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Stigma Diversity in Tropical Legumes with Considerations on Stigma Classification

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Abstract

The great stigma diversity in angiosperms implies a choice of criteria for stigma classification, which nowadays is characterized as dry (= little or no secretory surface and exudate retained by the cuticle and/or protein pellicle), wet (= conspicuous secretory surface, abundant in fluid exudate) and semidry (exudate retained by cuticle and/or protein pellicle). Despite being a very species-rich family, whose representatives exhibit a wide floral variation, no comparative studies of stigma diversity have been done for the whole Leguminosae. In order to assess the stigma morphological diversity in legumes and to evaluate the criteria used in the main classifications of the stigma, we compared the stigma morphology in 15 distinct legume lineages. In addition, we evaluated the stigma classification in other 152 legume species whose morphology was already described in the literature. Stigmas were removed from floral buds and flowers and processed for analyses under scanning electron and light microscopes. The stigma of the study legumes exhibits quite variable morphology, mainly concerning the diameter, the occurrence of an orifice or a furrow, the coating, the cellular composition, and the occurrence, chemical nature and release mechanism of the exudate. This diversity appears to be related mainly to the evolutionary history of the group and also to the selective pressures exerted by different types of pollen and pollinator. More conflicting criteria for stigma classification lie in defining the semidry type, found mostly in papilionoids. For better stigma classification we suggest that stigma morphology be evaluated at the time prior to anthesis, when the cuticle is not yet broken and the exudate is not exposed or drained. In addition, several techniques should be employed for a better classification.

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Literature Cited

  • Agostini, K. & M. Sazima. 2003. Plantas ornamentais e seus recursos para abelhas no campus da Universidade Estadual de Campinas, estado de São Paulo, Brasil. Bragantia 62: 335–343.

    Google Scholar 

  • Andreata, R. H. P., H. C. Lima, A. S. F. Vaz, J. F. A. Baumgratz & S. R. Profice. 2008. Diversity and floristic composition of the vascular plants in the Forest fragment in southeastern Rio de Janeiro, Brazil. Journal of the Botanichal Research Institute of Texas 2: 575–592.

    Google Scholar 

  • Arceo-Gómez, G., M. L. Martínez, V. Parra-Tabla & J. G. García-Franco. 2011. Anther and stigma morphology in mirror-image flowers of Chamaecrista chamaecristoides (Fabaceae): implications for buzz pollination. Plant biology 13(Suppl. 1): 19–24.

    PubMed  Google Scholar 

  • Arroyo, M. T. K. 1981. Breeding systems and pollination biology in Leguminosae. Pp 723–769. In: R. M. Polhill & P. H. Raven (eds). Advances in Legume Systematic, part 2. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Baird, L. M., M. J. Turano & B. D. Webster. 1988. Ultrastructure and histochemical characteristics of stigma of Cicer arietinum. American Journal of Botany 75: 551–557.

    Google Scholar 

  • Baker, H. G. & B. J. Harris. 1957. The pollination of Parkia by bats and its attendant evolucionary problems. Evolution 11: 449–460.

    Google Scholar 

  • Barrett, S. C. H. 2003. Mating strategies in flowering plants: the outcrossing-selfing paradigm and beyond. Philosophycal Transactions of The Royal Society of London B 358: 991–1004.

    Google Scholar 

  • Basso-Alves, J. P., K. Agostini & S. P. Teixeira. 2011. Pollen and stigma morphology of some Phaseoleae species (Leguminosae) with different pollinators. Plant Biology 13: 602–610.

    CAS  PubMed  Google Scholar 

  • Bawa, K. S. 1974. Breeding systems of tree species of a lowland tropical community. Evolution 28: 85–92.

    Google Scholar 

  • ———, D. R. Perry & J. H. Beach. 1985. Reproductive biology of tropical lowland rain forest trees. I. Sexual systems and incompatibility mechanisms.

  • Beck, C. B. 2005. An introduction to plant structure and development. Cambridge University Press, Cambridge.

    Google Scholar 

  • Bell, J. & G. Hicks. 1976. Transmitting tissue in the pistil of Tobacco. Light and electron microscopic observations. Planta 131: 187–200.

    CAS  Google Scholar 

  • Boff, S. V. 2008. Flora de capões e hymenoptera (abelhas e vespas) visitantes de flores no pantanal do miranda-abobral. Dissertação, Universidade Federal de Mato Grosso do Sul, Campo Grande.

