1932

Abstract

Pollination is the transfer of pollen grains from the stamens to the stigma, an essential requirement of sexual reproduction in flowering plants. Cross-pollination increases genetic diversity and is favored by selection in the majority of situations. Flowering plants have evolved a wide variety of traits that influence pollination success, including those involved in optimization of self-pollination, attraction of animal pollinators, and the effective use of wind pollination. In this review we discuss our current understanding of the molecular basis of the development and production of these various traits. We conclude that recent integration of molecular developmental studies with population genetic approaches is improving our understanding of how selection acts on key floral traits in taxonomically diverse species, and that further work in nonmodel systems promises to provide exciting insights in the years to come.

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2020-04-29
2024-04-25
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Literature Cited

  1. 1. 
    Adler LS. 2000. The ecological significance of toxic nectar. Oikos 91:3409–20
    [Google Scholar]
  2. 2. 
    Akhtar TA, Pichersky E. 2013. Veratrole biosynthesis in white campion. Plant Physiol 162:152–62
    [Google Scholar]
  3. 3. 
    Albert NW, Davies KM, Lewis DH, Zhang H, Montefiori M et al. 2014. A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. Plant Cell 26:3962–80
    [Google Scholar]
  4. 4. 
    Alcorn K, Whitney H, Glover B 2012. Flower movement increases pollinator preference for flowers with better grip. Funct. Ecol. 26:4941–47
    [Google Scholar]
  5. 5. 
    Almeida J, Rocheta M, Galego L 1997. Genetic control of flower shape in Antirrhinum majus. Development 124:71387–92
    [Google Scholar]
  6. 6. 
    Ambrose BA, Lerner DR, Ciceri P, Padilla CM, Yanofsky MF, Schmidt RJ 2000. Molecular and genetic analyses of the silky1 gene reveal conservation in floral organ specification between eudicots and monocots. Mol. Cell 5:3569–79
    [Google Scholar]
  7. 7. 
    Angert AL, Schemske DW. 2005. The evolution of species’ distributions: reciprocal transplants across the elevation ranges of Mimulus cardinalis and M. lewisii. Evolution 59:81671–84
    [Google Scholar]
  8. 8. 
    Ashman AT, Bradburn M, Cole DH, Blaney BH, Raguso RA 2005. The scent of a male: the role of floral volatiles in pollination of a gender dimorphic plant. Ecology 86:82099–105
    [Google Scholar]
  9. 9. 
    Balamurali G, Krishna S, Somanathan H 2015. Senses and signals: evolution of floral signals, pollinator sensory systems and the structure of plant–pollinator interactions. Curr. Sci. 108:1852–61
    [Google Scholar]
  10. 10. 
    Banba H. 1968. Pigments of lily flowers. II. Survey of carotenoid. J. Jpn. Soc. Horticult. Sci. 37:4368–78
    [Google Scholar]
  11. 11. 
    Barrett SCH. 2002. The evolution of plant sexual diversity. Nat. Rev. Genet. 3:4274–84
    [Google Scholar]
  12. 12. 
    Bateman RM. 1994. Evolutionary-developmental change in the growth architecture of fossil rhizomorphic lycopsids: scenarios constructed on cladistic foundations. Biol. Rev. 69:527–97
    [Google Scholar]
  13. 13. 
    Borchert R, Calle Z, Navarrete D, Tye A, Gautier L et al. 2005. Photoperiodic induction of synchronous flowering near the Equator. Nature 433:7026627–29
    [Google Scholar]
  14. 14. 
    Borghi M, Fernie AR, Schiestl FP, Bouwmeester HJ 2017. The sexual advantage of looking, smelling, and tasting good: the metabolic network that produces signals for pollinators. Trends Plant Sci 22:4338–50
    [Google Scholar]
  15. 15. 
    Bradshaw HD Jr., Schemske DW. 2003. Allele substitution at a flower colour locus produces a pollinatory shift in monkeyflowers. Nature 426:6963176–78
    [Google Scholar]
  16. 16. 
    Bradshaw HD Jr., Wilbert SM, Otto KG, Schemske DW. 1995. Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376:762–65
    [Google Scholar]
  17. 17. 
    Brockington SF, Alvarez-Fernandez R, Landis JB, Alcorn K, Walker RH et al. 2012. Evolutionary analysis of the MIXTA gene family highlights potential targets for the study of cellular differentiation. Mol. Biol. Evol. 30:3526–40
    [Google Scholar]
  18. 18. 
    Brockington SF, Walker RH, Glover BJ, Soltis PS, Soltis DE 2011. Complex pigment evolution in the Caryophyllales. New Phytol 190:4854–64
    [Google Scholar]
  19. 19. 
    Byers KJRP, Bradshaw HD Jr., Riffell JA 2014. Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J. Exp. Biol. 217:4614–23
    [Google Scholar]
  20. 20. 
    Byers KJRP, Vela JP, Peng F, Riffell JA, Bradshaw HD Jr 2014. Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkeyflowers (Mimulus). Plant J 80:61031–42
    [Google Scholar]
  21. 21. 
    Byzova MV, Franken J, Aarts MGM, de Almeida-Engler J, Engler G et al. 1999. Arabidopsis STERILE APETALA, a multifunctional gene regulating inflorescence, flower, and ovule development. Genes Dev 13:1002–14
    [Google Scholar]
  22. 22. 
