Gain and Loss of Floral Scent Production through Changes in Structural Genes during Pollinator-Mediated Speciation

Current Biology

Volumn 26, Issue 24, 2016, Pages 3303-3312

  Amrad, Avichai ^a   Moser, Michel ^a   Mandel, Therese ^a   de Vries, Michel ^b   Schuurink, Robert C ^b   Freitas, Loreta ^c   Kuhlemeier, Cris ^a  

^a UNIVERSITY OF BERN   (Switzerland)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

Author keywords

benzenoids; floral volatile; Petunia; pollination syndrome; speciation; speciation genes

Indexed keywords

FRAGRANCE; PLANT PROTEIN;

ANIMAL; CHROMOSOMAL MAPPING; EVOLUTION; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GENOTYPE; METABOLISM; MOTH; PHYSIOLOGY; PLANT CHROMOSOME; POLLINATION; QUANTITATIVE TRAIT LOCUS; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION;

ANIMALS; BIOLOGICAL EVOLUTION; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENETIC SPECIATION; GENOTYPE; MOTHS; ODORANTS; PLANT PROTEINS; POLLINATION; POLYMORPHISM, SINGLE NUCLEOTIDE; QUANTITATIVE TRAIT LOCI;

EID: 85006355109     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.10.023     Document Type: Article

References (66)