  • Borges, L. A., M. S. Sobrinho & A. V. Lopes. 2009. Phenology, pollination, and breeding system of the threatened tree Caesalpinia echinata Lam. (Fabaceae), and review of studies on the reproductive biology in the genus. Flora 204: 111–130.

    Google Scholar 

  • Bortoluzzi, R. L. C. 2000. Papilionoideae (Leguminosae) no Parque Estadual do Rio Doce, Minas Gerais. Dissertação, Universidade Federal de Viçosa, Viçosa.

  • Brink, R. A. & D. C. Cooper. 1936. The mechanism of pollination in Alfavaca (Medicago sativa). American Journal of Botany 23: 678–683.

    Google Scholar 

  • Capus, M. G. 1878. Anatomie du tissu conducteur. Annales des Sciences Naturelles 7: 207–291.

    Google Scholar 

  • Carmo-Oliveira, R. & B. L. Morretes. 2009. Stigmatic surface in the Vochysiaceae: reproductive and taxonomic implications. Acta Botanica Brasilica 23: 780–785.

    Google Scholar 

  • Carvalho, C. A. L. & L. C. Marchini. 1999. Tipos polínicos coletados por Nannotrigona testaceicornis e Tetragonisca angustula (Hymenoptera, Apidae, Meliponinae). Scientia Agricola 6: 717–722.

    Google Scholar 

  • Ciampolini, F., K. R. Shivanna & M. Cresti. 2001. Organization of the stigma and transmitting tissue of rice, Oryza sativa (L.). Plant Biology 3: 149–155.

    Google Scholar 

  • Cocucci, A. E. & J. E. A. Mariath. 2004. Gametogênese, fecundação, seleção do gametófito mais apto, embriogênese e diásporo maduro. Pp 17–30. In: A. G. Ferreira & F. Borghetti (eds). Germinação. Do básico ao aplicado. Artmed, Porto Alegre.

    Google Scholar 

  • Dulberger, R., M. B. Smith & K. S. Bawa. 1994. The stigmatic orifice in Cassia, Senna, and Chamaecrista (Caesalpiniaceae): morphological variation, function during pollination, and possible adaptive significance. American Journal of Botany 81: 1390–1396.

    Google Scholar 

  • Dumas, C., M. Rougier, P. Zandonella, F. Ciampolini, M. Cresti & E. Pacini. 1978. The secretory stigma in Lycopersicum peruvianum Mill.: ontogenesis and glandular activity. Protoplasma 96: 173–187.

    Google Scholar 

  • ——— 1978. Stigmates sécréteurs et lipids neutres sécrétés. Bulletin de la Société Botanique de France, Actualités Botaniques 1–2: 61–68.

    Google Scholar 

  • Dunphy, B. K., J. L. Hamrick & J. Schwagerl. 2004. A comparision of direct and indirect measures of gene flow in the bat-pollinated tree Hymenaea courbaril in the dry forest life zone of southwestern Puerto Rico. International Journal of Plant Science 165: 427–436.

    CAS  Google Scholar 

  • Edlund, A. F., R. Swanson & D. Preuss. 2004. Pollen and stigma structure and function: the role of diversity in pollination. The Plant Cell 16: S84–S97.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Endress, P. K. 1994. Diversity and evolutionary biology of tropical flowers. Cambridge University Press.

  • Etcheverry, A. V., M. M. Alemán & T. F. Fleming. 2008. Flower morphology, pollination biology and mating system of complex flower of Vigna caracalla (Fabaceae: Papionoideae). Annals of Botany 102: 305–316.

    PubMed Central  PubMed  Google Scholar 

  • ———, ———, T. Fuigueroa-Fleming, C. A. Gómez & D. López-Spahr. 2010. Anther-stigma separation in Desmodium species (Papilionoideae-Fabaceae) from northwestern Argentina. Acta Horticulturae (ISHS) 918: 183–188.

    Google Scholar 

  • ———, ———, ———, D. López-Spahr, C. A. Gómez, C. Yañes, D. M. Figueroa-Castro & P. Ortega-Baes. 2011. Pollen:ovule ratio and its relationship with other floral traits in Papilionoideae (Leguminosae): an evaluation with Argentine species. Plant Biology 14: 171–178.

    PubMed  Google Scholar 

  • ———, J. J. Protomastro & C. Westerkamp. 2003. Delayed autonomous self-pollination in the colonizer Crotalaria micans (Fabaceae: Papilionoideae): structural and functional aspects. Plant Systematics and Evolution 239: 15–28.

    Google Scholar 

  • Fahn, A. 1979. Secretory tissues in plants. Academic, London.

