Abstract
Petals in Ranunculales are nectariferous organs referred to as “nectary leaves” and show diversity in shape, color and structure due to various positions and structure of nectary tissue. Menispermaceae are in the core Ranunculales and have green and short nectary leaves, but the knowledge on structure and functions of the nectary leaves is limited. We use scanning electron microscopy, light microscopy and transmission electron microscopy to investigate nectary leaves structure, micro-morphology and ultrastructure in two species of Stephania in Menispermaceae. Our results show that secretory tissues present in the upper part of abaxial side of the nectary leaves and the specialized secretory epidermal cells are distinguished from other cells. In Stephania cepharantha, clusters of secreting epidermal cells are raised slightly above other cells to form some “bulges” (8–25 cells arranged in a cluster) and connected to distinct huge sieve tube elements. In contrast, in Stephania japonica, secretory epidermal cells are lower than non-secreting cells and result in many “well-like” structures (comprising 6–20 cells per “well”), and have no sieve tube element connection. Secretory epidermal cells have dense cytoplasm, large nucleus and abundant organelles. Nectar secretions are exuded via micro-channels or pores of cuticle on outer walls. The type of secretory tissue in Stephania is the variant of nectarioles.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Angiosperm Phylogeny Group (2016) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 161:105–121. https://doi.org/10.1111/j.1095-8339.2009.00996.x
Antoń S, Kamińska M (2015) Comparative floral spur anatomy and nectar secretion in four representatives of Ranunculaceae. Protoplasma 252:1587–1601. https://doi.org/10.1007/s00709-015-0794-5
Badole SL, Chaudhari SM, Zanwar AA (2013) Tinospora cordifolia (Willd.) Miers. (Menispermaceae): beneficial effect on skin diseases. In: Watson R, Zibadi S (eds) Bioactive dietary factors and plant extracts in dermatology. Humana Press, Totowa. https://doi.org/10.1007/978-1-62703-167-7_46
Baillon H (1866) Sur des pétales à structure anormale. Adansonia 6:253–254
Behrens J (1879) Anatomisch-physiologische Untersuchungen der Blüthen-Nectarien. Vorläufige Mittheilung. Flora 61:454–460
Bello AA, Hawkins JA, Rudall PJ (2010) Floral ontogeny in Polygalaceae and its bearing on the homologies of keeled flowers in Fabales. Int J Pl Sci 71:482–498. https://doi.org/10.1086/651945
Cronquist A (1988) The evolution and classification of flowering plants. New York Botanical Garden, New York
Deng YB, Hu ZH (1995) The comparative morphology of the floral necteries of cruciferae. Acta Phytotax Sin 33:209–220
Durkee LT (1983) The ultrastructure of floral and extrafloral nectaries. In: Bentley B, Thomas SE (eds) The biology of nectaries. Columbia University Press, New York, pp 1–29
Endress PK (1995) Floral structure and evolution in Ranunculanae. Pl Syst Evol 9:47–61. https://doi.org/10.1007/978-3-7091-6612-3_5
Endress PK (2010) Flower structure and trends of evolution in eudicots and their major subclades. Ann Missouri Bot Gard 97:541–583. https://doi.org/10.3417/2009139
Erbar C (2014) Nectar secretion and nectaries in basal angiosperms, magnoliids and non-core eudicots and a comparison with core eudicots. Pl Divers Evol 131:63–143. https://doi.org/10.1127/1869-6155/2014/0131-0075
Fahn A (1952) On the structure of floral nectaries. Bot Gaz 113:464–470
Fahn A (1979) Secretory tissue in plants. Academic Press, London
Fahn A (2000) Structure and function of secrectory cell. Advances Bot Res 31:25–37. https://doi.org/10.1016/S0065-2296(00)31006-0
Frei E (1955) Die Innervierung der floralen Nektarien dikotyler Pflanzenfamilien. Ber Schweiz Bot Ges 65:60–114
