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Comparative Study
. 2008 May 8;453(7192):175-83.
doi: 10.1038/nature06936.

Genome analysis of the platypus reveals unique signatures of evolution

Wesley C Warren  1 , LaDeana W Hillier, Jennifer A Marshall Graves, Ewan Birney, Chris P Ponting, Frank Grützner, Katherine Belov, Webb Miller, Laura Clarke, Asif T Chinwalla, Shiaw-Pyng Yang, Andreas Heger, Devin P Locke, Pat Miethke, Paul D Waters, Frédéric Veyrunes, Lucinda Fulton, Bob Fulton, Tina Graves, John Wallis, Xose S Puente, Carlos López-Otín, Gonzalo R Ordóñez, Evan E Eichler, Lin Chen, Ze Cheng, Janine E Deakin, Amber Alsop, Katherine Thompson, Patrick Kirby, Anthony T Papenfuss, Matthew J Wakefield, Tsviya Olender, Doron Lancet, Gavin A Huttley, Arian F A Smit, Andrew Pask, Peter Temple-Smith, Mark A Batzer, Jerilyn A Walker, Miriam K Konkel, Robert S Harris, Camilla M Whittington, Emily S W Wong, Neil J Gemmell, Emmanuel Buschiazzo, Iris M Vargas Jentzsch, Angelika Merkel, Juergen Schmitz, Anja Zemann, Gennady Churakov, Jan Ole Kriegs, Juergen Brosius, Elizabeth P Murchison, Ravi Sachidanandam, Carly Smith, Gregory J Hannon, Enkhjargal Tsend-Ayush, Daniel McMillan, Rosalind Attenborough, Willem Rens, Malcolm Ferguson-Smith, Christophe M Lefèvre, Julie A Sharp, Kevin R Nicholas, David A Ray, Michael Kube, Richard Reinhardt, Thomas H Pringle, James Taylor, Russell C Jones, Brett Nixon, Jean-Louis Dacheux, Hitoshi Niwa, Yoko Sekita, Xiaoqiu Huang, Alexander Stark, Pouya Kheradpour, Manolis Kellis, Paul Flicek, Yuan Chen, Caleb Webber, Ross Hardison, Joanne Nelson, Kym Hallsworth-Pepin, Kim Delehaunty, Chris Markovic, Pat Minx, Yucheng Feng, Colin Kremitzki, Makedonka Mitreva, Jarret Glasscock, Todd Wylie, Patricia Wohldmann, Prathapan Thiru, Michael N Nhan, Craig S Pohl, Scott M Smith, Shunfeng Hou, Mikhail Nefedov, Pieter J de Jong, Marilyn B Renfree, Elaine R Mardis, Richard K Wilson
Affiliations
Comparative Study

Genome analysis of the platypus reveals unique signatures of evolution

Wesley C Warren et al. Nature. .

Erratum in

  • Nature. 2008 Sep 11;455(7210):256. Nefedov, Mikhail [added]; de Jong, Pieter J [added]

Abstract

We present a draft genome sequence of the platypus, Ornithorhynchus anatinus. This monotreme exhibits a fascinating combination of reptilian and mammalian characters. For example, platypuses have a coat of fur adapted to an aquatic lifestyle; platypus females lactate, yet lay eggs; and males are equipped with venom similar to that of reptiles. Analysis of the first monotreme genome aligned these features with genetic innovations. We find that reptile and platypus venom proteins have been co-opted independently from the same gene families; milk protein genes are conserved despite platypuses laying eggs; and immune gene family expansions are directly related to platypus biology. Expansions of protein, non-protein-coding RNA and microRNA families, as well as repeat elements, are identified. Sequencing of this genome now provides a valuable resource for deep mammalian comparative analyses, as well as for monotreme biology and conservation.

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Figures

Figure 1
Figure 1. Emergence of traits along the mammalian lineage
Amniotes split into the sauropsids (leading to birds and reptiles) and synapsids (leading to mammal-like reptiles). These small early mammals developed hair, homeothermy and lactation (red lines). Monotremes diverged from the therian mammal lineage ~166 Myr ago and developed a unique suite of characters (dark-red text). Therian mammals with common characters split into marsupials and eutherians around 148 Myr ago (dark-red text). Geological eras and periods with relative times (Myr ago) are indicated on the left. Mammal lineages are in red; diapsid reptiles, shown as archosaurs (birds, crocodilians and dinosaurs), are in blue; and lepidosaurs (snakes, lizards and relatives) are in green.
Figure 2
Figure 2. Platypus miRNAs
a, Platypus has miRNAs shared with eutherians and chickens, and a set that is platypus-specific. miRNAs cloned from six platypus tissues were assigned to families based on seed conservation. Platypus miRNAs and families were divided into classes (indicated) based on their conservation patterns with eutherian mammals (mouse/human) and with chicken. b, Expression of platypus miRNAs. The cloning frequency of each platypus mature miRNA sequenced more than once is represented by a vertical bar and clustered by conservation pattern. miRNAs from a set of monotreme-specific miRNA clusters that are expressed in testis are shaded in red.
Figure 3
Figure 3. The platypus chemosensory receptor gene repertoire
a, b, The platypus genome contains only few olfactory receptor genes from olfactory receptor families that are greatly expanded among therians (three other mammals and a reptile shown), but many genes in olfactory receptor family 14 (a), and relatively numerous vomeronasal type 1 (V1R) receptors (b). These schematic phylogenetic trees show relative family sizes and pseudogene contents of different gene families (enumerated beside internal branches) and the V1R repertoire in platypus. Pie charts illustrate the proportions of intact genes (heavily shaded) versus disrupted pseudogenes (lightly shaded).
Figure 4
Figure 4. The evolution of β-defensin peptides in platypus venom gland
The diagram illustrates separate gene duplications in different parts of the phylogeny for platypus venom defensin-like peptides (vDLPs), for lizard venom crotamine-like peptides (vCLPs) and for snake venom crotamines. These venom proteins have thus been co-opted from pre-existing non-toxin homologues independently in platypus and in lizards and snakes.
Figure 5
Figure 5. Comparative mammalian analysis for a representative eutherian imprinted gene cluster (PEG1/MEST)
a, The gene arrangement is conserved between mammals. However, non-coding regions are expanded in therians. Arrows indicate genes and the direction of transcription; the scale shows base pairs. b, Summary of repeat distribution for the PEG1/MEST cluster. Histograms represent the sequence (%) masked by each repeat element within the MEST cluster; black bars represent repeat distribution across the entire genome. With the exception of SINEs, platypus has fewer repeats of LINEs, LTRs, DNA and simple repeats (Simple) than eutherian mammals. Low comp., low complexity; sRNAs, small RNAs.
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