The evolution and functional significance of leaf shape in the angiosperms

Article

<< Previous

Next >>

Contents Vol 38(7)

doi:10.1071/FP11057

Plant Function & Evolutionary Biology

	Search




	Advanced Search



	Journal Home

	About the Journal

	Editorial Board

	Contacts



	Content

	Online Early

	Current Issue

	Just Accepted

	All Issues

	Special Issues

	Research Fronts

	Reviews

	Evolutionary Reviews

	Sample Issue



	For Authors

	General Information

	Notice to Authors

	Submit Article

	Open Access



	For Referees

	Referee Guidelines

	Review Article



	For Subscribers

	Subscription Prices

	Customer Service

	Print Publication Dates

e-Alerts

Subscribe to our Email Alert or

feeds for the latest journal papers.

Connect with us

PrometheusWiki

Protocols in ecological and environmental plant physiology

The evolution and functional significance of leaf shape in the angiosperms

Adrienne B. Nicotra ^A ^H, Andrea Leigh ^B, C. Kevin Boyce ^C, Cynthia S. Jones ^D, Karl J. Niklas ^E, Dana L. Royer ^F and Hirokazu Tsukaya ^G

^A Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.
^B School of the Environment, University of Technology, Sydney, PO Box 123, Broadway, NSW 2007, Australia.
^C Department of the Geophysical Sciences, 5734 S. Ellis Avenue, Chicago, IL 60637, USA.
^D Department of Ecology and Evolutionary Biology, University of Connecticut, 75 N. Eagleville Road, Unit-3043, Storrs, CT 06269, USA.
^E Department of Plant Biology, Cornell University, 412 Mann Library Building, Cornell University, Ithaca, NY 14853, USA.
^F Department of Earth and Environmental Sciences, Wesleyan University, 265 Church Street, Middletown, CT 06459, USA.
^G Graduate School of Science, University of Tokyo, Science Build #2, 7-3-1 Hongo, Tokyo 113-0033, Japan.
^H Corresponding author. Email: adrienne.nicotra@anu.edu.au
This paper is part of an ongoing series: ‘The Evolution of Plant Functions’.

Functional Plant Biology 38(7) 535-552 http://dx.doi.org/10.1071/FP11057
Submitted: 28 February 2011 Accepted: 30 May 2011 Published: 12 July 2011





	Full Text



	PDF (1.2 MB)



	Export Citation

Print

Abstract

Angiosperm leaves manifest a remarkable diversity of shapes that range from developmental sequences within a shoot and within crown response to microenvironment to variation among species within and between communities and among orders or families. It is generally assumed that because photosynthetic leaves are critical to plant growth and survival, variation in their shape reflects natural selection operating on function. Several non-mutually exclusive theories have been proposed to explain leaf shape diversity. These include: thermoregulation of leaves especially in arid and hot environments, hydraulic constraints, patterns of leaf expansion in deciduous species, biomechanical constraints, adaptations to avoid herbivory, adaptations to optimise light interception and even that leaf shape variation is a response to selection on flower form. However, the relative importance, or likelihood, of each of these factors is unclear. Here we review the evolutionary context of leaf shape diversification, discuss the proximal mechanisms that generate the diversity in extant systems, and consider the evidence for each the above hypotheses in the context of the functional significance of leaf shape. The synthesis of these broad ranging areas helps to identify points of conceptual convergence for ongoing discussion and integrated directions for future research.

Additional keywords:compound leaf, leaf dissection, leaf margin, leaf size, leaves, lobbing.

References

Ackerly DD, Knight CA, Weiss SB, Barton K, Starmer KP (2002) Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia 130, 449–457.
| CrossRef |

Anderson S (1989) Variation in heteroblastic succession among populations of Crepis tectorum. Nordic Journal of Botany 8, 565–573.
| CrossRef |

Armbruster WS, Muchhala N (2009) Associations between floral specialization and species diversity: cause, effect, or correlation? Evolutionary Ecology 23, 159–179.
| CrossRef |

Armbruster WS, Di Stilio VS, Tuxill JD, Flores TC, Runk JLV (1999) Covariance and decoupling of floral and vegetative traits in nine neotropical plants: a re-evaluation of Berg’s correlation-pleiades concept. American Journal of Botany 86, 39–55.
| CrossRef | CAS | PubMed |

Ashby E (1948) Studies in the morphogenesis of leaves I. An essay on leaf shape. New Phytologist 47, 153–176.
| CrossRef |

Aso K, Kato M, Banks JA, Hasebe M (1999) Characterization of homeodomain-leucine zipper genes in the fern Ceratopteris richardii and the evolution of the homeodomain-leucine zipper gene family in vascular plants. Molecular Biology and Evolution 16, 544–552.
| CAS | PubMed |

Bailey IW, Sinnott EW (1915) A botanical index of Cretaceous and Tertiary climates. Science 41, 831–834.
| CrossRef | CAS | PubMed |

Bailey IW, Sinnott EW (1916) The climatic distribution of certain types of angiosperm leaves. American Journal of Botany 3, 24–39.
| CrossRef |

Baker-Brosh KF, Peet RK (1997) The ecological significance of lobed and toothed leaves in temperate forest trees. Ecology 78, 1250–1255.

