out not to be the case."

The evolution of multicellularity occurred repeatedly and independently in diverse lineages including animals, plants, fungi, as well as green and red algae. "This transition is one of the great evolutionary events that shaped life on earth," says co-first author Simon E. Prochnik, Ph.D., a Computationial Scientist at the DOE Joint Genome Institute. "It has generated much thought and speculation about what makes multicellular organisms different or more complex than their unicellular ancestors."

In most cases the switch from a solitary existence to a communal one happened so long ago-over 500 million years-that the genetic changes enabling it are very difficult to trace. An interesting exception to the rule are volvocine green algae. For them, the transition to multicellularity happened in a series of small, potentially adaptive changes, and the progressive increase in morphological and developmental complexity can still be seen in contemporary members of the group (see slide show).

Volvox, the most sophisticated member of the lineage, is believed to have evolved from a Chlamydomonas-like ancestor within the last 200 million years, making the two living organisms an appealing model to study the evolutionary changes that brought about multicellularity and cellular differentiation.

To gather data for the comparative genomic analysis, the researchers sequenced the 138 million base pair Volvox genome using a whole genome shotgun strategy. The genome itself is 17% larger than the previously sequenced genome of Chlamydomonas and the sequence divergence between the two is comparable to that between human and chicken.

Despite the modest increase in genome size, the number of predicted proteins turned out to be very similar for the two organisms (14,566 in Volvox vs. 14,516 in Chlamydomonas) and no significant differences could be identified in the repertoires of protein domains or domain combinations. Protein domains are parts of proteins that can evolve, function, and exist independently of the rest of the protein chain.

"This was somewhat unexpected," explains Umen, "since innovation at the domain level was previously thought to play a role in the evolution of multicellularity in the plant and animal lineages."

In contrast to the overall lack of innovation, protein families specific to volvocine algae, such as extracellular matrix proteins, were enriched in Volvox compared to Chlamydomonas. Each mature Volvox colony is composed of numerous flagellated cells similar to Chlamydomonas, which are embedded in the surface of a spheroid of elaborately patterned extracellular matrix (ECM) that is clearly related to the Chlamydomonas cell wall. Maybe not surprisingly, the difference in size and complexity between the Volvox extracellular matrix and Chlamydomonas cell wall is mirrored by a dramatic increase in the number and variety of Volvox genes for two major ECM protein families, pherophorins and VMPs.

Additionally, Umen and his collaborators identified an increase in the number of cyclin D proteins in Volvox, which govern cell division and may be necessary to ensure the complex regulation of cell division during Volvox development. Last but not least, Volvox adapted a few of its existing genes to acquire novel functions. Members of the pherophorin family, for one, not only help build the extracellular matrix; some subtypes evolved into a diffusible hormonal trigger for sexual differentiation.

Researchers who also contributed to this work include Alan Kuo, Uffe Hellsten, Jarrod Chapman, Astrid Terry, Jasmyn Pangilinan, Asaf Salamov, Harris Shapiro, Erika Lindquist, Susan Lucas, Igor V Grigoriev, Harris Shapiro and Daniel S. Rokhsar at U.S. Department of Energy Joint Genome Institute in Walnut Creek, Patrick Ferris at the Salk Institute for Biological Studies, Aurora Nedelcu at the University of New Brunswick in Fredericton, Canada, Arman Hallmann at the University of Bielefeld, Germany, Stephen M. Miller at the University of Maryland, Baltimore, Ichiro Nishii at the Nara Women's University in Nara-shi, Japan, Lillian K. Fritz-Laylin at the Center for Integrative Genomics, Berkeley, Oleg Simakov at the EMBL in Heidelberg, Germany, Stefan A. Rensing at the University of Freiburg, Germany, Vladimir Kapitonov and Jerzy Jurka at the Genetic Information Research Institute in Mountain View, Jeremy Schmutz at the HudsonAlpha Institute in Huntsville, Rüdiger Schmitt at the University of Regensburg, Germany and David Kirk at Washington University in St. Louis.

Looks like multicellularity was inevitable... again... and again.
Teleological (August 05, 2010, 07:43:55 AM):
More preadaptations:
Genome of Ancient Sponge Reveals Origins of First Animals, Cancer
ScienceDaily (Aug. 4, 2010) — The sponge, which was not recognized as an animal until the 19th century, is now the simplest and most ancient group of animals to have their genome sequenced.

In a paper appearing in the August 5 issue of the journal Nature, a team of researchers led by Daniel Rokhsar of the University of California, Berkeley, and the Department of Energy's Joint Genome Institute (JGI), report the draft genome sequence of the sea sponge Amphimedon queenslandica and several insights the genome gives into the origins of both the first animals and cancer.

