Repeated Inactivation of the First Committed Enzyme Underlies the Loss of Benzaldehyde Emission after the Selfing Transition in Capsella

Current Biology

Volumn 26, Issue 24, 2016, Pages 3313-3319

  Sas, Claudia ^a   Müller, Frank ^b   Kappel, Christian ^a   Kent, Tyler V ^c   Wright, Stephen I ^c   Hilker, Monika ^b   Lenhard, Michael ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

benzaldehyde; Capsella; cinnamate:CoA ligase; floral scent; selfing syndrome; shepherd's purse

Indexed keywords

BENZALDEHYDE; BENZALDEHYDE DERIVATIVE; FRAGRANCE; LIGASE; PLANT PROTEIN;

ANIMAL; CAPSELLA; CHEMISTRY; ENZYMOLOGY; EVOLUTION; GENE EXPRESSION REGULATION; GENETICS; INBREEDING; INSECT; METABOLISM; PHYLOGENY; POLLINATION; QUANTITATIVE TRAIT LOCUS;

ANIMALS; BENZALDEHYDES; BIOLOGICAL EVOLUTION; CAPSELLA; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; INBREEDING; INSECTA; LIGASES; ODORANTS; PHYLOGENY; PLANT PROTEINS; POLLINATION; QUANTITATIVE TRAIT LOCI;

EID: 85006341185     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.cub.2016.10.026     Document Type: Article

References (37)