Bakker FT, Culham A, Marais EM, Gibby M (2005) Nested radiation in Cape Pelargonium. In ‘Plant species-level systematics: new perspectives on pattern and process. Vol. 143’. (Eds FT Bakker, LW Chartrou, B Gravendeel, PB Pielser) pp. 75–100. (ARG Ganter Verlag KG: Ruggell, Lichtstein)

Balfour IB (Transl) (1969) ‘Organography of plants. I. General organography.’ by K. Goebel, 1900. (Hafner Publishing Co. Inc.: New York)

Ball MC, Cowan IR, Farquhar GD (1988) Maintenance of leaf temperature and the optimization of carbon gain in relation to water loss in a tropical mangrove forest. Australian Journal of Plant Physiology 15, 263–276.
| CrossRef |

Ball MC, Canny MJ, Huang CX, Heady RD (2004) Structural changes in acclimated and unacclimated leaves during freezing and thawing. Functional Plant Biology 31, 29–40.
| CrossRef |

Ball MC, Canny MJ, Huang CX, Egerton JJG, Wolfe J (2006) Freeze/thaw-induced embolism depends on nadir temperature: the heterogeneous hydration hypothesis. Plant, Cell & Environment 29, 729–745.
| CrossRef | CAS | PubMed |

Barkoulas M, Hay A, Kougioumoutzi E, Tsiantis M (2008) A developmental framework for dissected leaf formation in the Arabidopsis relative Cardamine hirsuta. Nature Genetics 40, 1136–1141.
| CrossRef | CAS | PubMed |

Beadle NCW (1966) Soil phosphate and its role in molding segments of the Australian flora and vegetation, with special reference to xeromorphy and sclerophylly. Ecology 47, 992–1007.
| CrossRef |

Berg RL (1960) The ecological significance of correlation pleiades. Evolution 14, 171–180.
| CrossRef |

Bharathan G, Goliber TE, Moore C, Kessler S, Pham T, Sinha NR (2002) Homologies in leaf form inferred from KNOXI gene expression during development. Science 296, 1858–1860.
| CrossRef | CAS | PubMed |

Billings FH (1905) Precursory leaf serrations of Ulmus. Botanical Gazette 40, 224–225.
| CrossRef |

Blein T, Pulido A, Vialette-Guiraud A, Nikovics K, Morin H, Hay A, Johansen IE, Tsiantis M, Laufs P (2008) A conserved molecular framework for compound leaf development. Science 322, 1835–1839.
| CrossRef | CAS | PubMed |

Bond WJ (1989) The tortoise and the hare: ecology of angiosperm dominance and gymnosperm persistence. Biological Journal of the Linnean Society. Linnean Society of London 36, 227–249.
| CrossRef |

Boyce CK (2005) Patterns of segregation and convergence in the evolution of fern and seed plant leaf morphologies. Paleobiology 31, 117–140.
| CrossRef |

Boyce CK (2007) Mechanisms of laminar growth in morphologically convergent leaves and flower petals. International Journal of Plant Sciences 168, 1151–1156.
| CrossRef |

Boyce CK (2008a) The fossil record of plant physiology and development – what leaves can tell us. Paleontological Society Papers 14, 133–146.

Boyce CK (2008b) How green was Cooksonia? The importance of size in understanding the early evolution of physiology in the vascular plant lineage. Paleobiology 34, 179–194.
| CrossRef |

Boyce CK (2009) Seeing the forest with the leaves – clues to canopy placement from leaf fossil size and venation characteristics. Geobiology 7, 192–199.
| CrossRef | CAS | PubMed |

Boyce CK (2010) The evolution of plant development in a paleontological context. Current Opinion in Plant Biology 13, 102–107.
| CrossRef | PubMed |

Boyce CK, Knoll AH (2002) Evolution of developmental potential and the multiple independent origins of leaves in Paleozoic vascular plants. Paleobiology 28, 70–100.
| CrossRef |

Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution was physiologically and environmentally transformative. Proceedings of the Royal Society B-Biological Sciences 276, 1771–1776.
| CrossRef |

Bragg JG, Westoby M (2002) Leaf size and foraging for light in a sclerophyll woodland. Functional Ecology 16, 633–639.
| CrossRef |

Brennan EB, Weinbaum SA, Rosenheim JA, Karban R (2001) Heteroblasty in Eucalyptus globulus (Myricales: Myricaceae) affects ovipositonal and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera: Psyllidae). Environmental Entomology 30, 1144–1149.
| CrossRef |

Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic capacity during early angiosperm diversification. Ecology Letters 13, 175–183.
| CrossRef | PubMed |

Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and venation are linked by hydraulics. Plant Physiology 144, 1890–1898.
| CrossRef | CAS | PubMed |

Brodribb TJ, Feild TS, Sack L (2010) Viewing leaf structure and evolution from a hydraulic perspective. Functional Plant Biology 37, 488–498.
| CrossRef |

Bruni NC, Young JP, Dengler NG (1996) Leaf developmental plasticity of Ranunculus flabellaris in response to terrestrial and submerged environments. Canadian Journal of Botany 74, 823–837.
| CrossRef |

Burnham RJ, Pitman NCA, Johnson KR, Wilf P (2001) Habitat-related error in estimating temperatures from leaf margins in a humid tropical forest. American Journal of Botany 88, 1096–1102.
| CrossRef | CAS | PubMed |

