"Cell Action in Evolution"
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1 "Cell Action in Evolution" James A. Shapiro University of Chicago Shapiro, JA A 21 st Century View Of Evolution: Genome System Architecture, Repetitive DNA, And Natural Genetic Engineering. Gene 345: Shapiro JA Mobile DNA and evolution in the 21 st Century. Mobile DNA 1:4.
2 Outstanding Questions Still at Issue in 21st Century Evolutionary Theory Where does novelty come from in evolution? (Nothing for selection to do with no differences.) Descent with modification: tree/web of life? how many cell types in the beginning? role of virosphere? Nature of heredity and hereditary change: vertical/ horizontal transmission, passive/active variations, micro/macromutations, isolated/interactive germ plasm, Central Dogma still valid? Role of selection: positive/neutral/purifying? Relationship of evolutionary change to planetary, environmental & ecological events?
3 The major novelty in evolution science: Knowledge of how genome change arises Horizontal Transfer (vectors) Naked DNA and liposomes Viruses Conjugation apparatus Symbionts, parasites and pathogens Cell fusions Fertilization symbiogenesis Natural genetic engineering (generic activities) DNA chain cleavage DNA & RNA chain ligation Polymerization (DNA templates, RNA templates, untemplated)
4 The bacterial apparatus of horizontal transfer DNA uptake during transformation in B. subtilis A. tumefaciens VirB/D4 system Inês Chen, Peter J. Christie, and David Dubnau. The Ins and Outs of DNA Transfer in Bacteria. Science 310 (2005):
5 Documented Horizontal Transfers
6 The virosphere NCLDVs and interkingdom DNA exchange Jonathan Filée &Michael Chandler. Gene Exchange and the Origin of Giant Viruses. Intervirology 2010;53: red corresponds to bacterial type genes, blue to eukaryotic genes, green to NCDLV genes and black to the orphan genes.
7 What genomes teach: protein evolution by domain accretion and shuffling International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, (2001)
8 What genomes teach: dispersed repeats in the human genome International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, (2001)
9 Natural Genetic Engineering: the cell toolkit for genome restructuring Nucleotide substitutions by mutator polymerases DNA import and export systems General and localized recombination systems (HR & NHEJ). Mobile DNA elements and large scale genome rearrangements. Mobile elements that transpose through RNA intermediates and mobilize shorter genome/rna segments. Direct integration of cellular RNAs into the genome by reverse splicing. Adaptive use of natural genetic engineering Protein switching, protein engineering and sex change by DNA rearrangement in diverse organisms. The mammalian immune system as an example of rapid protein evolution and specialization by natural genetic engineering.
10 Natural Genetic Engineering as the Source of Genetic Novelties Point mutation by trans-lesion polymerases DNA rearrangement modules (site-specific, cassettes, transposons, tandem arrays) - new insertions, large & small scale rearrangements (deletions, duplications, inversions) Retrotransposition, retrotransduction and reverse splicing - small scale rearrangements, amplification of coding sequences, exon accretion & shuffling Formation of novel exons - mobile element insertion and splice site selection (exonization) Mobile element insertions at dispersed locations to create new regulatory circuits
11 Natural genetic engineering in evolution: Pack MULE exon shuffling in the rice genome Jiang N, Bao Z, Zhang X, Eddy SR, Wessler SR: Pack-MULE transposable elements mediate gene evolution in plants. Nature 2004, 431:
12 Two critical implications of genetic change as cell activity regulation & targeting (i.e., non-randomness) Molecular control of transcription, translation and activities of essential proteins Specialized genome immunity systems CRISPRs in prokaryotes pirna loci in eukaryotes Responses to multiple stimuli, especially Nutritional stress Alarm signals Infection and endosymbiosis (abnormal cell fusions) Hybridization and changes in ploidy
13 Temporal & metabolic regulation of natural genetic engineering arab ClpPX, Lon RpoS MuA, HU, IHF U118 lacz Derepression (42C, starvation) Transposasome formation 200 MuB for replication (Crp-dependent starvationinduced functions inhibit and/or replace MuB?) arab arab U118 U118 CDC/Target complex Strand transfer STC = strand transfer complex lacz lacz Total fusion colonies 100 MCS2 (2 subclones) arab Replication (exponential growth) U118 ClpX Adjacent inversion (precludes fusion) lacz ClpX DNA processing (RpoS-, Crp-dependent functions?) arab lacz arab-lacz fusion 0 MCS1366 (4 subclones) Days/32 Shapiro, J.A. and D. Leach Action of a transposable element in coding sequence fusions. Genetics 126, Shapiro, J.A Genome organization, natural genetic engineering, and adaptive mutation. Trends in Genetics 13,
14 ncrna-directed regulation of natural genetic engineering CRISPRs (Clustered Regularly Interspaced Short Palindromic Repeats in prokaryotes) Brouns et al., Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes. Science 321, 960 (2008) pirna loci (Drosophila, mammals) Flamenco Brennecke, et al Discrete Small RNA Generating Loci as Master Regulators of Transposon Activity in Drosophila. Cell, Vol 128, , Endogenous small RNAs in plants (special loci?)
