Abstract
Flowers are an innovative characteristic of angiosperms, and elaborate petals usually have highly specialized structures to adapt to different living environments and pollinators. Petals of Eranthis have complex bilabiate structures with nectaries and pseudonectaries; however, the diversity of the petal micromorphology and structure is unknown. Petal development, micromorphology, structure and ultrastructure in four Eranthis species were investigated under SEM, TEM and LM. The results show that petals undergo 5 developmental stages, and accessory structure formation (stage 4) mainly determines the diversity of final mature petal morphology and pseudonectaries; the central depression formed in stage 2 will develop into nectary tissues. Petals are bilabiate and have hidden nectaries in nectary grooves; they consist of one layer of rounded and raised secretory epidermal cells and 3–14 layers of secretory cells with abundant plasmodesmata between cells. A large number of sieve tubes are distributed between the cells and extend to the epidermis; in addition, the vessel elements are located below the secretory area. Nectar is stored in the intercellular space between secretory parenchyma cells and escapes through microchannels or cell rupture. Pseudonectaries in all species of Eranthis except for E. hyemalis consist of smooth, ornamented epidermal cells and 9–12 layers of parenchyma cells with sparse cytoplasm, which may have the function of attracting pollinators.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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
Bernardello G (2007) A systematic survey of floral nectaries. In: Nicolson SW, Nepi M, Pacini E, eds. Nectaries and nectar. Springer, Dordrecht, 19–128.https://doi.org/10.1007/978-1-4020-5937-7_2
Brewer CA, Smith WK, Vogelmann TC (1991) Functional interaction between leaf trichomes, leaf wettability and the optical properties of water droplets. Plant Cell Environ 14:955–962. https://doi.org/10.1111/j.1365-3040.1991.tb00965.x
Brown W (1938) The bearing of nectaries on the phylogeny of flowering plants. Proc Am Philos Soc 79:549–595
Buchmann SL, Buchmann MD (1981) Anthecology of Mouriri myrtilloides (Melastomataceae: Memecyleae), an oil flower in Panama. Biotropica 13:7–24. https://doi.org/10.2307/2388066
Che XF (2012) Comparative morphological study on floral secretory tissue of Ranunculaceae. MD Thesis, Shaanxi Normal University, China.
Christensen KI, Hansen HV (1998) SEM-studies of epidermal patterns of petals in the angiosperms. Opera Botanica: 5–87.
Dafni A (1984) Mimicry and deception in pollination. Annu Rev Ecol Syst 15:259–278. https://doi.org/10.2307/2096949
Endress PK (1994) Floral structure and evolution of primitive angiosperms: recent advances. Plant Syst Evol 192:79–97. https://doi.org/10.1007/BF00985910
Endress PK (2011) The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci 162:1111–1140. https://doi.org/10.1086/321919
Endress PK, Matthews ML (2006) Elaborate petals and staminodes in eudicots: diversity, function, and evolution. Org Divers Evol 6:257–293. https://doi.org/10.1016/j.ode.2005.09.005
Endress PK, Steiner-Gafner B (1996) Diversity and evolutionary biology of tropical flowers. Cambridge University Press, Cambridge
Erbar C (2014) Nectar secretion and nectaries in basal angiosperms, magnoliids and non-core eudicots and a comparison with core eudicots. Plant Divers Evol 131:63–143. https://doi.org/10.1127/1869-6155/2014/0131-0075
Erst AS, Sukhorukov AP, Mitrenina EY, Skaptsov MV, Kostikova VA, Chernisheva OA, Troshkina V, Kushunina M, Krivenko DA, Ikeda H, Xiang K, Wang W (2020) An integrative taxonomic approach reveals a new species of Eranthis (Ranunculaceae) in North Asia. PhytoKeys 140:75–100. https://doi.org/10.3897/phytokeys.140.49048
wFrey-Wyssling A, Hausermann E 1960 Deutung der gestaltlosen nektarien Berichte Der Schweizerischen Botanischen Gesellschaft 70 150 162
Glover BJ, Whitney HM (2010) Structural colour and iridescence in plants: the poorly studied relations of pigment colour. Ann Bot 105:505–511. https://doi.org/10.1093/aob/mcq007
AA Green JR Kennaway AI Hanna J Andrew Bangham E Coen 2010 Genetic control of organ shape and tissue polarity PLoS Biol 8 https://doi.org/10.1371/journal.pbio.1000537
Heads PA, Lawton JH (1985) Bracken, ants and extrafloral nectaries. III. How insect herbivores avoid ant predation. Ecol Entomol 10:29–42. https://doi.org/10.1111/j.1365-2311.1985.tb00532.x
Heil M (2011) Nectar: Generation, regulation and ecological functions. Trends Plant Sci 16:191–200. https://doi.org/10.1016/j.tplants.2011.01.003
Huang ZX, Ren Y, Zhang XH (2021) Morphological and numerical variation patterns of floral organs in two species of Eranthis. Flora 276–277:151785. https://doi.org/10.1016/j.flora.2021.151785
Irish VF (2008) The Arabidopsis petal: a model for plant organogenesis. Trends Plant Sci 13:430–436. https://doi.org/10.1016/j.tplants.2008.05.006
Kay QON, Daoud HS, Stirton CH (1981) Pigment distribution, light reflection and cell structure in petals. Bot J Linn Soc 83:57–83. https://doi.org/10.1111/j.1095-8339.1981.tb00129.x
Knapp S (2013) A revision of the Dulcamaroid clade of Solanum L. (Solanaceae). PhytoKeys 22:1–428. https://doi.org/10.3897/phytokeys.22.4041
Kosuge K (1994) Petal evolution in Ranunculaceae. Early Evolution of Flowers 191:185–191. https://doi.org/10.1007/978-3-7091-6910-0_11
Kosuge K, Tamura M (1988) Morphology of the petal in Aconitum. Bot Mag Tokyo 101:223–237. https://doi.org/10.1007/BF02488601
Kosuge K, Tamura M (1989) Ontogenetic studies on petals of the Ranunculaceae. J Jpn Bot 64:65–74
Kugler H (1956) Über die optische Wirkung von Fliegenblumen auf Fliegen. Berichte Der Deutschen Botanischen Gesellschaft 69:387–398
Leppik EE (1964) Floral evolution in the Ranunculaceae. Iowa State Journal of Science 39: 1–101. https://core.ac.uk/display/14525125
Liao H, Fu XH, Zhao HQ, Cheng J, Zhang R, Yao X, Duan XS, Shan HY, Kong HZ (2020) The morphology, molecular development and ecological function of pseudonectaries on Nigella damascena (Ranunculaceae) petals. Nat Commun 11:1777. https://doi.org/10.1038/s41467-020-16194-9
Matthews ML, Endress PK (2002) Comparative floral structure and systematics in Oxalidales (Oxalidaceae, Connaraceae, Brunelliaceae, Cephalotaceae, Cunoniaceae, Elaeocarpaceae, Tremandraceae). Bot J Linn Soc 140:321–381. https://doi.org/10.1046/j.1095-8339.2002.00105.x
Matthews ML, Endress PK (2005) Comparative floral structure and systematics in Celastrales (Celastraceae, Parnassiaceae, Lepidobotryaceae). Bot J Linn Soc 149:129–194. https://doi.org/10.1111/j.1095-8339.2005.00445.x
Matthews ML, Endress PK (2011) Comparative floral structure and systematics in Rhizophoraceae, Erythroxylaceae and the potentially related Ctenolophonaceae, Linaceae, Irvingiaceae and Caryocaraceae (Malpighiales). Bot J Linn Soc 166:331–416. https://doi.org/10.1111/j.1095-8339.2011.01162.x
McDonald DJ, van der Walt JJA (1992) Observations on the pollination of Pelargonium tricolor, section Campylia (Geraniaceae). S Afr J Bot 58:386–392. https://doi.org/10.1016/S0254-6299(16)30826-2
Moyroud E, Wenzel T, Middleton R, Rudall PJ, Banks H, Reed A, Mellers G, Killoran P, Westwood MM, Steiner U, Vignolini S, Glover BJ (2017) Disorder in convergent floral nanostructures enhances signalling to bees. Nature 550:469–474. https://doi.org/10.1038/nature24285
Nepi M (2007) Nectary structure and ultrastructure. In: Nicolson SW, Nepi M, Pacini E, eds. Nectaries and nectar. Springer, Dordrecht, 129–166. DOI:https://doi.org/10.1007/978-1-4020-5937-7_3
Ojeda I, Francisco-Ortega J, Cronk QCB (2009) Evolution of petal epidermal micromorphology in Leguminosae and its use as a marker of petal identity. Ann Bot 104:1099–1110. https://doi.org/10.1093/aob/mcp211
Pemberton RW (2010) Biotic resource needs of specialist orchid pollinators. Bot Rev 76:275–292. https://doi.org/10.1007/s12229-010-9047-7
Plitmann U, Raven PH, Breedlove DE (1973) The systematics of Lopezieae (Onagraceae). Ann Mo Bot Gard 60:478–563. https://doi.org/10.2307/2395095
Puzey JR, Gerbode SJ, Hodges SA, Kramer EM, Ln M (2012) Evolution of spur-length diversity in Aquilegia petals is achieved solely through cell-shape anisotropy. Proc Royal Soc B: Biol Sci 279:1640–1645. https://doi.org/10.1098/rspb.2011.1873
Rasmussen DA, Kramer EM, Zimmer EA (2009) One size fits all? Molecular evidence for a commonly inherited petal identity program in Ranunculales. Am J Bot 96:96–109. https://doi.org/10.3732/ajb.0800038
Ren Y, Chang HL, Tian XH, Song P, Endress PK (2009) Floral development in Adonideae (Ranunculaceae). Flora 204:506–517. https://doi.org/10.1016/j.flora.2008.07.002
Ren Y, Chang HL, Endress PK (2010) Floral development in Anemoneae (Ranunculaceae). Bot J Linn Soc 162:77–100. https://doi.org/10.1111/j.1095-8339.2009.01017.x
Ren Y, Gu TQ, Chang HL (2011) Floral development of Dichocarpum, Thalictrum, and Aquilegia (Thalictroideae, Ranunculaceae). Plant Syst Evol 292:203–213. https://doi.org/10.1007/s00606-010-0399-6
Renner SS (1989) A survey of reproductive biology in neotropical Melastomataceae and Memecylaceae. Ann Mo Bot Gard 76:496
Ronse De Craene LP, Smets EF (1995) Evolution of the androecium in the Ranunculiflorae. Plant Syst Evol Suppl 9:63–70. https://doi.org/10.1007/978-3-7091-6612-3_6
Ronse De Craene LP (2010) Floral diagrams: an aid to understanding flower morphology and evolution. Cambridge University Press, Cambridge. https://doi.org/10.1017/CBO9780511806711
Sandvik SM, Totland Ø (2003) Quantitative importance of staminodes for female reproductive success in Parnassia palustris under contrasting environmental conditions. Can J Bot 81:49–56. https://doi.org/10.1139/b03-006
Tamura M (1993) The families and genera of vascular plants (K Kubitzki, JG Rohwer, and V Bittrich, Eds.). Berlin: Springer.
Tian M (2019) Adaptation of different way of nectar hidden in seven species of Ranunculaceae to pollinators. PhD Thesis, Shaanxi Normal University, China.
Tian M, Ren Y (2019) Evolutionary significance of discrete functional adaptations to pollinators in generalist flowers: a case study of three species of Ranunculus s.l. (Ranunculaceae) with distinct petal nectary scales. Bot J Linn Soc 189:281–292. https://doi.org/10.1093/botlinnean/boy073
Vesprini JL, Nepi M, Pacini E (1999) Nectary structure, nectar secretion patterns and nectar composition in two Helleborus species. Plant Biol 1:560–568. https://doi.org/10.1111/j.1438-8677.1999.tb00784.x
Vesprini JL, Pacini E, Nepi M (2012) Floral nectar production in Helleborus foetidus : an ultrastructural study. Botany 90:1308–1315. https://doi.org/10.1139/b2012-101
Wang W, Lu AM, Ren Y, Endress ME, Chen ZD (2009) Phylogeny and classification of Ranunculales: evidence from four molecular loci and morphological data. Perspect Plant Ecol Evol Syst 11:81–110. https://doi.org/10.1016/j.ppees.2009.01.001
Wang X, Gong JZ, Zhao L, Che XF, Li HN, Ren Y (2016) Flower morphology and development of the monotypic Chinese genus Anemoclema (Ranunculaceae). Plant Syst Evol 302:683–690. https://doi.org/10.1007/s00606-016-1298-2
Wang HZ, Zhang R, Cheng J, Duan XS, Zhao HQ, Shan HY, Kong HZ (2019) Diversity of flowers in basic structure and its underlying molecular mechanisms. Scientia Sinica Vitae 49:292–300. https://doi.org/10.1360/N052018-00219
Waser NM, Ollerton J, Erhardt A (2011) Typology in pollination biology: lessons from an historical critique. J Pollinat Ecol 3:1–7. https://doi.org/10.26786/1920-7603(2011)2