    Chen L, Hu B, Qin Y, Hu G, Zhao J 2019. Advance of the negative regulation of anthocyanin biosynthesis by MYB transcription factors. Plant Physiol. Biochem. 136:178–87
    [Google Scholar]
  23. 23. 
    Chuang YC, Hung YC, Tsai WC, Chen WH, Chen H 2018. PbbHLH4 regulates floral monoterpene biosynthesis in Phalaenopsis orchids. J. Exp. Bot. 69:184363–77
    [Google Scholar]
  24. 24. 
    Clare EL, Schiestl FP, Leitch AR, Chittka L 2013. The promise of genomics in the study of plant-pollinator interactions. Genome Biol 14:6207
    [Google Scholar]
  25. 25. 
    Clement JS, Mabry TJ, Wyler H, Dreiding AS 1994. Chemical review and evolutionary significance of the betalains. Caryophyllales HD Behnke, TJ Mabry 247–61 Berlin: Springer
    [Google Scholar]
  26. 26. 
    Cna'ani A, Spitzer-Rimon B, Ravid J, Farhi M, Masci T et al. 2015. Two showy traits, scent emission and pigmentation, are finely coregulated by the MYB transcription factor PH4 in petunia flowers. New Phytol 208:3708–14The Petunia PH4 gene is involved in regulation of both floral phenylpropanoid volatile emission and vacuolar acidification influencing petal coloration.
    [Google Scholar]
  27. 27. 
    Colquhoun TA, Verdonk JC, Schimmel BCJ, Tieman DM, Underwood BA, Clark DG 2010. Petunia floral volatile benzenoid/phenylpropanoid genes are regulated in a similar manner. Phytochemistry 71:2–3158–67
    [Google Scholar]
  28. 28. 
    Corley SB, Carpenter R, Copsey L, Coen E 2005. Floral asymmetry involves an interplay between TCP and MYB transcription factors in Antirrhinum. PNAS 102:145068–73
    [Google Scholar]
  29. 29. 
    Cronk QCB, Bateman RM, Hawkins JA 2004. Developmental Genetics and Plant Evolution London: CRC Press
  30. 30. 
    Cubas P. 2004. Floral zygomorphy, the recurring evolution of a successful trait. BioEssays 26:111175–84
    [Google Scholar]
  31. 31. 
    Cullen E, Fernández-Mazuecos M, Glover BJ 2018. Evolution of nectar spur length in a clade of Linaria reflects changes in cell division rather than in cell expansion. Ann. Bot. 122:5801–9
    [Google Scholar]
  32. 32. 
    Cunningham JP, Moore CJ, Zalucki MP, West SA 2004. Learning, odour preference and flower foraging in moths. J. Exp. Biol. 207:187–94
    [Google Scholar]
  33. 33. 
    Damerval C, Becker A. 2017. Genetics of flower development in Ranunculales - a new, basal eudicot model order for studying flower evolution. New Phytol 216:2361–66
    [Google Scholar]
  34. 34. 
    Davies KM, Albert NW, Schwinn KE 2012. From landing lights to mimicry: the molecular regulation of flower colouration and mechanisms for pigmentation patterning. Funct. Plant Biol. 39:8619–38
    [Google Scholar]
  35. 35. 
    De Barrera E, Nobel P 2004. Nectar: properties, floral aspects, and speculations on origin. Trends Plant Sci 9:21360–85
    [Google Scholar]
  36. 36. 
    De Craene LR. 2018. Understanding the role of floral development in the evolution of angiosperm flowers: clarifications from a historical and physico-dynamic perspective. J. Plant Res. 131:3367–93
    [Google Scholar]
  37. 37. 
    Detzel A, Wink M. 1993. Attraction, deterrence or intoxication of bees (Apis mellifera) by plant allelochemicals. Chemoecology 4:18–18
    [Google Scholar]
  38. 38. 
    Ding B, Patterson EL, Holalu SV, Li J, Johnson GA et al. 2018. Formation of periodic pigment spots by the reaction-diffusion mechanism. bioRxiv 403600. https://doi.org/10.1101/403600
    [Crossref]
  39. 39. 
    Donoghue MJ. 1989. Phylogenies and the analysis of evolutionary sequences, with examples from seed plants. Evolution 43:61137–56
    [Google Scholar]
  40. 40. 
    Dötterl S, Jürgens A, Seifert K, Laube T, Weißbecker B, Schütz S 2006. Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol 169:4707–18
    [Google Scholar]
  41. 41. 
    Dudareva N, Cseke L, Blanc VM, Pichersky E 2007. Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell 8:71137–48
    [Google Scholar]
  42. 42. 
    Dudareva N, Klempien A, Muhlemann JK, Kaplan I 2013. Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:116–32
    [Google Scholar]
  43. 43. 
    Dudareva N, Martin D, Kish CM, Kolosova N, Gorenstein N et al. 2003. (E)-β-ocimene and myrcene synthase genes of floral scent biosynthesis in snapdragon: function and expression of three terpene synthase genes of a new terpene synthase subfamily. Plant Cell 15:1227–41
    [Google Scholar]
  44. 44. 
    Dudareva N, Pichersky E. 2008. Metabolic engineering of plant volatiles. Curr. Opin. Biotechnol. 19:2181–89
    [Google Scholar]
  45. 45. 
    Duncan TM, Rausher MD. 2013. Evolution of the selfing syndrome in Ipomoea. Front. Plant Sci 4:301
    [Google Scholar]
  46. 46. 