15 What genomes teach: whole genome duplications in Paramecium speciation Global trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia Jean-Marc Aury, et al. Nature 444, (9 November 2006) doi: /nature Here we show that in the unicellular eukaryote Paramecium tetraurelia, a ciliate, most of the nearly 40,000 genes arose through at least three successive whole-genome duplications. Phylogenetic analysis indicates that the most recent duplication coincides with an explosion of speciation events that gave rise to the P. aurelia complex of 15 sibling species. We observed that gene loss occurs over a long timescale, not as an initial massive event.
16 Genome Duplications in Angiosperm Evolution ( That abominable mystery ) Haibao Tang, John E. Bowers, Xiyin Wang, Ray Ming, Maqsudul Alam, and Andrew H. Paterson. Synteny and Collinearity in Plant Genomes. Science 25 April : See also G. L. Stebbins, Jr. Cataclysmic Evolution. Scientific American April 1951, Volume 184 No 4 pp54 59.
17 What genomes teach: duplications in vertebrate evolution Jurg Spring. Genome duplication strikes back. Nature Genetics 31, (2002) doi: /ng
18 Whole genome duplica0ons in vertebrate evolu0on Nakatani Y. et.al Reconstruc2on of the vertebrate ancestral genome reveals dynamic genome reorganiza2on in early vertebrates. Genome Res. 2007;17:
19 Network Evolution by Whole Genome Duplication A. S. Veron, K. Kaufmann, and E. Bornberg-Bauer. Evidence of Interaction Network Evolution by Whole-Genome Duplications: A Case Study in MADS-Box Proteins. Mol Biol Evol March 1, :
20 Molecular Targeting of Natural Genetic Engineering DNA sequence homology - homologous recombination, targeted conversions, cassette exchanges, certain transposons Protein recognition of DNA sequences and secondary structures (nucleases, recombinases, transposases) RNA base-pairing to DNA guide sequences (reverse splicing, diversity-generating retroelements) Coupling to transcription retrotransposon integration (protein-protein tethering) transcription-dependent DS breaks in B cell CSR V region somatic hypermutation Coupling to chromatin (retrotransposon integration) P-element homing (colocalization in nuclear foci)
21 Searching Genome Space by Natural Genetic Engineering: More Efficient than a Random Walk Guided by Gradual Selection Combinatoric search using established functional modules (e.g. domain accretion and shuffling) Activation when most biologically useful by genome shock (including starvation, infection, hybridization) ==> bursts of coordinated changes Network adaptation after WGD, domain accretion & shuffling, establishment of novel interaction patterns, transcription signal insertions Molecular mechanisms for targeting coincident changes to functionally related locations (research agenda for the coming decades)
22 21 st Century view of evolutionary change: a generalized scenario Ecological disruption ==> changes in biota, food sources, adaptive needs & organismal behavior (cf. Michael Foote). Macroevolution triggered by cell fusions & interspecific hybridizations (WGDs) leading to massive episodes of horizontal transfer, genome rearrangements. Establishment of new cellular and genome system architectures; complex novelties arising from WGD and network exaptation. Survival and proliferation of organisms with useful adaptive traits in depleted ecology; elimination of non-functional architectures; selection largely purifying. Microevolution by localized natural genetic engineering after ecological niches occupied (immune system model).
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