Revisiting Evolution in the 21st Century

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1 Revisiting Evolution in the 21st Century James A. Shapiro University of Chicago Oxford, March 16, 2010

2 Why revisit now? May 8, 2009, debate with Lynn Margulis and Richard Dawkins at Balliol College ftp://eclogite.geo.umass.edu/pub/gaia/homage_to_dar win_part1.mp3 No real discussion of last 50 years research: cell repair, sensory and regulatory networks; signal transduction; natural genetic engineering; epigenetic interfaces with life history events; results of genome sequencing (major roles for cell fusions, horizontal transfer, whole genome doublings) - empirical results that have transformed the conceptual landscape

3 Disentangling basic issues in evolutionary debates Origin of life & the first cells - still on the fringes of serious scientific discussion Descent with modification of all related living organisms - more convincing with each new technological advance (e.g. detailed protein and genome phylogenies) The actual processes of evolutionary change over time - an ever growing number of documented events and molecular possibilities as we learn more about how cells control genome structure

4 Outstanding Questions Still at Issue in 21st Century Evolutionary Theory Descent with modification: tree/web of life, branching/merging topology, how many cell types in the beginning, role of virosphere? Nature of heredity: vertical/horizontal transmission, passive/active variations, micro/macromutations, isolated/interactive germ plasm, influence of life history events, Central Dogma still valid? Role of selection: positive/neutral/purifying? Relationship of evolutionary change to planetary, environmental & ecological events?

5 Molecules involved in cellular information transfer - revisiting the Central Dogma (Shapiro, 2009) 1970: (DNA --> 2X DNA) --> RNA --> Protein --> Phenotype (Crick, Central dogma of molecular biology. Nature 1970, 227: ) 2010: DNA > 0 DNA + Protein + ncrna --> chromatin/epigenetic markings (epigenotype) Chromatin + Protein + ncrna --> DNA replication, chromatin maintenance/reconstitution Protein + RNA + lipids + small molecules --> signal transduction Signals + Chromatin + Protein --> RNA (primary transcript) RNA + Protein + ncrna --> RNA (processed transcript) RNA + Protein + ncrna --> Protein (primary translation product) Protein + nucleotides + Ac-CoA + SAM + sugars + lipids --> Processed and decorated protein DNA + Protein --> New DNA sequence (mutator polymerases, terminal transferases) Chromatin + Protein --> New DNA structure (DNA-based rearrangements) RNA + Protein + chromatin --> New DNA structure and sequence (retrotransposition, retroduction, retrohoming, diversity-generating retroelements) Signals + chromatin + proteins + ncrna + lipids --> nuclear/nucleoid localization Protein + ncrna + chromatin + signals + other molecules + structures <--> Phenotype & Genotype & Epigenotype

6 Major Points 1. Evolution does not have to proceed by small changes and we know from the DNA record that major steps did occur rapidly. 2. DNA change is a cell-regulated, biological process, not a series of infrequent, random, independent accidents. (Genome as RW memory system) 3. We already know of numerous molecular processes that allow us to deal scientifically with complex evolutionary events and with the rapid evolution of complex, multi-component adaptations.

7 Darwin s 1859 gradualist view Origin of Species, p. 194 Darwin s later acknowledgment of other possibilities: "...variations which seem to us in our ignorance to arise spontaneously. It appears that I formerly underrated the frequency and value of these latter forms of variation, as leading to permanent modifications of structure independently of natural selection." (Origin of Species, 6th edition, Chapter XV, p. 395).