    Eckhart VM, Rushing NS, Hart GM, Hansen JD 2006. Frequency-dependent pollinator foraging in polymorphic Clarkia xantiana ssp. xantiana populations: implications for flower colour evolution and pollinator interactions. Oikos 112:2412–21
    [Google Scholar]
  47. 47. 
    Ehrlén J, Borg-Karlson AK, Kolb A 2012. Selection on plant optical traits and floral scent: effects via seed development and antagonistic interactions. Basic Appl. Ecol. 13:6509–15
    [Google Scholar]
  48. 48. 
    Endler JA. 1992. Signals, signal conditions, and the direction of evolution. Am. Nat. 139:125–53
    [Google Scholar]
  49. 49. 
    Faegri K, van der Pijl L 1979. Principles of Pollination Ecology Oxford, UK: Pergamon Press
  50. 50. 
    Fenske MP, Hewett Hazelton KD, Hempton AK, Shim JS, Yamamoto BM et al. 2015. Circadian clock gene LATE ELONGATED HYPOCOTYL directly regulates the timing of floral scent emission in Petunia. PNAS 112:319775–80A Petunia hybrida circadian clock gene regulates volatile emission patterns by restricting flavonoid biosynthesis gene expression to the evening.
    [Google Scholar]
  51. 51. 
    Fenske MP, Nguyen LAP, Horn EK, Riffell JA, Imaizumi T 2018. Circadian clocks of both plants and pollinators influence flower seeking behavior of the pollinator hawkmoth Manduca sexta. Sci. Rep 8:2842
    [Google Scholar]
  52. 52. 
    Feussner I, Wasternack C. 2002. The lipoxygenase pathway. Annu. Rev. Plant Biol. 53:275–97
    [Google Scholar]
  53. 53. 
    Forkmann G. 1991. Flavonoids as flower pigments: the formation of the natural spectrum and its extension by genetic engineering. Plant Breed 106:1–26
    [Google Scholar]
  54. 54. 
    Friedman J, Barrett SCH. 2008. A phylogenetic analysis of the evolution of wind pollination in the angiosperms. Int. J. Plant Sci. 169:149–58
    [Google Scholar]
  55. 55. 
    Friedman J, Barrett SCH. 2009. Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann. Bot. 103:91515–27
    [Google Scholar]
  56. 56. 
    Gandia-Herrero F, Garcia-Carmona F. 2013. Biosynthesis of betalains: yellow and violet plant pigments. Trends Plant Sci 18:61360–85
    [Google Scholar]
  57. 57. 
    Gaskett AC. 2011. Orchid pollination by sexual deception: pollinator perspectives. Biol. Rev. 86:133–75
    [Google Scholar]
  58. 58. 
    Gerats T, Vandenbussche M. 2005. A model system for comparative research. Petunia. Trends Plant Sci. 10:5251–56
    [Google Scholar]
  59. 59. 
    Glover BJ, Perez-Rodriguez M, Martin C 1998. Development of several epidermal cell types can be specified by the same MYB-related plant transcription factor. Development 125:173497–508
    [Google Scholar]
  60. 60. 
    Gould SJ, Lewontin RC. 1979. The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. R. Soc. B 205:1161581–98
    [Google Scholar]
  61. 61. 
    Grotewold E. 2006. The genetics and biochemistry of floral pigments. Annu. Rev. Plant Biol. 57:761–80
    [Google Scholar]
  62. 62. 
    Gupta AK, Akhtar TA, Widmer A, Pichersky E, Schiestl FP 2012. Identification of white campion (Silene latifolia) guaiacol O-methyltransferase involved in the biosynthesis of veratrole, a key volatile for pollinator attraction. BMC Plant Biol 12:158
    [Google Scholar]
  63. 63. 
    Hatlestad GJ, Akhavan NA, Sunnadeniya RM, Elam L, Cargile S et al. 2015. The beet Y locus encodes an anthocyanin MYB-like protein that activates the betalain red pigment pathway. Nat. Genet. 47:192–96
    [Google Scholar]
  64. 64. 
    Hendel-Rahmanim K, Masci T, Vainstein A, Weiss D 2007. Diurnal regulation of scent emission in rose flowers. Planta 226:61491–99
    [Google Scholar]
  65. 65. 
    Hermann K, Klahre U, Moser M, Sheehan H, Mandel T, Kuhlemeier C 2013. Tight genetic linkage of prezygotic barrier loci creates a multifunctional speciation island in Petunia. Curr. Biol 23:10873–77
    [Google Scholar]
  66. 66. 
    Hermann K, Klahre U, Venail J, Brandenburg A, Kuhlemeier C 2015. The genetics of reproductive organ morphology in two Petunia species with contrasting pollination syndromes. Planta 241:51241–54
    [Google Scholar]
  67. 67. 
    Hoballah ME, Stuurman J, Turlings TCJ, Guerin PM, Connétable S, Kuhlemeier C 2005. The composition and timing of flower odour emission by wild Petunia axillaris coincide with the antennal perception and nocturnal activity of the pollinator Manduca sexta. Planta 222:1141–50
    [Google Scholar]
  68. 68. 
    Hu S, Dilcher DL, Jarzen DM, Winship Taylor D 2008. Early steps of angiosperm–pollinator coevolution. PNAS 105:1240–45
    [Google Scholar]
  69. 69. 