    Google Scholar 

  • ——— 1990. Plant Anatomy, ed. 4th. Butterworth Heinemann, Jerusalem.

    Google Scholar 

  • Fisher, D. B. 1968. Protein staining of ribboned epon section for light microscopy. Histochemie 16: 92–96.

    CAS  PubMed  Google Scholar 

  • Fleming, T. H., C. Geiselman & W. J. Kress. 2009. The evolution of bat pollination: a phylogenetic perspective. Annals of Botany 104: 1017–1043.

    PubMed Central  PubMed  Google Scholar 

  • Flores, A. S. & R. S. Rodrigues. 2010. Diversidade de Leguminosae em uma área de Savana do estado de Roraima, Brasil. Acta Botanica Brasilica 24: 175–183.

    Google Scholar 

  • Galloni, M., L. Podda, D. Vivarelli & G. Cristofolini. 2007. Pollen presentation, pollen-ovule ratios, and other reproductive traits in Mediterranean Legumes (Fam. Fabaceae - Subfam. Faboideae). Plant Systematics and Evolution 266: 147–164.

    Google Scholar 

  • Gavilanes, M. L. & C. N. D’Angieri Filho. 1991. Flórula ruderal da cidade de Lavras, MG. Acta Botanica Brasilica 5: 77–88.

    Google Scholar 

  • Gemmill-Herren, B. 2007. Indigofera in Kenya. Pp 43–45. In: C. Eardley, B. Gemmill-Herren, M. Gikungu, R. Kagoiya, W. Kinuthia, P. Kwapong, D. Martins, G. Njoroge, & L. Njoroge (eds). Crops, Browse and Pollinators in Africa: An Initial Stock-Taking. Food and Agricultural Organization of the United Nations, Rome.

    Google Scholar 

  • Gibbs, P. & M. B. Bianchi. 1999. Does late-acting self-incompatibility (LSI) show family clustering? Two more species of Bignoniaceae with LSI: Dolichandra cynanchoides and Tabebuia nodosa. Annals of Botany 84: 449–457.

    Google Scholar 

  • ———, P. E. Oliveira & M. B. Bianchi. 1999. Postzygotic control of selfing in Hymenaea stigonocarpa (Leguminosae-Caesalpinioideae), a bat-pollinated tree of the Brazilian cerrados. International Journal of Plant Science 160: 72–78.

    Google Scholar 

  • ——— & R. Sassaki. 1998. Reproductive biology of Dalbergia miscolobium Benth. (Leguminosae-Papilionoideae) in SE Brazil: The effects of pistillate sorting on fruit. Annals of Botany 81: 735–740.

    Google Scholar 

  • Gerrits, P. 1991. The application of glycol methacrylate in histotechnology; some fundamental principles. Department of Anatomy and Embryology, State University Groningen, Netherlands.

    Google Scholar 

  • Ghosh, S. & K. R. Shivanna. 1982. Anatomical and cytochemical studies on the stigma and style in some legumes. Botanical Gazette 143: 311–318.

    Google Scholar 

  • Gifford, E. M. & A. S. Foster. 1989. Morphology and evolution of vascular plants. WH Freeman and company, New York.

    Google Scholar 

  • Greissl, R. 2006. Ontogeny of Calliandra - massulae (Mimosaceae: Ingeae), and the associated viscin body. Flora 201: 570–587.

    Google Scholar 

  • Hartig, T. 1842. New theory of the fertilization of plants. Collegium Carolinum, Brunswick.

    Google Scholar 

  • Heenan, P. B. 1998. The pollination system and stigmatic cuticle of Clianthus puniceus (Fabaceae). New Zealand Journal of Botany 36: 311–314.

    Google Scholar 

  • Heslop-Harrison, J. & Y. Heslop-Harrison. 1983. Pollen-stigma interaction in the Leguminosae: the organization of the stigma in Trifolium pratense L. Annals of Botany 51: 571–583.

    Google Scholar 

  • Heslop-Harrison, Y. 1981. Stigma characteristics and angiosperm taxonomy. Nordic Journal of Botany 1: 401–420.

    Google Scholar 

  • Heslop-Harrison, Y. 2000. Control gates and micro-ecology: the pollen-stigma interactions in perspective. Annals of Botany 85: 5–13.

  • ———, J. Heslop-Harrison & K. R. Shivanna. 1981. Heterostyly in Primula. 1. Fine-structural and cytochemical features of the stigma and style in Primula vulgaris Huds. Protoplasma 107: 171–187.

    Google Scholar 

  • ——— & K. R. Shivanna. 1977. The receptive surface of the angiosperm stigma. Annals of Botany 41: 1233–1258.

    Google Scholar 

  • Hiscock, S. J. 2000. Self-incompatibility in Senecio squalidus L. (Asteraceae). Annals of Botany 85: 181–190.

    CAS  Google Scholar 

  • ———, K. Hoedemaekers, W. E. Friedman & H. G. Dickinson. 2002. The stigma surface and pollen-stigma interactions in Senecio squalidus L. (Asteraceae) following cross (compatible) and self (incompatible) pollinations. International Journal of Plant Sciences 163: 1–16.

    Google Scholar 

  • ——— & S. M. McInnis. 2003. The diversity of self-incompatibility systems in flowering plants. Plant Biology 5: 23–32.

    CAS  Google Scholar 

  • Hopkins, H. C. 1984. Floral biology and pollination ecology of the Neotropical species of Parkia. Journal of Ecology 72: 1–23.

    Google Scholar 

  • Howel, G. J., A. T. Slater & R. B. Knox. 1993. Secondary pollen presentation in Angiosperms and its biological significance. Austranlian Journal of Botany 41: 417–438.

    Google Scholar 

  • Jacobi, C. M., M. Ramalho & M. Silva. 2005. Pollination biology of the exotic rattleweed Crotalaria retusa L. (Fabaceae) in NE Brazil. Biotropica 37: 357–363.

    Google Scholar 

  • Jensen, W. A. 1962. Botanical histochemistry: principles and practice. W.H. Freeman, San Francisco.

    Google Scholar 

  • Jobson, S., R. B. Knox, J. Kenrick & C. Dumas. 1983. Plastid development and ferritin content of stigmas of the Legumes Acacia, Lotus and Trifolium. Protoplasma 116: 213–218.

    CAS  Google Scholar 

  • Juncosa, A. M. & B. D. Webster. 1989. Pollination in Lupinus nanus subsp. latifolius (Leguminosae). American Journal of Botany 76: 59–66.

    Google Scholar 

  • Karnovsky, M. J. 1965. A formaldehyde-glutaraldehyde fixative of high osmolarity for use in eletron microscopy. Journal of Cell Biology 27: A137–A138.

    Google Scholar 

  • Kenrick, J. & R. B. Knox. 1981. Structure and histochemistry of the stigma and style of some Australian species of Acacia. Australian Journal of Botany 29: 733–745.

    Google Scholar 

  • Kiill, L. H. P. & M. A. Drumond. 2001. Biologia floral e sistema reprodutivo de Gliricidia sepium (Jacq.) Steud. (Fabaceae - Papilionoideae) na região de Petrolina, Pernambuco. Ciência Rural 31: 597–601.

    Google Scholar 

  • Kissmann, K. G. & D. Groth. 1999. Plantas infestantes e nocivas. Tomo II, ed. 2nd. BASF, São Bernardo do Campo.

    Google Scholar 

  • Knox, R. B., J. Kenrick, S. Jobson & C. Dumas. 1989. Reproductive function in the Mimosoid Legume Acacia retinodes: ultrastructural and cytochemical characteristics of stigma receptivity. Australian Journal of Botany 37: 103–124.

    Google Scholar 

  • Koptur, S. 1984. Outcrossing and pollinator limitation of fruit set: breeding systems of Neotropical Inga trees (Fabaceae: Mimosoideae). Evolution 38: 1130–1143.

    Google Scholar 

  • Kreitner, G. L. & E. L. Sorensen. 1984. Stigma development and stigmatic cuticle of Alfafa, Medicago sativa L. Botanical Gazette 145: 436–443.

    Google Scholar 

  • Ladd, P. G. 1994. Pollen presenters in the flowering plants - form and function. Botanical Journal of the Linnean Society 115: 165–195.

    Google Scholar 

  • Las Heras, M. A., P. J. Hidalgo & J. L. Ubera. 2001. Stigma cuticle in Hedysarum glomeratum: structure and function. International Journal of Developmental Biology 45: S41–S42.

    Google Scholar 

  • Lau, C. P. Y., R. M. K. Sauders & L. Ramsden. 2009. Floral biology, breeding systems and population genetic structure of three climbing Bauhinia species (Leguminosae: Caesalpinioideae) in Hong Kong, China. Journal of Tropical Ecology 25: 147–159.

    Google Scholar 

  • Lavin, M. & A. Delgado. 1990. Pollen brush of Papilionoideae (Leguminosae): morphological variation and systematic utility. American Journal of Botany 77: 1294–1312.

