AOBPreview originally published online on June 19, 2005
Annals of Botany 2005 96(3):345-352; doi:10.1093/aob/mci186
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BOTANICAL BRIEFING |
Leaf Evolution: Gases, Genes and Geochemistry
Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK
* E-mail d.j.beerling{at}sheffield.ac.uk
Received: 24 February 2005 Returned for revision: 23 March 2005 Accepted: 12 April 2005 Published electronically: 19 June 2005
ABSTRACT
• Aims This Botanical Briefing reviews how the integration of palaeontology, geochemistry and developmental biology is providing a new mechanistic framework for interpreting the 40- to 50-million-year gap between the origination of vascular land plants and the advent of large (megaphyll) leaves, a long-standing puzzle in evolutionary biology.
• Scope Molecular genetics indicates that the developmental mechanisms required for leaf production in vascular plants were recruited long before the advent of large megaphylls. According to theory, this morphogenetic potential was only realized as the concentration of atmospheric CO2 declined during the late Palaeozoic. Surprisingly, plants effectively policed their own evolution since the decrease in CO2 was brought about as terrestrial floras evolved accelerating the rate of silicate rock weathering and enhancing sedimentary organic carbon burial, both of which are long-term sinks for CO2.
• Conclusions The recognition that plant evolution responds to and influences CO2 over millions of years reveals the existence of an intricate web of vegetation feedbacks regulating the long-term carbon cycle. Several of these feedbacks destabilized CO2 and climate during the late Palaeozoic but appear to have quickened the pace of terrestrial plant and animal evolution at that time.
Key words: Carbon cycle, feedbacks, fossil plants, genetics, geochemistry, leaves, stomata
INTRODUCTION
Plants evolved leaves on at least two independent occasions and the legacy of these historic evolutionary events is represented in extant floras by microphylls in lycophytes (clubmosses, spikemosses and quillworts) and megaphylls in euphyllophytes (ferns, gymnosperms and angiosperms). Microphylls, with a distinctive vasculature and (usually) unbranched venation, are thought to have evolved from spine-like enations and predate megaphylls in the terrestrial plant fossil record (Gifford and Foster, 1988
). Of greater significance, however, was the origin of megaphylls in vascular plants through the developmental modification of lateral branches. Megaphylls altered the evolutionary trajectory of terrestrial plant and animal life, the biogeochemical cycling of nutrients, water and carbon dioxide and the exchange of energy between the land surface and the atmosphere. The vast majority of the estimated 250 000 or so extant species of flowering plants, as well as most gymnosperms and (extinct) pteridosperms, utilize(d) a flat-bladed megaphyll with a network of veins to capture solar energy for photosynthetic carbon assimilation. A true measure of their success in terrestrial environments is the capacity of leaves to endure climatic extremes between the tropics and the tundra whilst simultaneously facilitating the global scale net fixation of approx. 207 billion tonnes of CO2 (56·4 x 1015 g C) year–1 (Field et al., 1998). This primary production provides energy for virtually all forms of terrestrial life on Earth, especially tetrapods and insects, and links many ecosystem and biogeochemical processes.
Evidently, leaves are a global success. However, the advent of large megaphylls took place some 40–50 million years (Myr) after the origination of vascular land plants, suggesting that they were far from an evolutionary inevitability. The earliest ancestral vascular plants, dating to the late Silurian 410 Myr ago (Edwards and Wellman, 2001), were composed of simple or branched axial stems with sporangia but no leaves. Surprisingly, plants continued to remain leafless for the next 40–50 Myr, with megaphylls finally becoming widespread at the close of the Devonian period (360 Myr ago) (Kenrick and Crane, 1997; Boyce and Knoll, 2002; Osborne et al., 2004a,b). Surprise in the delayed appearance of a seemingly simple developmental modification is 3-fold. First, palaeontological evidence shows that the structural framework necessary for assembling a simple laminated leaf blade (meristem, vasculature, cuticle and epidermis) (Kenrick and Crane, 1997) was in place long before the advent of large megaphylls. Secondly, the same interval marks an unparalleled burst of evolutionary innovation in the history of plant life, which witnessed the rise of trees from herbaceous ancestors, and the evolution of complex life cycles, including the seed habit (Kenrick and Crane, 1997). Thirdly, the tiny deeply incised megaphylls of the rare early-Devonian plant Eophyllophyton bellum from Chinese rocks shows that plants had the capacity to produce a simple megaphyll (Hao and Beck, 1993; Hao et al., 2003). Why were plants unable to release this morphogenetic potential?
