Abstract
Main conclusion
In a co-evolutionary crosstalk amid plants and their pollinators, nectaries serve as a labile link between the relatively fixed structural domains of divergent flower forms and associated pollination syndromes.
Abstract
Floral nectary plays a crucial role in sexual plant reproduction by enabling interaction between plants and their pollinators. It is known to associate with different floral whorls, and exhibits variations in structure and location in different clades across angiosperms. To infer evolutionary patterns, it is important to map key features associated with the trait at various taxonomic ranks. In the present study, we analysed variability and distribution of floral nectaries in Solanaceae for the first time. Floral nectaries of 23 taxa representing different clades in the family were studied using bright-field and scanning electron microscopy. The study reveals that although floral nectaries share anatomical similarity, they differ in morphology, composition within cells, and locations within a flower across the clades. The analysis suggests that (i) there is a shift from symmetric, lobed type nectary in the early branching sub-families to asymmetric, annular type in the late branching ones, (ii) floral organization has shifted from asymmetry (zygomorphy) to symmetry (actinomorphy) in corolla, and (iii) the lobed nectary correlates with zygomorphic floral forms that are pollinated by birds and long-tongued vectors, while the annular nectary is predominant among species with bee-pollinated actinomorphic flowers.
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References
Anderson GJ, Bernardello G, Opel MR, Santos Guerra A, Anderson M (2006) Reproductive biology of the dioecious Canary Islands endemic Withania aristata (Solanaceae). Am J B 93:1295–1305. https://doi.org/10.3732/ajb.93.9.1295
Baker HG (1975) Sugar concentrations in nectars from hummingbird flowers. Biotropica 7:37–41
Baker HG, Baker I (1983) Floral nectar sugar constituents in relation to pollinator type. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 117–141
Barboza GE, García CC, Scaldaferro M, Bohs L (2020) An amazing new Capsicum (Solanaceae) species from the Andean-Amazonian Piedmont. PhytoKeys 167:13–29. https://doi.org/10.3897/phytokeys.167.57751
Barboza GE, Hunziker AT, Bernardello G, Cocucci AA, Moscone AE, García CC, Fuentes V, Dillon MO, Bittrich V, Cosa MT, Subils R (2016) Solanaceae. In: Kadereit J, Bittrich V (eds) Flowering plants Eudicots. The families and genera of vascular plants. Springer, Cham, pp 295–357. https://doi.org/10.1007/978-3-319-28534-4
Berlyn GP, Miksche JP (1976) Botanical microtechnique and cytochemistry. Iowa State University Press, Ames
Bernardello G (2007) A systematic survey of floral nectaries. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 19–128. https://doi.org/10.1007/978-1-4020-5937-7_2
Bernardello L, Rodriguez I, Stiefkens L, Galetto L (1995) The hybrid nature of Lycium ciliatum× cestroides (Solanaceae): experimental, anatomical, and cytological evidence. Can J Bot 73:1995–2005. https://doi.org/10.1139/b95-214
Bernardello G, Galetto L, Anderson GJ (2000) Floral nectary structure and nectar chemical composition of some species from Robinson Crusoe Island (Chile). Can J Bot 78:862–871. https://doi.org/10.1139/b00-055
Bowman JL, Smyth DR (1999) CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126:2387–2396
Brandenburg A, Dell’Olivo A, Bshary R, Kuhlemeier C (2009) The sweetest thing: advances in nectar research. Curr Opin Plant Biol 12:486–490
Buchmann SL, Cane JH (1989) Bees assess pollen returns while sonicating Solanum flowers. Oecologia 81:289–294. https://doi.org/10.1007/BF00377073
