Diversity and evolution of major groups of land plants
Robin Allaby
(http://www2.warwick.ac.uk/fac/sci/whri/research/archaeobotany/)
Notes available from website
Notes available from website
Overview
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Origin of land plants
Evolutionary history of land plants
– Major morphological innovations:
alternation of generations
cuticles and stomata
vascular tissues
heterospory
seeds
leaves
flowers
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Resultant phylogenetic tree of plants
Some evolutionary trends
convergence
polyploidy
genome expansion
Invasion of land was really an invasion of the air
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dessication and support are the principal problems
adaptation to dessication requires :
a cuticle (and consequentially stomata)
spores and seeds (ultimately)
vascular tissue (when plants are above a certain size)
What is a land plant?
•
Any photosynthetic eukaryote that can survive and sexually reproduce on
land
What is a land plant?
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Any photosynthetic eukaryote that can survive and sexually reproduce on
land
All land plants are embryophytes (= embryo bearing plants)
Embryophytes
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Defined by a true alternation of generations with multicellular
diploid and haploid phases, and the two phases remain physically
connected.
Gametophyte (haploid) stage
Sporophyte produces
sporangia which make
haploid spores
Gametophyte produces haploid
gametes, which unite in the
archegonium of the gametophyte
Sporophyte (diploid) stage
A brief history of time
545
495
Cambrian
440
Ordovician
417
Silurian
354
Devonian
292
Carboniferous
251
Permian
202
Triassic
Jurassic
142
65
Cretaceous
24
Palaeogene
1.8
Neogene
Q
Evidence of first land plants: 480-360 Mya
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cuticles & stomata
archegonium & sporopollenin walled spores
vascular systems
(417)
(440)
1 cm bar
458
(495)
Circa 415 Mya Cooksonia paranensis (Gerrienne et al 2006)
Vascular tissues: evolution of xylem and phloem
embryophytes
better adapted for moist
environments than
tracheophytes
amplification of
gametophyte
poikilohydric
better adapted for dry
environments than
bryophytes
amplification of
one stage must
reduce the other
amplification of
sporophyte
homoihydric
non vascular
vascular
(bryophytes)
(tracheophytes)
mosses,
liverworts and
hornworts
ferns, lycopods,
horsetails, and
seed plants
See Proctor 2007
Heterospory
unisexual
gametophytes,
manifest as
heterosporous
397 - 391 Mya
(Eifelian)
phyletic trend for taller
sporophytes, bisexual
gametophytes,
homosporous
plants that release spores = pteridophytes (fern like - includes lycopods (L), Horsetails (H)
and Ferns (F))
Heterospory
homospory
heterospory
Heterospory
• Seems odd - reduces the chances of fertilization by separating
egg and sperm. Cannot be good in a harsh environment, this is
a cost.
• Once separated, makes sense to increase energy investment in
the “female” gametophyte which must support the sporophyte,
and maximize chances of successful fertilization by making
male spore numerous, (and consequently small).
• Gives rise to out-crossing. Perhaps this is the advantage (?).
• That it is an advantage is proven by the convergence on the
habit - possibly as many as 11 times! (Bateman & DiMichele
1994).
The logical progression of heterospory
e.g. Barinophyton citrulliforme
e.g. Chaleuria cirrosa
e.g. Cystosporites devonicus
e.g. Archaeopteris & Selaginella
increasing investment in
megaspore causes
reduction in megaspore
number
Seed habit - the next step after heterospory
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retain megaspore in megasporangium
reduce functional megaspores to 1
retain megagametophyte (elimating requirement for external water
for fertilization)
modification of megasporangia to receive microspores
modification of microspores to enable them to deliver sperm cells to
eggs (ie pollen tube)
integument develops around megasporangia (later)
all seed plants = spermatophytes
first seed plants = gymnosperms (naked seeds)
Oldest seed plant 385 Mya (Mid Devonian)
salpinx
megasporangium
Integument does not
fully enclose ovule
Runcaria heinzelinii (Gerrienne et al 2004)
Basic Gymnosperm architecture
integument +
megasporangium
uncovered
Pollen tubes by early Carboniferous
(Rothwell 1972)
The late arrival of leaves: 360 Mya!! (end of
Devonian)
Leaf evolution associated with falling CO2 levels (first plants evolved in a CO2 rich
atmosphere)
(Beerling 2005)
A snapshot of the Carboniferous
Lycopod trees
(Lepidodendron)
Equisetoid trees
(Calamites)
Angiosperms appear 144 Mya (early Cretaceous)
Asteropollis sp. Pollen (Laurales) (Friis et al 2005)
Evolution of Angiosperms
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Angio = container - megasporangium (and integuments) enclosed
in carpel.
Flower structure (a determinate shoot built from leaves).
2 integuments not one (as in gymnosperms).
Double fertilization (resulting in triploid endosperm).
Xylem structure (vessel members and sieve tubes).
Other features to such as endopolyploidy ability (weed
technology!), vegetative reproductive ability (weed technology!).
Very versatile - numerous floral strategies possible - a single
mutation can result in sexual isolation and new species formation.
Introduction of animal based pollination strategies.
Explosion in Angiosperm speciesGnetales is
gymnosperm group closest to flowering plants
Angiosperms
220 000 species
Bryophytes
22 400 species
Pteridophytes
9 000 species
Gymnosperms
750 species
Fabaceae alone have 14000 species
Also only land plant group to reinvade
the sea (Zostera sp.)
Oldest flower fossils circa 125 Mya.