Until recently, our understanding of the evolution of megaphylls largely stemmed from Zimmermann's telome theory (Zimmermann, 1930, 1952) describing the sequence of overtopping, planation and webbing leading to appearance of the laminated leaf blade. The ancestral form of a dichotomizing axis branching out in three dimensions and typified by the rhyniophytes (Fig. 1) represents the basal state in the telome theory. Evolutionary ‘overtopping’ followed producing a main axis bearing reduced, lateral, determinate photosynthetic stems, branching out in three dimensions (e.g. trimerophytes). These 3-D lateral branch systems of terete stem segments then became ‘flattened’ into a single plane (e.g. cladoxyaleans). Finally, a webbing of photosynthetic mesophyll tissue joined the flattened segments of the lateral branches to form a laminate leaf blade (e.g. some progymnosperms) (Fig. 1). In this scheme, transformation of a branch into a leaf was achieved by simple modification of existing organs rather than a major change in body plan.
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Over 70 years ago, Zimmermann's scholarly telome theory provided a first glimpse of the ‘how’, but left unanswered the thorny question of ‘why’ it took 40–50 Myr to evolve leaves. This Botanical Briefing provides an overview of a new mechanistic explanation linking atmospheric CO2 decline with the delayed widespread appearance of megaphylls, and ideas concerning its molecular genetic basis and the resulting global environmental and evolutionary consequences. The explanation emerges from a theoretical analysis incorporating modern-day plant processes and biophysical principles governing the energy balance of photosynthetic organs (Beerling et al., 2001
). Developmental genetic mechanisms underpinning aspects of stomatal and leaf formation (Gray et al., 2000; Cronk, 2001; Floyd and Bowman, 2004; Harrison et al., 2005; Sano et al., 2005) provide additional new insight allowing progress towards a unified framework for understanding leaf evolution. In the final section of this Briefing, I consider how recognizing a role for CO2 in leaf evolution has shed new light on multiple biotic feedbacks within the geochemical carbon cycle and on evolutionary processes themselves (Oddling-Smee et al., 2003; Beerling and Berner, 2005).
EVOLUTION OF THE LEAF AND ATMOSPHERE
The mechanistic hypothesis of Beerling et al. (2001) links the gap between the earliest vascular plants and the advent of large megaphylls with a dramatic 90 % drop in the atmospheric CO2 concentration during the late Palaeozoic (Berner, 2004). The large fall in CO2 corresponded with a marked rise in the stomatal density of vascular land plants, with densities increasing a 100-fold from 5–10 mm–2 on early vascular plant axes to 800–1000 mm–2 on the cuticles of late Carboniferous megaphylls (McElwain and Chaloner, 1995; Edwards, 1998). These evolutionary shifts in leaf anatomy are consistent with the effects of CO2 on stomatal development observed in modern plants cultivated in controlled conditions under different CO2 concentrations (Woodward, 1987).
According to theoretical calculations with a model of leaf biophysics and physiology, the rise in stomatal density held special significance for the evolution of leaves by permitting greater evaporative cooling and alleviating the requirement for convective heat loss (Beerling et al., 2001). Simulations indicate that archaic land plants with axial stems, few stomata, and low transpiration rates only avoided lethal overheating because they intercepted a minimal quantity of solar energy (Beerling et al., 2001; Roth-Nebelsick, 2001). In contrast, a megaphyll intercepting at least twice as much solar energy (per unit area of the photosynthetic organ) reached temperatures approaching the highly conserved lethal threshold of extant tropical taxa (Beerling et al., 2001) because the same limited evaporative cooling was inadequate to dissipate the absorbed thermal energy. Theoretical arguments therefore indicate that early vascular land plants were prevented from developing large laminate leaves because their low stomatal densities placed a tight constraint on evaporative cooling.
Even if the stomatal density of the early vascular land plants was not under the influence of atmospheric CO2, and megaphylls evolved a high density, the transpiration rates required to maintain cool temperatures (approx. 9–13 mmol H2O m–2 s–1) are calculated to outstrip the capacity of xylem to supply it by factor of ten, assuming the primitive stele of Psilotum nudum is a reasonable analogue for that of the early rhyniophytes (Schulte et al., 1987). In this case, dehydration precluded the evolution of large megaphylls with high stomatal densities in early land plants; no fossils of such an anatomically modified organ have yet been discovered.
