Skip to main content
SpringerLink
Log in

Arabidopsisthaliana as a model for functional nectary analysis

  • Review
  • Published:
Sexual Plant Reproduction Aims and scope Submit manuscript

Abstract

Nectaries and nectar have received much research attention for well over 200 years due to their central roles in plant–pollinator interactions. Despite this, only a few genes have demonstrated impacts on nectary development, and none have been reported to mediate de novo nectar production. This scarcity of information is largely due to the lack of a model that combines sizeable nectaries, and high levels of nectar production, along with suitable genomics resources. For example, even though Arabidopsis thaliana has been useful for developmental studies, it has been largely overlooked as a model for studying nectary function due to the small size of its flowers. However, Arabidopsis nectaries, along with those of related species, are quite operational and can be used to discern molecular mechanisms of nectary form and function. A current understanding of the machinery underlying nectary function in plants is briefly presented, with emphasis placed on the prospects of using Arabidopsis as a model for studying these processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Aloni R, Schwalm K, Langhans M, Ullrich CI (2003) Gradual shifts in sites of free-auxin production during leaf-primordium development and their role in vascular differentiation and leaf morphogenesis in Arabidopsis. Planta 216:841–853

    CAS  PubMed  Google Scholar 

  • Aloni R, Aloni E, Langhans M, Ullrich CI (2006) Role of auxin in regulating Arabidopsis flower development. Planta 223:315–328

    Article  CAS  PubMed  Google Scholar 

  • Baker HG (1978) Chemical aspects of the pollination of woody plants in the tropics. In: Tomlinson PB, Zimmerman M (eds) Tropical trees as living systems. Cambridge University Press, New York, pp 57–82

    Google Scholar 

  • Baker H, Baker I (1973) Amino acids in nectar and their evolutionary significance. Nature 241:543–545

    Article  CAS  Google Scholar 

  • Baker HG, Baker I (1982) Chemical constituents of nectar in relation to pollination mechanisms and phylogeny. In: Nitecki MH (ed) Biochemical aspects of evolutionary biology. University of Chicago Press, Chicago, pp 131–171

  • Baker H, Baker I (1975) Studies of nectar-constitution and pollinator-plant coevolution. In: Gilbert LE, Raven PH (eds) Coevolution of animals and plants. University of Texas Press, Austin, pp 100–140

    Google Scholar 

  • Baker H, Baker I (1983) A brief historical review of chemistry of floral nectar. In: Bentley BL (ed) The biology of nectaries. Columbia University Press, New York, pp 126–152

    Google Scholar 

  • Baum SF, Eshed Y, Bowman JL (2001) The Arabidopsis nectary is an ABC-independent floral structure. Development 128:4657–4667

    CAS  PubMed  Google Scholar 

  • Bernardello G (2007) A systematic survey of floral nectaries. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Netherlands, pp 129–166

    Google Scholar 

  • Bowman JL (1994) Arabidopsis: an atlas of morphology and development. Springer-Verlag, New York

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Brandenburg A, Dell’olivo A, Bshary R, Kuhlemeier C (2009) The sweetest thing advances in nectar research. Curr Opin Plant Biol 12:1–5

    Article  Google Scholar 

  • Carter C, Thornburg RW (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci 9:320–324

    Article  CAS  PubMed  Google Scholar 

  • Carter C, Graham RA, Thornburg RW (1999) Nectarin I is a novel, soluble germin-like protein expressed in the nectar of Nicotiana sp. Plant Mol Biol 41:207–216

    Article  CAS  PubMed  Google Scholar 

  • Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97:3718–3723

    Article  CAS  PubMed  Google Scholar 

  • Davis AR (2001) Searching and breeding for structural features of flowers correlated with high nectar-carbohydrate production. Acta Hortic 561:107–121

    Google Scholar 

  • Davis A, Peterson R, Shuel R (1986) Anatomy and vasculature of the floral nectaries of Brassica napus (Brassicaceae). Can J Bot 64:2508–2516