Whitney HM, Chittka L, Bruce TJA, Glover BJ (2009) Conical epidermal cells allow bees to grip flowers and increase foraging efficiency. Curr Biol 19:948–953. https://doi.org/10.1016/j.cub.2009.04.051
Whitney HM, Bennett KMV, Dorling M, Sandbach L, Prince D, Chittka L, Glover BJ (2011) Why do so many petals have conical epidermal cells? Ann Bot 108:609–616. https://doi.org/10.1093/aob/mcr065
Whittall JB, Hodges SA (2007) Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature 447:706–709. https://doi.org/10.1038/nature05857
Wink M (2010) Mode of action and toxicology of plant toxins and poisonous plants. Julius-Kühn-Archiv: 93–112. https://www.researchgate.net/publication/279671686
Woodcock TS, Larson BM, Kevan PG, Inouye DW, Lunau K (2014) Flies and flowers II: floral attractants and rewards. J Pollinat Ecol 12:63–94. https://doi.org/10.26786/1920-7603(2014)5
KL Xiang AS Erst J Yang HW Peng R Ortiz del C, Jabbour F, Erst TV, Wang W 2021 Biogeographic diversification of Eranthis (Ranunculaceae) reflects the geological history of the three great Asian plateaus Proc R Soc B 288 20210281 https://doi.org/10.1098/rspb.2021.0281
Yao X, Zhang WG, Duan XS, Yuan Y, Zhang R, Shan HY, Kong HZ (2019) The making of elaborate petals in Nigella through developmental repatterning. New Phytol 223:385–396. https://doi.org/10.1111/nph.15799
Yin YY (2014) Micromorphology of the petal surface of Ranunculaceae. MD Thesis, Shaanxi Normal University, China.
Zhang R, Guo C, Shan H, Kong H (2014) Developmental repatterning and biodiversity. Biodivers Sci 22:66–71. https://doi.org/10.3724/SP.J.1003.2014.13248
Zhang JD (2019) The study on the pollination and breeding system of Cimicifugeae in Ranunculaceae. Xi’an, Shaanxi, China: PhD Thesis, Shaanxi Normal University, China.
Zhang R, Fu X, Zhao C, Cheng J, Liao H, Wang P, Yao X, Duan X, Yuan Y, Xu G, Kramer EM, Shan H, Kong H (2020) Identification of the key regulatory genes involved in elaborate petal development and specialized character formation in Nigella damascena (Ranunculaceae). Plant Cell 32:3095–3112. https://doi.org/10.1105/tpc.20.00330
Zhao L, Liu P, Che XF, Wang W, Ren Y (2011) Floral organogenesis of Helleborus thibetanus and Nigella damascena (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, Bachelier JB, Chang HL, Tian XH, Ren Y (2012a) Inflorescence and floral development in Ranunculus and three allied genera in Ranunculeae (Ranunculoideae, Ranunculaceae). Plant Syst Evol 298:1057–1071. https://doi.org/10.1007/s00606-012-0616-6
Zhao L, Wang W, Ren Y, Bachelier JB (2012b) Floral development in Asteropyrum (Ranunculaceae): implications for its systematic position. Ann Bot Fenn 49:31–42. https://doi.org/10.1071/SB12001
Zhao L, Gong JZ, Zhang XH, Liu YQ, Ma X, Ren Y (2015) 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
Zhao XH (2016) Morphological genesis of petal diversity in Ranunculaceae. MD Thesis, Shaanxi Normal University, China.
Acknowledgements
We thank Da-Lyu Zhong, Meng Han, Shan Su and Wen-Juan Li for sample collection, Siyu Xie for modification of Figure 2, Cheng Xue for comments on an earlier draft of this paper and other staff of Ren’s group for technical assistance. We sincerely thank two anonymous reviewers for providing valuable comments and suggestions.
Funding
This work was supported by the National Natural Science Foundation of China (No. 31770203, 31100141) and the Fundamental Research Funds for the Central Universities (No. GK201603067, No. GK202002011 and 2452017155).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Handling Editor: Dorota Kwiatkowska
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Huang, Z., Zhang, X. Floral nectaries and pseudonectaries in Eranthis (Ranunculaceae): petal development, micromorphology, structure and ultrastructure. Protoplasma 259, 1283–1300 (2022). https://doi.org/10.1007/s00709-022-01738-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-022-01738-1