By the time large laminate leaves became widespread in late Devonian/early Carboniferous fossil floras, the concentration of atmospheric CO2 had fallen, and stomatal densities had increased by up to a 100 times the value of early vascular land plant axes. Large leaves of late Devonian/early Carboniferous plants attained transpiration rates sufficiently high to maintain temperatures well below the lethal threshold, despite intercepting more solar energy (Beerling et al., 2001). Greater evaporative cooling also meant that large leaves stayed cool despite diminished convective heat loss, a flux that declines with increasing leaf size as friction across the surface slows the passage of air and the transfer of heat. Large-leaved perennials in today's deserts similarly rely on a high transpiration rate to prevent overheating and maintain leaf temperatures 8–18 °C below that of the air (Smith, 1978; Ehleringer, 1988), with some species in southern California even evolving a correspondingly lower temperature optimum for photosynthesis (Smith, 1978). For these large-leaved desert species, summertime precipitation permits high transpiration rates. But in the late Palaeozoic, the evolution of large leaves required the co-evolution of the root and vascular systems for improved water delivery and transport to sustain higher transpiration rates (Knoll et al., 1984; Raven and Edwards, 2001). Deeper roots accessed water and nutrients from a greater volume of soil, whilst xylem conduit enlargement and the appearance of secondary growth of xylem by the end of the Devonian increased the hydraulic conductance through stems and trunks to the leafy canopy, helping to maintain higher transpiration rates (Rowe and Speck, 2005).
The hypothesis of Beerling et al. (2001) makes the clear prediction that larger leaves gradually appeared as CO2 levels declined and stomatal numbers rose to increase evaporative cooling and ease the thermal burden of absorbed solar energy. Osborne et al. (2004a, b) achieved a successful test of this prediction with a morphometric analysis of 300 fossil specimens archived in major European collections. Their results showed a 25-fold enlargement of leaf blades as atmospheric CO2 fell during the late Palaeozoic (Fig. 2B). Leaf enlargement occurred first in the progymnosperms during the mid- to late-Devonian with the initial radiation of Archaeopteris and soon afterwards in the pteridosperms, a group attaining a larger maximum size coincident with a lower atmospheric CO2 concentration.
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The consistent pattern of leaf blade enlargement seen in these two phylogenetically independent clades (Boyce and Knoll, 2002
; Osborne et al., 2004a,b) is consistent with the argument that CO2 acted as an environmental driver for this aspect of plant evolution. But as the concentration of atmospheric CO2 declined to permit the evolution of leaves, competition for light and space between neighbouring plants intensified. Competition is therefore envisaged as providing a powerful selective force for plants to become leafier and taller. These shifting ecological interactions were most obviously manifested as the well-documented increase in plant size (Chaloner and Sheerin, 1979) that tracked historical patterns of leaf enlargement (Fig. 2C).
GENES, LEAVES AND STOMATA
Leaves in vascular plants are produced by determinate growth on the flanks of indeterminate shoot apical meristems. Inderminate growth of the shoot apical meristem is controlled by the knotted-like homeobox gene family (KNOX) (reviewed in Hake et al., 2004). KNOX genes are present in some green algae (e.g. Acetabularia), mosses, ferns, gymnosperms and angiosperms and their function may be highly conserved (Sano et al., 2005). Over-expression of fern KNOX-like genes in Arabidopsis thaliana, for example, produces a similar phenotype (altered leaf shape) as over-expression of arabidopsis KNOX-like genes in Arabidopsis (Sano et al., 2005). Proper development of leaves requires permanent negative repression of KNOX genes and several genes have so far been discovered in euphyllophyte species for maintaining the KNOX-off state, including PHANTASTICA (PHAN) isolated from snapdragon (Antirrhinum majus) (Waites and Hudson, 1995) and homologues of PHAN in maize (Timmermans et al., 1999) and Arabidopsis (Byrne et al., 2000). The two sets of genes operate in a co-ordinated manner with KNOX-like transcription factors repressing determinate growth promoted by PHAN, and PHAN-like transcription factors repressing KNOX to promote indeterminacy.