    Hu Z, Xu F, Guan L, Qian P, Liu Y et al. 2014. The tetratricopeptide repeat-containing protein slow green1 is required for chloroplast development in Arabidopsis. J. Exp. Bot 65:41111–23
    [Google Scholar]
  70. 70. 
    Hudson A, Critchley J, Erasmus Y 2008. The genus Antirrhinum (snapdragon): a flowering plant model for evolution and development. Cold Spring Harb. Protoc. 3:10 pdb.emo100
    [Google Scholar]
  71. 71. 
    Jacob F. 1977. Evolution and tinkering. Science 196:42951161–66
    [Google Scholar]
  72. 72. 
    Jain G, Gould KS. 2015. Are betalain pigments the functional homologues of anthocyanins in plants?. Environ. Exp. Bot. 119:48–53
    [Google Scholar]
  73. 73. 
    Deleted in proof
  74. 74. 
    Kaminaga Y, Schnepp J, Peel G, Kish CM, Ben-Nissan G et al. 2006. Plant phenylacetaldehyde synthase is a bifunctional homotetrameric enzyme that catalyzes phenylalanine decarboxylation and oxidation. J. Biol. Chem. 281:3323357–66
    [Google Scholar]
  75. 75. 
    Kelber A, Vorobyev M, Osorio D 2003. Animal colour vision—behavioural tests and physiological concepts. Biol. Rev. 78:81–118
    [Google Scholar]
  76. 76. 
    Kessler D, Gase K, Baldwin IT 2008. Field experiments with transformed plants reveal the sense of floral scents. Science 321:58931200–2
    [Google Scholar]
  77. 77. 
    Kessler D, Baldwin IT. 2007. Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:5840–54
    [Google Scholar]
  78. 78. 
    Klahre U, Gurba A, Hermann K, Saxenhofer M, Bossolini E et al. 2011. Pollinator choice in Petunia depends on two major genetic loci for floral scent production. Curr. Biol. 21:9730–39Two QTLs responsible for differences in scent production between Petunia species are identified.
    [Google Scholar]
  79. 79. 
    Knudsen JT, Eriksson R, Gershenzon J, Ståhl B 2006. Diversity and distribution of floral scent. Bot. Rev. 72:1–-120
    [Google Scholar]
  80. 80. 
    Koeduka T, Fridman E, Gang DR, Vassão DG, Jackson BL et al. 2006. Eugenol and isoeugenol, characteristic aromatic constituents of spices, are biosynthesized via reduction of a coniferyl alcohol ester. PNAS 103:2610128–33
    [Google Scholar]
  81. 81. 
    Kolosova N, Gorenstein N, Kish CM, Dudareva N 2001. Regulation of circadian methyl benzoate emission in diurnally and nocturnally emitting plants. Plant Cell 13:102333–47
    [Google Scholar]
  82. 82. 
    Leonard AS, Papaj DR. 2011. “X” marks the spot: the possible benefits of nectar guides to bees and plants. Funct. Ecol. 25:61293–301
    [Google Scholar]
  83. 83. 
    Linder HP. 1998. Morphology and the evolution of wind pollination. Reproductive Biology in Systematics, Conservation and Economic Botany SJ Owens, P Rudall 123–25 London: R. Bot. Gardens Kew
    [Google Scholar]
  84. 84. 
    Liu F, Xiao Z, Yang L, Chen Q, Shao L et al. 2017. PhERF6, interacting with EOBI, negatively regulates fragrance biosynthesis in petunia flowers. New Phytol 215:41490–502
    [Google Scholar]
  85. 85. 
    Lorenz-Lemke AP, Mäder G, Muschner VC, Stehmann JR, Bonatto SL et al. 2006. Diversity and natural hybridization in a highly endemic species of Petunia (Solanaceae): a molecular and ecological analysis. Mol. Ecol. 15:144487–97
    [Google Scholar]
  86. 86. 
    Luo D, Carpenter R, Vincent C, Copsey L, Coen E 1996. Origin of floral asymmetry in Antirrhinum. Nature 383:794–99
    [Google Scholar]
  87. 87. 
    Lv Z, Wang S, Zhang F, Chen L, Hao X et al. 2016. Overexpression of a novel NAC domain-containing transcription factor gene (AaNAC1) enhances the content of artemisinin and increases tolerance to drought and Botrytis cinerea in Artemisia annua. Plant Cell Physiol 57:91961–71
    [Google Scholar]
  88. 88. 
    Maeda H, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol. 63:73–105
    [Google Scholar]
  89. 89. 
    Manson JS, Rasmann S, Halitschke R, Thomson JD, Agrawal AA 2012. Cardenolides in nectar may be more than a consequence of allocation to other plant parts: a phylogenetic study of Asclepias. Funct. Ecol 26:51100–10
    [Google Scholar]
  90. 90. 
    Martins TR, Berg JJ, Blinka S, Rausher MD, Baum DA 2013. Precise spatio-temporal regulation of the anthocyanin biosynthetic pathway leads to petal spot formation in Clarkia gracilis (Onagraceae). New Phytol 197:3958–69
    [Google Scholar]
  91. 91. 
    Martins TR, Jiang P, Rausher MD 2017. How petals change their spots: cis-regulatory re-wiring in Clarkia (Onagraceae). New Phytol 216:2510–18
    [Google Scholar]
  92. 92. 
    McQuate GT, Peck SL. 2001. Enhancement of attraction of alpha-ionol to male Bactrocera latifrons (Diptera: Tephritidae) by addition of a synergist, cade oil. J. Econ. Entomol. 94:139–46
    [Google Scholar]
  93. 93. 
