The multiple fuzzy origins of woodiness within Balsaminaceae using an integrated approach. Where do we draw the line?

Annals of Botany

Volumn 109, Issue 4, 2012, Pages 783-799

  Lens, Frederic ^a   Eeckhout, Sharon ^b,c   Zwartjes, Rosa ^a   Smets, Erik ^a,b,d   Janssens, Steven B ^b  

^a NATURALIS BIODIVERSITY CENTER   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

^d LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Balsaminaceae; herbaceousness; Hydrocera; Impatiens; insular woodiness; light microscopy; primary woodiness; secondary woodiness; wood anatomy

Indexed keywords

ANATOMY; CLADISTICS; DICOTYLEDON; FUZZY MATHEMATICS; HERB; INTEGRATED APPROACH; MICROSCOPY; MOLECULAR ANALYSIS; OBSERVATIONAL METHOD; PHYLOGENY; SHRUB; TAXONOMY;

ARTICLE; BALSAMINACEAE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMPATIENS; MOLECULAR GENETICS; PHYLOGENY; WOOD;

BALSAMINACEAE; IMPATIENS; MOLECULAR SEQUENCE DATA; PHYLOGENY; WOOD;

BALSAMINACEAE; ERICALES; HYDROCERA; HYDROCERA TRIFLORA; IMPATIENS; MARCGRAVIACEAE; TETRAMERISTACEAE;

EID: 84857693972     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcr310     Document Type: Article

References (66)