Canales C, Barkoulas M, Galinha C, Tsiantis M (2010) Weeds of change: Cardamine hirsuta as a new model system for studying dissected leaf development. Journal of Plant Research 123, 25–33.
| CrossRef | PubMed |

Chuck G, O’Connor D (2010) Small RNAs going the distance during plant development. Current Opinion in Plant Biology 13, 40–45.
| CrossRef | CAS | PubMed |

Climent J, Chambel MR, Lopez R, Mutke S, Alia R, Gil L (2006) Population divergence for heteroblasty in the Canary Island pine (Pinus canariensis, Pinaceae). American Journal of Botany 93, 840–848.
| CrossRef | PubMed |

Clum HH (1926) The effect of transpiration and environmental factors on leaf temperatures 1. Transpiration. American Journal of Botany 13, 194–216.
| CrossRef |

Cowling RM, Lamont BB (1998) On the nature of Gondwanan species flocks: diversity of Proteaceae in Mediterranean south-western Australia and South Africa. Australian Journal of Botany 46, 335–355.
| CrossRef |

Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecological Monographs 69, 569–588.
| CrossRef |

Darrow HE, Bannister P, Burritt DJ, Jameson PE (2001) The frost resistance of juvenile and adult forms of some heteroblastic New Zealand plants. New Zealand Journal of Botany 39, 355–363.
| CrossRef |

de Reuille PB, Bohn-Courseau I, Ljung K, Morin H, Carraro N, Godin C, Traas J (2006) Computer simulations reveal properties of the cell–cell signaling network at the shoot apex in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 103, 1627–1632.
| CrossRef | PubMed |

Dengler N (1980) Comparative histological basis of sun and shade leaf dimorphism in Helianthus annuus. Canadian Journal of Botany 58, 717–730.
| CrossRef |

Dinneny JR, Yadegari R, Fischer RL, Yanofsky MF, Weigel D (2004) The role of JAGGED in shaping lateral organs. Development 131, 1101–1110.
| CrossRef | CAS | PubMed |

Doyle J, Hickey L (1976) Pollen and leaves from the mid-Cretaceous potomac group and their bearing on early angiosperm evolution. In ‘Origin and early evolution of Angiosperms’. (Ed. C Beck) pp. 139–206. (Columbia University Press: New York)

Drake BG, Raschke K, Salisbury FB (1970) Temperatures and transpiration resistances of Xanthium leaves as affected by air temperature, humidity, and wind speed. Plant Physiology 46, 324–330.
| CrossRef | CAS | PubMed |

Efroni I, Blum E, Goldshmidt A, Eshed Y (2008) A protracted and dynamic maturation schedule underlies Arabidopsis leaf development. The Plant Cell 20, 2293–2306.
| CrossRef | CAS | PubMed |

Efroni I, Eshed Y, Lifschitz E (2010) Morphogenesis of simple and compound leaves: a critical review. The Plant Cell 22, 1019–1032.
| CrossRef | CAS | PubMed |

Fadzly N, Jack C, Schaefer HM, Burns KC (2009) Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytologist 184, 495–501.
| CrossRef | PubMed |

Feild TS, Sage TL, Czerniak C, Iles WJD (2005) Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation-induced flooding of the mesophyll. Plant, Cell & Environment 28, 1179–1190.
| CrossRef | CAS |

Floyd SK, Bowman JL (2006) Distinct developmental mechanisms reflect the independent origins of leaves in vascular plants. Current Biology 16, 1911–1917.
| CrossRef | CAS | PubMed |

Floyd SK, Bowman JL (2010) Gene expression patterns in seed plant shoot meristems and leaves: homoplasy or homology? Journal of Plant Research 123, 43–55.
| CrossRef | CAS | PubMed |

Fonseca CR, Overton JM, Collins B, Westoby M (2000) Shifts in trait combinations along rainfall and phosphorus gradients. Journal of Ecology 88, 964–977.
| CrossRef |

Foreman BH, Hyland B (1995) Stenocarpus. In ‘Flora of Australia. Vol. 16’. (Ed. P McCarthy) pp. 364–366. (CSIRO Publishing: Melbourne)

Forster MA, Bonser SP (2009) Heteroblastic development and the optimal partitioning of traits among contrasting environments in Acacia implexa. Annals of Botany 103, 95–105.
| CrossRef | PubMed |

Forster MA, Ladd B, Bonser SP (2011) Optimal allocation of resources in response to shading and neighbours in the heteroblastic species, Acacia implexa. Annals of Botany 103, 95–105.
| CrossRef |

Frohlich MW, Chase MW (2007) After a dozen years of progress the origin of angiosperms is still a great mystery. Nature 450, 1184–1189.
| CrossRef | CAS | PubMed |

Galtier J (1981) Structures foliaires de fougères et Ptéridospermales du Carbonifère Inférieur et leur signification évolutive. Palaeontographica Abt. B 180, 1–38.

Gamage HK, Jesson L (2007) Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light. New Zealand Journal of Ecology 31, 245–254.