    Google Scholar 

  • Lersten, N. R. 2004. Flowering Plant Embryology. Blackwell Publishing, Ames.

    Google Scholar 

  • Lewis, G., B. Schrire, B. Mackinder & M. Lock. 2005. Legumes of the World. Royal Botanic Gardens, Kew.

    Google Scholar 

  • Lillie, R. D. 1954. Histopathologic technic and practical histochemistry. McGraw- Hill Book Co, New York.

    Google Scholar 

  • Llamas, K. A. 2003. Tropical flowering plants. A guide to identification and cultivation. Timber Press, Portland.

    Google Scholar 

  • Lloyd, D. G. & C. J. Webb. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms I. Dichogamy. New Zealand Journal of Botany 24: 135–162.

    Google Scholar 

  • López-Forment, W. 1985. Pollination of Hymenaea courbaril by frugivorous bats on the Pacific coast of Mexico. Acta Zoologica Fennica 173: 291–292.

    Google Scholar 

  • Lord, E. M. & Y. Heslop-Harrison. 1984. Pollen-stigma interaction in the Leguminosae: stigma organization and the breeding system in Vicia faba L. Annals of Botany. 54: 827–836.

    Google Scholar 

  • ——— & S. D. Russell. 2002. The mechanisms of pollination and fertilization in plants. Annual Review of Cell and Developmental Biology 18: 81–105.

    CAS  PubMed  Google Scholar 

  • ——— & B. D. Webster. 1979. The stigmatic exudate of Phaseolus vulgaris L. Botanical Gazette 140: 266–271.

    CAS  Google Scholar 

  • Lorenzi, H. 2002. Árvores brasileiras: manual de identificação e cultivo de plantas arbóreas nativas do Brasil. Plantarum, Nova Odessa.

    Google Scholar 

  • Maheshwari, P. 1950. An Introduction to the Embryology of Angiosperms. McGraw-Hill, New York.

    Google Scholar 

  • Marangon, L. C., J. J. Soares & A. L. P. Feliciano. 2003. Florística arbórea da Mata da Pedreira, município de Viçosa, Minas Gerais. Revista Árvore 27: 207–215.

    Google Scholar 

  • Marazzi, B., E. Conti & P. K. Endress. 2007. Diversity in anthers and stigmas in the buzz-pollinated genus Senna (Leguminosae, Cassiinae). International Journal of Plant Sciences 168: 371–391.

    Google Scholar 

  • Marques-Souza, A. C., I. P. A. Miranda, C. O. Moura, A. Rabelo & E. M. Barbosa. 2002. Características morfológicas e bioquímicas do pólen coletado por cinco espécies de melipolíneos da Amazônia central. Acta Amazonica 32: 217–229.

    CAS  Google Scholar 

  • Martins, M. A. G. & D. M. T. Oliveira. 2001. Morfo-anatomia e ontogênese do fruto e da semente de Tipuana tipu (Benth.) O. Kuntze (Fabaceae: Faboideae). Revista Brasileira de Botânica 24: 109–121.

    Google Scholar 

  • Maués, M. M., M. S. de Souza, M. Kanashiro. 2004. The importance of solitary bees on the reproductive biology of timber trees at the Tapajós National Forest, Brazil. In: B. M. Freitas & J. O. P. Pereira (orgs.). Solitaty bees - conservation, rearing and management for pollination (pp 241–254). Imprensa Universitária, Fortaleza.

  • Mcclure, B. A. & V. Franklin-Tong. 2006. Gametophytic self-incompatibility: understanding the cellular mechanisms involved in “self” pollen tube inhibition. Planta 224: 233–245.

    CAS  PubMed  Google Scholar 

  • Moço, M. C. C. & M. C. B. Pinheiro. 1999. Pollination ecology of Swartzia apetala Raddi var. apetala (Leguminosae-Papilionoideae). Brazilian Archives of Biology and Technology 42: 0–0.

  • Moreira, J. L. D. & A. M. G. A. Tozzi. 1997. Indigofera L. (Leguminosae, Papilionoideae) no estado de São Paulo, Brasil. Revista Brasileira de Botânica 20: 97–117.

    Google Scholar 

  • Munin, R. L., R. C. Teixeira & M. R. Sigrist. 2008. Esfingofilia e sistema de reprodução de Bauhinia curvula Benth. (Leguminosae: Caesalpinioideae) em cerrado no Centro-Oeste brasileiro. Revista Brasileira de Botânica 31: 15–25.