    Article  Google Scholar 

  • Davis AR, Fowke LC, Sawhney VK, Low NH (1996) Floral nectar secretion and ploidy in Brassica rapa and B. napus (Brassicaceae) II. Quantified variability of nectary structure and function in rapid-cycling lines. Ann Bot 77:223–234

    Article  Google Scholar 

  • Davis AR, Pylatuik JD, Paradis JC, Low NH (1998) Nectar-carbohydrate production and composition vary in relation to nectary anatomy and location within individual flowers of several species of Brassicaceae. Planta 205:305–318

    Article  CAS  PubMed  Google Scholar 

  • De la Barrera E, Nobel PS (2004) Nectar: properties, floral aspects, and speculations on origin. Trends Plant Sci 9:65–69

    Article  PubMed  CAS  Google Scholar 

  • Deeken R, Geiger D, Fromm J, Koroleva O, Ache P, Langenfeld-Heyser R, Sauer N, May ST, Hedrich R (2002) Loss of the AKT2/3 potassium channel affects sugar loading into the phloem of Arabidopsis. Planta 216:334–344

    Article  CAS  PubMed  Google Scholar 

  • Deinzer ML, Thomson PA, Burgett DM, Isaacson DL (1977) Pyrrolizidine alkaloids: their occurrence in honey from tansy ragwort (Senecio jacobaea L.). Science 195:497–499

    Article  CAS  PubMed  Google Scholar 

  • Di Sansebastiano GP, Paris N, Marc-Martin S, Neuhaus JM (2001) Regeneration of a lytic central vacuole and of neutral peripheral vacuoles can be visualized by green fluorescent proteins targeted to either type of vacuoles. Plant Physiol 126:78–86

    Article  CAS  PubMed  Google Scholar 

  • Durkee LT (1982) The floral and extra-floral nectaries of Passiflora. II. The extra-floral nectary. Am J Bot 69:1420–1428

    Article  Google Scholar 

  • Durkee LT (1983) The ultrastructure of floral and extrafloral nectaries. In: Bentley B, Elias T (eds) The biology of nectaries. Columbia University Press, New York, pp 1–29

    Google Scholar 

  • Ecroyd CE, Franich RA, Kroese HW, Steward D (1995) Volatile constituents of Cactylanthus taylorii flower nectar in relation to flower pollination and browsing by animals. Phytochemistry 40:1387–1389

    Article  CAS  Google Scholar 

  • Elias T, Gelband H (1977) Morphology, anatomy, and relationship of extrafloral nectaries and hydathodes in two species of Impatiens (Balsaminaceae). Botanical Gazette 138:206–212

    Article  Google Scholar 

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

    Google Scholar 

  • Fahn A (1979a) Secretory tissues in plants. Academic Press, London

    Google Scholar 

  • Fahn A (1979b) Ultrastructure of nectaries in relation to nectar secretion. Am J Bot 66:977–985

    Article  CAS  Google Scholar 

  • Fahn A (1988) Tansley review No. 14 secretory tissues in vascular plants. New Phytol 108:229–257

    Article  Google Scholar 

  • Fallahi H, Scofield GN, Badger MR, Chow WS, Furbank RT, Ruan YL (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J Exp Bot 59:3283–3295

    Article  CAS  PubMed  Google Scholar 

  • Ferreres F, Andrade P, Gil MI, Tomas Barberan FA (1996) Floral nectar phenolics as biochemical markers for the botanical origin of heather honey. Z Lebensm Unters Forsch 202:40–44

    Article  CAS  Google Scholar 

  • Galliot C, Hoballah ME, Kuhlemeier C, Stuurman J (2006a) Genetics of flower size and nectar volume in Petunia pollination syndromes. Planta 225:203–212

    Article  CAS  PubMed  Google Scholar 

  • Galliot C, Stuurman J, Kuhlemeier C (2006b) The genetic dissection of floral pollination syndromes. Curr Opin Plant Biol 9:78–82