Gates DM (1968) Transpiration and leaf temperature. Annual Review of Plant Physiology 19, 211–238.
| CrossRef |

Gates DM (1980) ‘Biophysical ecology.’ (Springer-Verlag: New York)

Gates DM, Alderfer R, Taylor E (1968) Leaf temperatures of desert plants. Science 159, 994–995.
| CrossRef | CAS | PubMed |

Geller GN, Smith WK (1982) Influence of leaf size, orientation, and arrangement on temperature and transpiration in three high-elevation, large leafed herbs. Oecologia 53, 227–234.
| CrossRef |

Givnish TJ (1978) Ecological aspects of plant morphology: leaf form in relation to environment. Acta Biotheoretica 27, 83–142.

Givnish TJ (1979) On the adaptive significance of leaf form. In ‘Topics in plant population biology’. (Eds OT Solbrig, J Subodh, GB Johnson, PH Raven) pp. 375–407. (Columbia University Press: New York)

Goliber TE, Feldman LJ (1990) Developmental analysis of leaf plasticity in the heterophyllous aquatic plant Hippuris vulgaris. American Journal of Botany 77, 399–412.
| CrossRef |

Gottschlich DE, Smith AP (1982) Convective heat transfer characteristics of toothed leaves. Oecologia 53, 418–420.
| CrossRef |

Grace J, Fasehun FE, Dixon M (1980) Boundary layer conductance of the leaves of some tropical timber trees. Plant, Cell & Environment 3, 443–450.

Greenwood DR (2005a) Leaf form and the reconstruction of past climates. New Phytologist 166, 355–357.
| CrossRef | PubMed |

Greenwood DR (2005b) Leaf margin analysis: taphonomic constraints. Palaios 20, 498–505.
| CrossRef |

Groom PK, Lamont BB, Leighton S, Leighton P, Burrows C (2004) Heat damage in sclerophylls is influenced by their leaf properties and plant environment. Ecoscience 11, 94–101.

Gurevitch J, Schuepp PH (1990a) Boundary layer properties of highly dissected leaves – an investigation using an electrochemical fluid tunnel. Plant, Cell & Environment 13, 783–792.
| CrossRef |

Gurevitch J, Schuepp PH (1990b) Boundary layer properties of highly dissected leaves: an investigation using an electrochemical fluid tunnel. Plant, Cell & Environment 13, 783–792.
| CrossRef |

Hansen DH (1986) Water relations of compound leaves and phyllodes in Acacia koa var. latifolia. Plant, Cell & Environment 9, 439–445.
| CrossRef |

Harrison CJ, Corley SB, Moylan EC, Alexander DL, Scotland RW, Langdale JA (2005) Independent recruitment of a conserved developmental mechanism during leaf evolution. Nature 434, 509–514.
| CrossRef | CAS | PubMed |

Hegazy AK, El Amry MI (1998) Leaf temperature of desert sand dune plants: perspectives on the adaptability of leaf morphology. African Journal of Ecology 36, 34–43.
| CrossRef |

Hilton J, Bateman RM (2006) Pteridosperms are the backbone of seed–plant phylogeny. Journal of the Torrey Botanical Society 133, 119–168.
| CrossRef |

Hofer J, Turner L, Hellens R, Ambrose M, Matthews P, Michael A, Ellis N (1997) UNIFOLIATA regulates leaf and flower morphogenesis in pea. Current Biology 7, 581–587.
| CrossRef | CAS | PubMed |

Hoot SB, Douglas AW (1998) Phylogeny of the Proteaceae based on atpB and atpB-rbcL intergenic spacer region sequences. Australian Systematic Botany 11, 301–320.
| CrossRef |

Horiguchi G, Kim GT, Tsukaya H (2005) The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana. The Plant Journal 43, 68–78.
| CrossRef | CAS | PubMed |

Horiguchi G, Fujikura U, Ferjani A, Ishikawa N, Tsukaya H (2006) Large-scale histological analysis of leaf mutants using two simple leaf observation methods: identification of novel genetic pathways governing the size and shape of leaves. The Plant Journal 48, 638–644.
| CrossRef | CAS | PubMed |

Huff PM, Wilf P, Azumah EJ (2003) Digital future for paleoclimate estimation from fossil leaves? Preliminary results. Palaios 18, 266–274.
| CrossRef |

Husbands AY, Chitwood DH, Plavskin Y, Timmermans MCP (2009) Signals and prepatterns: new insights into organ polarity in plants. Genes & Development 23, 1986–1997.
| CrossRef | CAS | PubMed |

Illing N, Klak C, Johnson C, Brito D, Negrao N, Baine F, van Kets V, Ramchurn KR, Seoighe C, Roden L (2009) Duplication of the Asymmetric Leaves1/Rough Sheath 2/Phantastica (ARP) gene precedes the explosive radiation of the Ruschioideae. Development Genes and Evolution 219, 331–338.
| CrossRef | CAS | PubMed |

Jaya E, Kubien DS, Jameson PE, Clemens J (2010) Vegetative phase change and photosynthesis in Eucalyptus occidentalis: architectural simplification prolongs juvenile traits. Tree Physiology 30, 393–403.
| CrossRef | PubMed |

Jones HG (1992) ‘Plants and microclimate: a quantitative approach to environmental plant physiology.’ 2nd edn. (Cambridge University Press: Cambridge)

Jones CS (1995) Does shade prolong juvenile development? A morphological analysis of leaf shape changes in Cucurbita argyrosperma subsp. sororia (Cucurbitaceae). American Journal of Botany 82, 346–359.
| CrossRef |

Jones CS (1999) An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160, S105–S111.
| CrossRef | PubMed |

Jones CS (2001) The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Bulletin of the Botanical Society of Argentina 36, 171–184.

