Floral morphology and development in quillajaceae and surianaceae (fabales), the species-poor relatives of Leguminosae and Polygalaceae

Annals of Botany

Volumn 100, Issue 7, 2007, Pages 1491-1505

  Bello, M A ^a,b   Hawkins, J A ^a   Rudall, P J ^b  

^a UNIVERSITY OF READING   (United Kingdom)

^b JODRELL LABORATORY   (United Kingdom)

Author keywords

Eurosids I; Fabales; Floral ontogeny; Floral symmetry; Leguminosae; Polygalaceae; Quillajaceae; Surianaceae

Indexed keywords

DICOTYLEDON; FLORAL TRAIT; LEGUME; MOLECULAR ANALYSIS; ONTOGENY; SCANNING ELECTRON MICROSCOPY;

ANGIOSPERM; ARTICLE; CLASSIFICATION; FLOWER; HISTOLOGY; LEGUME; POLYGALACEAE; SCANNING ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ANGIOSPERMS; FABACEAE; FLOWERS; MICROSCOPY, ELECTRON, SCANNING; POLYGALACEAE;

EUROSIDS I; FABACEAE; FABALES; POLYGALACEAE; QUILLAJA; QUILLAJACEAE; SURIANA; SURIANACEAE;

EID: 36448948332     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcm228     Document Type: Article

References (118)