1. Agusti J, Lichtenberger R, Schwarz M, Nehlin L, Greb T. 2011. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genetics 7: E1001312. http://dx.doi.org/10.1371/journal.pgen. 1001312.
2. Bailey IW. 1920. The cambium and its derivative tissues. II. Size variations of cambial initials in gymnosperms and angiosperms. American Journal of Botany 7: 355-367.
3. Böhle UR, Hilger HH, Martin WF. 1996. Island colonization and evolution of the insular woody habit in Echium L. (Boraginaceae). Proceedings of the National Academy of Sciences, USA 93: 11740-11745. (Pubitemid 26347193)
4. Caris PL, Geuten KP, Janssens SB, Smets EF. 2006. Floral development in three species of Impatiens (Balsaminaceae). American Journal of Botany 93: 1-14. (Pubitemid 43187869)
5. Carlquist S. 1962. A theory of paedomorphosis in dicotyledonous woods. Phytomorphology 12: 30-45.
6. Carlquist S. 1970. Wood anatomy of insular species of Plantago and the problem of raylessness. Bulletin of the Torrey Botanical Club 97: 353-361.
7. Carlquist S. 1974. Insular woodiness. In: Island biology. New York: Columbia University Press, 350-428.
8. Carlquist S. 1992. Wood anatomy of sympetalous dicotyledon families: A summary, with comments on systematic relationships and evolution of the woody habit. Annals of the Missouri Botanic Garden 79: 303-332.
9. Carlquist S. 2009. Xylem heterochrony: An unappreciated key to angiosperm origin and diversifications. Botanical Journal of the Linnean Society 161: 26-65.
10. Chaffey N, Cholewa E, Regan S, Sundberg B. 2002. Secondary xylem development in Arabidopsis: A model for wood formation. Physiologia Plantarum 114: 594-600. (Pubitemid 34463633)
11. Cheek M, Fischer E. 1999. A tuberous and epiphytic new species of Impatiens (Balsaminaceae) from southwest Cameroon. Kew Bulletin 57: 669-674.
12. Darwin C. 1859. On the origin of species by means of natural selection. London: John Murray.
13. Dharmawardhana P, Brunner AM, Strauss SH. 2010. Genome-wide transcriptome analysis of the transition from primary to secondary stem development in Populus trichocarpa. BMC Genomics 11: 150. http://dx.doi.org/10.1186/1471-2164- 11-150.
14. Dulin MW, Kirchoff BK. 2010. Paedomorphosis, secondary woodiness, and insular woodiness in plants. Botanical Review 76: 405-490.
15. Edgar RC. 2004. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics 5: 113. http://dx.doi.org/10. 1186/1471-2105-5-113.
16. Francisco-Ortega F, Fuerte-Aguilar F, Kim SC, Santos-Guerra A, Crawford DJ, Jansen RK. 2002. Phylogeny of the Macaronsesian endemic Crambe section Dendrocrambe (Brassicaceae) based on internal transcribed spacer sequences of nuclear ribosomal DNA. American Journal of Botany 89: 1984-1990. (Pubitemid 36080470)
17. Gerard AM. 1917. Recherches sur la spécification histologique de différents bois de Madagascar, avec étude comparative des principaux bois industriels d'Europe. Lons-Le-Saunier, France.
18. Givnish TJ. 1995. Plant stems: Biomechanical adaptation for energy capture and influence on species distributions. In: Gartner BL. ed. Plant stems: physiology and functional morphology. New York: Chapman and Hall, 3-49.
19. Givnish TJ. 1998. Adaptive plant evolution on islands: Classical patterns, molecular data, new insights. In: Grant PR. ed. Evolution on islands. Oxford: Oxford University Press, 281-304.
20. Grey-Wilson C. 1980a. Impatiens of Africa. Rotterdam: Balkema.
21. Grey-Wilson C. 1980b. Hydrocera triflora, its floral morphology and relationship with Impatiens. Studies in Balsaminaceae. Kew Bulletin 34: 221-227.
22. Groover AT. 2005. What genes make a tree a tree? Trends in Plant Science 10: 210-214. (Pubitemid 40607967)
23. Hamann TD, Smets E, Lens F. 2011. A comparison of paraffin and resinbased techniques used in bark anatomy. Taxon 60: 841-851.
24. Hillis DM, Bull JJ. 1993. An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42: 182-192.
25. Hooker JD, Thomson T. 1859. Praecursores ad floram Indicam. Balsaminaceae. Botanical Journal of the Linnean Society 4: 106-157.
26. IAWA Committee. 1989. IAWA list of microscopic features for hardwood identification. International Association of Wood Anatomists Bulletin, New Series 10: 219-332.
27. Janssens SB, Geuten K, Yuan Y-M, Küpfer P, Smets EF. 2006. Phylogenetics of Impatiens and Hydrocera using chloroplast atpB-rbcL spacer sequences. Systematic Botany 31: 171-180.
28. Janssens SB, Geuten KP, Viaene T, Yuan Y-M, Song Y, Smets E. 2007. Phylogenetic utility of the AP3/DEF K-domain and its molecular evolution in Impatiens (Balsaminaceae). Molecular Phylogenetics and Evolution 43: 225-239. (Pubitemid 46484360)
29. Janssens SB, Viaene T, Huysmans S, Smets EF, Geuten KP. 2008. Selection on length mutations after frameshift can explain the origin and retention of the AP3/DEF-like paralogues in Impatiens. Journal of Molecular Evolution 66: 424-435.
30. Janssens SB, Knox EB, Huysmans S, Smets EF, Merckx VSFT. 2009. Rapid radiation of Impatiens (Balsaminaceae) during Pliocene and Pleistocene: Result of a global climate change. Molecular Phylogenetics and Evolution 52: 806-824.
31. Janssens SB, Fischer E, Stévart T. 2010. New insights on the origin of epiphytic Impatiens (Balsaminaceae) in West Equatorial Africa based on molecular phylogenetic and biogeographical analysis. Taxon 59: 1508-1518.