Jones CS, Bakker FT, Schlichting CD, Nicotra AB (2009) Leaf shape evolution in the South African genus Pelargonium L’ Her. (Geraniaceae). Evolution 63, 479–497.
| CrossRef | PubMed |

Jonsson H, Heisler MG, Shapiro BE, Meyerowitz EM, Mjolsness E (2006) An auxin-driven polarized transport model for phyllotaxis. Proceedings of the National Academy of Sciences of the United States of America 103, 1633–1638.
| CrossRef | PubMed |

Karban R, Thaler JS (1999) Plant phase change and resistance to herbivory. Ecology 80, 510–517.
| CrossRef |

Kawamura E, Horiguchi G, Tsukaya H (2010) Mechanisms of leaf tooth formation in Arabidopsis. The Plant Journal 62, 429–441.
| CrossRef | CAS | PubMed |

Kay KM, Sargent RD (2009) The role of animal pollination in plant speciation: Integrating ecology, geography, and genetics. Annual Review of Ecology, Evolution, and Systematics 40, 637–656.
| CrossRef |

Kenrick P, Crane PR (1997) The origin and early evolution of plants on land. Nature 389, 33–39.
| CrossRef | CAS |

Kerstetter RA, Poethig RS (1998) The specification of leaf identity during shoot development. Annual Review of Cell and Developmental Biology 14, 373–398.
| CrossRef | CAS | PubMed |

Kidner CA (2010) The many roles of small RNAs in leaf development. Journal of Genetics and Genomics 37, 13–21.
| CrossRef | CAS | PubMed |

Kim GT, Tsukaya H, Saito Y, Uchimiya H (1999) Changes in the shapes of leaves and flowers upon overexpression of cytochrome P450 in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 96, 9433–9437.
| CrossRef | CAS | PubMed |

Kim M, McCormick S, Timmermans M, Sinha N (2003) The expression domain of PHANTASTICA determines leaflet placement in compound leaves. Nature 424, 438–443.
| CrossRef | CAS | PubMed |

Kleiman D, Aarssen LW (2007) The leaf size/number trade-off in trees. Journal of Ecology 95, 376–382.
| CrossRef |

Kowalski EA, Dilcher DL (2003) Warmer paleotemperatures for terrestrial ecosystems. Proceedings of the National Academy of Sciences of the United States of America 100, 167–170.
| CrossRef | CAS | PubMed |

Kubien DS, Jaya E, Clemens J (2007) Differences in the structure and gas exchange physiology of juvenile and adult leaves in Metrosideros excelsa. International Journal of Plant Sciences 168, 563–570.
| CrossRef |

Kuwabara A, Nagata T (2006) Cellular basis of developmental plasticity observed in heterophyllous leaf formation of Ludwigia arcuata (Onagraceae). Planta 224, 761–770.
| CrossRef | CAS | PubMed |

Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Plant development: signals from mature to new leaves. Nature 411, 154
| CrossRef | CAS | PubMed |

Latimer AM, Silander JA, Cowling RM (2005) Neutral ecological theory reveals isolation and rapid speciation in a biodiversity hot spot. Science 309, 1722–1725.
| CrossRef | CAS | PubMed |

Lee YK, Kim GT, Kim IJ, Park J, Kwak SS, Choi G, Chung WI (2006) LONGIFOLIA1 and LONGIFOLIA2, two homologous genes, regulate longitudinal cell elongation in Arabidopsis. Development 133, 4305–4314.
| CrossRef | CAS | PubMed |

Leigh A, Zwieniecki MA, Rockwell FE, Boyce CK, Nicotra AB, Holbrook NM (2011) Structural and physiological correlates of heterophylly in Ginkgo biloba L. New Phytologist 189, 459–470.
| CrossRef | CAS | PubMed |

Levitt J (1980) ‘Responses of plants to environmental stresses.’ 2nd edn. (Academic Press: New York)

Lewis MC (1972) Physiological significance of variation in leaf structure. Science Progress 60, 25–51.

Linder HP (2005) Evolution of diversity: the Cape flora. Trends in Plant Science 10, 536–541.
| CrossRef | CAS | PubMed |

Little SA, Kembel SW, Wilf P (2010) Paleotemperature proxies from leaf fossils reinterpreted in light of evolutionary history. PLoS ONE 5, e15161
| CrossRef | CAS | PubMed |

Martinez-Cabrera HI (2010) Influence of climate in functional and species diversification in South African Pelargonium. PhD Thesis, University of Connecticut, Storrs, CT, USA.

