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RNA Diversity Lecture 12 microRNAs and Metazoan Complexity by John R. Finnerty RNA Diversity Type Length Function mRNA ~500 - 4500 nt encode proteins tRNA ~80 nt translation rRNA 18S mouse (1.9 kb) translation; catalytic component of ribosomes; (large subunit: 28S mouse (4.7 kb) 5S, 5.8S 28S) (small subunit: 18S) miRNA 21-22 nt bind and generally repress complementary mRNAs siRNAs 21-25 nt similar to miRNAs, bind and generally repress mRNAs long ncRNAs >200 nt regulate transcription; many are not polyadenylated; the Xist RNA (17,000 nt long) plays a key role in X-chromosome inactivation snRNAs ~150 nt part of the spliceosome complex which removes introns from pre-mRNAs to make mature mRNAs snoRNAs 60-300 nt located in the nucleolus, these participate in nucleotide modifications of rRNAs, tRNAs, snRNAs, or mRNAs “One of the most interesting challenges facing paleobiologists is explaining the Cambrian explosion, the dramatic appearance of most metazoan animal phyla in the Early Cambrian, and the subsequent stability of these body plans over the ensuing 530 million years.” The mystery of the Cambrian explosion “First, although chock full of organic forms, the Ediacaran is remarkably reticent with its animal ancestors—besides sponges, only Kimberella has received broad acceptance as a metazoan, possibly a molluscan metazoan.” The mystery of the Cambrian explosion “And second, the geologic fossil record is a fairly accurate representation of biotic evolution such that both molecular clock analyses and paleoecological considerations agree that mobile macrophagous animals are no older than about the Ediacaran itself.” Non-BILATERIA 3 phyla / 20,000 described species Porifera Ctenophora Cnidaria Deuterostomia Ecdysozoa Lophotrochozoa Chordata Arthropoda Annelida Hemichordata Onychophora Mollusca EchinodermataNematoda Platyhelminthes Acoelomorpha Silicispongiae Calcispongia PROTOSTOMIA 525 MYA ~600 MYA BILATERIA 30 phyla / 1.5 million described species “Explosions” or rapid radiations of particular taxa Mammals, Pollinating Insects, Angiosperms Dinosaurs Many Insects Orders Gymnosperms Bony fishes Coelomate metazoa Pre-coelomate metazoa Two Early Metazoan Fossil Assemblages Ediacaran Cambrian Key site Ediacara Hills, Burgess Shale, Australia Canadian Rockies Fossil Sandstone Shale bearing (coarse grain) (fine grain) rocks Range of 580-565 MYA 544-525 dates Two Early Metazoan Fossil Assemblages Ediacaran Cambrian Niches Sessile benthic Sessile benthic organisms occupied organisms (epifaunal) Drifting pelagic organisms Drifting pelagic Directed swimmers organisms Benthic crawlers Burrowing animals (infaunal) Body plans medusoid forms medusoid forms fronds fronds possible bilaterians? worms e.g., Kimberella, which shelled animals some suggest is a mollusc like animal; undulatory swimmers Dickinsonia which some segmented animals suggested is an annelid- animals with paired like animal. appendages Two Early Metazoan Fossil Assemblages Ediacaran Cambrian Ancient NON-BILATERIA NON-BILATERIA metazoan Porifera ! Porifera ! lineages represented Ctenophora " Ctenophora ! Cnidaria ? Cnidaria ! BILATERIA BILATERIA Deuterostomia " Deuterostomia ! Lophotrochozoa ? Lophotrochozoa ! Ecdysozoa " Ecdysozoa ! ! Ediacaran faunal assemblage Crucible of Creation, Simon Conway Morris,1998 Ediacaran Medusoid & Frond Charnia masoni Mawsonites spriggi An Ediacaran Annelid? Dickinsonia An Enigmatic Ediacaran Spriggina — Frond or benthic crawler? head shield holdfast (anchor) Cambrian fossils—the Burgess Shale Charles Doolittle Walcott Typical Cambrian Preservation Burgess Shale—Preservation Quality Pennatulaceans (Cnidaria:Anthozoa) Ediacaran Burgess extant Charniodiscus Thaumaptilon Cambrian sponge Eiffelia Burgess sponge Vauxia gracilenta Burgess polychaete annelid Burgessochaeta setigera Burgess Onychophoran Aysheaia Peripatus Burgess Chordate Pikaia Branchiostoma Burgess Chordate Ctenorhabdotus Mnemiopsis Trace Fossils Lower Cambrian Upper Cambrian Possible Passive Flow Network Spiral-Sinusoidal McMenamin & McMenamin, 1990 Cambrian faunal assemblage Crucible of Creation, Simon Conway Morris,1998 Cambrian infaunal assemblage Crucible of Creation, Simon Conway Morris,1998 Cambrian faunal assemblage Crucible of Creation, Simon Conway Morris,1998 Ecological Trigger “The marine ecosystem of the Ediacaran was primarily benthic, with macroscopic organisms largely restricted to the sediment–water interface, whereas the explosion of animals in the Cambrian changed this two-dimensional world into one of three dimensions with macrophagous eumetaozans invading both the infaunal benthos as well as the pelagos. In fact, the origin of these macrophagous mobile metazoans early in the Ediacaran is most likely the trigger of the Cambrian explosion