Water lily (Nymphaeales) (Friis et al 2001)
The diversification of angiosperms: Darwin’s
abominable mystery
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The rapid appearance of so many species of angiosperm was a
problem for Darwin’s theory
In his version of events, evolution proceeds gradually, selecting
minute changes
Saltation was an opposing view point – gives more emphasis to
mutation (internally driven) than Natural Selection (externally
driven)
Darwin discovered the reason, and founded ‘pollination biology’
Floral evolution – protection to attraction
Bisexual flowers
Nectar reward, bees, predominate
birds, moths, bats
wind pollination
First pollinators:
beetles in small
inconspicuous
flowers
Friis et al 2006
Unisexual flowers
predominate
Angiosperms diversified because of floral
morphology and pollinator co-evolution
water lillies
pepper (spice)
magnolia
basal complex:
primitive dicots
bay laurel
peace lillies
Based on DNA
sequences such
as rbcL, matK,
nadh, atpB, 18S
rDNA
30 Mya CO2
levels crashed:
C4 metabolism
evolved 62 times
independently!!
26 in monocots
and 36 in
eudicots
Angiosperm
Phylogeny basal
monocots
asparagus
Lillies, daffodils etc
yams
palms
pineapples/air plants
reeds and rushes
grasses
ginger, bird of paradise plants
basal
buttercups, poppies
grapes
cactus
Docks, rhubarb & sorrels
witch hazel, stone crops
mistletoe
geraniums
Oldest tricolpate
pollen 120 Mya
basal
core
rosids
Euphorbia, willow
wood sorrel
beans, peas, acacia
roses, apples
cucumber, melons &pumpkins
Oaks, birch, beech
evening primrose
Cabbages, Arabidopsis
cotton, lime trees
oranges, lemons
dogwood
asterids
heather, rhododendron, primrose
Potato, tomoto, deadly nightshade
coffee
Mint, basil, rosemary, thyme etc., olives
Tricolpate
Angiosperms
holly
carrots, parsley. fennel
honeysuckle, elder
daisy, asters, thistles, bellflowers
Evolutionary Trends: convergence (on tree habit)
Evolutionary Trends: convergence (on cactus habit)
Evolutionary trends: polyploidy
Blanc and Wolfe 2004
Evolutionary trends: genome obesity
Leitch et al 2005
Obesity in the Liliales
Fritillaria (Liliales) 127 000 Mb
Large cells, slow replication - good for
bulbs
Arabidopsis (Brassicales)
157 Mb
Small cells, fast replication good for weed habit
Endangered species?
Why is there an over-representation of large genomes in the plant Red List?
Vinogradov 2003, but read also Cavalier-Smith 2005
Suggested reading
Crane PR, Friis EM, Pedersen KR (1995) The origin and early
diversification of angiosperms. Nature 374: 27-33.
Friis EM, Pederson KR, Crane PR (2005) When the earth started
blooming: insights from the fossil record. Current Opinion in Plant
Biology 8:5-12.
Judd WS, Campbell CS, Kellogg EA, Stevens PF (1999). Plant
Systematics: A Phylogenetic Approach. Sinauer Associates,
Sunderland, Massachusetts.
Kenrick P and Crane PR (1997) The origin and early evolution of
plants on land. Nature 389:33-39.
Niklas K (1997) The evolutionary biology of plants. University of
Chicago Press, Chicago.
Other source material
Bateman RM and DiMichele WA (1994) Heterospory: The most
iterative key innovation in the evolutionary history of the plant
kingdom. Biological Reviews of the Cambridge Philosophical Society
69:345-417.
Beerling DJ (2005. Leaf Evolution: Gases, Genes and Geochemistry.
Annals of Botany 96:345-352.
Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in mode plant
species inferred from age distributions of duplicate genes. The Plant
Cell 16:1667-1678.
Cavalier-Smith T (2005) Economy, sped and size matter: evolutionary
forces driving nuclear genome miniaturization and expansion. Annals
of Botany 95:147-175.
Cavalier-Smith T (2004) Only six kingdoms of life. Proceedings of the
Royal Society of London Series B. 271:1251-1262.
Friis EM, Pederson KR, Crane PR (2001) Fossil evidence of water
lilies (Nymphaeales) in the early cretaceous. Nature 410: 357-360.
Friis et al 2006 Cretaceous angiosperm flowers: Innovation and
evolution in plant reproduction. Palaeogeography,
Palaeoclimatology, Palaeoecology 232 (2006) 251–293
Friis et al 2010 Diversity in obscurity: fossil flowers and the early
history of angiosperms. Phil. Trans. R. Soc. B 2010 365, 369-382
Gerrienne P, Meyer-Berthaud B, Fairon-Demaret M, Streel M,
Steemans P (2004) Runcaria, a Middle Devonian Seed Plant Precursor.
Science 306:856-858.
Gerrienne P et al. (2006) An exceptional specimen of the early land
plant Cooksonia paranensis, and a hypothesis on the life cycle of the
earliest eutracheophytes. Review of Palaeontology and Palynology
142:123-130.
Leitch IJ, Soltis DE, Soltis PS, Bennett MD (2005) Evolution of DNA
amounts across land plants (Embryophyta). Annals of Botany 95:207217.
Proctor M (2007) Ferns, evolution, scale and intellectual impedimenta.
New Phytologist 176:504-506.
Rothwell GW (1972) Evidence of Pollen Tubes in Palaeozoic
Pteridosperms. Science 175:772-774.
Vinogradov AE (2003) Selfish DNA is maladaptive: evidence from the
plant Red List. Trends in Genetics 19:609-614.