McDonald PG, Fonseca CR, Overton JM, Westoby M (2003) Leaf-size divergence along rainfall and soil-nutrient gradients: is the method of size reduction common among clades? Functional Ecology 17, 50–57.
| CrossRef |

Melville R (1969) Leaf venation pattern and origin of angiosperms. Nature 224, 121–125.
| CrossRef |

Monteith JL, Unsworth MH (1990) ‘Principles of environmental physics.’ 2nd edn. (Edward Arnold: London)

Mueller RJ (1982) Shoot ontogeny and the comparative development of the heteroblastic leaf series in Lygodium japonicum (Thunb.) Sw. Botanical Gazette (Chicago, Ill.) 143, 424–438.
| CrossRef |

Nath U, Crawford BCW, Carpenter R, Coen E (2003) Genetic control of surface curvature. Science 299, 1404–1407.
| CrossRef | CAS | PubMed |

Nicotra AB (2010) Leaf size and shape. PrometheusWiki. Available at http://prometheuswiki.publish.csiro.au/tiki-index.php?page=Leaf+size+and+shape [Verified 2 June 2011]

Nicotra AB, Cosgrove MJ, Cowling A, Schlichting CD, Jones CS (2008) Leaf shape linked to photosynthetic rates and temperature optima in South African Pelargonium species. Oecologia 154, 625–635.
| CrossRef | CAS | PubMed |

Niklas KJ (1988) The role of phyllotactic pattern as a developmental constraint on the interception of light by leaf surfaces. Evolution 42, 1–16.
| CrossRef |

Niklas KJ (1997) ‘The evolutionary biology of plants.’ (University of Chicago Press: Chicago)

Niklas KJ (2000) The evolution of plant body plans – a biomechanical perspective. Annals of Botany 85, 411–438.
| CrossRef |

Niklas KJ (2004) Plant allometry: is there a grand unifying theory? Biological Reviews of the Cambridge Philosophical Society 79, 871–889.
| CrossRef | PubMed |

Niklas KJ, Cobb ED (2008) Evidence for ‘diminishing returns’ from the scaling of stem diameter and specific leaf area. American Journal of Botany 95, 549–557.
| CrossRef | PubMed |

Niklas KJ, Cobb ED (2010) Ontogenetic changes in the numbers of short- v. long-shoots account for decreasing specific leaf area in Acer rubrum (Aceraceae) as trees increase in size. American Journal of Botany 97, 27–37.
| CrossRef | PubMed |

Niklas KJ, Cobb ED, Niinemets U, Reich PB, Sellin A, Shipley B, Wright IJ (2007) ‘Diminishing returns’ in the scaling of functional leaf traits across and within species groups. Proceedings of the National Academy of Sciences of the United States of America 104, 8891–8896.
| CrossRef | CAS | PubMed |

Niklas KJ, Cobb ED, Spatz H-C (2009) Predicting the allometry of leaf surface area and dry mass. American Journal of Botany 96, 531–536.
| CrossRef | PubMed |

Nobel PS (1988) ‘Environmental biology of Agaves and Cacti.’ (Cambridge University Press: Cambridge)

Oguchi R, Hikosaka K, Hirose T (2005) Leaf anatomy as a constraint for photosynthetic acclimation: differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees. Plant, Cell & Environment 28, 916–927.
| CrossRef |

Okada K, Ueda J, Komaki MK, Bell CJ, Shimura Y (1991) Requirement of the auxin polar transport-system in early stages of Arabidopsis floral bud formation. The Plant Cell 3, 677–684.
| CAS | PubMed |

Parkhurst DF, Loucks OL (1972) Optimal leaf size in relation to environment. Journal of Ecology 60, 505–537.
| CrossRef |

Parkhurst DF, Duncan PR, Gates DM, Kreith F (1968) Wind-tunnel modelling of convection of heat between air and broad leaves of plants. Agricultural Meteorology 5, 33–47.
| CrossRef |

Pasquet-Kok J, Creese C, Sack L (2010) Turning over a new ‘leaf’: multiple functional significances of leaves versus phyllodes in Hawaiian Acacia koa. Plant, Cell & Environment 33, 2084–2100.
| CrossRef | PubMed |

Peppe DJ, Royer DL, Cariglino B, Oliver SY, Newman S, et al (2011) Sensitivity of leaf size and shape to climate: global patterns and paleoclimatic applications. New Phytologist 190, 724–739.
| CrossRef | PubMed |

Perez-Perez JM, Serrano-Cartagena J, Micol JL (2002) Genetic analysis of natural variations in the architecture of Arabidopsis thaliana vegetative leaves. Genetics 162, 893–915.
| CAS | PubMed |

Perez-Perez JM, Candela H, Robles P, Quesada V, Ponce MR, Micol JL (2009) Lessons from a search for leaf mutants in Arabidopsis thaliana. The International Journal of Developmental Biology 53, 1623–1634.
| CrossRef | CAS | PubMed |

Poethig RS, Sussex IM (1985a) The cellular-parameters of leaf development in tobacco – a clonal analysis. Planta 165, 170–184.
| CrossRef |

Poethig RS, Sussex IM (1985b) The developmental morphology and growth dynamics of the tobacco leaf. Planta 165, 158–169.
| CrossRef |

Pray TR (1955) Foliar venation of angiosperms. 2. Histogenesis of the venation of Liriodendron. American Journal of Botany 42, 18–27.
| CrossRef |

Pray TR (1960) Ontogeny of the open dichotomous venation in the pinna of the fern Nephrolepis. American Journal of Botany 47, 319–328.
| CrossRef |

Pryer KM, Hearn DJ (2009) Evolution of leaf form in Marsileaceous ferns: evidence for heterochrony. Evolution 63, 498–513.
| CrossRef | PubMed |

Raschke K (1960) Heat transfer between the plant and the environment. Annual Review of Plant Physiology and Plant Molecular Biology 11, 111–126.