The system is likely controlled by auxin, which determines the site of leaf initiation and is correlated with decreased KNOX and increased PHAN activity. Environmental influences on KNOX and PHAN are not known. However, it is interesting to note that the original PHAN mutation in Antirrhinum was temperature-sensitive so that plant morphology was approximately normal at 25 °C but altered at lower temperatures (Waites and Hudson, 1995), implying an interaction of PHAN-mediated morphogenesis with temperature-sensitive elements of leaf development. Genes such as PHAN may be prime candidates for involvement in the first stage of the telome theory, i.e. the evolution of determinant lateral shoot systems in trimerophytes (Fig. 1) (Cronk, 2001).
Leaf production also requires differentiation between adaxial (upper) and abaxial (lower) surfaces because the former is specialized for the efficient capture of solar energy and the latter for gas exchange. Deriving from the apical vegetative meristem flank, the abaxial surface is as old as land plants themselves, so genes specifying adaxial identity constitute a key innovation in leaf evolution (Cronk, 2001). Plants appear to have evolved a complex hierarchy of transcription factor activation and depression, with the HD-ZIP (homeodomain–leucine zipper) gene family promoting adaxial leaf surfaces and others promoting abaxial differentiation (Cronk, 2001). Interestingly, HD-ZIP gene expression is subject to a novel form of post-transcriptional regulation involving microRNAs found in bryophytes, lycopods, ferns and seed plants suggesting that it may be very ancient, dating back more than 400 Myr (Floyd and Bowman, 2004). Interactions between HD-ZIP gene and vascular tissue polarity have been demonstrated in Arabidopsis (Emery et al., 2003) and, since vascular tissue predates the leaf (Kenrick and Crane, 1997), this suggests that the same developmental unit was recruited for leaf polarity (Emery et al., 2003).
Whether megaphylls, which arose independently in four vascular plant lineages (ferns, sphenopsids, progymnosperms and seed plants) (Boyce and Knoll, 2002; Osborne et al., 2004a, b), recruited the same gene systems is open to investigation (Cronk, 2001). However, this does seem a possibility given that a common developmental mechanism for leaf production appears to have been recruited independently at least twice in the evolution of land plants (Harrison et al., 2005).
Current understanding of the genetic controls of stomatal formation in response to environment signals is limited, although it is clear that genetic modification more strongly alters the relationship between stomatal density and pore size, with attendant effects on leaf gas exchange, than short-term changes in environmental conditions (Hetherington and Woodward, 2003). Stomatal research on Arabidopsis has identified the HIC (high carbon dioxide) gene, which responds to CO2 and negatively regulates stomatal formation (Gray et al., 2000). HIC encodes a putative 3-ketoacyl coenzyme-A synthase, an enzyme involved in the synthesis of wax components found in the cuticle. Wax-deficient mutant plants show a 42 % increase in stomatal density with CO2 enrichment to 1000 ppm compared with that at 400 ppm CO2 (Gray et al., 2000). The possible involvement of the HIC gene (or similar) in mediating stomatal formation under different CO2 concentrations in other plant groups remains to be seen.
VEGETATION FEEDBACKS AND THE LONG-TERM CARBON CYCLE
The realization that aspects of plant evolution may be directed by changes in atmospheric CO2 gains greater significance when considered alongside the impact that plants themselves exert on the long-term carbon cycle. Before plants, Earth's global climate and atmospheric CO2 were regulated on a multi-million year timescale by the inorganic carbon cycle, in which CO2 is supplied to the atmosphere by volcanism and metamorphic degassing, and removed by the chemical weathering of Ca–Mg silicate rocks (Walker et al., 1981; Berner et al., 1983). The closed cycle can be represented as a simple systems diagram with arrows indicating a direct response (no bull's-eyes) or an inverse response (with bull's-eyes) (Fig. 3A). In these diagrams an even number of arrows with or without bull's-eyes defines a positive feedback and an odd number with bull's-eyes a negative feedback. The inorganic carbon cycle (Fig. 3A) is stabilized by a negative feedback loop because silicate-weathering rates increase with temperature (Walker et al., 1981; Berner et al., 1983). Rising CO2 levels, for example, strengthen the greenhouse effect, warm the climate, accelerate the chemical weathering of Ca–Mg silicate rocks, remove CO2 from the atmosphere and lead to a cooler climate (Fig. 3A).
