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Parachnowitsch AL, Kessler A. 2010. Pollinators exert natural selection on
flower size and floral display in Penstemon digitalis. New Phytologist 188:
393–402.
Peakall R, Ebert D, Poldy J, Barrow RA, Francke W, Bower CC, Schiestl
FP. 2010. Pollinator specificity, floral odour chemistry and the
phylogeny of Australian sexually deceptive Chiloglottis orchids:
implications for pollinator-driven speciation. New Phytologist 188:
437–450.
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flower classes. Evolution 15: 44–59.
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Rymer PD, Johnson SD, Savolainen V. 2010. Pollinator behaviour and
plant speciation: can assortative mating and disruptive selection
maintain distinct floral morphs in sympatry? New Phytologist 188: 426–
436.
Sapir Y. 2009a. Effects of floral traits and plant genetic composition
on pollinator behavior. Arthropod–Plant Interactions 3: 115–129.
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floral traits to study pollination ecology in an evolutionary context. Israel
Journal of Plant Sciences 57: 141–149.
Sargent RD. 2004. Floral symmetry affects speciation rates in angiosperms.
Proceedings of the Royal Society B: Biological Sciences 271: 603–608.
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New Phytologist 188: 418–425.
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Key words: candidate genes, evolutionary dynamics, evolutionary
pollination ecology, mutualism, pollinator-mediated selection,
quantitative genetics.
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The invasion of the land by
plants: when and where?
The origin of land plants was one of the most important
events in the history of life on Earth. It was a major macroevolutionary event in its own right, with profound ecological consequences, but it also had enormous effects on the
environment of planet Earth, altering atmospheric composition, weathering and soil formation, etc., and hence climate
and biogeochemical cycles. Understanding the timing of
the origin of land plants is a long term goal. In this issue of
New Phytologist, Rubinstein et al. (pp. 365–369) provide
new evidence that this event occurred 8–12 million yr
earlier than previously accepted.
‘Thus, although reports are currently few, attention
is turning to the possibility that the centre of origin
of land plants may have been located on
Gondwana.’
The land plants (Embryophytes) are a monophyletic
group that evolved as an adaptive response to the migration
from a freshwater aquatic to terrestrial subaerial habitat.
Phylogenetic analysis of extant plants suggests that charophycean green algae share a sister group relationship with
the Embryophytes, that is, the land plants probably evolved
from a freshwater aquatic multicellular green alga similar to
extant Chara and Coleochaete (Graham, 1993). Within the
Embryophytes liverworts are the most basal group, followed
by mosses, and then hornworts and vascular plants sharing
a sister group relationship (Qiu et al., 2006). However, it is
to the fossil record we must turn if we are to understand
what the first land plants were like and when and where
they evolved.
Traditionally the earliest evidence for land plants was
actual megafossils (fossils representing a significant portion
of the plant). Until the late 1950s the simple rhyniophytoid
plant Cooksonia provided this benchmark (Lang, 1937),
and it is still the oldest generally accepted megafossil, being
reported from the Late Silurian (late Wenlock) (Edwards
et al., 1983). However, evidence from a new technique
called palynology became widely available from the late
1950s. This technique involves dissolving rock to release
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small organic particles trapped within it as it was deposited.
Among these particles are the subaerially released spores of
land plants.
All land plants produce spores, or their homologue
pollen, in vast numbers. They are enclosed within a thick
resistant wall that protects them from physical abrasion and
exposure to UV-B radiation during dispersal. Upon release,
spores ⁄ pollen are widely dispersed by wind (or other vectors
such as insects) before eventually being deposited, often
after remobilization by water. Thus, spores ⁄ pollen tend
to accumulate wherever sediment is being deposited.
Sporopollenin is one of the most resistant organic macromolecules known to man and readily fossilizes. Thus palynology yields a remarkably complete fossil record of the
dispersed spores ⁄ pollen of land plants. However, it is
important to note that spores ⁄ pollen enclosed in a resistant
sporopollenin wall are a synapomorphy of land plants
(Wellman, 2003). When plants migrated out of water and
into the subaerial environment sexual reproduction became
problematic as reproductive structures could no longer
simply be released into the aquatic environment to swim to
one another. Rather, they must be transported through the
harsh subaerial environment. Thus sporopollenin-coated
spores ⁄ pollen are absolutely essential for subaerial existence
as a land plant, but of little or no use to an aquatic plant
(in fact, secondarily aquatic ‘land plants’ generally lose the
sporopollenin coat of their spores ⁄ pollen).
