Do plants evolve differently?

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Do plants evolve differently?
Thorsten Reusch IFM-GEOMAR Kiel
Eelgrass megaclone, Aland Islands. Fotograph
Chris Boström,
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Genetic variation as fuel for evolution

• selection
• recombination
• drift
• ultimate input mutation

• usual estimates of mutation rates
• 10-7 -10-9 per nucelotideper generation

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Common views about mutation

• somatic mutation
• -evolutionary dead end
• -often deleterious, e.g. may cause cancer
• -will not be passed into next generation
• -no change of allele frequencies

• meiotic (germline) mutations
• -evolutionary change

animal centered view originating from
overinterpretation of Weismanns germline concept
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Weismanns germline concept 1892
Das Keimplasma eine Theorie der Vererbung. The
germ plasm a theory of heredity 1892
August Weismann 1834-1914
zygote
embyo

• soma cell lines are separate from germline from
  the onset of ontogeny
• only germline cells keep totipotency

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The Weismann barrier

• during modern synthesis provided final blow
  against Lamarckism and pangenesis ideas of Darwin

soma
germline
protein
genetic information
John Maynard Smith The theory of evolution 1993
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Darwins pangenesis theory
...was actually pretty close to Lamarckian ideas

• Pangenesis view introduces gemmules that are
  derived from all body cells and are the carrier
  of hereditary changes
• gemmules collectively migrate to reproductive
  organs
• information from gemmules is somehow tranferred
  to germ cells

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the Weismann barrier

• central to Modern Evolutionary Synthesis!

Weismann is the second most notable evolutionary
theorist of the nineteenth century, after Charles
Darwin.
Ernst Mayr
Weismann was instrumentalized to save Darwin from
Lamarckism
8
But the Weismann barrier is not general
... and this is why botanists never really liked
it
plant meristematic tissue can re-differentiate
into reproductive organs (flowers)
9
moreover plants are modular
Genetic individual or genet (clone)
Module or ramet
Many plants ( animals) are facultative clonal
asexuals to a degree
10
somatic mutation may affect one module
mutation
tree
clone
...and thus defective mutants (e.g.
chlorophyll-) may be nourished by neighboring
twigs/modules
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Consequences of plant modular growth
chlorophyll-defective somatic mutants in mangrove
Klekowski Godfrey Nature 1989
gt plants may carry a somatic genetic load
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Evidence for other somatically derived variation?
Agricultural and horticultural varieties
pink Fosters grapefruit
normal
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Genetic mosaics also possible
Rio red chimera Texas, 1990
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Meristem composed of (two) different genotypes
somatic mutation leads to genetic mosaic
meristemtic tissue of vascular plants is
stratified, i.e. consisting of independently
dividing sublineages
15
spatial arrangement of meristematic tissues...
...determines type of mosaic
Variegated Pelargonium
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Genetic detection of mosaics with microsatellites
...because mutation rates much higher (10-3 -
10-4)
allele (TC)11
allele (TC)10
DNA-Sequence
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Genetic mosaics in grapevine ....
...allow for the separation of different Cabernet
Sauvignon cultivars
Moncada et al Genome 2006
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Mosaic genotypes as mixtures of bi-allelic
genotypes
125131133
125133
125131
step-wise Mutation
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Are there any genetic mosaics in the wild?

• hypotheses
• the larger older the plant, the more important
  become somatic mutations and genetic mosaics
• (and cultivars propgated by grafting are very old
  clones)

• because sexual reproduction restores genetic
  uniformity by introducing a single-cell phase
  (zygote), sexual reproduction should be
  negatively correlated with mosaics