Raunkiaer C (1934) ‘The life forms of plants and statistical plant geography.’ (Clarendon Press: Oxford)

Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Annals of Botany 78, 137–142.
| CrossRef |

Roth-Nebelsick A (2001) Computer-based analysis of steady-state and transient heat transfer of small-sized leaves by free and mixed convection. Plant, Cell & Environment 24, 631–640.
| CrossRef |

Royer DL, Wilf P (2006) Why do toothed leaves correlate with cold climates? Gas exchange at leaf margins provides new insights into a classic paleotemperature proxy. International Journal of Plant Sciences 167, 11–18.
| CrossRef |

Royer DL, Wilf P, Janesko DA, Kowalski EA, Dilcher DL (2005) Correlations of climate and plant ecology to leaf size and shape: potential proxies for the fossil record. American Journal of Botany 92, 1141–1151.
| CrossRef | PubMed |

Royer DL, Kooyman RM, Wilf P (2009a) Ecology of leaf teeth: a multi-site analysis from an Australian subtropical rainforest. American Journal of Botany 96, 738–750.
| CrossRef | PubMed |

Royer DL, Meyerson LA, Robertson KM, Adams JM (2009b) Phenotypic plasticity of leaf shape along a temperature gradient in Acer rubrum. PLoS ONE 4, e7653
| CrossRef | PubMed |

Sack L, Frole K (2006) Leaf structural diversity is related to hydraulic capacity in tropical rain forest trees. Ecology 87, 483–491.
| CrossRef | PubMed |

Sack L, Holbrook NM (2006) Leaf hydraulics. Annual Review of Plant Biology 57, 361–381.
| CrossRef | CAS | PubMed |

Sack L, Tyree MT (2005) Leaf hydraulics and its implications in plant structure and function. In ‘Vascular transport in plants.’ (Eds NM Holbrook, MA Zwieniecki) pp. 93–114. (Elsevier Academic Press: Burlington, MA, USA)

Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell & Environment 26, 1343–1356.
| CrossRef |

Sack L, Streeter CM, Holbrook NM (2004) Hydraulic analysis of water flow through leaves of sugar maple and red oak. Plant Physiology 134, 1824–1833.
| CrossRef | CAS | PubMed |

Sakakibara K, Nishiyama T, Kato M, Hasebe M (2001) Isolation of homeodomain-leucine zipper genes from the moss Physcomitrella patens and the evolution of homeodomain-leucine zipper genes in land plants. Molecular Biology and Evolution 18, 491–502.
| CAS | PubMed |

Sanders H, Rothwell GW, Wyatt S (2007) Paleontological context for the developmental mechanisms of evolution. International Journal of Plant Sciences 168, 719–728.
| CrossRef | CAS |

Sarojam R, Sappl PG, Goldshmidt A, Efroni I, Floyd SK, Eshed Y, Bowman JL (2010) Differentiating Arabidopsis shoots from leaves by combined YABBY activities. The Plant Cell 22, 2113–2130.
| CrossRef | CAS | PubMed |

Sauquet H, Weston PH, Anderson CL, Barker NP, Cantrill DJ, Mast AR, Savolainen V (2009) Contrasted patterns of hyperdiversification in Mediterranean hotspots. Proceedings of the National Academy of Sciences of the United States of America 106, 221–225.
| CrossRef | CAS | PubMed |

Schmid M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nature Genetics 37, 501–506.
| CrossRef | CAS | PubMed |

Schuepp PH (1993) Tansley Review No. 59. Leaf boundary layers. New Phytologist 125, 477–507.
| CrossRef |

Sculthorpe CD (1967) Vegetative polymorphism and the problem of heterophylly. In ‘The biology of aquatic vascular plants’. pp. 218–247. (Koeltz Scientific Books: Konigstein, West Germany)

Shalit A, Rozman A, Goldshmidt A, Alvarez JP, Bowman JL, Eshed Y, Lifschitz E (2009) The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proceedings of the National Academy of Sciences of the United States of America 106, 8392–8397.
| CrossRef | CAS | PubMed |

Sharkey TD (2005) Effects of moderate heat stress on photosynthesis: importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant, Cell & Environment 28, 269–277.
| CrossRef | CAS |

Smith WK, Nobel PS (1977) Temperature and water relations for sun and shade leaves of a desert broadleaf, Hyptis emoryi. Journal of Experimental Botany 28, 169–183.
| CrossRef |

Specht RL, Specht A (1999) ‘Australian plant communities. Dynamics of structure, growth and biodiversity.’ (Oxford University Press: Oxford)

Street NR, Sjödin A, Bylesjö M, Gustafsson P, Trygg J, Jansson S (2008) A cross-species transcriptomics approach to identify genes involved in leaf development. BMC Genomics 9, 589
| CrossRef | PubMed |

Taiz L, Zeiger E (2002) ‘Plant physiology.’ 3rd edn. (Sinauer Associates: Sunderland, MA, USA)

Thoday D (1931) The significance of reduction in the size of leaves. Journal of Ecology 19, 297–303.
| CrossRef |

Thom AS (1968) Exchange of momentum mass and heat between an artificial leaf and airflow in a wind tunnel. Quarterly Journal of the Royal Meteorological Society 94, 44–55.
| CrossRef |

Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New Phytologist 161, 193–198.
| CrossRef | CAS |

Tomescu AMF (2009) Megaphylls, microphylls and the evolution of leaf development. Trends in Plant Science 14, 5–12.
| CrossRef | CAS | PubMed |