1. APG. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: 399-436.
2. Bamert U. 1990. Aspekte der Struktur, Funktion und Diversität der Blüten bei Polygalaceae. PhD thesis, Zurich University, Zurich.
3. Bate-Smith EC 1965. Investigation of the chemistry and taxonomy of subtribe Quillajeae of the Rosaceae using comparisons of fresh and herbarium material. Phytochemistry 4: 535-539.
4. Bateman RM. 1999. Integrating molecular and morphological evidence of evolutionary radiations. In: Hollingsworth PM, Bateman RM, Gornall RJ, eds. Molecular systematics and plant evolution. London: Taylor & Francis, 432-471.
5. Bateman RM, DiMichele WA. 2002. Generating and filtering major phenotypic novelties: neoGoldschmidtian saltation revisited. In: Cronk QCB, Bateman RM, Hawkins JA, eds. Developmental genetics and plant evolution. London: Taylor & Francis, 109-159.
6. Behnke HD, Kiritsis U, Patrick SJ, Kenneally KF. 1996. Form-Pfs plastids, stem anatomy and systematic affinities of Stylobasium Desf. (Stylobasiaceae). A contribution of the knowledge of sieve-element plastids in the Rutales and Sapindales. Botanical Acta 109: 346-359.
7. Bernhard A, Endress PK. 1999. Androecial development and systematics of Flacourtiaceae s.l. Plant Systematics and Evolution 215: 141-155.
8. Bruneau A, Klitgaard BB, Fougere-Danezan M, Tucker SC. 2005. Phylogenetic analysis of floral ontogenetic and molecular characters in Caesalpinioideae: insights into floral evolution in the basal Leguminosae. XVII International Botanical Congress, Vienna, Austria: 201.
9. Caris PL, Smets E. 2004. A floral ontogenetic study on the sister group relationship between the genus Samolus (Primulaceae) and the Theophrastaceae. American Journal of Botany 91: 627-643.
10. Caris PL, Ronse de Craene LP, Smets E, Clinckemaillie D. 2000. Floral development of three Maesa species, with special emphasis on the position of the genus within Primulales. Annals of Botany 86: 87-97.
11. Caris PL, Ronse de Craene LP, Smets E, Clinckemaillie D. 2002. The uncertain systematic position of Symplocos (Symplocaceae): evidence from a floral ontogenetic study. International Journal of Plant Sciences 163: 67-74.
12. Chase MW, Soltis DE, Olmstead RG, Morgan D, Les DH, Mishler BD, et al. 1993. Phylogenetics of seed plants: an analysis of nucleotide sequences from the plastid gene rbcL. Annals of the Missouri Botanical Garden 80: 528-580.
13. Claßen-Bockhoff R, Speck T, Tweraser E, Wester P, Thimm S, Reith M. 2004. The staminal lever mechanism in Salvia (Lamiaceae): a key innovation for adaptive radiation? Organisms, Diversity and Evolution 4: 189-205.
14. Claxton F, Banks H, Klitgaard BB, Crane PR. 2005. Pollen morphology of families Quillajaceae and Surianaceae (Fabales). Review of Paleobotany and Palynology 133: 221-233.
15. Crayn DM, Fernando ES, Gadeck PA, Quinn CJ. 1995. A reassessment of the familial affinity of the Mexican genus Recchia Mocino & Sessé ex DC. Brittonia 47: 397-402.
16. Cronquist A. 1981. An integrated system of classification of flowering plants. New York: Columbia University Press.
17. Cronquist A. 1983. Some realignments in the dicotyledons. Nordic Journal of Botany 3: 75-83.
18. Dahlgren RMT. 1980. A revised system of classification of the angiosperms. Botanical Journal of the Linnean Society 80: 91-124.
19. Dahlgren RMT. 1988. Rhizophoraceae and Anisophyllaceae: summary statement, relationships. Annals of the Missouri Botanical Garden 75: 1259-1277.
20. Daniel P, Umamaheswari P, Sampath Kumar K. 1997. Observations on the distribution of the rare Suriana maritima L. (Surianaceae) in the Gulf of Mannar biosphere reserve, Southern India. Bulletin of the Botanical Survey of India 39: 149-156.
21. Donoghue MJ, Sanderson MJ. 1992. The suitability of molecular and morphological evidence in reconstructing plant phylogeny. In: Soltis PS, Soltis DE, Doyle JJ, eds. Molecular systematics of plants. London: Chapman and Hall, 340-368.
22. Eckert G. 1966. Entwicklungsgeschichtliche und blütenanatomische Untersuchungen zum Problem der Obdiplostemonie. Botanische Jahrbücher für Systematik 85: 523-604.