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marine angiosperm Zostera marina
pollen
female flowers
vegetative propoagation
seeds in inflorescens
sexual reproduction
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Z. marina may from very large old clones
in Archipelago and Aland Sea (Baltic) clones are
160 m in extension and possibly gt1000 yr old
Reusch et al 1999
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Using clonal richness as a surrogate for sexual
/ vegetative reproduction
High clonal richness
Low clonal richness
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Detection of mosaics using 2 hypervariable
microsats
site Kolaviken, Archipelago Sea, Finnland
mosaic genotype
locus GA17H
normal bi-allelic genotype
normal bi-allelic genotype
mosaic genotype
normal bi-allelic genotype
locus 35
normal bi-allelic genotype
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Detection of clones using 7 less polymorphic loci
genotypeA
B
C
C
C
D
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normal bi-allelic genotypes can be recovered
seagrass leaf
basal meristematic tissue
step-wise Mutation
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The data set 36 European populations
Nramets 20-60
Aland-Islands 5
ArchipelagoSea 12
NorthSea 8
SW Baltic 5
South Portugal 4
Sampling together with Chris Boström, Jeanine
Olsen, Ester Serrao
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The less sex, the more mutations
Exponential function, R2 0.64 P lt 0.001
4
3
2
Minimal Mutations per clone
1
0
1
.8
.6
.4
.2
0
Clonal Richness
Sex
No sex
Reusch Boström, Evol Ecol in press
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Correlation also present on the basis of
subregions
1.5
Exponential function, R2 0.97 P 0.007
Aland 5
Archipleago, 12
1
Minimal Mutations per clone
0.5
SW Baltic 5
North Sea 8
Portu 4
0
1
.8
.6
.4
.2
0
Mean Clonal Richness
Sex
No sex
Reusch Boström, Evol Ecol in press
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The less sex the fewer mutation-free genotypes
Sex
No sex
Reusch Boström, Evol Ecol in press
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So what..
microsatellite loci are selectively
neutral (tested for Zos mar Oetjen Reusch Mol
Ecol 2007)
nevertheless, microsatellite polymorphism may
indicate potential of processes at level of
selected genes
depending on the age of plants or plant clones,
input by somatic mutations may be much larger
than input by meiotic mutations (e.g. modelling
by Orive J theor Biol 2001)
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Mutation without meiosis and dispersal stages
...is expected to lead to high between-population
differentiation
complete population separation
random walk allele length
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Isolation-by-distance in 4 European coastal
regions
S Portugal
Finland
plt0.01
plt0.01
genetic distance (theta)
SW Baltic
Wadden Sea
clonal richness
ns
ns
geographic distance between pop pairs (log-scale)
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Adaptive implications
adaptive genetic variation may also arise by
somatic mutations, and reside as mosaics within
genets or plant modules (cf cultivars)
how come that oldest clones of Zostera marina can
survive under drastical environmental change in
past 4000 yrs in northern Baltic?
testable hypothesis mutation selection may
have happened within clones
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Trees are just three-dimensional clones
www.inkart.con
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Genetic mosaic hypothesis
Why are large, long-lived trees not overrun by
pests and pathogens?
hypothesis somatic mutation create mosaics at
the level of branches Witham Slobotkin 1981
Gill 1988
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Do plants evolve differently? - Yes
....but many clonal animals (19 phyla) do so as
well
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Do plants evolve differently? - Yes

• 1 because they do not posses a germline
• because many of them grow to very large size
  (i.e. have time to accumulate somatic mutations)
• because plants grow in modular fashion, opening
  the possibility for within individual selection
  variation
• hierarchical levels of selection needs more
  attention in population genetics

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Empty red circles indicate mutation sites, filled
red circles indicate all(?) other sites that have
been genotyped through the years...
FINLAND
Äppelö
Rankoskär
Turku/Åbo
Sandö
Kakskerta, Eerikinvallanniemi
Kollinpää
Åland
Prästö
Lökholm
Ängsö
Sandö
Hinderbengtsviken
Högsåra
Ryssholm
Vänö
Fårö
Utö
Holma
Plagen
Husskär, Långören, Sandskär
Henriksberg
The old Danish itinerary in the1250s
Other medieval sailing routes, just marked one of
very many