Evolution of oil-producing trichomes in Sisyrinchium (Iridaceae): Insights from the first comprehensive phylogenetic analysis of the genus

Annals of Botany

Volumn 107, Issue 8, 2011, Pages 1287-1312

  Chauveau, Olivier ^a   Eggers, Lilian ^b   Raquin, Christian ^c   Silvério, Adriano ^a,b   Brown, Spencer ^d   Couloux, Arnaud ^e   Cruaud, Corine ^e   Kaltchuk Santos, Eliane ^b   Yockteng, Roxana ^f   Souza Chies, Tatiana T ^b   Nadot, Sophie ^a  

^a UNIVERSITÉ PARIS SACLAY   (France)

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

^c UNIVERSITÉ PARIS SUD   (France)

^d INSTITUT DES SCIENCES DU VÉGÉTAL   (France)

^e CENTRE NATIONAL DE SÉQUENÇAGE   (France)

^f MUSÉUM NATIONAL D'HISTOIRE NATURELLE   (France)

Author keywords

elaiophores; glandular trichomes; lipids; Oil bee pollination; Olsynium; phylogeography; Sisyrinchieae; Solenomelus

Indexed keywords

PLANT DNA; VEGETABLE OIL;

BEE; LIPID; MONOCOTYLEDON; NATIVE SPECIES; PHYLOGENETICS; PHYLOGEOGRAPHY; POLLINATION; TAXONOMY; TRICHOME;

ANIMAL; ARTICLE; BAYES THEOREM; BEE; CHEMISTRY; CLASSIFICATION; EVOLUTION; FLOWER; GENETICS; GEOGRAPHY; IRIDACEAE; METABOLISM; MITOCHONDRION; NORTH AMERICA; PHYLOGENY; PHYSIOLOGY; PLANT GENE; PLASTID; POLLINATION; SEQUENCE ALIGNMENT; SOUTH AMERICA; STATISTICAL MODEL;

ANIMALS; BAYES THEOREM; BEES; BIOLOGICAL EVOLUTION; DNA, PLANT; FLOWERS; GENES, PLANT; GEOGRAPHY; IRIDACEAE; LIKELIHOOD FUNCTIONS; MITOCHONDRIA; NORTH AMERICA; PHYLOGENY; PLANT OILS; PLASTIDS; POLLINATION; SEQUENCE ALIGNMENT; SOUTH AMERICA;

ARGENTINA; CHILE;

APOIDEA; IRIDACEAE; OLSYNIUM; SISYRINCHIUM; SOLENOMELUS;

EID: 79957828645     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr080     Document Type: Article

References (75)