Gulyás S, Pesti J (1966) Angaben zur Anatomie der Nektarien der Centaureae. Acta Biol Szeged 12:17–23
Hiepko P (1965) Vergleichend-morphologische und entwicklungsgeschichtliche Untersuchungen über das Perianth bei den Polycarpicae. Bot Jahrb Syst 84:359–508
Hoot SB, Zautke H, Harris DJ, Crane PR, Neves SS (2009) Phylogenetic patterns in Menispermaceae based on multiple chloroplast sequence data. Syst Bot 34:44–56. https://doi.org/10.1600/036364409787602339
Horner HT, Healy RA, Cervantes-Martinez T, Palmer RG (2003) Floral nectary fine structure and development in Glycin max L. (Fabaceae). Int J Pl Sci 64:675–690. https://doi.org/10.1086/377060
Hu QM, Luo XR, Chen T, Gibert MG (2008) Menispermaceae through Capparaceae. In: Wu ZY, Raven PH, Hong DY (eds) Flora of China, vol. 7. Science Press and Missouri Botanical Garden Press, Beijing and St. Louis, pp 1–31
Jabbour F, Renner S (2012) Spurs in a spur: Perianth evolution in the Delphinieae (Ranunculaceae). Int J Pl Sci 173:1036–1054. https://doi.org/10.1086/667613
Jacques FMB, Wang W, Ortiz RDC, Li HL, Zhou ZK, Chen ZD (2011) Integrating fossils in a molecular-based phylogeny and testing them as calibration points for divergence time estimates in Menispermaceae. J Syst Evol 49:25–49. https://doi.org/10.1111/j.1759-6831.2010.00105.x
Jeffrey C (1962) Notes on Cucurbitaceae: including a proposed new classification of the family. Kew Bull 15:337–371
Kang Y, Jabbour F, Cao SJ, Wang YQ, Guo JX, Huang JM (2017) Leaf epidermal features of Chinese Stephania Lour. (Menispermaceae) and their systematic significance. Kew Bull 72:26. https://doi.org/10.1007/s12225-017-9697-2
Kartashova NN (1965) Structure and function of nectaries in dicotyledonous flowering plants. Izdatel’stvo Tomskogo Universiteta, Tomsk
Kessler PJA (1993) Menispermaceae. In: Kubitzki K, Rohwer JG, Bittrich V (eds) The families and genera of vascular plants. Springer, Berlin, pp 402–418
Kosuge K (1994) Petal evolution in Ranunculaceae. In: Endress PK, Friis EM (eds) Early evolution of flowers. Springer, Vienna, pp 185–191. https://doi.org/10.1007/978-3-7091-6910-0_11
Kral R (1960) A revision of Asimina and Deeringothamnus (Annonaceae). Brittonia 12:233–278. https://doi.org/10.2307/2805119
Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032. https://doi.org/10.1242/dev.02067
Meng AP, Zhang ZG, Li JQ, De Craene LR, Wang HC (2012) Floral development of Stephania (Menispermaceae): impact of organ reduction on symmetry. Int J Pl Sci 173:861–874. https://doi.org/10.1086/667235
Nepi M (2007) Nectary structure and ulstrastructure. In: Nicolson SW, Nepi N, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 129–166
Ortiz RDC, Kellogg EA, Van der Werff H (2007) Molecular phylogeny of the moonseed family (Menispermaceae): implications for morphological diversification. Amer J Bot 94:1425–1438. https://doi.org/10.3732/ajb.94.8.1425
Prantl K (1887) Beiträge zur Morphologie und Systematik der Ranunculaceen. Bot Jahrb Syst 9:225–273
Rasmussen DA, Kramer EM, Zimmer EA (2009) One size fits all? Molecular evidence for a commonly inherited petal identity program in Ranunculales. Amer J Bot 96:96–109. https://doi.org/10.3732/ajb.0800038
Ronse De Craene LP, Soltis PS, Soltis DE (2003) Evolution of Floral Structures in Basal Angiosperms. Int J Pl Sci 164:S329–S363. https://doi.org/10.1086/377063
Semwal DK, Badoni R, Semwal R, Kothiyal SK, Singh GJP, Rawat U (2010) The genus Stephania (Menispermaceae): chemical and pharmacological perspectives. J Ethnopharmacol 132:369–383. https://doi.org/10.1016/j.jep.2010.08.047
Silberbauer-Gottsberger I, Gottsberger G, Webber AC (2003) Morphological and functional flower characteristics of new and old world Annonaceae with respect to their mode of pollination. Taxonomy 52:701–718. https://doi.org/10.2307/3647345