Cachelin S (2015) Morphology, anatomy and development of floral nectaries associated to pollinator shifts in neotropical Gesneriaceae. Ph.D Thesis, University of Geneva
Caraballo-Ortiz MA, Santiago-Valentín E, Carlo TA (2011) Flower number and distance to neighbours affect the fecundity of Goetzea elegans (Solanaceae). J Trop Ecol 27(5):521–528
Cole TCH (2020) Solanaceae Phylogeny Poster
Dellinger AS, Artuso S, Pamperl S, Michelangeli FA, Penneys DS, Fernández-Fernández DM, Schönenberger J (2019) Modularity increases rate of floral evolution and adaptive success for functionally specialized pollination systems. Commun Biol 2:1–11. https://doi.org/10.1038/s42003-019-0697-7
Duffy KJ, Johnson SD (2011) Effects of pollen reward removal on fecundity in a self-incompatible hermaphrodite plant. Plant Biol 13:556–560
Endress PK (1996) Diversity and evolutionary biology of tropical flowers. Cambridge University Press
Endress PK (2001) Evolution of floral symmetry. Curr Opin Plant Biol 4:86–91. https://doi.org/10.1016/S1369-5266(00)00140-0
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
Erbar C, Leins P (2010) Nectaries in Apiales and related groups. Plant Divers Evol 128:269–295
Fahn A (1952) On the structure of floral nectaries. Bot Gaz 113:464–470. https://doi.org/10.1086/335735
Fahn A (1953) The topography of the nectary in the flower and its phylogenetical trend. Phytomorphology 3:424–425
Figueiredo MCC, Passos AR, Hughes FM, dos Santos KS, da Silva AL, Soares TL (2020) Reproductive biology of Physalis angulata L. (Solanaceae). Sci Hortic. https://doi.org/10.1016/j.scienta.2020.109307
Filipowicz N, Renner SS (2012) Brunfelsia (Solanaceae): a genus evenly divided between South America and radiations on Cuba and other Antillean islands. Mol Phylogenet Evol 64:1–11
Gahan PB (1984) Plant Histochemistry and Cytochemistry: An Introduction. Academic Press, London
Galetto L, Bernardello G, Sosa CA (1998) The relationship between floral nectar composition and visitors in Lycium (Solanaceae) from Argentina and Chile: What does it reflect? Flora 193:303–314
Goodwillie C, Sargent RD, Eckert CG, Elle E, Geber MA, Johnston MO, Kalisz S, Moeller DA, Ree RH, Vallejo-Marin M, Winn AA (2010) Correlated evolution of mating system and floral display traits in flowering plants and its implications for the distribution of mating system variation. New Phyto 185:311–321
Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J Bot 38:125–174
Hainsworth FR, Wolf LL (1976) Nectar characteristics and foodselection by hummingbirds. Oecologia 25:101–113
Jeiter J, Hilger HH, Smets EF, Weigend M (2017a) The relationship between nectaries and floral architecture: a case study in Geraniaceae and Hypseocharitaceae. Ann Bot 120:791–803. https://doi.org/10.1093/aob/mcx101
Jeiter J, Weigend M, Hilger HH (2017b) Geraniales flowers revisited: evolutionary trends in floral nectaries. Ann Bot 119:395–408. https://doi.org/10.1093/aob/mcw230
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York
Kaczorowski RL, Gardener MC, Holtsford TP (2005) Nectar traits in Nicotiana section Alatae (Solanaceae) in relation to floral traits, pollinators, and mating system. Am J Bot 92:1270–1283. https://doi.org/10.3732/ajb.92.8.1270
Karnovsky YM (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. J Cell Biol 27:1A-149A
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press, Colorado
Knapp S (2002) Tobacco to tomatoes: a phylogenetic perspective on fruit diversity in the Solanaceae. J Exp Bot 53:2001–2022. https://doi.org/10.1093/jxb/erf068
Knapp S (2010) On ‘various contrivances’: pollination, phylogeny and flower form in the Solanaceae. Philos Trans R Soc Lond B Biol Sci 365:449–460. https://doi.org/10.1098/rstb.2009.0236