1. Alves-dos-Santos I, Melo GAR, Rozen JG. 2002. Biology and immature stages of the bee tribe Tetrapediini (Hymenoptera: Apidae). American Museum Novitates 3377: 1-45.
2. APG III. 2009. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Botanical Journal of the Linnean Society 161: 105-121.
3. Baker JG. 1878. Systema Iridaceanum. Botanical Journal of the Linnean Society 16: 61-180.
4. Barker C. 2004. World checklist of Iridaceae. The Board of Trustees of the Royal Botanic Gardens, Kew. Published on the Internet: http://www. kew.org/wcsp/ accessed 5 November 2009.
5. Bentham G, Hooker JD. 1883. Irideae: no.29. Sisyrinchium. In: Bentham G, Hooker JD. eds. Genera plantarum, Vol. 3(2). London: L. Reeve and Co., 698-699.
6. Bicknell EP. 1900. Studies in Sisyrinchium. VIII. Sisyrinchium californicum and related species of the neglected genus Hydastylus. Bulletin of the Torrey Botanical Club 27: 373-387.
7. Buchmann SL. 1987. The ecology of oil flowers and their bees. Annual Review of Ecology and Systematics 18: 343-369.
8. Cane JH, Eickwort GC, Wesley FR, Spielholz J. 1983. Foraging, grooming, and mate-seeking behaviors of Macropis nuda (Hymenoptera, Melittidae) and use of Lysimachia ciliata (Primulaceae) oils in larval provisions and cell linings. The American Midland Naturalist 110: 257-264. (Pubitemid 15270445)
9. Chase MW, Cowan RS, Hollingsworth PM, et al. 2007. A proposal for a standardised protocol to barcode all land plants. Taxon 56: 295-299. (Pubitemid 47025828)
10. Chat J, Jauregui B, Petit RJ, Nadot S. 2004. Reticulate evolution in kiwifruit (Actinidia, Actinidiaceae) identified by comparing their maternal and paternal phylogenies. American Journal of Botany 91: 736-747. (Pubitemid 43175026)
11. Cholewa AF, Henderson DM. 1984. Biosystematics of Sisyrinchium section Bermudiana (Iridaceae) of the Rocky Mountains. Brittonia 36: 342-363.
12. Cholewa AF, Henderson DM. 2002. Sisyrinchium Linnaeus, Vol. 26. In: Flora of North America Editorial Committee. eds. Flora of North America north of Mexico. New York, NY: Oxford University Press: 351-371.
13. Cocucci AA, Vogel S. 2001. Oil-producing flowers of Sisyrinchium species (Iridaceae) and their pollinators in southern South America. Flora 196: 26-46. (Pubitemid 32219137)
14. Cocucci AA, Sércic A, Roig-Alsina AH. 2000. Oil-collecting structures in Tapinotaspidini: their diversity, function, and probable origin. Mitteilungen Der Münchner Entomologischen Gesellschaft 90: 51-74.
15. Delpino F. 1874. Ulteriori osservazioni sulla dicogamia nel regno vegetale. Atti della Societás Italiana di Scienze Naturali 16: 151-349.
16. Diaz G, Melis M, Batetta B, Angius F, Falchi AM. 2008. Hydrophobic characterization of intracellular lipids in situ by Nile Red red/yellow emission ratio. Micron 39: 819-824.
17. Edgar RC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797. (Pubitemid 38832724)
18. Fahn A. 2000. Structure and function of secretory cells. Advances in Botanical Research 31: 37-75.
19. Felsenstein J. 1981. Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution 17: 368-376. (Pubitemid 11016207)
20. Freudenstein JV, Chase MW. 2001. Analysis of mitochondrial nad1b-c intron sequences in Orchidaceae: utility and coding of length-change characters. Systematic Botany 26: 643-657. (Pubitemid 32908117)
21. Goldblatt P, Manning JC. 2008. Sisyrinchium Linnaeus. In: Goldblatt P, Manning JC. eds. The iris family - natural history and classification. Portland, OR: Timber Press, 221-224.
22. Goldblatt P, Henrich JE, Keating RC. 1989. Seed morphology of Sisyrinchium (Iridaceae - Sisyrinchieae) and its allies. Annals of the Missouri Botanical Garden 76: 1109-1117.
23. Goldblatt P, Rudall P, Henrich JE. 1990. The genera of the Sisyrinchium alliance (Iridaceae: Iridoideae): phylogeny and relationships. Systematic Botany 15: 497-510.
24. Goldblatt P, Rodriguez A, Powell MP, et al. 2008. Iridaceae 'out of Australasia'? Phylogeny, biogeography, and divergence time based on plastid DNA sequences. Systematic Botany 33: 495-508.
25. Greenspan P, Mayer EP, Fowler SD. 1985. Nile Red: a selective fluorescent stain for intracellular lipids droplets. The Journal of Cell Biology 100: 965-973. (Pubitemid 15135357)