    McQuinn RP, Giovannoni JJ, Pogson BJ 2015. More than meets the eye: from carotenoid biosynthesis, to new insights into apocarotenoid signaling. Curr. Opin. Plant Biol. 27:172–79
    [Google Scholar]
  94. 94. 
    Meinhardt H, Gierer A. 2000. Pattern formation by local self-activation and lateral inhibition. BioEssays 22:8753–60
    [Google Scholar]
  95. 95. 
    Miyamoto K, Nishizawa Y, Minami E, Nojiri H, Yamane H, Okada K 2015. Overexpression of the bZIP transcription factor OsbZIP79 suppresses the production of diterpenoid phytoalexin in rice cells. J. Plant Physiol. 173:19–27
    [Google Scholar]
  96. 96. 
    Muhlemann JK, Klempien A, Dudareva N 2014. Floral volatiles: from biosynthesis to function. Plant Cell Environ 37:81936–49
    [Google Scholar]
  97. 97. 
    Muhlemann JK, Maeda H, Chang CY, San Miguel P, Baxter I et al. 2012. Developmental changes in the metabolic network of snapdragon flowers. PLOS ONE 7:7e40381
    [Google Scholar]
  98. 98. 
    Nagegowda DA, Gutensohn M, Wilkerson CG, Dudareva N 2008. Two nearly identical terpene synthases catalyze the formation of nerolidol and linalool in snapdragon flowers. Plant J 55:2224–39
    [Google Scholar]
  99. 99. 
    Neal PR, Dafni A, Giurfa M 2002. Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu. Rev. Ecol. Syst. 29:345–73
    [Google Scholar]
  100. 100. 
    Nilsson LA. 1992. Orchid pollination biology. Trends Ecol. Evol. 7:8255–59
    [Google Scholar]
  101. 101. 
    Nisar N, Li L, Lu S, Khin NC, Pogson BJ 2015. Carotenoid metabolism in plants. Mol. Plant 8:168–82
    [Google Scholar]
  102. 102. 
    Noda K, Glover BJ, Linstead P, Martin C 1994. Flower colour intensity depends on specialized cell shape controlled by a Myb-related transcription factor. Nature 369:6482661–64
    [Google Scholar]
  103. 103. 
    Ojeda DI, Valido A, Fernandez de Castro AG, Ortega-Olivencia A, Fuertes-Aguilar J et al. 2016. Pollinator shifts drive petal epidermal evolution on the Macaronesian Islands bird-flowered species. Biol. Lett. 12:420160022
    [Google Scholar]
  104. 104. 
    Ojeda I, Santos-Guerra A, Caujapé-Castells J, Jaén-Molina R, Marrero Á, Cronk QCB 2012. Comparative micromorphology of petals in Macaronesian Lotus (Leguminosae) reveals a loss of papillose conical cells during the evolution of bird pollination. Int. J. Plant Sci. 173:4365–74
    [Google Scholar]
  105. 105. 
    Ollerton J, Winfree R, Tarrant S 2011. How many flowering plants are pollinated by animals?. Oikos 120:3321–26This paper combines community-level studies of pollinator type in different habitats with latitudinal diversity data to estimate global animal pollination.
    [Google Scholar]
  106. 106. 
    One Thousand Plant Transcr. Initiat 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:679–85
    [Google Scholar]
  107. 107. 
    Owen CR, Bradshaw HD. 2011. Induced mutations affecting pollinator choice in Mimulus lewisii (Phrymaceae). Arthropod Plant Interact 5:3235–44
    [Google Scholar]
  108. 108. 
    Owens SJ, Rudall P 1998. Reproductive Biology in Systematics, Conservation and Economic Botany London: R. Bot. Gardens Kew
  109. 109. 
    Peach DAH, Gries R, Huimin Z, Young N, Gries G 2019. Multimodal floral cues guide mosquitoes to tansy inflorescences. Sci. Rep.9:3908. Erratum. 2019. Sci. Rep. 9:8038
    [Google Scholar]
  110. 110. 
    Peitsch D, Fietz A, Hertel H, De Souza J, Ventura DF, Menzel R 1992. The spectral input systems of hymenopteran insects and their receptor-based colour vision. J. Comp. Physiol. A 170:23–40
    [Google Scholar]
  111. 111. 
    Peng F, Byers KJRP, Bradshaw HD 2017. Less is more: Independent loss-of-function OCIMENE SYNTHASE alleles parallel pollination syndrome diversification in monkeyflowers (Mimulus). Am. J. Bot. 104:71055–59A study of the molecular basis of variation in E-β-ocimene emission between species within a Mimulus clade.
    [Google Scholar]
  112. 112. 
    Pichersky E, Lewinsohn E, Croteau R 1994. Purification and characterisation of S-linalool synthase, an enzyme involved in the production of floral scent in Clarkia breweri. Arch. Biochem. Biophys 316:2803–7
    [Google Scholar]
  113. 113. 
    Pichersky E, Raguso RA. 2018. Why do plants produce so many terpenoid compounds. New Phytol 220:3692–702
    [Google Scholar]
  114. 114. 
    Polturak G, Aharoni A. 2018. “La Vie en Rose”: biosynthesis, sources, and applications of betalain pigments. Mol. Plant 11:17–22
    [Google Scholar]
  115. 115. 