Tsukaya H (2006) Mechanism of leaf-shape determination. Annual Review of Plant Biology 57, 477–496.
| CrossRef | CAS | PubMed |

Tsukaya H (2010) Leaf development and evolution. Journal of Plant Research 123, 3–6.
| CrossRef | PubMed |

Tsukaya H, Shoda K, Kim GT, Uchimiya H (2000) Heteroblasty in Arabidopsis thaliana (L.) Heynh. Planta 210, 536–542.
| CrossRef | CAS | PubMed |

Usami T, Horiguchi G, Yano S, Tsukaya H (2009) The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136, 955–964.
| CrossRef | CAS | PubMed |

van der Niet T, Johnson SD, Linder HP (2006) Macroevolutionary data suggest a role for reinforcement in pollination system shifts. Evolution 60, 1596–1601.
| CrossRef | PubMed |

Vogel S (1968) ‘Sun leaves’ and ‘shade leaves’: differences in convective heat dissipation. Ecology 49, 1203–1204.
| CrossRef |

Vogel S (1970) Convective cooling at low airspeeds and the shapes of broad leaves. Journal of Experimental Botany 21, 91–101.
| CrossRef |

von Goethe JW (2009) ‘The metamorphosis of plants’. (Reprinted by MIT Press: Cambridge, MA, USA) Originally published in 1790.

Wagner WH (1952) Types of foliar dichotomy in living ferns. American Journal of Botany 39, 578–592.
| CrossRef |

Waites R, Hudson A (1995) Phantastica – a gene required for dorsoventrality of leaves in Antirrhinum majus. Development 121, 2143–2154.
| CAS |

Weston PH (1995) Athertonia. In ‘Flora of Australia. Vol. 16’. Ed. P McCarthy) pp. 413–415. (CSIRO Publishing: Melbourne)

Weston PH (2007) ‘Proteaceae in the families and genera of vascular plants. Vol. 9. Flowering plants – Eudicots’. (Volume Eds C Jeffrey, JW Kadereit, Series Ed. K Kubitzki) (Springer: Berlin)

Wright IJ, Reich PB, Westoby M, Ackerly DD, Baruch Z, et al (2004) The worldwide leaf economics spectrum. Nature 428, 821–827.
| CrossRef | CAS | PubMed |

Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750–759.
| CrossRef | CAS | PubMed |

Yamaguchi T, Tsukaya H (2010) Evolutionary and developmental studies of unifacial leaves in monocots: Juncus as a model system. Journal of Plant Research 123, 35–41.
| CrossRef | PubMed |

Yamaguchi T, Yano S, Tsukaya H (2010) Genetic framework for flattened leaf blade formation in unifacial leaves of Juncus prismatocarpus. The Plant Cell 22, 2141–2155.
| CrossRef | CAS | PubMed |

Yang D, Li G, Sun S (2008) The generality of leaf size versus number trade-off in temperate woody species. Annals of Botany 102, 623–629.
| CrossRef | PubMed |

Yano S, Terashima I (2001) Separate localization of light signal perception for sun or shade type chloroplast and palisade tissue differentiation in Chenopodium album. Plant & Cell Physiology 42, 1303–1310.
| CrossRef | CAS | PubMed |

Yano S, Terashima I (2004) Developmental process of sun and shade leaves in Chenopodium album L. Plant, Cell & Environment 27, 781–793.
| CrossRef |

Yapp RH (1912) Spirea ulmaria, L., and its bearing on the problem of xeromorphy in marsh plants. Annals of Botany 26, 815–870.

Yates MJ, Verboom GA, Rebelo AG, Cramer MD (2010) Ecophysiological significance of leaf size variation in Proteaceae from the Cape Floristic Region. Functional Ecology 24, 485–492.
| CrossRef |

Zhong RQ, Ye ZH (1999) IFL1, a gene regulating interfascicular fiber differentiation in Arabidopsis, encodes a homeodomain-leucine zipper protein. The Plant Cell 11, 2139–2152.
| CAS | PubMed |

Zurakowski KA, Gifford EM (1988) Quantitative studies of pinnule development in the ferns Adiantum raddianum and Cheilanthes viridis. American Journal of Botany 75, 1559–1570.
| CrossRef |

Zwieniecki MA, Melcher PJ, Boyce CK, Sack L, Holbrook NM (2002) Hydraulic architecture of leaf venation in Laurus nobilis L. Plant, Cell & Environment 25, 1445–1450.
| CrossRef |

Zwieniecki MA, Boyce CK, Holbrook NM (2004a) Functional design space of single-veined leaves: role of tissue hydraulic properties in constraining leaf size and shape. Annals of Botany 94, 507–513.
| CrossRef | PubMed |

Zwieniecki MA, Boyce CK, Holbrook NM (2004b) Hydraulic limitations imposed by crown placement determine final size and shape of Quercus rubra L. leaves. Plant, Cell & Environment 27, 357–365.
| CrossRef |

Zwieniecki MA, Stone HA, Leigh A, Boyce CK, Holbrook NM (2006) Hydraulic design of pine needles: one-dimensional optimization for single-vein leaves. Plant, Cell & Environment 29, 803–809.
| CrossRef | PubMed |

Legal & Privacy | Contact Us | Help