Knapp S, Bohs L, Nee M, Spooner DM (2004) Solanceae—a model for linking genomics with biodiversity. Comp Funct Genom 5:285–291. https://doi.org/10.1002/cfg.393
Kumari DS (1986) Evolution of floral nectary in Lamiaceae. Proc Lndian Acad Sci 96:281–288
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
Liu ML, Yu WB, Kuss P, Li DZ, Wang H (2015) Floral nectary morphology and evolution in Pedicularis (Orobanchaceae). Bot J Linn Soc 178:592–607. https://doi.org/10.1111/boj.12288
Mach J (2018) Nectary specification in Petunia and Arabidopsis. Plant Cell 30:1949. https://doi.org/10.1105/tpc.18.00692
Maddison WP, Maddison DR (2019) Mesquite: a modular system for evolutionary analysis. Version 3.61 http://www.mesquiteproject.org
Maheepala DC, Emerling CA, Rajewski A, Macon J, Strahl M, Pabón-Mora N, Litt A (2019) Evolution and diversification of FRUITFULL genes in Solanaceae. Front Plant Sci 10:43. https://doi.org/10.3389/fpls.2019.00043
Martins TR, Barkman TJ (2005) Reconstruction of Solanaceae phylogeny using the nuclear gene SAMT. Syst Bot 30:435–447. https://doi.org/10.1600/0363644054223675
Mione T, Kostyun J, Leiva González S (2020) Breeding system features and a novel method for locating floral nectar secretion in a South American nightshade (Jaltomata quipuscoae). Plant Biosyst 154:67–73. https://doi.org/10.1080/11263504.2019.1578277
Moré M, Cocucci AA, Sérsic AN, Barboza GE (2015) Phylogeny and floral trait evolution in Jaborosa (Solanaceae). Taxon 64:523–534
Morel P, Heijmans K, Ament K et al (2018) The floral C-lineage genes trigger nectary development in Petunia and Arabidopsis. Plant Cell 30:2020–2037. https://doi.org/10.1105/tpc.18.00425
Neal PR, Dafni A, Giurfa M (1998) Floral symmetry and its role in plant-pollinator systems: terminology, distribution, and hypotheses. Annu Rev Ecol Evol Syst 29:345–373. https://doi.org/10.1146/annurev.ecolsys.29.1.345
Nepi M, Human H, Nicolson SW, Cresti L, Pacini E (2006) Nectary structure and nectar presentation in Aloe castanea and A. greatheadii var. davyana (Asphodelaceae). Plant Syst Evol 257:45–55. https://doi.org/10.1007/s00606-005-0376-7
Nicolson SW, Nepi M, Pacini E (2007) Nectaries and nectar. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-5937-7
O’Brien TP, McCully ME (1981) The study of plant structure principles and selected methods. Termacarphi Pty Ltd., Sass JE, Australia
Ohno S (1970) Evolution by gene duplication. Springer, Berlin
Olmstead RG, Palmer JD (1992) A chloroplast DNA phylogeny of the Solanaceae: subfamilial relationships and character evolution. Ann Missouri Bot Gard 79:346–360. https://doi.org/10.2307/2399773
Olmstead RG, Sweere JA (1994) Combining data in phylogenetic systematics: an empirical approach using three molecular data sets in the Solanaceae. Syst Biol 43:467–481. https://doi.org/10.1093/sysbio/43.4.467
Olmstead RG, Bohs L, Migid HA, Santiago-Valentin E, Garcia VF, Collier SM (2008) A molecular phylogeny of the Solanaceae. Taxon 57:1159–1181
Paucar JOA, Isaias RMS, Stehmann JR (2020) Unravelling the structure and function of the petal appendages in the tribe Schwenckieae (Solanaceae). Plant Biol 22:146–156. https://doi.org/10.1111/plb.13061
Pearse AGE (1985) Histochemistry: theoretical and applied. In: Analytical technology. Churchill Livingstone, Edinburgh
Phukela B, Adit A, Tandon R (2020a) A Snapshot of Evolutionary History of floral nectaries across angiosperm lineages. In: Tandon R, Shivanna K, Koul M (eds) Reproductive ecology of flowering plants: patterns and processes. Springer, Singapore. https://doi.org/10.1007/978-981-15-4210-7_6
Phukela B, Geeta R, Das S, Tandon R (2020b) Ancestral segmental duplication in Solanaceae is responsible for the origin of CRCa–CRCb paralogues in the family. Mol Genet Genom 295:563–577