    Article  CAS  PubMed  Google Scholar 

  • Ge YX, Angenent GC, Wittich PE, Peters J, Franken J, Busscher M, Zhang LM, Dahlhaus E, Kater MM, Wullems GJ, Creemers-Molenaar T (2000) NEC1, a novel gene, highly expressed in nectary tissue of Petunia hybrida. Plant J 24:725–734

    Article  CAS  PubMed  Google Scholar 

  • Grebe M, Xu J, Mobius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387

    Article  CAS  PubMed  Google Scholar 

  • Griebel C, Hess G (1990) The vitamin C content of flower nectar of certain Labiatae. Z Unters Lebensm 79:168–171

    Article  Google Scholar 

  • Heil M (2004) Induction of two indirect defences benefits Lima bean (Phaseolus lunatus, Fabaceae) in nature. J Ecol 92:527–536

    Article  Google Scholar 

  • Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair K (2001) Extrafloral nectar production of the ant-associated plant, Macaranga tanarius, is an induced, indirect, defensive response elicited by jasmonic acid. Proc Natl Acad Sci USA 98:1083–1088

    Article  CAS  PubMed  Google Scholar 

  • Heinrich G (1989) Analysis of cations in nectars by means of a laser microprobe mass analyser (LAMMA). Beitr Biol Pflanz 64:293–308

    Google Scholar 

  • Hoffmann MH, Bremer M, Schneider K, Burger F, Stolle E, Moritz G (2003) Flower visitors in a natural population of Arabidopsis thaliana. Plant Biol 5:491–494

    Article  Google Scholar 

  • Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase A1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191–2209

    Article  CAS  PubMed  Google Scholar 

  • Jolivet P (1992) Insects and plants: parallel evolution & adaptations. CRC Press, Boca Raton

    Google Scholar 

  • Kram BW, Bainbridge EA, Perera MADN, Carter C (2008) Identification, cloning and characterization of a GDSL lipase secreted into the nectar of Jacaranda mimosifolia. Plant Mol Biol 68:173–183

    Article  CAS  PubMed  Google Scholar 

  • Kram BW, Xu WW, Carter CJ (2009) Uncovering the Arabidopsis thaliana nectary transcriptome: investigation of differential gene expression in floral nectariferous tissues. BMC Plant Biol 9:92

    Article  PubMed  CAS  Google Scholar 

  • Lee JY, Baum SF, Alvarez J, Patel A, Chitwood DH, Bowman JL (2005a) Activation of CRABS CLAW in the nectaries and carpels of Arabidopsis. Plant Cell 17:25–36

    Article  CAS  PubMed  Google Scholar 

  • Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL (2005b) Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132:5021–5032

    Article  CAS  PubMed  Google Scholar 

  • Matile P (1956) On the metabolism and the auxin dependence of nectar secretion. Berichte der Schweizerischen Botanischen Gesellschaft 66:237–266

    CAS  Google Scholar 

  • McKim SM, Stenvik GE, Butenko MA, Kristiansen W, Cho SK, Hepworth SR, Aalen RB, Haughn GW (2008) The BLADE-ON-PETIOLE genes are essential for abscission zone formation in Arabidopsis. Development 135:1537–1546

    Article  CAS  PubMed  Google Scholar 

  • Mishra R, Sharma S (1988) Growth regulators affect nectar-pollen production and insect foraging in Brassica seed crops. Curr Sci India 57:1297–1299

    CAS  Google Scholar 

  • Nelson DE, Glaunsinger B, Bohnert HJ (1997) Abundant accumulation of the calcium-binding molecular chaperone calreticulin in specific floral tissues of Arabidopsis thaliana. Plant Physiol 114:29–37

    Article  CAS  PubMed  Google Scholar 

  • Nepi M (2007) Nectary structure and ultrastructure. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 129–166