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The advent of rooted vascular land plants introduced a potent biotic feedback into the long-term carbon cycle (Berner, 2004
). Plant activities greatly enhance silicate rock weathering rates through a wide variety of processes. Weathering proceeds as described by the overall reaction:
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). Plant roots are especially effective at accelerating chemical and physical weathering of rocks and soils (Raven and Edwards, 2001; Berner et al., 2003) by increasing the surface area of soil–root interface directly and by fracturing mineral grains (Fig. 4). Roots also anchor soils, and decelerate physical erosion, thus increasing the water contact time of primary minerals. At the regional scale, recirculation of precipitation by evapotranspiration dissolves minerals more efficiently and enhances transport of bicarbonate ions from soils into rivers (Berner et al., 2003). After transport to the oceans by rivers, weathering products are removed by the formation of carbonates. Plants are also the primary source of organic matter buried in sediments.
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For the past two decades, only two negative stabilizing feedbacks on the long-term carbon cycle involving plants, weathering and organic carbon cycle and have been identified (Volk, 1987
, 1989). Recognizing CO2 as a driver of plant evolution has revealed, through a systems analysis of the intricate web of interactions, several new positive feedback loops (PFLs) that operate only when plants encounter a warm climate (Beerling and Berner, 2005). These feedbacks operate whether CO2 is rising or falling. However, in the context of this Briefing, my comments are confined to the late Palaeozoic (falling CO2) situation.
The four most important PFLs involve the action of CO2 on plant evolution and its feedback on rock weathering rates, and sedimentary organic carbon burial (Fig. 3). In the first PFL (Fig. 3B) a drop in the atmospheric CO2 concentration and a rise in stomatal density permits the evolution of larger leaves through the mechanisms discussed earlier. Higher stomatal densities maximize CO2 diffusion into the leaf under conditions favourable for photosynthesis, and larger leaves capture more solar energy; both traits promote primary production and leafier canopies (Beerling and Berner, 2005). Higher densities are also associated with smaller stomata that can open and close more rapidly helping to protect the xylem water pathway from cavitation and allowing taller plants (Hetherington and Woodward, 2003). Taller, leafier plants require deeper rooting systems and more symbionts, including mycorrhizae, for uptake of water and nutrients (Raven and Edwards, 2001). Deeper roots and more abundant mycorrhizae increase nutrient removal and the surface area of the soil–root interface, accelerating the chemical weathering of silicates and further enhancing the removal of CO2 from the atmosphere (Berner et al., 2003).
In the second PFL, a similar chain of cause and effect follows a drop in atmospheric CO2, but with larger more productive plants enhancing organic carbon burial, both in terrestrial wetlands and marine environments after transport to the sea by rivers. Increasing organic carbon burial with falling atmospheric CO2 reflects a major evolutionary trend towards woody plants containing a high proportion of the relatively non-biodegradable compound lignin (Berner, 2004). An expanding terrestrial biomass, promoting CO2 removal from the atmosphere, is recorded as an enormous increase in sedimentary organic carbon burial on land and in the sea (Fig. 2D), most obviously manifested as carboniferous coal deposits. Two further complementary PFLs to those already described operate through the direct action of CO2 on climate, via the greenhouse effect (Fig. 3D and E).
The strengthening of this suite of PFLs during the late Palaeozoic evolution of the terrestrial flora, especially rooted forests, strongly amplified the extent and rate of both silicate weathering and sedimentary organic carbon burial. It was by way of these geochemical effects that plants brought about the precipitous decline in atmospheric CO2 that led ultimately to the Permo-Carboniferous glaciation (Berner, 2004; Beerling and Berner, 2005). The accelerated removal of CO2 from the atmosphere was only stabilized by the negative CO2-climate feedback loop of the inorganic carbon cycle (Fig. 3A), as the climate cooled and decelerated rates of silicate weathering.
In the long term, plants brought about a gradual and continual alteration of the global environment that modified selection pressures on subsequent generations, effectively facilitating their own evolution through the process of niche construction (Odling-Smee et al., 2003). Moreover, plant activities appear to have caused rates of evolution in terrestrial animals to accelerate. Late Palaeozoic insect and tetrapod faunas diversified together with terrestrial plants, and enhanced burial of organic carbon raised global oxygen levels (Berner, 2004), fuelling a spectacular radiation of insect gigantism (Graham et al., 1995).