Powo (2020) http://www.plantsoftheworldonline.org/taxon/urn:lsid:ipni.org:names:30000631-2 Accessed 15 Dec 2020
Rego LN, Da Silva CR, Torezan JM, Gaeta ML, Vanzela AL (2009) Cytotaxonomical study in Brazilian species of Solanum, Lycianthes and Vassobia (Solanaceae). Plant Syst Evol 279:93–102. https://doi.org/10.1007/s00606-009-0149-9
Ren G, Healy RA, Klyne AM, Horner HT, James MG, Thornburg RW (2007) Transient starch metabolism in ornamental tobacco floral nectaries regulates nectar composition and release. Plant Sci 173:277–290
Rodriguez I (2000) Flower anatomy and morphology of Exodeconus maritimus (Solanaceae, Solaneae) and Nicandra physalodes (Solanaceae, Nicandreae): importance for their systematic relationships. Adansonia 22:187–199
Rudall PJ, Manning JC, Goldblatt P (2003) Evolution of floral nectaries in Iridaceae. Ann Missouri Bot Gard 90:613–631. https://doi.org/10.2307/3298546
Ruzin SE (1999) Plant microtechnique and microscopy. Oxford University Press, New York
Saini MS, Raina RH, Khan ZH (2012) Taxonomy and pollination ecology of Bombus rufofasciatus (Hymenoptera: Apidae) from the Indian Himalaya. Polish J Entomol 81:347–363
Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evol Biol 13:214. https://doi.org/10.1186/1471-2148-13-214
Sazima M, Vogel S, Cocucci A, Hausner G (1993) The perfume flowers of Cyphomandra (Solanaceae): pollination by euglossine bees, bellows mechanism, osmophores, and volatiles. Plant Syst Evol 187:51–88
Singh VK, Barman C, Tandon R (2014) Nectar robbing positively influences the reproductive success of Tecomella undulata (Bignoniaceae). PLoS ONE 9:1–11. https://doi.org/10.1371/journal.pone.0102607
Smith SD, Ané C, Baum DA (2008) The role of pollinator shifts in the floral diversification of Iochroma (Solanaceae). Evolution 62:793–806
Solís SM, Zini LM, González VV, Ferrucci MS (2017) Floral nectaries in Sapindaceae s.s.: morphological and structural diversity, and their systematic implications. Protoplasma 254:2169–2188. https://doi.org/10.1007/s00709-017-1108-x
Stahl JM, Nepi M, Galetto L, Guimarães E, Machado SR (2012) Functional aspects of floral nectar secretion of Ananas ananassoides, an ornithophilous bromeliad from the Brazilian savanna. Ann Bot 109:1243–1252. https://doi.org/10.1093/aob/mcs053
Tölke ED, Bachelier JB, Lima EA, Galetto L, Demarco D, Carmello-Guerreiro SM (2018) Diversity of floral nectary secretions and structure, and implications for their evolution in Anacardiaceae. Bot J Linn Soc 187:209–231. https://doi.org/10.1093/botlinnean/boy016
Van der Niet T, Peakall R, Johnson SD (2014) Pollinator-driven ecological speciation in plants: new evidence and future perspectives. Ann Bot 113:199–212
Vogel S (1998) Remarkable nectaries: structure, ecology, organophyletic perspectives III. Nectar Ducts Flora 193:113–131. https://doi.org/10.1016/S0367-2530(17)30827-7
Willmer P (2011) Pollination and floral ecology. University Press, Princeton
Zumajo-Cardona C, Pabón-Mora N, Ambrose B (2018) Duplication and diversification of REPLUMLESS-a case study in the Papaveraceae. Front Plant Sci 9:1833. https://doi.org/10.3389/fpls.2018.01833
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Financial support from the Institution of Eminence, University of Delhi (IoE/FRP/LS/2020/27) is gratefully acknowledged. BP and AA are thankful to the Council of Scientific and Industrial Research for the award of Senior Research Fellowship.
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Phukela, B., Adit, A. & Tandon, R. Evolutionary trends and diversity of major floral nectary types across Solanaceae. Planta 254, 55 (2021). https://doi.org/10.1007/s00425-021-03705-1
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DOI: https://doi.org/10.1007/s00425-021-03705-1