An early palynological discovery was that the fossil record
of trilete spores (similar to the isospores of homosporous
plants such as many modern lycopsids and ferns) extends
back into the earliest Silurian (Hoffmeister, 1959). This
predated the earliest land plant megafossils and provided a
new benchmark for the origin of land plants (Fig. 1). It also
suggested that the land plant megafossil record was patchy
(i.e. incomplete and biased) as might be expected: megafossils are produced in smaller numbers and are much less
likely to survive the fossilization process than dispersed
spores ⁄ pollen.
A further palynological shockwave was provided by Gray
& Boucot (1971). They described spores that occur in unusual configurations (now termed cryptospores) in even older
rocks, subsequently shown to extend down into the
Ordovician (Gray, 1985). This work was at first highly controversial. Many claimed that these spores did not represent
land plants. After all, where were the plant megafossils?
However, supporting evidence has subsequently accumulated to the extent that land plant affinities are almost universally accepted. It was also realized that the earliest land
plants were probably ‘bryophyte-like’ (liverworts are the
most basal extant land plants). Bryophytes lack abundant
recalcitrant (e.g. lignified) tissues and consequently do not
fossilize easily and have a negligible fossil record. This probably explains why the earliest land plants left a rich dispersed spore record but only a very limited megafossil
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Fig. 1 Geological time scale for the Ordovician–Silurian illustrating
benchmark palaeontological studies relevant to dating the origin of
land plants. Figures refer to ages in millions of years.
record (Wellman et al., 2003). The evidence for land plant
affinities of cryptospores may be summarized as follows:
(1) Cryptospores are morphologically similar to land plant
spores in terms of size and possession of a thick, resistant
wall (see (7) below). However, they occur as monads, dyads
and tetrads, rather than strictly as monads formed from the
dissociation of a meiotic tetrad. Furthermore, they are often
enclosed within a thin envelope that is difficult to equate
with similar structures in extant plants (e.g. Richardson,
1996) (Fig. 2).
(2) Cryptospores occur in terrestrial deposits. They are also
recovered from marine deposits where they decline rapidly
in abundance offshore (as do modern spores ⁄ pollen flushed
into the sea).
(3) Phylogenetic analyses in the mid-1980s suggested that
liverworts are the most basal extant land plants. Certain
cryptospores (notably permanent tetrads enclosed within an
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308 Forum
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Commentary
(a)
(b)
(c)
(d)
Fig. 2 Cryptospores from the Late Ordovician (Katian) of Oman. (a) Naked dyad; (b) dyad enclosed in a thin walled envelope, part of which is
discernible on the edges of the specimen; (c) naked tetrad; (d) tetrad enclosed in a thin-walled envelope, part of which is discernible on the
edges of the specimen. All specimens approx. 30 microns in maximum diameter.
envelope) resemble the spores of certain extant liverworts
(Gray, 1985).
(4) Taylor (1995) demonstrated that some cryptospore
dyads have spore wall ultrastructure only known among
extant liverworts.
(5) Remarkably preserved Lower Devonian plants contain
in situ cryptospores and these plants have certain bryophytic
characters (Edwards et al., 1999).
(6) Complete sporangia (including covering) with in situ
cryptospores were recovered from the Ordovician (Katian)
of Oman (Wellman et al., 2003). Those containing dyads
also have spore wall ultrastructure known only among
extant liverworts.
(7) Recent geochemical analysis has demonstrated that the
spore wall in cryptospores is chemically similar to that of
known land plant spores (Steemans et al., 2010).
Until now the earliest reported cryptospores were from
the Darriwilian (Middle Ordovician) from the Czech
Republic and Saudi Arabia (Strother et al., 1996).
Interestingly both of these reports concern the large
Ordovician supercontinent of Gondwana and its margins.
Now Rubinstein et al. provide an even earlier report (by
some 8–12 million yr) of cryptospores from the early
Middle Ordovician (Fig. 1). This provides a new benchmark for the origin of land plants. Their report is from
Argentina which was also situated on the supercontinent of
Gondwana. Thus, although reports are currently few, attention is turning to the possibility that the centre of origin of
land plants may have been located on Gondwana. This mirrors the situation whereby the centre of origin of vascular
plants is currently hypothesized to have occurred on this
continent (Steemans et al., 2009).