CONCLUSIONS
Establishing a framework for understanding the origin and diversification of leaves in the Palaeozoic requires information from a broad range of disciplines that include palaeontology, plant physiology, geochemistry and molecular developmental genetics. Progress in many of these fields of research has seen such a framework begin to emerge and suggests that the exceptionally long 40- to 50-Myr delay in the advent of large megaphylls was a product of environmental opportunity and genetic potential. Once the morphogenetic potential of plants was released by falling atmospheric CO2 concentrations, leaf evolution entrained global consequences not only for the regulation of CO2 and climate but also for terrestrial organisms. Plants themselves effectively policed their own evolution through their influence on the silicate-rock-weathering–CO2-climate feedback cycle.
ACKNOWLEDGEMENTS
I thank Robert Berner, Ben Fletcher and Colin Osborne for comments on the manuscript, Andrew Fleming for discussions on the evolutionary developmental biology of leaves, Carl Bowser (University of Wisconsin) for permission to reproduce his photograph in Fig. 4 and Elizabeth and Robert Berner for drawing it to my attention. I am indebted to Bill Chaloner for many stimulating discussions on the evolution of megaphylls.
LITERATURE CITED
-
Beerling DJ, Berner RA. 2005. Feedbacks and the coevolution of plants and atmospheric CO2. Proceedings of the National Academy of Sciences of the USA 102: 1302–1305.
Beerling DJ, Osborne CP, Chaloner WG. 2001. Evolution of leaf-form in land plants linked to atmospheric CO2 decline in the Late Palaeozoic. Nature 410: 352–354.
Berner EK, Berner RA, Moulton KL. 2003. Plants and mineral weathering: present and past. Treatise on Geochemistry 5: 169–188.
Berner RA. 2004. The phanerozoic carbon cycle: CO2 and O2. Oxford: Oxford University Press.
Berner RA, Lasaga AC, Garrels RM. 1983. The carbonate-silicate geochemical cycle and its effect on atmospheric carbon dioxide and climate. American Journal of Science 283: 641–683.
Boyce CK, Knoll AH. 2002. Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28: 70–100.
Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA. 2000. Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408: 967–971.[CrossRef][Medline]
Chaloner WG, Sheerin A. 1979. Devonian macrofloras. In: House MR, Scrutton CT, Bassett MG. The Devonian system. Palaeontological Society Special Paper in Palaeontology 23: 145–161.
Cronk QCB. 2001. Plant evolution and development in a post-genomic context. Nature Reviews, Genetics 2: 607–619.[CrossRef][Web of Science][Medline]
Edwards D. 1998. Climate signals in Palaeozoic land plants. Philosophical Transactions of the Royal Society, Series B 353: 141–157.
Edwards D, Wellman C. 2001. Embryophytes invade the land. In: Gensel PG, Edwards D, eds. Plants invade the land. New York, NY: Columbia University Press, 3–28.
Ehleringer JR. 1988. Comparative ecophysiology of Encelia farinosa and Encelia frutescens. 1. Energy balance considerations. Oecologia 76: 553–561.
Emery JF, Floyd SK, Alvarez J, Eshed Y, Hawker NP, Izhaki A, et al. 2003. Radial patterning of Arabidopsis shoots by class III HD-ZIP and KANADI genes. Current Biology 13: 1768–1774.[CrossRef][Web of Science][Medline]
Field CB, Behrenfeld MJ, Randerson JT, Falkowski P 1998. Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281: 237–240.
Floyd SK, Bowman JL. 2004. Ancient microRNA target sequences in plants. Nature 428: 485–486.[CrossRef][Medline]
Gifford EM, Foster AS. 1988. Morphology and evolution of vascular plants. New York, NY: Freeman.
Graham JB, Dudley R, Aguilar NM, Gans C. 1995. Implications of the late Palaeozoic oxygen pulse for physiology and evolution. Nature 375: 117–120.[CrossRef]
Gray JE, Holroyd GH, van der Lee FM, Bahrami AR, Sijmons PC, Woodward FI, Schuch W, Hetherington AM. 2000. The HIC signalling pathway links CO2 perception to stomatal development. Nature 408: 713–716.[CrossRef][Medline]
Hake S, Smith HMS, Holtan H, Magnani E, Mele G, Ramirez J. 2004. The role of KNOX genes in plant development. Annual Review of Cell and Developmental Biology 20: 125–151.[CrossRef][Web of Science][Medline]
Hao SG, Beck CB. 1993. Further observations on Eophyllophyton bellum from the lower Devonian (Siegenian) of Yunnan, China. Palaeontographica 230: 27–47.