1. 1 Mitchell, R.J., Irwin, R.E., Flanagan, R.J., Karron, J.D., Ecology and evolution of plant-pollinator interactions. Ann. Bot. (Lond.) 103 (2009), 1355–1363.
2. 2 Grant, V., Pollination systems as isolating mechanisms in angiosperms. Evolution 3 (1949), 82–97.
3. 3 Fenster, C.B., Armbruster, W.S., Wilson, P., Dudash, M.R., Thomson, J.D., Pollination syndromes and floral specialization. Annu. Rev. Ecol. Evol. Syst. 35 (2004), 375–403.
4. 4 Knapp, S., On ‘various contrivances’: pollination, phylogeny and flower form in the Solanaceae. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365 (2010), 449–460.
5. 5 Whittall, J.B., Hodges, S.A., Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447 (2007), 706–709.
6. 6 Bradshaw, H.D. Jr., Otto, K.G., Frewen, B.E., McKay, J.K., Schemske, D.W., Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149 (1998), 367–382.
7. 7 Bradshaw, H.D. Jr., Schemske, D.W., Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426 (2003), 176–178.
8. 8 Bouck, A., Wessler, S.R., Arnold, M.L., QTL analysis of floral traits in Louisiana iris hybrids. Evolution 61 (2007), 2308–2319.
9. 9 Klahre, U., Gurba, A., Hermann, K., Saxenhofer, M., Bossolini, E., Guerin, P.M., Kuhlemeier, C., Pollinator choice in Petunia depends on two major genetic loci for floral scent production. Curr. Biol. 21 (2011), 730–739.
10. 10 Brothers, A.N., Barb, J.G., Ballerini, E.S., Drury, D.W., Knapp, S.J., Arnold, M.L., Genetic architecture of floral traits in Iris hexagona and Iris fulva. J. Hered. 104 (2013), 853–861.
11. 11 Wessinger, C.A., Hileman, L.C., Rausher, M.D., Identification of major quantitative trait loci underlying floral pollination syndrome divergence in Penstemon. Philos. Trans. R. Soc. Lond. B Biol. Sci., 369, 2014, 20130349.
12. 12 Byers, K.J.R.P., Vela, J.P., Peng, F., Riffell, J.A., Bradshaw, H.D. Jr., Floral volatile alleles can contribute to pollinator-mediated reproductive isolation in monkeyflowers (Mimulus). Plant J. 80 (2014), 1031–1042.
13. 13 Bradshaw, H.D. Jr., Wilbert, S.M., Otto, K.G., Schemske, D.W., Genetic mapping of floral traits associated with reproductive isolation in monkeyflowers (Mimulus). Nature 376 (1995), 762–765.
14. 14 Nakazato, T., Rieseberg, L.H., Wood, T.E., The genetic basis of speciation in the Giliopsis lineage of Ipomopsis (Polemoniaceae). Heredity (Edinb) 111 (2013), 227–237.
15. 15 Yuan, Y.-W., Sagawa, J.M., Young, R.C., Christensen, B.J., Bradshaw, H.D. Jr., Genetic dissection of a major anthocyanin QTL contributing to pollinator-mediated reproductive isolation between sister species of Mimulus. Genetics 194 (2013), 255–263.
16. 16 Hopkins, R., Rausher, M.D., Identification of two genes causing reinforcement in the Texas wildflower Phlox drummondii. Nature 469 (2011), 411–414.
17. 17 Hopkins, R., Rausher, M.D., Pollinator-mediated selection on flower color allele drives reinforcement. Science 335 (2012), 1090–1092.
18. 18 Des Marais, D.L., Rausher, M.D., Parallel evolution at multiple levels in the origin of hummingbird pollinated flowers in Ipomoea. Evolution 64 (2010), 2044–2054.
19. 19 Schwinn, K., Venail, J., Shang, Y., Mackay, S., Alm, V., Butelli, E., Oyama, R., Bailey, P., Davies, K., Martin, C., A small family of MYB-regulatory genes controls floral pigmentation intensity and patterning in the genus Antirrhinum. Plant Cell 18 (2006), 831–851.
20. 20 Quattrocchio, F., Wing, J., van der Woude, K., Souer, E., de Vetten, N., Mol, J., Koes, R., Molecular analysis of the anthocyanin2 gene of Petunia and its role in the evolution of flower color. Plant Cell 11 (1999), 1433–1444.
21. 21 Hoballah, M.E., Gübitz, T., Stuurman, J., Broger, L., Barone, M., Mandel, T., Dell'Olivo, A., Arnold, M., Kuhlemeier, C., Single gene-mediated shift in pollinator attraction in Petunia. Plant Cell 19 (2007), 779–790.
22. 22 Kessler, D., Kallenbach, M., Diezel, C., Rothe, E., Murdock, M., Baldwin, I.T., How scent and nectar influence floral antagonists and mutualists. eLife, 4, 2015, e07641.
23. 23 Dötterl, S., Jürgens, A., Seifert, K., Laube, T., Weissbecker, B., Schütz, S., Nursery pollination by a moth in Silene latifolia: the role of odours in eliciting antennal and behavioural responses. New Phytol. 169 (2006), 707–718.
24. 24 Schiestl, F.P., Ayasse, M., Paulus, H.F., Löfstedt, C., Hansson, B.S., Ibarra, F., Francke, W., Orchid pollination by sexual swindle. Nature, 399, 1999, 421.