32. Janssens SB, Dessein S, Smets E. 2011. Portrayal of Impatiens nzabiana (Balsaminaceae): A morphological, molecular and biogeographic study of a new Gabonese species. Systematic Botany 36: 440-448.
33. Ko JH, Han KH, Yang J. 2004. Plant body weight-induced secondary growth in Arabidopsis and its transcription phenotype revealed by wholetranscriptome profiling. Plant Physiology 135: 1069-1083. (Pubitemid 38819050)
34. Koek-Noorman J. 1976. Juvenile chracters in the wood of certain Rubiaceae with special emphasis to Rubia fruticosa Ait. International Association of Wood Anatomists Bulletin 3: 38-42.
35. Krumbiegel A, Kästner A. 1993. Sekundäres Dickenwachstum von Sproß und Wurzel bei annuellen dicotylen. Österreichische Akademie der Wissenschaften, Biosystematics and Ecology Series 4: 1-49.
36. Lee C, Kim S-C, Lundy K, Santos-Guerra A. 2005. Chloroplast DNA phylogeny of the woody Sonchus alliance (Asteraceae: Sonchinae) in the Macaronesian islands. American Journal of Botany 92: 2072-2085. (Pubitemid 43194533)
37. Lens F, Caris P, Smets E, Serlet L, Jansen S. 2005a. Comparative wood anatomy of the primuloid clade (Ericales s.l.). Systematic Botany 30: 162-182.
38. Lens F, Dressler S, Jansen S, Van Evelghem L, Smets E. 2005b. Relationships within balsaminoid Ericales: A wood anatomical approach. American Journal of Botany 92: 941-953. (Pubitemid 40728481)
39. Lens F, Schönenberger J, Baas P, Jansen S, Smets E. 2007. The role of wood anatomy in phylogeny reconstruction of Ericales. Cladistics 23: 229-254. (Pubitemid 46918638)
40. Lens F, Groeninckx I, Smets E, Dessein S. 2009. Woodiness within the Spermacoceae-Knoxieae alliance (Rubiaceae): Retention of the basal woody condition in Rubiaceae or recent innovation? Annals of Botany 103: 1049-1064.
41. Lens F, Sperry JS, Christman MA, Choat B, Rabaey D, Jansen S. 2011. Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytologist 190: 709-723.
42. Lens F, Smets E, Melzer S. 2012. Stem anatomy supports Arabidopsis thaliana as a model for insular woodiness. New Phytologist 193: 12-17.
43. Maddison DR, Maddison WP. 2002. MacClade 4.04. Sunderland, MS: Sinauer Associates Inc.
44. Melzer S, Lens F, Gennen J, Vanneste S, Rhode A, Beeckman T. 2008. Flowering time genes modulate meristem determinacy and growth form in Arabidopsis. Nature Genetics 40: 1489-1492.
45. Newman MF. 2008. Impatiens pachycaulon (Balsaminaceae) a new species from Laos. Edinburgh Botanical Journal 65: 23-26. (Pubitemid 351317003)
46. Nieminen KM, Kauppinen L, Helariutta Y. 2004. A weed for wood? Arabidopsis as a genetic model for xylem development. Plant Physiology 135: 635-659.
47. Oh S, Park S, Han KH. 2003. Transcriptional regulation of secondary growth in Arabidopsis thaliana. Journal of Experimental Botany 54: 2709-2722. (Pubitemid 37537862)
48. Perrier de la Bathie H. 1948. Révision des Impatiens de Madagascar et des Comores. Mémoires de l'Académie des Sciences 67: 1-16.
49. Raunkiaer C. 1934. Life forms of plants and statistical plant geography. Oxford: Clarendon.
50. Sattler R. 1996. Classical morphology and continuum morphology: Opposition and continuum. Annals of Botany 78: 577-581. (Pubitemid 26420287)
51. Schols P, D'Hondt C, Geuten K, Merckx V, Janssens S, Smets E. 2004. MorphoCode: Coding quantitative data for phylogenetic analyses. Phyloinformatics 4: 1-4.
52. Schrader J, Nilsson J, Mellerowicz E, et al. 2004. A high-resolution transcript profile across the wood-forming meristem of poplar identifies potential regulators of cambial stem identity. The Plant Cell 16: 2278-2292. (Pubitemid 39247072)
53. Schweingruber FH. 2007. Wood structure and environment. Berlin: Springer.
54. Schweingruber FH, Börner A, Schulze E-D. 2011. Atlas of stem anatomy in herbs, shrubs and trees, Vol. 1. Heidelberg: Springer.
55. Solereder H. 1899. Systematische Anatomie der Dicotyledonen. Stuttgart: Verlag von Ferdinand Enke.
56. Soltis PS, Soltis DE. Applying the bootstrap in phylogeny reconstruction. Statistical Science 2: 256-267.
57. Sperry JS, Hacke UG, Pittermann J. 2006. Size and function in conifer tracheids and angiosperm vessels. American Journal of Botany 93: 1390-1500.
58. Sperry JS, Hacke UG, Field TS, Sano Y, Sikkema EH. 2007. Hydraulic consequences of vessel evolution in angiosperms. International Journal of Plant Sciences 168: 1127-1139. (Pubitemid 47580434)
59. Spicer R, Groover A. 2010. Evolution of development of vascular cambia and secondary growth. New Phytologist 186: 577-592.
60. Stamatakis A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690. (Pubitemid 44642609)
61. Stamatakis A, Ludwig T, Meier H. 2005. RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics 21: 456-463. (Pubitemid 40310232)
62. Swofford DL. 2002. PAU.P.*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b. Sunderland, MA: Sinauer Associates.
63. Thiele K. 1993. The holy grail of the perfect character: The cladistic treatment of morphometric data. Cladistics 9: 275-304.
64. Tilman D. 1988. Resource competition and community structure. Princeton, NJ: Princeton University Press.
65. Wallace AR. 1878. Tropical nature and other essays. London: Macmillan.
66. Yuan Y-M, Song Y, Geuten K, et al. 2004. Phylogeny and biogeography of Balsaminaceae inferred from ITS sequence data. Taxon 53: 391-404.