    Google Scholar 

  • Nasrallah, J. B. 2002. Recognition and rejection of self in plant reproduction. Science 296: 305–308.

    CAS  PubMed  Google Scholar 

  • ——— 2005. Recognition and rejection of self in plant self-incompatibility: comparisons to animal histocompatibility. Trends in Immunology 26: 412–418.

    CAS  PubMed  Google Scholar 

  • Nogueira-Neto, P. 2002. Management of plants to maintain and study pollinating bee species, and also to protect vertebrate frugivorous fauna. Pp 21–28. In: P. Kevan & V. L. Imperatriz Fonseca (eds). Pollinating Bees - The conservation link between agriculture and nature. Ministry of Environment, Brasília.

    Google Scholar 

  • O’Brien, T. P., N. Feder & M. E. McCully. 1964. Polychromatic staining of plant cell walls by Toluidine Blue O. Protoplasma 59: 368–373.

    Google Scholar 

  • ——— & M. E. McCully. 1981. The study of plants structure. Principles and selected methods. Thermarcarphy Ltd., Melbourne.

    Google Scholar 

  • Oliveira, M. C. P., I. D. K. Ferraz & G. J. Oliveira. 2006. Dispersão e superação da dormência de sementes de Parkia pendula (Willd.) Walp. (visgueiro) na Amazônia central, AM, Brasil. Hoehnea 33: 485–493.

    Google Scholar 

  • Owens, S. J. 1990. The morphology of the wet, non-papillate (WN) stigma form in the tribe Caesalpinieae (Caesalpinioideae: Leguminosae). Botanical Journal of the Linnean Society 104: 293–302.

    Google Scholar 

  • ——— & N. J. Horsfield. 1982. A light and electron microscopic study of stigmas in Aneilema and Commelina species (Commelinaceae). Protoplasma 112: 26–36.

    Google Scholar 

  • ——— & G. P. Lewis. 1989. Taxonomic and functional implications of stigma morphology in species of Cassia, Chamaecrista and Senna (Leguminosae, Caesalpinioideae). Plant Systematics and Evolution 163: 93–105.

    Google Scholar 

  • ——— & ———. 1996. Stigma morphology in the Leguminosae: The wet, papillate (WP) stigma in Caesalpinioideae. Kew Bulletin 51: 119–131.

    Google Scholar 

  • ———, C. Prychid & A. V. Cox. 1995. Structure and development of the stigma, style and ovary of Caesalpinia pulcherrima (L.) Sw., post-anthesis, pre- and post-pollination. Botanical Journal of the Linnean Society 118: 275–288.

    Google Scholar 

  • Pacini, E. 2010. Relationships between tapetum, loculus, and pollen during development. International Journal of Plant Sciences 171: 1–11.

    Google Scholar 

  • ———, M. Guarnieri & M. Nepi. 2006. Pollen carbohydrates and water content during development, presentation and dispersal: a short review. Protoplasma 228: 73–77.

    CAS  PubMed  Google Scholar 

  • ——— & M. Hesse. 2004. Cytophysiology of pollen presentation and dispersal. Flora 199: 273–285.

    Google Scholar 

  • Pedersoli, G. D., J. V. Paulino, V. G. Leite & S. P. Teixeira. 2010. Elucidating enigmatic floral issues in Copaifera langsdorffii Desf. (Leguminosae, Caesalpinioideae). International Journal of Plant Sciences 171: 834–846.

    Google Scholar 

  • Pennington, T. D. 1997. The Genus Inga - Botany. The Royal Botanic Gardens, Kew.

    Google Scholar 

  • Pires, J. P. A. & L. Freitas. 2008. Reproductive biology of two tree species of Leguminosae in a Montane Rain Forest in southeastern Brazil. Flora 203: 491–498.

    Google Scholar 

  • Raghavan, V. 1997. Molecular Embryology of Flowering Plants. University Press, Cambridge.

    Google Scholar 

  • Raspail, M. 1824. Essai d’une classification générale des Graminées, fondée sur l’étude physiologique des charactères de cette famille. Annales des Sciences Naturelles 5(287–311): 433–460.

    Google Scholar 

  • Richards, A. J. 1997. Plant breeding systems. Chapman & Hall, Londres.

    Google Scholar 

  • Rodríguez-Riaño, T., A. Ortega-Olivencia & J. A. Devesa. 1999. Reproductive biology in two Genisteae (Papilionoideae) endemic of the western Mediterranean region: Cytisus striatus and Retama sphaerocarpa. Canadian Journal of Botany 77: 809–820.