Hao S, Beck CB, Deming W. 2003. Structure of the earliest leaves: adaptations to high concentrations of CO2. International Journal of Plant Sciences 164: 71–75.
Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA. 2005. Independent recruitment of a conserved developmental mechanism during leaf formation. Nature 434: 509–514.[CrossRef][Medline]
Hetherington AM, Woodward FI. 2003. The role of stomata in sensing and driving environmental change. Nature 424: 901–908.[CrossRef][Medline]
Kenrick P, Crane PR. 1997. The origin and early evolution of plants on land. Nature 389: 33–39.[CrossRef]
Knoll AH, Niklas KJ, Gensel PG, Tiffney BH. 1984. Character diversification and patterns of evolution in early vascular plants. Paleobiology 10: 34–47.[Abstract]
McElwain JC, Chaloner WG. 1995. Stomatal density and index of fossil plants track atmospheric carbon dioxide in the Palaeozoic. Annals of Botany 76: 389–395.
Matten LC. 1968. Actinoxylon banksii Gen. Et. Sp. Nov.: a progymnosperm from the middle Devonian of New York. American Journal of Botany 55: 773–782.
Odling-Smee FJ, Laland KN, Feldman MW. 2003. Niche construction. The neglected process in evolution. Princeton, NJ: Princeton University Press.
Osborne CP, Beerling DJ, Lomax BH, Chaloner WG. 2004a. Biophysical constraints on the origin of leaves inferred from the fossil record. Proceedings of the National Academy of Sciences of the USA 101: 10360–10362.
Osborne CP, Chaloner WG, Beerling DJ. 2004b. Falling atmospheric CO2 – the key to megaphyll leaf origins. In: Poole I, Hemsley AR. The evolution of plant physiology. Kew: Elsevier Academic Press, 197–215.
Raven JA, Edwards D. 2001. Roots: evolutionary origins and biogeochemical significance. Journal of Experimental Botany 52: 381–401.
Roth-Nebelsick A. 2001. Heat transfer of Rhyniophytic plant axes. Review of Palaeobotany and Palynology 116: 109–122.[CrossRef][Web of Science]
Rowe N, Speck T. 2005. Plant growth forms: an ecological and evolutionary perspective. New Phytologist doi:10.1111/j.1469-8137.2004.01309.x.
Sano R, Jurárez CM, Hass B, Sakakibara K, Ito M, Banks JA, et al. 2005. KNOX homeobox genes potentially have similar function in both diploid unicellular and multicellular meristems, but not haploid meristems. Evolution and Development 7: 69–78.[CrossRef]
Schulte PJ, Gibson AC, Nobel PS. 1987. Xylem anatomy and hydraulic conductance of Psilotum nudum. American Journal of Botany 74: 1438–1445.[CrossRef][Web of Science]
Smith WK. 1978. Temperature of desert plants: another perspective on the adaptability of leaf size. Science 201: 614–616.
Timmermans MCP, Hudson A, Becraft PW, Nelson T. 1999. ROUGH SHEATH2: a Myb protein that represses knox homeobox genes in maize lateral organ primordial. Science 284: 151–153.
Volk T. 1987. Feedbacks between weathering and atmospheric CO2 over the last 100 million years. American Journal of Science 287: 763–779.
Volk T. 1989. Rise of angiosperms as a factor in long-term climatic cooling. Geology 17: 107–110.
Waites R, Hudson A. 1995. PHANTASTICA: a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121: 2143–2154.[Abstract]
Walker JCG, Hays PB, Kasting JF. 1981. A negative feedback mechanism for the long-term stabilization of Earth's surface temperature. Journal of Geophysical Research 86: 9776–9782.[CrossRef]
Woodward FI. 1987. Stomatal numbers are sensitive to CO2 increases from pre-industrial levels. Nature 327: 617–618.[CrossRef]
Zimmermann W. 1930. Die Phylogenie der Pflanzen. Fischer: Jena.
Zimmermann W. 1952. Main results of the telome theory. The Palaeobotanist 1: 456–470.
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