1. 1 Harder, L.D., Johnson, S.D., Darwin's beautiful contrivances: evolutionary and functional evidence for floral adaptation. New Phytol. 183 (2009), 530–545.
2. 2 Stebbins, G.L., Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination mechanisms. Annu. Rev. Ecol. Syst. 1 (1970), 307–326.
3. 3 Raguso, R.A., Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39 (2008), 549–569.
4. 4 Schiestl, F.P., Johnson, S.D., Pollinator-mediated evolution of floral signals. Trends Ecol. Evol. 28 (2013), 307–315.
5. 5 Schiestl, F.P., Schlüter, P.M., Floral isolation, specialized pollination, and pollinator behavior in orchids. Annu. Rev. Entomol. 54 (2009), 425–446.
6. 6 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.
7. 7 Galen, C., Kaczorowski, R., Todd, S.L., Geib, J., Raguso, R.A., Dosage-dependent impacts of a floral volatile compound on pollinators, larcenists, and the potential for floral evolution in the alpine skypilot Polemonium viscosum. Am. Nat. 177 (2011), 258–272.
8. 8 Theis, N., Adler, L.S., Advertising to the enemy: enhanced floral fragrance increases beetle attraction and reduces plant reproduction. Ecology 93 (2012), 430–435.
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 Schlüter, P.M., Xu, S., Gagliardini, V., Whittle, E., Shanklin, J., Grossniklaus, U., Schiestl, F.P., Stearoyl-acyl carrier protein desaturases are associated with floral isolation in sexually deceptive orchids. Proc. Natl. Acad. Sci. USA 108 (2011), 5696–5701.
11. 11 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.
12. 12 Dudareva, N., Cseke, L., Blanc, V.M., Pichersky, E., Evolution of floral scent in Clarkia: novel patterns of S-linalool synthase gene expression in the C. breweri flower. Plant Cell 8 (1996), 1137–1148.
13. 13 Nam, K.H., Dudareva, N., Pichersky, E., Characterization of benzylalcohol acetyltransferases in scented and non-scented Clarkia species. Plant Cell Physiol. 40 (1999), 916–923.
14. 14 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.
15. 15 Dudareva, N., Klempien, A., Muhlemann, J.K., Kaplan, I., Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol. 198 (2013), 16–32.
16. 16 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.
17. 17 Abd El-Mawla, A.M.A., Beerhues, L., Benzoic acid biosynthesis in cell cultures of Hypericum androsaemum. Planta 214 (2002), 727–733.
18. 18 Amrad, A., Moser, M., Mandel, T., de Vries, M., Schuurink, R.C., Freitas, L., Kuhlemeier, C., Gain and loss of floral scent production through changes in structural genes during pollinator-mediated speciation. Curr. Biol., 2016, 10.1016/j.cub.2016.10.023 Published online December 1, 2016.
19. 19 Barrett, S.C., The evolution of plant sexual diversity. Nat. Rev. Genet. 3 (2002), 274–284.
20. 20 Sicard, A., Lenhard, M., The selfing syndrome: a model for studying the genetic and evolutionary basis of morphological adaptation in plants. Ann. Bot. (Lond.) 107 (2011), 1433–1443.
21. 21 Doubleday, L.A.D., Raguso, R.A., Eckert, C.G., Dramatic vestigialization of floral fragrance across a transition from outcrossing to selfing in Abronia umbellata (Nyctaginaceae). Am. J. Bot. 100 (2013), 2280–2292.
22. 22 Hurka, H., Friesen, N., German, D.A., Franzke, A., Neuffer, B., ‘Missing link’ species Capsella orientalis and Capsella thracica elucidate evolution of model plant genus Capsella (Brassicaceae). Mol. Ecol. 21 (2012), 1223–1238.
23. 23 Brandvain, Y., Slotte, T., Hazzouri, K.M., Wright, S.I., Coop, G., Genomic identification of founding haplotypes reveals the history of the selfing species Capsella rubella. PLoS Genet., 9, 2013, e1003754.
24. 24 Foxe, J.P., Slotte, T., Stahl, E.A., Neuffer, B., Hurka, H., Wright, S.I., Recent speciation associated with the evolution of selfing in Capsella. Proc. Natl. Acad. Sci. USA 106 (2009), 5241–5245.
25. 25 Guo, Y.L., Bechsgaard, J.S., Slotte, T., Neuffer, B., Lascoux, M., Weigel, D., Schierup, M.H., Recent speciation of Capsella rubella from Capsella grandiflora, associated with loss of self-incompatibility and an extreme bottleneck. Proc. Natl. Acad. Sci. USA 106 (2009), 5246–5251.
26. 26 Dudareva, N., Murfitt, L.M., Mann, C.J., Gorenstein, N., Kolosova, N., Kish, C.M., Bonham, C., Wood, K., Developmental regulation of methyl benzoate biosynthesis and emission in snapdragon flowers. Plant Cell 12 (2000), 949–961.
27. 27 Loughrin, J.N., Hamilton-Kemp, T.R., Andersen, R.A., Hildebrand, D.F., Volatiles from flowers of Nicotiana sylvestris, N. otophora and Malus × domestica: headspace components and day/night changes in their relative concentrations. Phytochemistry 29 (1990), 2473–2477.
28. 28 Schiestl, F.P., Ayasse, M., Paulus, H.F., Erdmann, D., Francke, W., Variation of floral scent emission and postpollination changes in individual flowers of Ophrys sphegodes subsp. sphegodes. J. Chem. Ecol. 23 (1997), 2881–2895.
29. 29 Sicard, A., Stacey, N., Hermann, K., Dessoly, J., Neuffer, B., Bäurle, I., Lenhard, M., Genetics, evolution, and adaptive significance of the selfing syndrome in the genus Capsella. Plant Cell 23 (2011), 3156–3171.
30. 30 Knauer, A.C., Schiestl, F.P., Bees use honest floral signals as indicators of reward when visiting flowers. Ecol. Lett. 18 (2015), 135–143.
31. 31 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 Petuniaxhybrida cv. ‘Mitchell Diploid’ flower. J. Exp. Bot. 63 (2012), 4821–4833.
32. 32 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.
33. 33 Josephs, E.B., Lee, Y.W., Stinchcombe, J.R., Wright, S.I., Association mapping reveals the role of purifying selection in the maintenance of genomic variation in gene expression. Proc. Natl. Acad. Sci. USA 112 (2015), 15390–15395.
34. 34 Theis, N., Fragrance of Canada thistle (Cirsium arvense) attracts both floral herbivores and pollinators. J. Chem. Ecol. 32 (2006), 917–927.
35. 35 MacKintosh, R.W., Fewson, C.A., Benzyl alcohol dehydrogenase and benzaldehyde dehydrogenase II from Acinetobacter calcoaceticus. Purification and preliminary characterization. Biochem. J. 250 (1988), 743–751.
36. 36 Shaw, J.P., Harayama, S., Purification and characterisation of TOL plasmid-encoded benzyl alcohol dehydrogenase and benzaldehyde dehydrogenase of Pseudomonas putida. Eur. J. Biochem. 191 (1990), 705–714.
37. 37 He, A., Li, T., Daniels, L., Fotheringham, I., Rosazza, J.P., Nocardia sp. carboxylic acid reductase: cloning, expression, and characterization of a new aldehyde oxidoreductase family. Appl. Environ. Microbiol. 70 (2004), 1874–1881.