Download Cell Action in Evolution - James A. Shapiro

"Cell Action in Evolution"
James A. Shapiro
University of Chicago
[email protected] http://shapiro.bsd.uchicago.edu • Shapiro, JA. 2005. A 21st Century View Of Evolution: Genome System Architecture,
Repetitive DNA, And Natural Genetic Engineering. Gene 345: 91-100 • Shapiro JA 2010. Mobile DNA and evolution in the 21st Century. Mobile DNA 1:4.
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?
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)
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): 1456-1460. Documented
Horizontal
Transfers
The virosphere – NCLDVs and interkingdom DNA exchange
Jonathan Filée &Michael Chandler. Gene Exchange and the Origin of Giant Viruses.
Intervirology 2010;53:354–361
red corresponds to
bacterial type genes,
blue to eukaryotic
genes, green to
NCDLV genes and
black to the orphan
genes.
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, 860 - 921 (2001) What genomes teach: dispersed repeats in the human genome
International Human Genome Sequencing Consortium. Initial sequencing and analysis of
the human genome. Nature 409, 860 - 921 (2001)
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.
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
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, 431:569-573.
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
Temporal & metabolic regulation of natural genetic
engineering
araB
U118
lacZ
Derepression
(42C, starvation)
ClpPX, Lon RpoS
200
MuA, HU, IHF
CDC/Target complex
U118
araB
lacZ
Strand transfer
U118
STC = strand transfer complex
MuB for replication
(Crp-dependent starvationinduced functions inhibit
araB
and/or replace MuB?)
lacZ
Replication
(exponential growth)
ClpX
ClpX
lacZ
araB
DNA processing
(RpoS-, Crp-dependent
functions?)
araB
lacZ
U118
Adjacent inversion (precludes fusion)
araB-lacZ fusion
Total fusion colonies
Transposasome
formation
MCS2 (2 subclones)
100
MCS1366 (4 subclones)
0
0
10
20
Days/32
Shapiro, J.A. and D. Leach. 1990. Action of a transposable element in coding sequence fusions. Genetics 126, 293-299.
Shapiro, J.A. 1997. Genome organization, natural genetic engineering, and adaptive mutation. Trends in Genetics 13, 98-104
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. 2007. Discrete Small RNA Generating Loci as Master Regulators of Transposon Activity in
Drosophila. Cell, Vol 128, 1089-1103,
Endogenous small RNAs in plants (special loci?)
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, 171-178(9 November 2006) doi:10.1038/nature 05230 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.
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 2008 320: 486-488. See also G. L. Stebbins, Jr. Cataclysmic
Evolution. Scientific American April
1951, Volume 184 No 4 pp54 –59. What genomes
teach:
duplications in
vertebrate
evolution
• Jurg Spring. Genome duplication strikes back. Nature
Genetics †31, 128 - 129 (2002) doi:10.1038/ng0602-128
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;17:1254-­‐1265 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, 2007 24:670-678.
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)
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)
21st 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).