    Chapter  Google Scholar 

  • Nepi M, Stpiczynska M (2008) The complexity of nectar: secretion and resorption dynamically regulate nectar features. Naturwissenschaften 95:177–184

    Article  CAS  PubMed  Google Scholar 

  • Nieuwhof M (1963) Pollination and contamination of Brassica oleracea L. Euphytica 12:17–26

    Article  Google Scholar 

  • Nieuwhof M (1969) Cole crops. Leonard Hill, London

    Google Scholar 

  • Pacini E, Nepi M (2007) Nectar production and presentation. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 167–214

    Chapter  Google Scholar 

  • Pai H, Mariani C, Kao T (1997) Cytological study of pollen tube growth and early seed development in Petunia inflata. J Plant Biol 40:212–219

    Article  Google Scholar 

  • Pearson OH (1933) Study of the life history of Brassica oleracea. Bot Gaz 94:534–550

    Article  Google Scholar 

  • Peng YB, Li YQ, Hao YJ, Xu ZH, Bai SN (2004) Nectar production and transportation in the nectaries of the female Cucumis sativus L. flower during anthesis. Protoplasma 224:71–78

    CAS  PubMed  Google Scholar 

  • Peumans WJ, Smeets K, Van Nerum K, Van Leuven F, Van Damme EJ (1997) Lectin and alliinase are the predominant proteins in nectar from leek (Allium porrum L.) flowers. Planta 201:298–302

    Article  CAS  PubMed  Google Scholar 

  • Pichersky E, Gershenzon J (2002) The formation and function of plant volatiles: perfumes for pollinator attraction and defense. Curr Opin Plant Biol 5:237–243

    Article  CAS  PubMed  Google Scholar 

  • Rahman KA (1940) Insect pollinators of toria (Brassica napus Linn., var. dichotoma prain) and sarson (B. campestris Linn., var. sarson prain) at Lyallpur. Indian J Agr Sci 10:422–447

    Google Scholar 

  • Rathman ES, Lanza J, Wilson J (1990) Feeding preferences of flesh flies (Sarcophaga bullata) for sugar-only vs. sugar-amino acid nectars. Am Midl Nat 124:379–389

    Article  Google Scholar 

  • Ren G, Healy RA, Klyne AM, Horner HT, James MG, Thornburg RW (2007a) Transient starch metabolism in ornamental tobacco floral nectaries regulates nectar composition and release. Plant Sci 173:277–290

    Article  CAS  Google Scholar 

  • Ren G, Healy RA, Horner HT, Martha GJ, Thornburg RW (2007b) Expression of starch metabolic genes in the developing nectaries of ornamental tobacco plants. Plant Sci 173:621–637

    Article  CAS  Google Scholar 

  • Robert HS, Friml J (2009) Auxin and other signals on the move in plants. Nature Chemical Biology 5:325–332

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T (1999) Source-sink regulation by sugar and stress. Curr Opin Plant Biol 2:198–206

    Article  CAS  PubMed  Google Scholar 

  • Roshchina VV, Roshchina VD (1993) The excretory function of higher plants. Springer-Verlag, New York

    Google Scholar 

  • Rusterholz HP, Erhardt A (2000) Can nectar properties explain sex-specific flower preferences in the Adonis blue butterfly Lysandra bellargus? Ecol Entomol 25:81–90

    Article  Google Scholar 

  • Schmid R, Alpert PH (1977) A test of Burk’s hypothesis relating anther dehiscence to nectar secretion. New Phytol 78:487–498

    Article  Google Scholar 

  • Seo HS, Song JT, Cheong JJ, Lee YH, Lee YW, Hwang I, Lee JS, Choi YD (2001) Jasmonic acid carboxyl methyltransferase: a key enzyme for jasmonate-regulated plant responses. Proc Natl Acad Sci USA 98:4788–4793

    Article  CAS  PubMed  Google Scholar 

  • Sherson SM, