Arthropod-Plant Interactions

, Volume 1, Issue 3, pp 147–158 | Cite as

Morphology and development of floral features recognised by pollinators

Review Paper


The diversity of angiosperm flowers is astounding. The conventional explanation for this diversity is that it represents the great variety of ways in which flowers have adapted to attract an even greater diversity of animal pollinators. Many animal behaviourists are therefore interested in how changes in floral morphology affect pollinator behaviour. The establishment of well-characterised model plant species has greatly furthered our understanding of how floral morphology is generated and varied. Many of these model species are pollinated by animals and attract their pollinators through the production of colour, shape, scent, size and rewards. An understanding of the developmental plasticity of floral morphology, and the constraints upon it, should inform research into animal responses to flowers. The use of genetically characterised model species, and the isogenic and near-isogenic lines available in them, will allow dissection of the different components of floral attraction and reward in natural systems.


Angiosperm Floral reward Flower colour Flower development Flower scent Flower shape Flower size Flower symmetry Pollination Pollinator 

Supplementary material


  1. Almeida J, Rocheta M, Galego L (1997) Genetic control of flower shape in Antirrhinum majus. Development 124:1387–1392PubMedGoogle Scholar
  2. Armbruster WS, Di Stilio V, Tuxill J, Flores TC, Velasquez Runk J (1999) Covariance and decoupling of floral and vegetative traits in nine neotropical plants: a re-evaluation of Berg’s correlation-pleiades concept. Am J Bot 86:39–55CrossRefGoogle Scholar
  3. Bateman RM, DiMichele WA (2002) Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Cronk QCB, Bateman RM, Hawkins JA (eds) Developmental genetics and plant evolution. Taylor and Francis, London, pp 109–159Google Scholar
  4. Baumann K, Perez-Rodriguez M, Bradley D, Venail J, Bailey P, Jin H, Koes R, Roberts K, Martin C (2007) Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 134:1691–1701PubMedCrossRefGoogle Scholar
  5. Benlloch R, Navarro C, Beltrán J, Cañas L (2003) Floral development of the model legume Medicago truncatula: ontogeny studies as a tool to better characterize homeotic mutations. Sex Plant Reprod 15:231–241Google Scholar
  6. Bohlmann J, Meyer-Gauen G, Croteau R (1998) Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci USA 95:4126–4133PubMedCrossRefGoogle Scholar
  7. Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396PubMedGoogle Scholar
  8. Bradshaw A (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–156Google Scholar
  9. Bradshaw HD, Schemske DW (2003) Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176–178PubMedCrossRefGoogle Scholar
  10. Buchmann S (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New YorkGoogle Scholar
  11. Buchmann S (1986) Vibratile pollination in Solanum and Lycopersicon: a look at pollen chemistry. In: D’Arcy WG (ed) Solanaceae biology and systematics. Columbia University Press, New YorkGoogle Scholar
  12. Bushue L, Mann C, Gorenstein N, Dudareva N (1999) Floral scent production in Antirrhinum majus. In: Plant Biology 99. American society of Plant Physiologists, Rockvill, MD, p 80Google Scholar
  13. Chittka L, Raine NE (2006) Recognition of flowers by pollinators. Curr Opin Plant Biol 9:428–435PubMedCrossRefGoogle Scholar
  14. Citerne H, Pennington RT, Cronk QCB (2006) An apparent reversal in floral symmetry in the legume Cadia is a homeotic transformation. Proc Natl Acad Sci USA 103:12017–12020PubMedCrossRefGoogle Scholar