23. Edman G. 1936. Zur Verkieselung und Systematik der Simaroubaceae. Svensk Botanisk Tidskrift 30: 491-514.
24. Eichler AW. 1875. Blüthendiagramme. Leipzig: W. Engelmann.
25. Endress PK. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge: Cambridge University Press.
26. Endress PK. 1999. Symmetry in flowers: diversity and evolution. International Journal of Plant Sciences 160: S3-S23.
27. Endress PK, Friis EM. 2006. Rosids - Reproductive structures, fossil and extant, and their bearing on deep relationships: introduction. Plant Systematics and Evolution 260: 83-85.
28. Endress PK, Matthews ML. 2006. First steps towards a floral structural characterization of the major rosid subclades. Plant Systematics and Evolution 260: 223-251.
29. Endress PK, Stumpf S. 1991. The diversity of the stamen structures in "Lower" Rosidae (Rosales, Fabales, Proteales, Sapindales). Botanical Journal of the Linnean Society 107: 217-293.
30. Erbar C, Porembski S, Leins P. 2005. Contributions to the systematic position of Hydrolea (Hydroleaceae) based on floral development. Plant Systematics and Evolution 252: 71-83.
31. Eriksen B. 1993. Floral anatomy and morphology in the Polygalaceae. Plant Systematics and Evolution 186: 17-32.
32. Eriksen B, Persson C. 2007. Polygalaceae. In: Kubitzki K, ed. The families and genera of vascular plants. Berlin: Springer-Verlag, 345-363.
33. Evans RC, Dickinson TA. 1999a. Floral ontogeny morphology in subfamily Spiraeoideae Endl. (Rosaceae). International Journal of Plant Sciences 160: 981-1012.
34. Evans RC, Dickinson TA. 1999b. Floral ontogeny morphology in subfamily Amygdaloideae T. & G. (Rosaceae). International Journal of Plant Sciences 160: 955-979.
35. Evans RC, Dickinson TA. 2005. Floral ontogeny and morphology in Gillenia ("Spiraeoideae") and subfamily Maloideae C. Weber (Rosaceae). International Journal of Plant Sciences 166: 427-447.
36. Eyde RH. 1975. The bases of angiosperm phylogeny: floral anatomy. Annals of the Missouri Botanical Garden 62: 521-537.
37. Fehrenbach S, Barthlott W. 1988. Mikromorphologie der Epicuticular-Wachse der Rosales s.l. und deren systematische Gliederung. Botanische Jahrbücher für Systematik 109: 407-428.
38. Fernando ES, Quinn CJ. 1992. Pericarp anatomy and systematics of Simaroubaceae sensu lato. Australian Journal of Botany 40: 263-289.
39. Fernando ES, Gadeck PA, Crayn DM, Quinn CJ. 1993. Rosid affinities of Suriananceae: molecular evidence. Molecular Phylogenetics and Evolution 2: 344-350.
40. Fuks R. 1983. O genero Quillaja Molina (Rosaceae) no Brasil. Arquivos do Jardim Botânico do Rio de Janeiro 26: 61-67.
41. Goldblatt P. 1976. Cytotaxonomic studies in the tribe Quillajeae (Rosaceae). Annals of the Missouri Botanical Garden 63: 200-206.
42. Guo S, Kenne L, Lundgren LN, Rönnberg B, Sundquist BG. 1998. Triterpenoid saponins from Quillaja saponaria. Phytochemistry 48: 175-180.
43. Gutzwiller MA. 1961. Die phylogenetische Stellung von Suriana maritima L. Botanische Jahrbücher für Systematik 81: 1-49.
44. von Hagen KB, Kadereit JW. 2003. The diversification of Halenia (Gentianaceae): ecological opportunity versus key innovation. Evolution 57: 2507-2518.
45. van Heel WA. 1993. Floral ontogeny of Archidendron lucyi (Mimosaceae), with remarks on Amherstia nobilis (Caesalpiniaceae). Botanische Jahrbücher für Systematik 109: 17-23.
46. Heilbuth JC. 2000. Lower species richness in dioecious clades. The American Naturalist 156: 221-241.
47. Heo K, Tobe H. 1994. Embryology and relationships of Suriana maritima L. (Surianaceae). Journal of Plant Research 107: 29-37.
48. Herendeen P, Lewis G, Bruneau A. 2003. Floral morphology in caesalpinioid legumes: testing the monophyly of the "Umtiza clade". International Journal of Plant Sciences 164: S393-S407.
49. Jäger-Zürn I, Mathew CJ. 2002. Cupule structure of Dalzellia ceylanica and Indotristicha ramosissima (Podostemaceae). Aquatic Botany 72: 79-91.