25. 25 Byers, K.J.R.P., Bradshaw, H.D. Jr., Riffell, J.A., Three floral volatiles contribute to differential pollinator attraction in monkeyflowers (Mimulus). J. Exp. Biol. 217 (2014), 614–623.
26. 26 Chen, C., Song, Q., Proffit, M., Bessière, J.-M., Li, Z., Hossaert-McKey, M., Private channel: a single unusual compound assures specific pollinator attraction in Ficus semicordata. Funct. Ecol. 23 (2009), 941–950.
27. 27 Schiestl, F.P., Kirk, H., Bigler, L., Cozzolino, S., Desurmont, G.A., Herbivory and floral signaling: phenotypic plasticity and tradeoffs between reproduction and indirect defense. New Phytol. 203 (2014), 257–266.
28. 28 Willmer, P.G., Nuttman, C.V., Raine, N.E., Stone, G.N., Pattrick, J.G., Henson, K., Stillman, P., McIlroy, L., Potts, S.G., Knudsen, J.T., Floral volatiles controlling ant behaviour. Funct. Ecol. 23 (2009), 888–900.
29. 29 Junker, R.R., Blüthgen, N., Floral scents repel facultative flower visitors, but attract obligate ones. Ann. Bot. (Lond.) 105 (2010), 777–782.
30. 30 Kessler, D., Diezel, C., Clark, D.G., Colquhoun, T.A., Baldwin, I.T., Petunia flowers solve the defence/apparency dilemma of pollinator attraction by deploying complex floral blends. Ecol. Lett. 16 (2013), 299–306.
31. 31 Theis, N., Adler, L.S., Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93 (2012), 430–435.
32. 32 Gregg, K.B., Variation in floral fragrances and morphology: incipient speciation in Cycnoches?. Bot. Gaz. 144 (1983), 566–576.
33. 33 Knudsen, J.T., Floral scent variation in the Pyrola rotundifolia complex in Scandinavia and western Greenland. Nord. J. Bot. 14 (1994), 277–282.
34. 34 Raguso, R.A., Levin, R.A., Foose, S.E., Holmberg, M.W., McDade, L.A., Fragrance chemistry, nocturnal rhythms and pollination “syndromes” in Nicotiana. Phytochemistry 63 (2003), 265–284.
35. 35 Levin, R.A., Raguso, R.A., McDade, L.A., Fragrance chemistry and pollinator affinities in Nyctaginaceae. Phytochemistry 58 (2001), 429–440.
36. 36 Waelti, M.O., Muhlemann, J.K., Widmer, A., Schiestl, F.P., Floral odour and reproductive isolation in two species of Silene. J. Evol. Biol. 21 (2008), 111–121.
37. 37 Hoballah, M.E., Stuurman, J., Turlings, T.C.J., Guerin, P.M., Connétable, S., Kuhlemeier, C., 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 (2005), 141–150.
38. 38 Xu, S., Schlüter, P.M., Grossniklaus, U., Schiestl, F.P., The genetic basis of pollinator adaptation in a sexually deceptive orchid. PLoS Genet., 8, 2012, e1002889.
39. 39 Muhlemann, J.K., Klempien, A., Dudareva, N., Floral volatiles: from biosynthesis to function. Plant Cell Environ. 37 (2014), 1936–1949.
40. 40 Sheehan, H., Hermann, K., Kuhlemeier, C., Color and scent: how single genes influence pollinator attraction. Cold Spring Harb. Symp. Quant. Biol. 77 (2012), 117–133.
41. 41 Riffell, J.A., Lei, H., Christensen, T.A., Hildebrand, J.G., Characterization and coding of behaviorally significant odor mixtures. Curr. Biol. 19 (2009), 335–340.
42. 42 Riffell, J.A., Lei, H., Abrell, L., Hildebrand, J.G., Neural basis of a pollinator's buffet: olfactory specialization and learning in Manduca sexta. Science 339 (2013), 200–204.
43. 43 Hermann, K., Klahre, U., Moser, M., Sheehan, H., Mandel, T., Kuhlemeier, C., Tight genetic linkage of prezygotic barrier loci creates a multifunctional speciation island in Petunia. Curr. Biol. 23 (2013), 873–877.
44. 44 Verdonk, J.C., Haring, M.A., van Tunen, A.J., Schuurink, R.C., ODORANT1 regulates fragrance biosynthesis in Petunia flowers. Plant Cell 17 (2005), 1612–1624.
45. 45 Bombarely, A., Moser, M., Amrad, A., Bao, M., Bapaume, L., Barry, C.S., Bliek, M., Boersma, M.R., Borghi, L., Bruggmann, R., et al. Insight into the evolution of the Solanaceae from the parental genomes of Petunia hybrida. Nat. Plants, 2, 2016, 16074.
46. 46 Verdonk, J.C., Ric de Vos, C.H., Verhoeven, H.A., Haring, M.A., van Tunen, A.J., Schuurink, R.C., Regulation of floral scent production in Petunia revealed by targeted metabolomics. Phytochemistry 62 (2003), 997–1008.
47. 47 Klempien, A., Kaminaga, Y., Qualley, A., Nagegowda, D.A., Widhalm, J.R., Orlova, I., Shasany, A.K., Taguchi, G., Kish, C.M., Cooper, B.R., et al. Contribution of CoA ligases to benzenoid biosynthesis in Petunia flowers. Plant Cell 24 (2012), 2015–2030.