Four kinds of rapid, multi-character changes Darwin could not have imagined Multiple cell types and cell fusions in evolution; Horizontal DNA transfer in

8 Four kinds of rapid, multi-character changes Darwin could not have imagined Multiple cell types and cell fusions in evolution; Horizontal DNA transfer in evolution; Genome doublings at key steps of eukaryotic evolution; Built-in mechanisms of genetic change = natural genetic engineering Barbara McClintock, 1951

9 Carl Woese, molecular phylogeny, and three cell kingdoms (1977) Rampant horizontal transfer within & between kingdoms

10 Mitochondria and chloroplasts are endosymbiotic bacteria inside eukaryotic cells

11 What genomes teach: cell fusions at key places in eukaryotic evolution diatoms T. M. Embley and W. Martin Eukaryotic evolution, changes and challenges. Nature 440,

12 Evolution in real time using horizontal DNA transfer: Bacterial antibiotic resistance experimentally confirmed mutation theory of resistance (1950s) clinically resistant bacteria carry transmissible plasmids (Watanabe, 1963)

13 Transmissible Antibiotic Resistance Also transposons, integrons, integrative conjugating elements, genomic islands

14 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 :

15 Genomic duplications in vertebrate evolution Jurg Spring. Genome duplication strikes back. Nature Genetics 31, (2002) doi: /ng

16 What genomes teach: whole genome duplications at the root of vertebrate evolution The 2R hypothesis: an update. Kasahara, M Current Opinion in Immunology 19 (5), pp

17 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, :

18 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)

19 Natural Genetic Engineering Nucleotide substitutions by mutator polymerases DNA import and export systems General and localized recombination systems. 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 changes by diverse organisms. The mammalian immune system as an example of rapid protein evolution and specialization by natural genetic engineering.

20 What genomes teach: protein evolution by domain shuffling International Human Genome Sequencing Consortium. Initial sequencing and analysis of the human genome. Nature 409, (2001)

Wessler SR: Pack-MULE transposable elements mediate

21 Natural genetic engineering in evolution: Pack MULEs 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:

22 Stimuli that Activate Natural Genetic Engineering and Disrupt Epigenetic Silencing Chromosome breaks (McClintock, 1944) Pheromones, hormones & cytokines Starvation (Shapiro, 1984) DNA damage (mutagens) Telomere erosion Antibiotics, Phenolics, Osmolites Oxidants Pressure, Temperature, Wounding Protoplasting & growth in tissue culture Bacterial or fungal infection & endosymbiosis Changes in ploidy & DNA content (genome doubling) Hybridization (interspecific mating)

23 Temporal & metabolic regulation of natural genetic engineering arab U118 lacz ClpPX, Lon RpoS MuA, HU, IHF arab U118 Derepression (42C, starvation) U118 Transposasome formation CDC/Target complex lacz Strand transfer Total fusion colonies MCS2 (2 subclones) MuB for replication (Crp-dependent starvationinduced functions inhibit and/or replace MuB?) arab STC = strand transfer complex lacz 0 MCS1366 (4 subclones) Days/32 Replication (exponential growth) ClpX ClpX DNA processing (RpoS-, Crp-dependent functions?) arab lacz arab lacz U118 Adjacent inversion (precludes fusion) arab-lacz fusion Shapiro, J.A. 1997b. Genome organization, natural genetic engineering, and adaptive mutation. Trends in Genetics 13,

24 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?)

25 21 st Century view of evolutionary change: the importance of a cognitive systems perspective McClintock (1984): In the future, attention undoubtedly will be centered on the genome, with greater appreciation of its significance as a highly sensitive organ of the cell that monitors genomic activities and corrects common errors, senses unusual and unexpected events, and responds to them, often by restructuring the genome. Ecological events and subsequent biological challenges activate natural genetic engineering functions that can act at multiple genomic locations within one or a few generations Molecular basis for rapid genome restructuring affecting multiple adaptive features at the same time in response to abrupt challenges

26 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) ==> coordinated changes network adaptation after WGD, domain shuffling, establishment of novel interaction patterns molecular mechanisms for targeting coincident changes to functionally related locations (research agenda for the coming decades)

27 21 st Century view of evolutionary change: a generalized scenario Ecological disruption ==> changes in biota, food sources, adaptive needs & organismal behavior; 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).

"Cell Action in Evolution"

"Cell Action in Evolution" James A. Shapiro University of Chicago jsha@uchicago.edu http://shapiro.bsd.uchicago.edu Shapiro, JA. 2005. A 21 st Century View Of Evolution: Genome System Architecture, Repetitive