50. Janzen DH. 1989. Natural history of a wind pollinated Central American legume tree (Ateleia herbert-smithii). In: Stirton CH, Zarucchi JL, eds. Advances in legume biology. Monographs in Systematic Botany from the Missouri Botanical Garden, 293-376.
51. Juàrez-Sierra C. 1988. Surianaceae. In: Flora de Veracruz, No. 58. Xalapa, Veracruz: Instituto Nacional de Investigaciones sobre Recursos Biòticos.
52. Kay KM, Voelckel C, Yang JY, Hufford KM, Kaska DD, Hodges SA. 2006. Floral characters and species diversification. In: Harder LD, Barret SCH, eds. Ecology and evolution of flowers. New York: Oxford University Press, 311-325.
53. Kim YJ, Wang PF, Navarro-Villalobos M, Rohde BD, Derryberry J, Gin DY. 2006. Synthetic studies of complex immunostimulants from Quillaja saponaria: synthesis of the potent clinical immunoadjuvant QS-21A(api). Journal of the American Chemical Society 128: 11906-11915.
54. Klitgaard BB. 1999. Floral ontogeny in tribe Dalbergieae (Leguminosae: Papilionoideae): Dalbergia brasiliensis, Machaerium villosum s. l., Platymiscium floribundum, and Pterocarpus rotundifolius. Plant Systematics and Evolution 219: 1-25.
55. Kruger H, van der Merwe MJ, Robbertse PJ. 1988. Floral organogenesis in Securidaca longepedunculata and Polygala virgata var. decora (Polygalaceae). South African Journal of Science 84: 308-313.
56. Kubitzki K. 2007. Quillajaceae. In: Kubitzki K, ed. The families and genera of vascular plants IX. Berlin: Springer-Verlag, 407-408.
57. Lewis GP, Simpson BB, Neff JL. 2000. Progress in understanding the reproductive biology of the Caesalpinioideae (Leguminosae). In: Herendeen PS, Bruneau A, eds. Advances in legume systematics 9. Kew: Royal Botanic Gardens, 65-78.
58. Lewis GP, Schrire B, Mackinder B, Lock M. 2005. Legumes of the world. Kew: Royal Botanic Gardens.
59. Li RQ, Chen ZD, Lu AM. 2005. Organogenesis of the inflorescence and flowers in Platycarya strobilacea (Juglandaceae). International Journal of Plant Sciences 166: 449-457.
60. Loesener T, Solereder H. 1905. Ueber die bisher wenig bekannte südmexikanische Gattung Rigiostachys. Verhandlungen des Botanischen Vereins der Provinz Brandenburg 47: 3-62.
61. Matthews ML, Endress PK. 2002. Comparative floral structure and systematics in Oxalidales (Oxalidaceae, Connaraceae, Brunelliaceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Tremandraceae). Botanical Journal of the Linnean Society 140: 321-381.
62. Matthews ML, Endress PK. 2004. Comparative floral structure and systematics in Cucurbitales (Corynocarpaceae, Coriariaceae, Tetramelaceae, Datiscaceae, Begoniaceae, Cucurbitaceae, Anisophylleaceae). Botanical Journal of the Linnean Society 145: 129-185.
63. Matthews ML, Endress PK. 2005. Comparative floral structure and systematics in Celastrales (Celastraceae, Parnassiaceae, Lepidobotryaceae). Botanical Journal of the Linnean Society 149: 129-194.
64. Matthews ML, Endress PK. 2006. Floral structure and systematics in four orders of Rosids, including a broad survey of floral mucilage cells. Plant Systematics and Evolution 260: 199-221.
65. Matthews ML, Endress P, Schönenberger J, Friis EM. 2001. A comparison of floral structures of Anisopylleaceae and Cunoniaceae and the problem of their systematic position. Annals of Botany 88: 439-455.
66. Medan D, Hilger HH. 1992. Comparative flower and fruit morphogenesis in Colubrina (Rhamnaceae) with special reference to C. asiatica. American Journal of Botany 79: 809-819.
67. van der Meijden R. 1982. Systematics and evolution of Xanthophyllum (Polygalaceae). Leiden: Leiden University Press.
68. Merino Sutter D, Endress PK. 2003. Female flower and cupule structure in Balanopaceae, an enigmatic rosid family. Annals of Botany 92: 459-469.
69. Mitchell RE, Geismann TA. 1971. Constituents of Suriana maritima: a triterpene diol of novel structure and a new flavonol glycoside. Phytochemistry 10: 1559-1567.
70. Morgan D, Soltis DE, Robertson KR. 1994. Systematic and evolutionary implications of the rbcL sequence variation in Rosaceae. American Journal of Botany 81: 890-903.
71. Nelson G. 1978. Ontogeny, phylogeny, paleontology, and the biogenetic law. Systematic Zoology 27: 324-345.