48. 48 Colquhoun, T.A., Marciniak, D.M., Wedde, A.E., Kim, J.Y., Schwieterman, M.L., Levin, L.A., Van Moerkercke, A., Schuurink, R.C., Clark, D.G., A peroxisomally localized acyl-activating enzyme is required for volatile benzenoid formation in a Petunia×hybrida cv. ‘Mitchell Diploid’ flower. J. Exp. Bot. 63 (2012), 4821–4833.
49. 49 Kapila, J., De Rycke, R., Van Montagu, M., Angenon, G., An Agrobacterium-mediated transient gene expression system for intact leaves. Plant Sci. 122 (1997), 101–108.
50. 50 Segatto, A.L.A., Cazé, A.L.R., Turchetto, C., Klahre, U., Kuhlemeier, C., Bonatto, S.L., Freitas, L.B., Nuclear and plastid markers reveal the persistence of genetic identity: a new perspective on the evolutionary history of Petunia exserta. Mol. Phylogenet. Evol. 70 (2014), 504–512.
51. 51 Turchetto, C., Segatto, A.L.A., Mäder, G., Rodrigues, D.M., Bonatto, S.L., Freitas, L.B., High levels of genetic diversity and population structure in an endemic and rare species: implications for conservation. AoB Plants, 8, 2016, plw002.
52. 52 Sheehan, H., Moser, M., Klahre, U., Esfeld, K., Dell'Olivo, A., Mandel, T., Metzger, S., Vandenbussche, M., Freitas, L., Kuhlemeier, C., MYB-FL controls gain and loss of floral UV absorbance, a key trait affecting pollinator preference and reproductive isolation. Nat. Genet. 48 (2016), 159–166.
53. 53 Negre, F., Kish, C.M., Boatright, J., Underwood, B., Shibuya, K., Wagner, C., Clark, D.G., Dudareva, N., Regulation of methylbenzoate emission after pollination in snapdragon and Petunia flowers. Plant Cell 15 (2003), 2992–3006.
54. 54 Boatright, J., Negre, F., Chen, X., Kish, C.M., Wood, B., Peel, G., Orlova, I., Gang, D., Rhodes, D., Dudareva, N., Understanding in vivo benzenoid metabolism in Petunia petal tissue. Plant Physiol. 135 (2004), 1993–2011.
55. 55 Orlova, I., Marshall-Colón, A., Schnepp, J., Wood, B., Varbanova, M., Fridman, E., Blakeslee, J.J., Peer, W.A., Murphy, A.S., Rhodes, D., et al. Reduction of benzenoid synthesis in Petunia flowers reveals multiple pathways to benzoic acid and enhancement in auxin transport. Plant Cell 18 (2006), 3458–3475.
56. 56 Rockman, M.V., The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution 66 (2012), 1–17.
57. 57 Martin, A., Orgogozo, V., The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution 67 (2013), 1235–1250.
58. 58 Dittmar, E.L., Oakley, C.G., Conner, J.K., Gould, B.A., Schemske, D.W., Factors influencing the effect size distribution of adaptive substitutions. Proc. Biol. Sci., 283, 2016, 20153065.
59. 59 Shields, V.D.C., Hildebrand, J.G., Responses of a population of antennal olfactory receptor cells in the female moth Manduca sexta to plant-associated volatile organic compounds. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 186 (2000–2001), 1135–1151.
60. 60 Theis, N., Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J. Chem. Ecol. 32 (2006), 917–927.
61. 61 Yuan, Y.-W., Byers, K.J.R.P., Bradshaw, H.D. Jr., The genetic control of flower-pollinator specificity. Curr. Opin. Plant Biol. 16 (2013), 422–428.
62. 62 Colquhoun, T.A., Kim, J.Y., Wedde, A.E., Levin, L.A., Schmitt, K.C., Schuurink, R.C., Clark, D.G., PhMYB4 fine-tunes the floral volatile signature of Petunia×hybrida through PhC4H. J. Exp. Bot. 62 (2011), 1133–1143.
63. 63 Spitzer-Rimon, B., Farhi, M., Albo, B., Cna'ani, A., Ben Zvi, M.M., Masci, T., Edelbaum, O., Yu, Y., Shklarman, E., Ovadis, M., Vainstein, A., 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 (2012), 5089–5105.
64. 64 Spitzer-Rimon, B., Marhevka, E., Barkai, O., Marton, I., Edelbaum, O., Masci, T., Prathapani, N.-K., Shklarman, E., Ovadis, M., Vainstein, A., EOBII, a gene encoding a flower-specific regulator of phenylpropanoid volatiles’ biosynthesis in Petunia. Plant Cell 22 (2010), 1961–1976.
65. 65 Sas, C., Müller, F., Kappel, C., Kent, T.V., Wright, S.I., Hilker, M., Lenhard, M., Repeated inactivation of the first committed enzyme underlies the loss of benzaldehyde emission after the selfing transition in Capsella. Curr. Biol., 2016, 10.1016/j.cub.2016.10.026 Published online December 1, 2016.
66. 66 Shaipulah, N.F.M., Muhlemann, J.K., Woodworth, B.D., Van Moerkercke, A., Verdonk, J.C., Ramirez, A.A., Haring, M.A., Dudareva, N., Schuurink, R.C., CCoAOMT down-regulation activates anthocyanin biosynthesis in Petunia. Plant Physiol. 170 (2016), 717–731.