    Posé D, Yant L, Schmid M 2012. The end of innocence: Flowering networks explode in complexity. Curr. Opin. Plant Biol. 15:145–50
    [Google Scholar]
  116. 116. 
    Puzey JR, Gerbode SJ, Hodges SA, Kramer EM, Mahadevan L 2011. Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy. Proc. R. Soc. B 279:17331640–45
    [Google Scholar]
  117. 117. 
    Raguso RA. 2004. Flowers as sensory billboards: progress towards an integrated understanding of floral advertisement. Curr. Opin. Plant Biol. 7:4434–40
    [Google Scholar]
  118. 118. 
    Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69
    [Google Scholar]
  119. 119. 
    Raguso RA. 2016. More lessons from linalool: insights gained from a ubiquitous floral volatile. Curr. Opin. Plant Biol. 32:31–36
    [Google Scholar]
  120. 120. 
    Raguso RA, Thompson JN, Campbell DR 2015. Improving our chemistry: challenges and opportunities in the interdisciplinary study of floral volatiles. Nat. Prod. Rep. 32:7893–903
    [Google Scholar]
  121. 121. 
    Raguso RA, Willis MA. 2005. Synergy between visual and olfactory cues in nectar feeding by wild hawkmoths. Manduca sexta. Anim. Behav. 69:2407–18
    [Google Scholar]
  122. 122. 
    Raimundo J, Sobral R, Bailey P, Azevedo H, Galego L et al. 2013. A subcellular tug of war involving three MYB-like proteins underlies a molecular antagonism in Antirrhinum flower asymmetry. Plant J 75:4527–38An elegant series of experiments define the mechanism by which dorsalizing and ventralizing factors determine overall flower shape.
    [Google Scholar]
  123. 123. 
    Ramsey J, Bradshaw HD. 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57:71520–34
    [Google Scholar]
  124. 124. 
    Ramya M, Kwon OK, An HR, Park PM, Baek YS, Park PH 2017. Floral scent: regulation and role of MYB transcription factors. Phytochem. Lett. 19:114–20
    [Google Scholar]
  125. 125. 
    Ravid J, Spitzer-Rimon B, Takebayashi Y, Seo M, Cna'ani A et al. 2017. GA as a regulatory link between the showy floral traits color and scent. New Phytol 215:1411–22
    [Google Scholar]
  126. 126. 
    Robinson GE, Hackett KJ, Purcell-Miramontes M, Brown SJ, Evans JD et al. 2011. Creating a buzz about insect genomes. Science 331:1386–88
    [Google Scholar]
  127. 127. 
    Rosas-Guerrero V, Quesada M, Armbruster WS, Pérez-Barrales R, DeWitt Smith S 2011. Influence of pollination specialization and breeding system on floral integration and phenotypic variation in Ipomoea. Evolution 65:2350–64
    [Google Scholar]
  128. 128. 
    Roy R, Schmitt AJ, Thomas JB, Carter CJ 2017. Nectar biology: from molecules to ecosystems. Plant Sci 262:148–64
    [Google Scholar]
  129. 129. 
    Rudall PJ, Bateman RM. 2003. Evolutionary change in flowers and inflorescences: evidence from naturally occurring terata. Trends Plant Sci 8:276–82
    [Google Scholar]
  130. 130. 
    Sagawa JM, Stanley LE, Lafountain AM, Frank HA, Liu C, Yuan Y 2016. An R2R3-MYB transcription factor regulates carotenoid pigmentation in Mimulus lewisii flowers. New Phytol 209:31049–57The first positive regulator of floral carotenoid biosynthesis (RCP1) is identified through bulk segregant analysis and characterized.
    [Google Scholar]
  131. 131. 
    Salzmann CC, Cozzolino S, Schiestl FP 2007. Floral scent in food-deceptive orchids: species specificity and sources of variability. Plant Biol 9:6720–29
    [Google Scholar]
  132. 132. 
    Schemske DW, Bradshaw HD. 1999. Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). PNAS 96:2111910–15
    [Google Scholar]
  133. 133. 
    Schiestl FP, Huber FK, Gomez JM 2011. Phenotypic selection on floral scent: trade-off between attraction and deterrence. Evol. Ecol. 25:2237–48
    [Google Scholar]
  134. 134. 
    Schlüter PM, Xu S, Gagliardini V, Whittle E, Shanklin J et al. 2011. Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids. PNAS 108:145696–701
    [Google Scholar]
  135. 135. 
    Schmitt AJ, Roy R, Klinkenberg PM, Jia M, Carter CJ 2018. The octadecanoid pathway, but not COI1, is required for nectar secretion in Arabidopsis thaliana. Front. Plant Sci 9:1060
    [Google Scholar]
  136. 136. 
    Segatto ALA, Cazé ALR, Turchetto C, Klahre U, Kuhlemeier C et al. 2014. Nuclear and plastid markers reveal the persistence of genetic identity: a new perspective on the evolutionary history of Petunia exserta. Mol. Phylogenet. Evol 70:1504–12
    [Google Scholar]
  137. 137. 
    Shang Y, Venail J, Mackay S, Bailey PC, Schwinn KE et al. 2011. The molecular basis for venation patterning of pigmentation and its effect on pollinator attraction in flowers of Antirrhinum. New Phytol 189:2602–15
    [Google Scholar]
  138. 138. 
    Sicard A, Kappel C, Lee YW, Woźniak NJ, Marona C et al. 2016. Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella. PNAS 113:4813911–16A comparative genetic approach is used to determine the molecular basis of petal size reduction in a selfing species.