72. Nooteboom HP. 1966. Flavonols, leuco-anthocyanins, cinnamic acids and alkaloids in dried leaves of some Asiatic and Malesian Simaroubaceae. Blumea 14: 309-315.
73. Okamoto M, Kosuge K, Fukuoka N. 1992. Pistil development and parietal placentation in the pseudomonomerous ovary of Zelkova serrata (Ulmaceae). American Journal of Botany 79: 921-927.
74. Pennington RT, Klitgaard BB, Ireland H, Lavin M. 2000. New insights into floral evolution of basal Papilionoideae from molecular phylogenies. In: Herendeen PS, Bruneau A, eds. Advances in legume systematics 9. Kew: Royal Botanic Gardens, 233-248.
75. Prance GT. 1965. The systematic position of Stylobasium Desf. Bulletin du Jardin Botanique de L'État, Bruxelles 35: 435-448.
76. Prenner G. 2004a. The asymmetric androecium in Papilionoideae (Leguminosae): definition, occurrence, and possible systematic value. International Journal of Plant Sciences 165: 499-510.
77. Prenner G. 2004b. Floral development in Polygala myrtifolia (Polygalaceae) and its similarities with Leguminosae. Plant Systematics and Evolution 249: 67-76.
78. Ree RH. 2005. Detecting the historical signature of key innovations using stochastic models of character evolution and cladogenesis. Evolution 59: 257-265.
79. Ronse de Craene LP, Miller AG. 2004. Floral development and anatomy of Dirachma socotrana (Dirachmaceae): a controversial member of the Rosales. Plant Systematics and Evolution 249: 111-127.
80. Ronse de Craene LP, Smets EF. 1991. Androecium and floral nectaries of Harungana madagascariensis (Clusiaceae). Plant Systematics and Evolution 178: 179-194.
81. Ronse de Craene LP, Smets EF. 1994. Merosity in flowers: definition, origin, and taxonomic significance. Plant Systematics and Evolution 191: 83-104.
82. Ronse de Craene LP, Smets EF. 1995. The distribution and systematic relevance of the androecial character oligomery. Botanical Journal of the Linnean Society 118: 193-247.
83. Ronse de Craene LP, Smets EF. 1998. Meristic changes in gynoecium morphology, exemplified by floral ontogeny and anatomy. In: Owens SJ, Rudall PJ, eds. Reproductive biology. Kew: Royal Botanic Gardens, 85-112.
84. Ronse de Craene LP, Smets EF. 2001. Floral developmental evidence for the systematic relationship of Tropaeolum (Tropaeolaceae). Annals of Botany 88: 879-892.
85. Ronse de Craene LP, Linder HP, Smets EF. 2000. The questionable relationship of Montinia (Montiniaceae): evidence from a floral ontogenetic and anatomical study. American Journal of Botany 87: 1408-1424.
86. Rozefelds AC, Drinnan AN. 2002. Ontogeny of pistillate flowers and inflorescences in Nothofagus subgenus Lophozonia (Nothofagaceae). Plant Systematics and Evolution 233: 105-126.
87. Sanderson MJ, Donoghue MJ. 1994. Shifts in diversification rate with the origin of angiosperms. Science 264: 1590-1593.
88. Sargent RD. 2004. Floral symmetry affects speciation rates in angiosperms. Proceedings of The Royal Society of London B 271: 603-608.
89. Savolainen V, Chase MW, Hoot SB, Morton CM, Soltis DE, Bayer C, et al. 2000a. Phylogenetics of flowering plants based upon a combined analysis of plastid atpB and rbcL gene sequences. Systematic Biology 49: 306-362.
90. Savolainen V, Fay MF, Albach DC, Blacklund A, van der Bank M, Cameron KM, et al. 2000b. Phylogeny of eudicots: a nearly complete familial analysis based on rbcL gene sequences. Kew Bulletin 55: 257-309.
91. Schneider JV. 2007. Surianaceae. In: Kubitzki K, ed. The families and genera of vascular plants IX. Berlin: Springer-Verlag, 449-455.
92. Schönenberger J, von Balthazar M. 2006. Reproductive structures and phylogenetic framework of the rosids - progress and prospects. Plant Systematics and Evolution 260: 87-106.
93. Sheahan MC. 2007. Zygophyllaceae. In: Kubitzki K, ed. The families and genera of vascular plants IX. Berlin: Springer-Verlag, 488-500.
94. Simpson BB. 2007. Krameriaceae. In: Kubitzki K, ed. The families and genera of vascular plants IX. Berlin: Springer-Verlag, 208-212.
95. Soltis PS, Soltis DE. 2004. The origin and diversification of angiosperms. American Journal of Botany 91: 1614-1626.