26. Guindon S, Lethiec F, Duroux P, Gascuel O. 2005. PHYML Online-a web server for fast maximum likelihood-based phylogenetic inference. Nucleic Acids Research 33 (Suppl. 2): W557-W559. (Pubitemid 44529983)
27. Henderson DM. 1976. A biosystematic study of Pacific northwestern blue-eyed grasses (Sisyrinchium, Iridaceae). Brittonia 28: 149-176.
28. Hollingsworth ML, Clark A, Forrest LL, et al. 2009. Selecting barcoding loci for plants: evaluation of seven candidate loci with species-level sampling in three divergent groups of land plants. Molecular Ecology Resources 9: 439-457.
29. Johnston IM. 1938. The species of Sisyrinchium in Uruguay, Paraguay and Brazil. Journal of the Arnold Arboretum 19: 376-401.
30. Kenton AY, Rudall PJ, Johnson AR. 1986. Genome size variation in Sisyrinchium L. (Iridaceae) and its relationship to phenotype and habitat. Botanical Gazette 147: 342-354.
31. Klatt FW. 1861. Monographia generis Sisyrinchium. Linnaea 31: 61-100.
32. Kress WJ, Wurdack KJ, Zimmer EA, Weigt LA, Janzen DH. 2005. Use of DNA barcodes to identify flowering plants. Proceedings of the National Academy of Sciences of the USA 102: 8369-8374. (Pubitemid 40803501)
33. McVaugh R. 1989. Bromeliaceae to Dioscoreacae. In: McVaugh R. ed. Flora Novo-Galiciana: a descriptive account of the vascular plants of the western Mexico, Vol. 15. Ann Arbor, MI: The University of Michigan Herbarium, 294-347.
34. Machado IC. 2004. Oil-collecting bees and related plants: a review of the studies in the last twenty years and case histories of plants occurring in NE Brazil. In: Freitas B, Pereira JOP. eds. Solitary bees, conservation, rearing and management for pollination. Fortaleza, BR: Editora Universitária, 255-280.
35. Maddison WP, Maddison DR. 2010. Mesquite: a modular system for evol-. utionary analysis. Version 2 73, distributed by the authors, website: http://mesquiteproject.org
36. Michener CD. 2007. The bees of the World. Baltimore, MD: Johns Hopkins University Press.
37. Minckley RL, Roulston TH. 2006. Incidental mutualisms and pollen specialization among bees. In: Waser NM, Ollerton J. eds. Plant-pollinator interactions: from specialisation to generalisation. London: University of Chicago Press, 69-98.
38. Neff JL, Simpson BB. 2005. Other rewards: oils, resins, and gums. In: Dafni A, Kevan PG, Husband BC. eds. Practical pollination biology. Cambridge: Enviroquest, 314-328.
39. Nixon KC. 1999. The parsimony ratchet, a new method for rapid parsimony analysis. Cladistics 15: 407-414. (Pubitemid 30203167)
40. Nylander JAA. 2004. MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.
41. Pagel M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Systematic Biology 48: 612-622. (Pubitemid 129479567)
42. Rasmussen C, Olesen JM. 2000. Oil flowers and oil-collecting bees. Det Norske Videnskaps-Akademi. I. Matematisk Naturvidenskapelige Klasse, Skrifter 39: 23-31.
43. Ravenna P. 2000. Revisional studies in the genus Sisyrinchium (Iridaceae) VI. Onira Leaflets 5(4): 13-19.
44. Ravenna P. 2001a. Revisional studies in the genus Sisyrinchium (Iridaceae) VII. Onira Leaflets 5(12): 54-61.
45. Ravenna P. 2001b. The Iridaceae of the Cuyo region Argentina. Onira Leaflets 6(1): 1-18.
46. Ravenna P. 2002. Revisional studies in the genus Sisyrinchium (Iridaceae) IX. Onira Leaflets 7(6): 20-41.
47. Ravenna P. 2003a. Revisional studies in the genus Sisyrinchium (Iridaceae) X. Onira Leaflets 8(6): 20-24.
48. Ravenna P. 2003b. Revisional studies in the genus Sisyrinchium (Iridaceae) XI. Onira Leaflets 8(13): 48-54.
49. Renner SS, Schaefer H. 2010. The evolution and loss of oil-offering flowers: new insights from dated phylogenies for angiosperms and bees. Philosophical Transactions of the Royal Society 365: 423-435.
50. Rieseberg LH, Willis JH. 2007. Plant speciation. Science 317: 910-914. (Pubitemid 47301311)
51. Ronquist F. 1996. DIVA version 1.1, distributed by the author, website: http ://www.ebc.uu.se/systzoo/research/diva/diva.html
52. Ronquist F. 1997. Dispersal-vicariance analysis: a new approach to the quantification of historical biogeography. Systematic Biology 46: 195-203.