All living animals are descended from the common ancestor of sponges and humans, which lived more than 600 million years ago. A sponge-like creature may have been the first organism with more than one cell type and the ability to develop from a fertilized egg produced by the merger of sperm and egg cells.- that is, an animal.

"Our hypothesis is that multicellularity and cancer are two sides of the same coin," said Rokhsar, program head for computational genomics at JGI and a professor of molecular and cell biology and of physics at UC Berkeley. "If you are a cell in a multicellular organism, you have to cooperate with other cells in your body, making sure that you divide when you are supposed to as part of the team. The genes that regulate this cooperation are also the ones whose disruption can cause cells to behave selfishly and grow in uncontrolled ways to the detriment of the organism."

As part of the new analysis, the team looked in the sponge genome for more than 100 genes that have been implicated in human cancers and found about 90 percent of them. Future research will show what roles these genes play in endowing sponge cells with team spirit.

Sponges are often described as the "simplest" living animals, while humans are considered relatively "complex," but how this differential complexity is encoded in the genome is still a major question in biology The new study shows that, while the sponge genome contains most of the gene families found in humans, the number of genes in each family has changed significantly over the past 600 million years. By analyzing which gene families were enriched or depleted in different groups of animals, the authors identified groups of gene functions that are associated with morphological complexity.

"The genome raises questions of what it means to be an animal," said first author Mansi Srivastava, a former UC Berkeley graduate student who now is a post-doctoral associate at the Whitehead Institute for Biomedical Research in Cambridge, Mass.

"Though we think of a sponge as a simple creature whose skeleton we take to the bathtub, it has a lot of the major biochemical and developmental pathways we associate with complex functions in humans and other more complex animals," she said. "But there are certain missing components. Future studies will reveal how sponges operate as bona fide animals without those components, and how the addition of those components led to the evolution of more complex animals."

Some of the missing components are involved in the cell cycle, the series of steps cells go through in order to divide. Among these is the enzyme family known as cyclin-dependent kinase 4/6 (CDK 4/6), which in mammals is crucial to transitioning between phases of the cell cycle. Though CDK4/6 was not found in the sponge genome, it is present in the sea anemone genome, raising the question of whether the appearance of CDK4/6 in the ancestor of "true" animals (eumetazoans) changed the animal cell cycle in a fundamental way. Inhibitors of CDK 4/6 halt the cell cycle and are used to treat breast cancer.

The authors also identified in the sponge many of the same genes that characterize all other animals: genes involved not only in cell division and growth, but also in programmed cell death; the adhesion of cells to other tissue and to one another, signaling pathways during development, recognition of self and non-self; and genes leading to the formation of different cell types.

What sponges lack, however, are a gut, muscles and neurons.

"This incredibly old ancestor possessed the same core building blocks for multicellular form and function that still sits at the heart of all living animals, including humans," said coauthor Bernie Degnan, a professor of biology at the University of Queensland, Australia, who collected the sponge whose genome was sequenced from the Great Barrier Reef. "It now appears that the evolution of these genes not only allowed the first animals to colonize the ancient oceans, but underpinned the evolution of the full biodiversity of animals we see today."

According to Degnan, essentially all the genomic innovations that we deem necessary for intricate modern animal life have their origins much further back in time that anyone anticipated, predating the Cambrian explosion by tens if not hundreds of millions of years.

"What marked the evolutionary origin of animals was the ability of individual cells to assume specialized properties and work together for the greater good of the entire organism. The sponge represents a window on this ancient and momentous event," said coauthor Dr. Kenneth S. Kosik, the Harriman Professor of Neuroscience at UC Santa Barbara and co-director of the Neuroscience Research Institute.

"Remarkably, the sponge genome now reveals that, along the way toward the emergence of animals, genes for an entire network of many specialized cells evolved and laid the basis for the core gene logic of organisms that no longer functioned as single cells," he said, "but as a cooperative community of specialized cells all geared toward the survival of a complex multi-cellular creature."

"The beauty of having this genome is that now we can ask about all known biological processes, and go through hundreds of genes to tell definitively whether or not our common animal ancestor had them or not," Srivastava said.

The sponge genome may also have more practical implications, according to Degnan.

"Sponges produce an amazing array of chemicals of direct interest to the pharmaceutical industry," he said. "They also biofabricate silica fibers directly from sea water in an environmentally benign manner, which is of great interest in communications. With the genome in hand, we can decipher the methods used by these simple animals to produce materials that far exceed our current engineering and chemistry capabilities."


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