    [Google Scholar]
  139. 139. 
    Sicard A, Lenhard M. 2011. The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann. Bot. 107:91433–43
    [Google Scholar]
  140. 140. 
    Sicard A, Stacey N, Hermann K, Dessoly J, Neuffer B et al. 2011. Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella. Plant Cell 23:93156–71
    [Google Scholar]
  141. 141. 
    Solhaug EM, Roy R, Chatt EC, Klinkenberg PM, Hampton NMM et al. 2019. An integrated transcriptomics and metabolomics analysis of the Cucurbita pepo nectary implicates key modules of primary metabolism involved in nectar synthesis and secretion. Plant Direct 3:2e00120
    [Google Scholar]
  142. 142. 
    Song B, Niu Y, Stöcklin J, Chen G, Peng DL et al. 2015. Pollinator attraction in Cornus capitata (Cornaceae): the relative role of visual and olfactory cues. J. Plant Ecol. 8:2173–81
    [Google Scholar]
  143. 143. 
    Spencer V, Kim M. 2018. Re“CYC”ling molecular regulators in the evolution and development of flower symmetry. Semin. Cell Dev. Biol. 79:116–26
    [Google Scholar]
  144. 144. 
    Spitzer-Rimon B, Farhi M, Albo B, Cna'ani A, Ben Zvi MM et al. 2012. The R2R3-MYB-like regulatory factor EOBI, acting downstream of EOBII, regulates scent production by activating ODO1 and structural scent-related genes in petunia. Plant Cell 24:125089–105
    [Google Scholar]
  145. 145. 
    Spitzer-Rimon B, Marhevka E, Barkai O, Marton I, Edelbaum O et al. 2010. EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles’ biosynthesis in Petunia. Plant Cell 22:61961–76
    [Google Scholar]
  146. 146. 
    Stankowski S, Sobel JM, Streisfeld MA 2017. Geographic cline analysis as a tool for studying genome-wide variation: a case study of pollinator-mediated divergence in a monkeyflower. Mol. Ecol. 26:1107–22
    [Google Scholar]
  147. 147. 
    Stanley LE, Ding B, Sun W, Mou F-J, Hill C et al. 2020. A tetratricopeptide repeat protein regulates carotenoid biosynthesis and chromoplast development in monkeyflower (Mimulus). Plant Cell In press. https://doi.org/10.1105/tpc.19.00755
    [Crossref] [Google Scholar]
  148. 148. 
    Steen R, Norli HR, Thöming G 2019. Volatiles composition and timing of emissions in a moth-pollinated orchid in relation to hawkmoth (Lepidoptera: Sphingidae) activity. Arthropod Plant Interact 13:4581–92
    [Google Scholar]
  149. 149. 
    Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L 2018. Carotenoid metabolism in plants: the role of plastids. Mol. Plant 11:158–74
    [Google Scholar]
  150. 150. 
    Tedder A, Carleial S, Gołebiewska M, Kappel C, Shimizu KK, Stift M 2015. Evolution of the selfing syndrome in Arabis alpina (Brassicaceae). PLOS ONE 10:6e0126618
    [Google Scholar]
  151. 151. 
    Toräng P, Vikström L, Wunder J, Wötzel S, Coupland G, Ågren J 2017. Evolution of the selfing syndrome: Anther orientation and herkogamy together determine reproductive assurance in a self-compatible plant. Evolution 71:92206–18
    [Google Scholar]
  152. 152. 
    Turing AM. 1953. The chemical basis of morphogenesis. Bull. Math. Biol. 52:1153–97
    [Google Scholar]
  153. 153. 
    Tzuri G, Zhou X, Chayut N, Yuan H, Portnoy V et al. 2015. A ‘golden’ SNP in CmOr governs the fruit flesh color of melon (Cucumis melo). Plant J 82:2267–79
    [Google Scholar]
  154. 154. 
    Underwood BA, Tieman DM, Shibuya K, Dexter RJ, Loucas HM et al. 2005. Ethylene-regulated floral volatile synthesis in petunia corollas. Plant Physiol 138:1255–66
    [Google Scholar]
  155. 155. 
    Ushimaru A, Watanabe T, Nakata K 2007. Colored floral organs influence pollinator behavior and pollen transfer in Commelina communis (Commelinaceae). Am. J. Bot. 94:2249–58
    [Google Scholar]
  156. 156. 
    Valadon LRG, Mummery RS. 1967. Carotenoids in floral parts of a narcissus, a daffodil and a tulip. Biochem. J. 106:2479–84
    [Google Scholar]
  157. 157. 
    Valadon LRG, Mummery RS. 1967. Carotenoids of certain compositae flowers. Phytochemistry 6:7983–88
    [Google Scholar]
  158. 158. 
    Vallejo-Marín M, Walker C, Friston-Reilly P, Solís-Montero L, Igic B 2014. Recurrent modification of floral morphology in heterantherous Solanum reveals a parallel shift in reproductive strategy. Philos. Trans. R. Soc. B 369:164920130256
    [Google Scholar]
  159. 159. 
    Verdonk JC, Haring MA, Van Tunen AJ, Schuurink RC 2005. ODORANT1 regulates fragrance biosynthesis in petunia flowers. Plant Cell 17:51612–24
    [Google Scholar]
  160. 160. 