Takhtajan A (2009) Flowering plants. Springer, New York
Vesprini JL, Nepi M, Pacini E (1999) Nectary structure, nectar secretion patterns and nectar composition in two Helleborus species. Pl Biol 1:560–568. https://doi.org/10.1055/s-2007-978553
Vogel S (1977) Nektarien und ihre ökologische Bedeutung. Apidologie 8:321–335. https://doi.org/10.1051/apido:19770403
Vogel S (1998) Remarkable nectaries: structure, ecology, organophyletic perspectives. II. Nectarioles. Flora 193:1–29. https://doi.org/10.1016/S0367-2530(17)30812-5
Wang HC, Meng AP, Li JQ, Feng M, Chen ZD, Wang W (2006) Floral organogenesis of Cocculus orbiculatus and Stephania dielsiana (Menispermaceae). Int J Pl Sci 167:951–960. https://doi.org/10.1086/505755
Wang HF, Qin HN, Zhou QY, Guo C (2007a) Study on reproductive biology of Sargentodoxa cuneate. Acta Bot Boreal-Occid Sin 10:1860–1866
Wang W, Wang HC, Chen ZD (2007b) Phylogeny and morphological evolution of tribe Menispermeae (Menispermaceae) inferred from chloroplast and nuclear sequences. Perspect Pl Ecol Syst 8:141–154. https://doi.org/10.1016/j.ppees.2009.01.001
Wang W, Ortiz RDC, Jacques FMB, Xiang XG, Li HL, Lin L, Li RQ, Liu Y, Soltis PS, Soltis DE, Chen ZD (2012) Menispermaceae and the diversification of tropical rainforests near the Cretaceous-Paleogene boundary. New Phytol 195:470–478. https://doi.org/10.1111/j.1469-8137.2012.04158.x
Wielgorskaya T (1995) Dictionary of generic names of seed plants. Columbia University Press, New York
Willis JC (1973) A dictionary of flowering plants and ferns. Cambridge University Press, Cambridge
Wist TJ, Davis AR (2006) Floral nectar production and nectary anatomy and ultrastructure of Echinacea purpurea (Asteraceae). Ann Bot (Oxford) 97:177–193. https://doi.org/10.1093/aob/mcj027
Xie DT, He JY, Huang JM, Xie H, Wang YQ, Kang Y, Jabbour F, Guo JX (2015) Molecular phylogeny of Chinese Stephania Lour. (Menispermaceae) and reassessment of the subgeneric and sectional classifications. Austral Syst Bot 28:246–255. https://doi.org/10.1071/SB14023
Zhang XH, Sawhney V, Davis A (2014) Annular floral nectary with oil-producing trichomes in Salvia farinacea (Lamiaceae): anatomy, histochemistry, ultrastructure, and significance. Amer J Bot 101:1849–1867. https://doi.org/10.3732/ajb.1400368
Zhao L, Liu P, Che XF, Wang W, Ren Y (2011) Floral organogenesis of Helleborus thibetanus and Nigella damascene (Ranunculaceae) and its systematic significance. Bot J Linn Soc 166:431–443. https://doi.org/10.1111/j.1095-8339.2011.01142.x
Zhao L, Wang W, Ren Y, Bachelier JB (2012) Floral development in Asteropyrum (Ranunculaceae): implication for its systematic position. Ann Bot Fenn 49:31–42. https://doi.org/10.5735/085.049.0105
Zhao L, Gong JZ, Zhang XH, Liu YQ, Ma X, Ren Y (2016) Floral organogenesis in Urophysa rockii, a rediscovered endangered and rare species of Ranunculaceae. Botany 94:215–224. https://doi.org/10.1139/cjb-2015-0232
Acknowledgements
We would like to thank Prof. Xun Gong and Dr. Jian Liu (Kunming Institute of Botany, Chinese Academy of Sciences) for collecting materials.
Funding
The project was funded by the National Natural Science Foundation of China (Nos. 31770203, 31100141, 31770200) and the Fundamental Research Funds for the Central Universities (Nos. GK201603067 and 2452017155).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Handling Editor: Louis P. Ronse De Craene.
Rights and permissions
About this article
Cite this article
Wang, Qj., Yan, Xl., Zhao, L. et al. Comparative studies on petals structure, micromorphology and ultrastructure in two species of Stephania (Menispermaceae). Plant Syst Evol 304, 911–921 (2018). https://doi.org/10.1007/s00606-018-1522-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00606-018-1522-3