96. Soltis DE, Soltis PS, Morgan DR, Swensen SM, Mullin BC, Dowd JD, Martin PG. 1995. Chloroplast gene sequence data suggest a single origin of the predisposition for symbiotic nitrogen fixation in angiosperms. Proceedings of the National Academy of Sciences USA 92: 2647-2651.
97. Soltis DE, Soltis PS, Nickrent D, Johnson LA, Hahn WH, Hoot SB, et al. 1997. Angiosperm phylogeny inferred from 18S ribosomal DNA sequences. Annals of the Missouri Botanical Garden 84: 1-49.
98. Sterling C. 1966. Comparative morphology of the carpel in the Rosaceae. IX. Spiraeoideae: Quillajaeae, Sorbarieae. American Journal of Botany 53: 951-960.
99. Suzuki H, Achnine L, Xu R, Matsuda SPT, Dixon RA. 2002. A genomics approach to the early stages of triterpene saponin biosynthesis in Medicago truncatula. Plant Journal 32: 1033-1048.
100. Takhtajan A. 1997. Diversity and classification of flowering plants. New York: Columbia University Press.
101. Thorne RF. 1992. Classification and geography of the flowering plants. Botanical Review 58: 225-348.
102. Tucker SC. 1987. Floral initiation and development in legumes. In: Stirton CH, ed. Advances in legume systematics 3. Kew: Royal Botanic Gardens, 183-279.
103. Tucker SC. 1991. Helical floral organogenesis in Gleditsia, a primitive caesalpinioid legume. American Journal of Botany 78: 1130-1149.
104. Tucker SC. 1992. The developmental basis for sexual expression in Ceratonia siliqua (Leguminosae: Caesalpinioideae: Cassieae). American Journal of Botany 79: 318-327.
105. Tucker SC. 1998. Floral ontogeny in legume genera Petalostylis, Labichea, and Dialum (Caesalpinioideae: Cassieae), a series in floral reduction. American Journal of Botany 85: 184-208.
106. Tucker SC. 1999. Evolutionary lability of symmetry in early floral development. International Journal of Plant Sciences 160: S25-S39.
107. Tucker SC. 2000a. Floral development and homeosis in Saraca (Leguminosae: Caesalpinioideae: Detarieae). International Journal of Plant Sciences 161: 537-549.
108. Tucker SC. 2000b. Floral development in tribe Detarieae (Leguminosae: Caesalpinioideae): Amherstia, Brownea, and Tamarindus. American Journal of Botany 87: 1385-1407.
109. Tucker SC. 2001a. The ontogenetic basis for missing petals in Crudia (Leguminosae: Caesalpinioideae: Detarieae). International Journal of Plant Sciences 162: 83-89.
110. Tucker SC. 2001b. Floral development in Schotia and Cynometra (Leguminosae: Caesalpinioideae: Detarieae). American Journal of Botany 88: 1164-1180.
111. Tucker SC. 2002a. Floral ontogeny of Cercis (Leguminosae: Caesalpinioideae: Cercideae): does it show convergence with papilionoids? International Journal of Plant Sciences 163: 75-87.
112. Tucker SC. 2002b. Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). 1. Radially symmetrical taxa lacking organ suppression. American Journal of Botany 89: 875-887.
113. Tucker SC. 2003. Comparative floral ontogeny in Detarieae (Leguminosae: Caesalpinioideae). III. Adaxially initiated whorls in Julbernardia and Sindora. International Journal of Plant Sciences 164: 275-286.
114. Tucker SC, Douglas AW. 1994. Ontogenetic evidence and phylogenetic relationships among basal taxa of legumes. In: Ferguson IK, Tucker S, eds. Advances in legume systematics 6: structural botany. Kew: Royal Botanic Gardens, 11-32.
115. Tucker SC, Kantz KE. 1997. Comparative floral development and evolution in tribe Caesalpinieae (Leguminosae: Caesalpinioideae). Haematoxylum. American Journal of Botany 84: 1047-1063.
116. Tucker SC, Stirton CH. 1991. Development of the cymose inflorescence, cupulum and flower of Psoralea pinnata (Leguminosae: Papilionoideae). Botanical Journal of the Linnean Society 106: 209-227.
117. Weberling F. 1989. Structure and evolutionary tendencies of inflorescences in the Leguminosae. In: Stirton CH, Zarucchi JL, eds. Advances in legume biology. St. Louis, MO: Monographs in Systematic Botany from the Missouri Botanical Garden, 35-58.
118. Zhang SY. 1992. Systematic wood anatomy of the Rosaceae. Blumea 37: 81-158.