    Google Scholar 

  • ———, ——— & ———. 2004. Reproductive biology in Cytisus multiflorus (Fabaceae). Annales Botanici Fennici 41: 179–188.

    Google Scholar 

  • Sage, T. L., K. Hristova-Sarkovski, V. Koehl, J. Lyew, V. Pontieri, P. Bernhardt, P. Weston, S. Bagha & G. Chiu. 2009. Transmitting tissue architecture in basal-relictual angiosperms: implications for transmitting tissue origins. American Journal of Botany 96: 183–206.

    PubMed  Google Scholar 

  • Sahai, K. 2009. Reproductive biology of two species of Canavalia DC. (Fabaceae) – A non-conventional wild legume. Flora 204: 762–768.

    Google Scholar 

  • Sanzol, J., P. Rallo & M. Herrero. 2003. Asynchronous development of stigmatic receptivity in the pear (Pyrus communis; Rosaceae) flower. American Journal of Botany 90: 78–84.

    PubMed  Google Scholar 

  • Schlindwein, C. 1998. Frequent oligolecty characterizings a diverse bee-plant community in a xerophytic bushland of subtropical Brazil. Studies on Neotropical Fauna & Environment 33: 46–59.

    Google Scholar 

  • Scribailo, R. W. & S. C. H. Barrett. 1991. Pollen-pistil interactions in tristylous Pontederia sagittata (Pontederiaceae). I. Floral heteromorphism and structural features of the pollen tube pathway. American Journal of Botany 78: 1643–1661.

    Google Scholar 

  • Seavey, S. R. & K. S. Bawa. 1986. Late-acting self-incompatibility in Angiosperms. Botanical Review. 52: 195–219.

    Google Scholar 

  • Sigrist, M. R. & M. Sazima. 2004. Pollination and reproctive biology of twelve species of neotropical Malpighiaceae: stigma morphology and its implications for the breeding system. Annals of Botany 94: 33–41.

    PubMed  Google Scholar 

  • Silva, N. F. & D. R. Goring. 2001. Mechanisms of self-incompatibility in flowering plants. Cellular and Molecular Life Sciences 58: 1988–2007.

  • Sornsathapornkul, P. & J. N. Owens. 1998. Pollination biology in a tropical Acacia hybrid (A. mangium Willd. X A. auriculiformis A. Cunn. ex Benth.). Annals of Botany 81: 631–645.

    Google Scholar 

  • Souza, L. A. & I. S. Moscheta. 1999. Morfo-anatomia da flor de Ocotea puberula (Rich.) Nees (Lauraceae). Acta Scientiarum 21: 343–348.

    Google Scholar 

  • ———, K. S. M. Mourão, I. S. Moscheta & S. M. Rosa. 2003. Morfologia e anatomia da flor de Pilocarpus pennatifolius Lem. (Rutaceae). Revista Brasileira de Botânica 26: 175–184.

    Google Scholar 

  • Soverna, A. F., B. Galati & P. Hoc. 2003. Study of ovule and megagametophyte development in four species of subtribe Phaseolinae (Leguminosae). Acta Biologica Cracoviensia 45: 63–73.

    Google Scholar 

  • Speroni, G., P. Izaguirre, G. Bernardello & J. Franco. 2009. Intrafloral phenology of Trifolium polymorphum Poir. (Leguminosae) aerial flowers and reproductive implications. Acta Botanica Brasilica 23: 881–888.

    Google Scholar 

  • Spinelli, F., F. Ciampolini, M. Cresti, K. Geider & G. Costa. 2005. Influence of stigmatic morphology on flower colonization by Erwinia amylovora and Pantoea agglomerans. Europhean Journal of Plant Patology 113: 395–405.

    Google Scholar 

  • Tandon, R., K. R. Shivanna & H. Y. Mohan Ram. 2001. Pollination biology and breeding system of Acacia senegal. Botanical Journal of the Linnean Society 135: 251–262.

    Google Scholar 

  • ———, ——— & ———. 2003. Reproductive biology of Butea monosperma (Fabaceae). Annals of Botany 92: 715–723.

    PubMed  Google Scholar 

  • Teixeira, S. P., M. C. Dornelas, H. A. B. A. Zaia & A. M. S. Correa. 2008. Formação da flor, do fruto e da semente. Pp 33–40. In: R. C. L. Figueiredo-Ribeiro, C. J. Barbedo, E. S. Alves, M. Domingos, & M. R. Braga (eds). Pau-brasil, da semente a madeira: conhecer para conservar. Instituto de Botânica/SMA, São Paulo.