53. Ronquist F, Huelsenbeck JP. 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574. (Pubitemid 37038874)
54. Rudall P, Kenton AY, Lawrence TJ. 1986. An anatomical and chromosomal investigation of Sisyrinchium and allied general. Botanical Gazette 147: 466-477.
55. Schlindwein C. 1998. Frequent oligolecty characterizing a diverse bee-plant community in a xerophytic bushland of subtropical Brazil. Studies on Neotropical Fauna and Environment 33: 46-59. (Pubitemid 128670813)
56. Schluter D, Price T, Mooers AO, Ludwig D. 1997. Likelihood of ancestor states in adaptive radiation. Evolution 51: 1699-1711. (Pubitemid 28104532)
57. Shaw J, Lickey EB, Beck JT, et al. 2005. The tortoise and the hare II: relative utility of 21 noncoding chloroplast DNA sequences for phylogenetic analysis. American Journal of Botany 92: 142-166. (Pubitemid 40113117)
58. Shaw J, Lickey EB, Schilling EE, Small RL. 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phyloge-netic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94: 275-288. (Pubitemid 46955026)
59. Silvera K. 2002. Adaptive radiation of oil-reward compound among Neotropical orchid species (Oncidiinae). MSc Thesis, University of Florida, USA.
60. Simmons MP, Ochoterena H. 2000. Gaps as characters in sequence-based phylogenetic analyses. Systematic Biology 49: 369-381.
61. Simpson BB, Neff JL. 1981. Floral rewards: alternatives to pollen and nectar. Annals of the Missouri Botanical Garden 68: 301-322.
62. Starr JF, Naczi RFC, Chouinard BN. 2009. Plant DNA barcodes and species resolution in sedges (Carex, Cyperaceae). Molecular Ecology Resources 9: 151-163.
63. Steffan-Dewenter I, Klein AM, Gaebele V, Alfert T, Tscharntke T. 2006. Bee diversity and plant-pollinator interactions in fragmented landscapes. In: Waser NM, Ollerton J. eds. Plant-pollinator interactions: from specialisation to generalisation. London: University of Chicago Press, 387-407.
64. Steiner KE, Whitehead VB. 2002. Oil secretion and the pollination of Colpias mollis (Scrophulariaceae). Plant Systematics and Evolution 235: 53-66. (Pubitemid 36016987)
65. Swofford DL. 2002. PAUP*: Phylogenetic analysis using parsimony (*and other methods), beta version 4.0. Sinauer, Sunderland, MA, USA.
66. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular . Evolutionary Genetics Analysis (MEGA) software version 4 0. Molecular Biology and Evolution 24: 1596-1599.
67. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24: 4876-4882. (Pubitemid 28022245)
68. Vogel S. 1969. Flowers offering fatty oil instead of nectar. In: Starr RC. ed. : Proceedings of the XI International Botanical Congress. University of Washington, Seattle, Washington, DC, 229.
69. V̈ogel S. 1974. Olblumen und ölsammelnde Bienen. Abhandlungen Akademie Wissenschaften Mathematisch-Naturwissenschaften Klasse, Tropische und Subtropische Pflanzenwelt 7: 1-267.
70. Vogel S. 2009. The non-African oil-flowers and their bees: a brief survey. SAAB Annual Meeting Abstract. South African Journal of Botany 75: 389-390.
71. Wang RJ, Cheng CL, Chang CC, Wu CL, Tu TM, Chaw SM. 2008. Dynamics and evolution of the inverted repeat-large single copy junction in the chloroplast genomes of monocots. BMC Evolutionary Biology 8: 36. doi:10.1186/1471-2148-8-36. (Pubitemid 351674324)
72. Waser NM. 2006. Specialization and generalization in plant-pollinator interactions: a historical perspective. In: Waser NM, Ollerton J. eds. Plant- pollinator interactions: from specialisation to generalisation. London: University of Chicago Press, 3-17.
73. White TJ, Bruns T, Lee S, Taylor J. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA. eds. PCR protocols: a guide to methods and applications. San Diego, CA: Academy Press, 315-322.
74. Yang Z, Rannala B. 1997. Bayesian phylogenetic inference using DNA sequences: a Markov Chain Monte Carlo method. Molecular Biology and Evolution 14: 717-724. (Pubitemid 27287292)
75. Young ND, Healy J. 2003. GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinformatics 4: 6. doi:10.1186/1471-2105-4-6. (Pubitemid 38751264)