itself.” Genome Hypothesis “The genome hypothesis suggests that the metazoan genome has changed through time, initially allowing for a relatively broad exploration of metazoan morphospace, but becoming more and more canalized since the Cambrian, which generally precluded the ability to evolve new high-level morphological innovations once phyla evolved.” Canalization A concept developed by Waddington. A reduction the degree of phenotypic variation that is caused by either environmental variation or genomic variation. Waddington’s “epigenetic landscape.” Canalization A concept developed by Waddington. A reduction the degree of phenotypic variation that is caused by either environmental variation or genomic variation. Problems with Genome Hypothesis “....two problems exist when thinking about this genomic hypothesis. First, contrary to expectation, the genomes of protostomes and deuterostomes, the animals that make up the taxonomic bulk of the ‘‘Cambrian explosion,’’ are not only similar in terms of the developmental tool kit (i.e., the types and diversity of components that regulate gene expression), but much of this tool kit is now known to exist in cnidarians and even sponges. Second, when thinking about the subsequent constraints upon phylum-level body plan evolution, if genomic constraints are operational in metazoan macroevolution, then they must have been acquired numerous times independently by each major phylum of animals.” “Temporal Asymmetry of Morphological Innovation” “morphological variation higher in earlier representatives as compared to later representatives” “Temporal Asymmetry of Morphological Innovation” “morphological variation higher in earlier representatives as compared to later representatives” Early trilobite species (left, order Redlichiida, early Cambrian) exhibit more morphological variation than later species (right, order Phacopida, Ordivician) “Temporal Asymmetry of Morpological Innovation” “....not only was morphological variation higher in earlier representatives as compared to later representatives, but that protostomes and deuterostomes have indeed acquired numerous and novel genes with each phylum having its own unique repertoire, and that these genes are continually being acquired by animals through geologic time. We hypothesize that these genes, known as microRNAs (miRNAs), serve to both increase complexity and canalization, and thus they might shape, at least in part, the macroevolutionary history of Metazoa.” MicroRNAs The first microRNA, lin-4, was discovered in the nematode C. elegans in 1993. Cell. 1993 Dec 3;75(5):843-54. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Lee RC, Feinbaum RL, Ambros V. Harvard University, Department of Cellular and Developmental Biology, Cambridge, Massachusetts 02138. Abstract lin-4 is essential for the normal temporal control of diverse postembryonic developmental events in C. elegans. lin-4 acts by negatively regulating the level of LIN-14 protein, creating a temporal decrease in LIN-14 protein starting in the first larval stage (L1). We have cloned the C. elegans lin-4 locus by chromosomal walking and transformation rescue. We used the C. elegans clone to isolate the gene from three other Caenorhabditis species; all four Caenorhabditis clones functionally rescue the lin-4 null allele of C. elegans. Comparison of the lin-4 genomic sequence from these four species and site-directed mutagenesis of potential open reading frames indicated that lin-4 does not encode a protein. Two small lin-4 transcripts of approximately 22 and 61 nt were identified in C. elegans and found to contain sequences complementary to a repeated sequence element in the 3' untranslated region (UTR) of lin-14 mRNA, suggesting that lin-4 regulates lin-14 translation via an antisense RNA-RNA interaction. MicroRNAs The widespread importance of microRNAs was not recognized until the discovery that let-7 was widely conserved in Bilateria. Nature. 2000 Nov 2;408(6808):86-9. Conservation of the sequence and temporal expression of let-7 heterochronic regulatory RNA. Pasquinelli AE, Reinhart BJ, Slack F, Martindale MQ, Kuroda MI, Maller B, Hayward DC, Ball EE, Degnan B, Müller P, Spring J, Srinivasan A, Fishman M, Finnerty J, Corbo J, Levine M, Leahy P, Davidson E, Ruvkun G. Department of Molecular Biology, Massachusetts General Hospital, Harvard Medical School, Boston 02114, USA. Abstract Two small RNAs regulate the timing of Caenorhabditis elegans development. Transition from the first to the second larval stage fates requires the 22-nucleotide lin-4 RNA, and transition from late larval to adult cell fates requires the 21-nucleotide let-7 RNA. The lin-4 and let-7 RNA genes are not homologous to each other, but are each complementary to sequences in
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