    Google Scholar 

  • ———, N. Prakash & N. T. Ranga. 2001. Ovule and early seed development related to seed abortion in Dahlstedtia pinnata and D. pentaphylla (Leguminosae, Papilionoideae). Phytomorphology 51: 41–50.

    Google Scholar 

  • Tilton V. R. & H. T. Horner Jr. 1980. Stigma, style and obturator of Ornithogalum caudatum (Liliaceae) and their function in the reproductive process. American Journal of Botany 67:1113–1131.

  • Tilton, V. R., L. W. Wilcox, R. G. Palmer & M. C. Albertsen. 1984. Stigma, style, and obturator of Soybean, Glycine max (L.) Merr. (Leguminosae) and their function in the reproductive process. American Journal of Botany 71: 676–686.

    Google Scholar 

  • Tropicos.org. Missouri Botanical Garden. 07. Dec. 2012 <http://www.tropicos.org>

  • Tucker, S. C. 1996. Trends in Evolution of Floral Ontogeny in Cassia Sensu Stricto, Senna, and Chamaecrista (Leguminosae: Caesalpinioideae: Cassieae: Cassiinae): A Study in Convergence. American Journal of Botany 83: 687–711.

    Google Scholar 

  • Valtueña, F. J., A. Ortega-Olivencia, T. Rodríguez-Riaño & J. López. 2008. Reproductive biology in Anagyris foetida L. (Leguminosae), an autumn-winter flowering and ornithophilous Mediterranean shrub. Botanical Journal of the Linnean Society 157: 519–532.

    Google Scholar 

  • Vargas, G. U. 1987. Estudio quantitative y bioclimatológico de La vegetación leñosa de Sabana en el Parque Nacional de Santa Rosa, Costa Rica. Yarbook. Conference of Latin Americanist Geographers 13: 72–81.

    Google Scholar 

  • Verkerke, W. 1989. Structure and fuction of the fig. Experientia 45: 612–622.

    Google Scholar 

  • Vidal, B. C. 1970. Dichroism in collagen bundles stained with Xylidine Ponceau 2R. Annales d’Histochimie 15: 289–296.

    Google Scholar 

  • Waltert, M., A. Mardiastuti & M. Mühlenberg. 2004. Effects of land use on bird species richness in Sulawesi, Indonesia. Conservation Biology 18: 1339–1346.

    Google Scholar 

  • Webb, C. J. & D. G. Lloyd. 1986. The avoidance of interference between the presentation of pollen and stigmas in angiosperms II. Herkogamy. New Zealand Journal of Botany 24: 163–178.

    Google Scholar 

  • Weberling, F. 1992. Morphology of flowers and inflorescences. Cambridge University Press, Cambridge.

    Google Scholar 

  • Went, J. L. & M. T. M. Willemse. 1984. Fertilization. In: B. M. Johri (ed). Embryology of Angiosperms (pp 273–314). Springer, Berlin.

    Google Scholar 

  • Westerkamp, C. 2004. Ricochet pollination in Cassias - and how bees explain enantiostyly - preliminary communication. In: B. M. Freitas & J. O. P. Pereira (orgs.). Solitary bees - conservation, rearing and management for pollination (pp 225–230). Imprensa Universitária, Fortaleza.

  • Westerkamp, C. & A. Weber. 1999. Keel flowers of Polygalaceae and Fabaceae: a functional comparison. Botanical Journal of the Linnean Society 129: 207–221.

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Acknowledgments

We thank to Fundação de Amparao à Pesquisa do Estado de São Paulo (process numbers 2002/11834-5, 2008/57487-0 and 2009/01057-0), Conselho Nacional de Desenvolvimento Científico e Tecnológico (process numbers 142876/2008-9, 301960/2009-7 and 152759/2010-7), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Proex) for financial support; Edmárcio S. Campos (FCFRP/USP), Maria Dolores S. Ferreira (FMRP/USP), Paulo D. Frighetto (FMRP/USP), Rodrigo F. Silva (FFCLRP/USP) and Adriane C. S. Sprogis (IB/UNICAMP) for technical assistance; and Dewey Litwiller (University of Saskatchewan, Saskatoon, Saskatchewan, Canada) for English review.

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Costa, M.F.B., Paulino, J.V., Marinho, C.R. et al. Stigma Diversity in Tropical Legumes with Considerations on Stigma Classification. Bot. Rev. 80, 1–29 (2014). https://doi.org/10.1007/s12229-014-9131-5

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