Understanding the origin of land plants is a multidisciplinary effort with diverse strands of evidence derived from
palaeontological, biological and geological investigation.
Palaeontological research continues to throw up new finds,
like that reported by Rubinstein et al., that modify an emerging picture of the nature of the earliest land plants, where
and when they first appeared, and how they colonized the
Earth’s surface. However, much work remains to be done as
we struggle to unravel the vagaries of the fossil record and
many controversies persist. There are claims that thickwalled palynomorphs from the Cambrian represent an even
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earlier record for land plants. However, many interpret these
as the resting cysts, or even body cells, of aquatic algae
(Wellman, 2003). The jury is out and more evidence is
required. Even more intriguing is the unusual configuration
of the earliest land plant spores (cryptospores). What does
the envelope represent? Why do they often occur in dyads? It
is clear that most extant and fossil land plants produce
spores ⁄ pollen in tetrads by meiosis and usually the tetrads
dissociate into four monads before dispersal. Presumably,
dyads are normal meiotic products but developed via separation between two successive meiotic divisions. But why did
dyad formation operate among land plants for the first
65 million yr of their existence before entirely disappearing?
Possibly two lineages of embryophyte existed and the dyadproducers were simply outcompeted by the tetrad producers
owing to some other factor unrelated to reproduction.
These, and other problems will be addressed by new evidence
from a variety of disciplines. This will include new fossil
finds, interpreted, as always, in the light cast by our understanding of extant plants. I suspect that this will be forced
onward by the current revolution in evo-devo studies, fuelled
by the proliferation of molecular data, including wholegenome sequences from more basal land plants such as
Physcomitrella and Selaginella.
Charles H. Wellman
Department of Animal and Plant Sciences, University of
Sheffield, Alfred Denny Building, Western Bank, Sheffield
S10 2TN, UK
(tel +44 (0)114 2223689; email [email protected])
References
Edwards D, Feehan J, Smith DG. 1983. A late Wenlock flora from Co.
Tipperary, Ireland. Botanical Journal of the Linnean Society 86:
19–36.
Edwards D, Wellman CH, Axe L. 1999. Tetrads in sporangia and
spore masses from the Upper Silurian and Lower Devonian of the
Welsh Borderland. Botanical Journal of the Linnean Society 130:
111–115.
Graham LE. 1993. Origin of land plants. New York, USA: Wiley.
Gray J, Boucot AJ. 1971. Early Silurian spore tetrads from New York:
earliest New World evidence for vascular plants. Science 173: 918–921.
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Gray J. 1985. The microfossil record of early land plants; advances in
understanding of early terrestrialization, 1970–1984. Philosophical
Transactions of the Royal Society of London, Series B, Biological Sciences
309: 167–195.
Hoffmeister WS. 1959. Lower Silurian plant spores from Libya.
Micropaleontology 5: 331–334.
Lang WH. 1937. On plant-remains from the Downtonian of England and
Wales. Philosophical Transactions of the Royal Society of London. Series B,
Biological Sciences 227: 245–291.
Qiu Y-L, Li L, Bin W, Chen Z, Knoop V, Groth-Malonek M,
Dombrovska O, Lee J, Kent L, Rest J et al. 2006. The deepest
divergences in land plants inferred from phylogenomic evidence.
Proceedings of the National Academy of Sciences, USA 103: 15511–15516.
Richardson JB. 1996. Chapter 18A. Lower and Middle Palaeozoic records
of terrestrial palynomorphs. In: Jansonius J, McGregor DC, eds.
Palynology: principles and applications. Salt Lake City, UT, USA:
American Association of Stratigraphic Palynologists Foundation 2:
555–574.
Rubinstein CV, Gerrienne P, de la Puente GS, Astini RA, Steemans P.
2010. Early Middle Ordovician evidence for land plants in Argentina
(eastern Gondwana). New Phytologist 188: 365–369.
Steemans P, Le Herisse A, Melvin J, Miller MA, Paris F, Verniers J,
Wellman CH. 2009. Origin and radiation of the earliest vascular land
plants. Science 324: 353.