    Vlasáková B, Kalinová B, Gustafsson MHG, Teichert H 2008. Cockroaches as pollinators of Clusia aff. sellowiana (Clusiaceae) on inselbergs in French Guiana. Ann. Bot. 102:3295–304
    [Google Scholar]
  161. 161. 
    Vranová E, Coman D, Gruissem W 2013. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu. Rev. Plant Biol. 64:665–700
    [Google Scholar]
  162. 162. 
    Wang TN, Clifford MR, Martínez-Gómez J, Johnson JC, Riffell JA, Di Stilio VS 2019. Scent matters: differential contribution of scent to insect response in flowers with insect versus wind pollination traits. Ann. Bot. 123:2289–301
    [Google Scholar]
  163. 163. 
    Wang Z, Li N, Jiang S, Gonzalez N, Huang X et al. 2016. SCFSAP controls organ size by targeting PPD proteins for degradation in Arabidopsis thaliana. Nat. Commun 7:11192
    [Google Scholar]
  164. 164. 
    Wasternack C, Feussner I. 2018. The oxylipin pathways: biochemistry and function. Annu. Rev. Plant Biol. 69:363–86
    [Google Scholar]
  165. 165. 
    Weiss D, van der Luit A, Knegt E, Vermeer E, Mol JNM, Kooter JM 1995. Identification of endogenous gibberellins in petunia flowers. Plant Physiol 107:695–702
    [Google Scholar]
  166. 166. 
    Whitney HM, Chittka L, Bruce TJA, Glover BJ 2009. Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr. Biol. 19:11948–53
    [Google Scholar]
  167. 167. 
    Woźniak NJ, Kappel C, Marona C, Altschmied L, Neuffer B, Sicard A 2019. A common molecular basis to the convergent evolution of the selfing syndrome in Capsella. bioRxiv 653139. https://doi.org/10.1101/653139
    [Crossref]
  168. 168. 
    Xu W, Dubos C, Lepiniec L 2015. Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WDR complexes. Trends Plant Sci 20:3176–85
    [Google Scholar]
  169. 169. 
    Yant L, Collani S, Puzey J, Levy C, Kramer EM 2015. Molecular basis for three-dimensional elaboration of the Aquilegia petal spur. Proc. R. Soc. B 282:180320142778
    [Google Scholar]
  170. 170. 
    Yon F, Kessler D, Joo Y, Cortés Llorca L, Kim SG, Baldwin IT 2017. Fitness consequences of altering floral circadian oscillations for Nicotiana attenuata. J. Integr. Plant Biol 59:3180–89
    [Google Scholar]
  171. 171. 
    Yoshida H. 2012. Is the lodicule a petal: molecular evidence. Plant Sci 184:121–28
    [Google Scholar]
  172. 172. 
    Yoshida K, Oyama-Okubo N, Yamagishi M 2018. An R2R3-MYB transcription factor ODORANT1 regulates fragrance biosynthesis in lilies (Lilium spp.). Mol. Breed. 38:12144
    [Google Scholar]
  173. 173. 
    Yuan H, Owsiany K, Sheeja TE, Zhou X, Rodriguez C et al. 2015. A single amino acid substitution in an ORANGE protein promotes carotenoid overaccumulation in Arabidopsis. Plant Physiol 169:421–31
    [Google Scholar]
  174. 174. 
    Yuan Y-W. 2018. Monkeyflowers (Mimulus): new model for plant developmental genetics and evo-devo. New Phytol 222:2694–700
    [Google Scholar]
  175. 175. 
    Yuan Y-W, Byers KJRP, Bradshaw HD Jr 2013. The genetic control of flower–pollinator specificity. Curr. Opin. Plant Biol. 16:4422–28
    [Google Scholar]
  176. 176. 
    Yuan Y-W, Rebocho AB, Sagawa JM, Stanley LE, Bradshaw HD Jr 2016. Competition between anthocyanin and flavonol biosynthesis produces spatial pattern variation of floral pigments between Mimulus species. PNAS 113:92448–53
    [Google Scholar]
  177. 177. 
    Yuan Y-W, Sagawa JM, Frost L, Vela JP, Bradshaw HD Jr 2014. Transcriptional control of floral anthocyanin pigmentation in monkeyflowers (Mimulus). New Phytol 204:41013–27
    [Google Scholar]
  178. 178. 
    Yue Y, Yu R, Fan Y 2015. Transcriptome profiling provides new insights into the formation of floral scent in Hedychium coronarium. BMC Genom 16:470
    [Google Scholar]
  179. 179. 
    Zeng L, Wang X, Kang M, Dong F, Yang Z 2017. Regulation of the rhythmic emission of plant volatiles by the circadian clock. Int. J. Mol. Sci. 18:112408
    [Google Scholar]
  180. 180. 
    Zhao D, Tao J. 2015. Recent advances on the development and regulation of flower color in ornamental plants. Front. Plant Sci. 6:261
    [Google Scholar]
  181. 181. 
    Zhu F, Luo T, Liu C, Wang Y, Yang H et al. 2017. An R2R3-MYB transcription factor represses the transformation of α- and β-branch carotenoids by negatively regulating expression of CrBCH2 and CrNCED5 in flavedo of Citrus reticulate. New Phytol 216:178–92
    [Google Scholar]
  182. 182. 
    Zvi MMB, Shklarman E, Masci T, Kalev H, Debener T et al. 2012. PAP1 transcription factor enhances production of phenylpropanoid and terpenoid scent compounds in rose flowers. New Phytol 195:2335–45
    [Google Scholar]
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