  15. Clegg MT, Durbin ML (2003) Tracing floral adaptations from ecology to molecules. Nat Rev Genetics 4:206–215CrossRefGoogle Scholar
  16. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  17. Comba L, Corbet SA, Hunt H, Outram S, Parker JS, Glover BJ (2000) The role of genes influencing the corolla in pollination of Antirrhinum majus. Plant Cell Environ 23:639–647CrossRefGoogle Scholar
  18. Corley SB, Carpenter R, Copsey L, Coen E (2005) Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. Proc Natl Acad Sci USA 102:5068–5073PubMedCrossRefGoogle Scholar
  19. Crawford BC, Nath U, Carpenter R, Coen ES (2004) CINCINNATA controls both cell differentiation and growth in petal lobes and leaves of Antirrhinum. Plant Physiol 135:244–253PubMedCrossRefGoogle Scholar
  20. Cubas P (2003) Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:1175–1184CrossRefGoogle Scholar
  21. de Vlaming P, Scram AW, Wiering H (1983) Genes affecting flower colour and pH of flower limb homogenates in Petunia hybrida. Theor Appl Genet 66:271–278CrossRefGoogle Scholar
  22. Dewitte W, Riou-Khamlichi C, Scofield S, Healy JMS, Jacqmard A, Kilby NJ, Murray JAH (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92PubMedCrossRefGoogle Scholar
  23. Dudareva N, Pichersky E (2000) Biochemical and molecular genetic aspects of floral scents. Plant Physiol 122:627–633PubMedCrossRefGoogle Scholar
  24. Dudareva N, Raguso RA, Wang J, Ross JR, Pichersky E (1998) Floral scent production in Clarkia breweri. III. Enzymatic synthesis and emission of benzenoid esters. Plant Physiol 116:599–604PubMedCrossRefGoogle Scholar
  25. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525PubMedCrossRefGoogle Scholar
  26. Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2007) Mutations perturbing petal cell shape and anthocyanin synthesis influence bumblebee perception of Antirrhinum majus flower colour. Arthropod Plant Interact 1:45–55CrossRefGoogle Scholar
  27. Endersby J (2007) A guinea pig’s history of biology. William Heinemann, LondonGoogle Scholar
  28. Endress PK (1996) Structure and function of female and bisexual organ complex in Gnetales. Int J Plant Sci 157:S113–S125CrossRefGoogle Scholar
  29. Endress PK (2001) Evolution of floral symmetry. Curr Opin Plant Biol 4:86–91PubMedCrossRefGoogle Scholar
  30. Feng X, Zhao Z, Tian Z (2006) Control of petal shape and floral zygomorphy in Lotus japonicus. Proc Natl Acad Sci USA 103:4970–4975PubMedCrossRefGoogle Scholar
  31. Fukada-Tanaka S, Inagaki Y, Yamaguchi T, Saito N, Iida S (2000) Colour-enhancing protein in blue petals. Nature 407:581PubMedCrossRefGoogle Scholar
  32. Galego L, Almeida J (2002) Role of DIVARICATA in the control of dorsoventral asymmetry in Antirrhinum flowers. Genes Dev 16:880–891PubMedCrossRefGoogle Scholar
  33. Galen C, Cuba J (2001) Down the tube: pollinators, predators, and the evolution of flower shape in the alpine skypilot, Polemonium viscosum. Evolution 55:1963–1971PubMedGoogle Scholar
  34. Glover BJ, Martin C (1998) The role of petal cell shape and pigmentation in pollination success in Antirrhinum majus. Heredity 80:778–784CrossRefGoogle Scholar
  35. Golz JF, Keck EJ, Hudson A (2002) Spontaneous mutations in KNOX genes give rise to a novel floral structure in Antirrhinum. Curr Biol 12:515–522PubMedCrossRefGoogle Scholar
  36. Gorton HL, Vogelmann TC (1996) Effects of epidermal cell shape and pigmentation on optical properties of Antirrhinum petals at visible and ultraviolet wavelengths. Plant Physiol 112:879–888PubMedGoogle Scholar
  37. Grimaldi D (1999) The co-radiation of pollinating insects and angiosperms in the Cretaceous. Ann Mo Bot Gard 86:373–406CrossRefGoogle Scholar
  38. Grotewold E (2006) The genetics and biochemistry of floral pigments. Annu Rev Plant Biol 57:761–780PubMedCrossRefGoogle Scholar
  39. Guerrieri F, Schubert M, Sandoz J, Giurfa M 2005 Perceptual and neural olfactory similarity in honeybees. PLoS Biol 3:e60PubMedCrossRefGoogle Scholar
  40. Harborne JB (1993) Introduction to ecological biochemistry. Academic Press, LondonGoogle Scholar
  41. Hoballah M, Guebitz T, Stuurman J, Broger L, Barone M, Mandel T, Dell’Olivo A, Arnold M, Kuhlemeier C (2007) Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19:779–790PubMedCrossRefGoogle Scholar
  42. Jones AM, Im KH, Savka MA, Wu MJ, DeWitt NG, Shillito R, Binns AN (1998) Auxin-dependent cell expansion mediated by overexpressed auxin binding protein 1. Science 282:1114–1117PubMedCrossRefGoogle Scholar
  43. Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–84CrossRefGoogle Scholar
  44. Kevan PG, Lane MA (1985) Flower petal microtexture is a tactile cue for bees. Proc Natl Acad Sci USA 82:4750–4752PubMedCrossRefGoogle Scholar
  45. Knudsen JT, Tollsten L, Bergstrom LG (1993) Floral scents. A checklist of volatile compounds isolated by head-space techniques. Phytochemistry 33:253–280CrossRefGoogle Scholar
  46. Kramer E, Holappa L, Gould B, Jaramillo MA, Setnikov D, Santiago P (2007) Elaboration of B gene function to include the identity of novel floral organs in the lower eudicot Aquilegia. Plant Cell 19:750–766PubMedCrossRefGoogle Scholar
  47. Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698PubMedCrossRefGoogle Scholar
  48. Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032PubMedCrossRefGoogle Scholar
  49. Luo D, Carpenter R, Vincent C, Copsey L, Coen E (1996) Origin of floral asymmetry in Antirrhinum. Nature 383:794–799PubMedCrossRefGoogle Scholar
  50. Martin C, Gerats T (1993) The control of flower colouration. In: Jordan B (ed) The molecular biology of flowering. CAB International, Wallingford UK, pp 219–256Google Scholar
  51. Mitchell RJ (2004) Heritability of Nectar Traits: why do we know so little? Ecology 85:1527–1533CrossRefGoogle Scholar
  52. Mizukami Y, Fischer RL (2000) Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proc Natl Acad Sci USA 97:942–947PubMedCrossRefGoogle Scholar
  53. Mol J, Grotewold E, Koes R (1998) How genes paint flowers and seeds. Trends Plant Sci 3:212–217CrossRefGoogle Scholar
  54. Nath U, Crawford BCW, Carpenter R, Coen E 2003 Genetic control of surface curvature. Science 299:1404–1407PubMedCrossRefGoogle Scholar
  55. Newman DA, Thomson JD (2005) Effects of nectar robbing on dynamics and bumblebee foraging strategies in Linaria vulgaris (Scrophulariaceae). Oikos 110:309–320CrossRefGoogle Scholar
  56. Nishihara M, Nakatsuka T, Yamamura S (2005) Flavonoid components and flower color change in transgenic tobacco plants by suppression of chalcone isomerase gene. FEBS Lett 579:6074–6078PubMedCrossRefGoogle Scholar
  57. Noda K, Glover BJ, Linstead P, Martin C (1994) Flower colour intensity depends on specialised cell shape controlled by a MYB-related transcription factor. Nature 369:661–664PubMedCrossRefGoogle Scholar
  58. Odell E, Raguso R, Jones KN (1999) Bumblebee foraging responses to variation in floral scent and color in Snapdragons (Antirrhinum: Scrophulariaceae). Am Midl Nat 142:257–265CrossRefGoogle Scholar
  59. Pang P, Meyerowitz E (1987) Arabidopsis thaliana: a model system for plant molecular biology Bio/Technology 5:1177–1181CrossRefGoogle Scholar
  60. Perez-Rodriguez M, Jaffe FW, Butelli E, Glover BJ, Martin C (2005) Development of three different cell types is associated with the activity of a specific MYB transcription factor in the ventral petal of Antirrhinum majus flowers. Development 132:359–370PubMedCrossRefGoogle Scholar
  61. Procter M, Yeo P, Lack A (1996) The natural history of pollination. HarperCollins, LondonGoogle Scholar
  62. Ramsay NA, Glover BJ 2005 MYB-bHLH-WD40 protein complex, the evolution of cellular diversity. Trends Plant Sci 10:63–70PubMedCrossRefGoogle Scholar
  63. Rolland-Lagan AG, Bangham JA, Coen E (2003) Growth dynamics underlying petal shape and asymmetry. Nature 422:161–163PubMedCrossRefGoogle Scholar
  64. Rudall PJ, Manning JC, Goldblatt P (2003) Evolution of floral nectaries in Iridaceae. Ann Mo Bot Gard 90:613–631CrossRefGoogle Scholar
  65. Schwinn K, Venail J, Shang Y, Mackay S, Alm V, Butelli E, Oyama R, Bailey P, Davies K, Martin C (2006) A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18:831–851PubMedCrossRefGoogle Scholar
  66. Shimamoto K, Kyozuka J (2002) Rice as a model for comparative genomics of plants. Annu Rev Plant Biol 53:399–419PubMedCrossRefGoogle Scholar
  67. Shiono M, Matsugaki N, Takeda K (2005) Structure of the blue cornflower pigment. Nature 436:791PubMedCrossRefGoogle Scholar
  68. Shpak ED, Lakeman MB, Torii KU (2003) Dominant-negative receptor uncovers redundancy in the Arabidopsis ERECTA Leucine-rich repeat receptor-like kinase signalling pathway that regulates organ shape. Plant Cell 15:1095–1110PubMedCrossRefGoogle Scholar
  69. Spaethe J, Tautz J, Chittka L (2001) Visual constraints in foraging bumblebees: flower size and colour affect search time and flight behaviour. Proc Natl Acad Sci USA 98:3898–3903PubMedCrossRefGoogle Scholar
  70. Stinchcombe J, Weinig C, Ungerer M, Olsen K, Mays C, Halldorsdottir S, Purugganan M, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci USA 101:4712–4717PubMedCrossRefGoogle Scholar
  71. Stuurman J, Hoballah ME, Broger L, Moore J, Basten C, Kuhlemeier C (2004) Dissection of floral pollination syndromes in Petunia. Genetics 168:1585–1599PubMedCrossRefGoogle Scholar
  72. Thien LB, Azuma H, Kawano S (2000) New perspectives on the pollination biology of basal angiosperms. Int J Plant Sci 161:S225–S235CrossRefGoogle Scholar
  73. Verdonk JC, Haring MA, van Tunen AJ, Schuurink RC (2005) ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:1612–1624PubMedCrossRefGoogle Scholar
  74. Whibley A, Langlade N, Andalo C, Hanna A, Bangham A, Thebaud C, Coen E (2006) Evolutionary paths underlying flower colour variation in Antirrhinum. Science 313:963–966PubMedCrossRefGoogle Scholar
  75. Whittall JB, Voelckel C, Kliebenstein DJ, Hodges SA (2006) Convergence, constraint and the role of gene expression during adaptive radiation: floral anthocyanins in Aquilegia. Mol Ecol 15:4645–4657PubMedCrossRefGoogle Scholar
  76. Yamaguchi T, Fukada-Tanaka S, Inagaki Y, Saito N, Yonekura-Sakakibara K, Tanaka Y, Kusumi T, Iida S (2001) Genes encoding the vacuolar Na+/H+ exchanger and flower coloration. Plant Cell Physiol 42:451–461PubMedCrossRefGoogle Scholar
  77. Yoshida K, Kondo T, Okazaki Y, Katou K (1995) Cause of blue petal colour. Nature 373:291CrossRefGoogle Scholar
  78. Yoshida K, Kawachi M, Mori M, Maeshima M, Kondo M, Nishimura M, Kondo T (2005) The involvement of tonoplast proton pumps and Na+(K+)/H+ exchangers in the change of petal colour during flower opening of morning glory, Ipomoea tricolor cv. Heavenly Blue. Plant Cell Physiol 46:407–415PubMedCrossRefGoogle Scholar
  79. Zufall RA, Rausher MD (2004) Genetic changes associated with floral adaptation restrict future evolutionary potential. Nature 428:847–850PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Plant SciencesUniversity of CambridgeCambridgeUK

Personalised recommendations