Steemans P, Lepot K, Marshall CP, Javaux EJ. 2010. FTIR
characterisation of the chemical composition of Silurian cryptospores
from Gotland, Sweden. Review of Palaeobotany and Palynology. doi:
10.1016/j.revpalbo.2010.07.006.
Strother PK, Al-Hajri S, Traverse A. 1996. New evidence for land plants
from the lower Middle Ordovician of Saudi Arabia. Geology 24: 55–58.
Taylor WA. 1995. Spores in earliest land plants. Nature 373: 391–392.
Wellman CH. 2003. Dating the origin of land plants. In: Donoghue PCJ,
Smith MP, eds. Telling the evolutionary time: molecular clocks and the
fossil record. London, UK: CRC Press, 119–141.
Wellman CH, Osterloff PL, Mohiuddin U. 2003. Fragments of the
earliest land plants. Nature 425: 282–285.
Key words: cryptospores, Embryophytes, evo-devo, Gondwana, land
plants, megafossils, palynology, sporopollenin.
Tracing photosynthetic
isotope discrimination from
leaves to soil
The fate of carbon (C) following photosynthetic assimilation
is, quite rightly, currently the subject of intense research. The
principal reason for this interest is that the rate of C turnover
in ecosystems feeds back into the global C cycle, where
anthropogenic emissions increase CO2 concentrations by an
estimated 10 Gt every year (IPCC, 2007). While this constant addition of CO2 is currently compensated in part by the
biosphere acting as a net sink for the globe, there is an urgent
need to understand how different ecosystems will respond
under changed environmental conditions. Predicting the
rates of C turnover in ecosystems requires a good understand-
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ing of C assimilation, allocation and respiration in plants and
soil, in order to inform process modelling. However, despite
abundant research into respiration, we still lack a fundamental understanding of the way in which C moves through the
plant–soil–atmosphere continuum. In this issue of New
Phytologist, Wingate et al. (2010b, pp. 576–589) make use of
the natural fluctuation in the isotopic composition of assimilated C in order to trace its fate to a number of respiratory
fluxes. The approach is both elegant and novel: by continuously measuring the photosynthetic discrimination between
the stable isotopes 12C and 13C, they obtained a continuous
‘signal’ for the newly assimilated C. This discrimination
showed fluctuations from diurnal to seasonal temporal scales,
and Wingate et al. (2010b) were able to follow the temporal
trends observed during assimilation (which were verified
using isotope-specific C assimilation modelling) into respiration fluxes from tree stems and the soil. While previous studies
have demonstrated the transmission of the photosynthetic
isotope signal within the plant on the basis of intermittent
measurements, this study breaks new ground by monitoring
C isotope fluxes of assimilation and respiration continuously
and over an extended period. This unique data set therefore
allows a thorough analysis of the temporal correlation between
the isotopic ‘signal’ from assimilation and respiration terms.
The time lags observed, from leaf to stem and soil, are broadly
similar to those observed using alternative methods (Ekblad
& Högberg, 2001; Högberg et al., 2008; Subke et al., 2009;
Mencuccini & Hölttä, 2010). However, rather than simply
confirming these results, the authors were able to identify variations in these time lags likely to be linked to phenological
phases when there is tight coupling between the supply of fresh
photosynthates and respiratory activity in the soil (whether this
occurs inside the roots or is carried out by heterotrophic organisms receiving plant C through exudations). Rather than simply
showing that C allocation differs during different periods in
the growing season (Högberg et al., 2010), Wingate et al.
(2010b) can identify the exact timing of when a synchronicity
between assimilation and belowground respiration occurs
and when it does not occur. This suggests that it may not be
possible simplistically to use natural abundance 13CO2 measurements for short-term partitioning of soil autotrophic and
heterotrophic respiratory fluxes in forest ecosystems, especially during periods in which autotrophic respiration is
weakly linked to photosynthesis. At the same time, a gradual
shift in photosynthetic discrimination over the length of the
growing season was detectable in the soil CO2 efflux signal,
and there is considerable potential in using multi-year
measurements to derive long-term flux partitioning between
autotrophic and heterotrophic sources. Also, such isotope
data may improve our ability to model and constrain both
contemporary and historic global C transfers, making more
widespread measurements of isotope specific C fluxes in ecosystems throughout the world a realistic and exciting prospect.
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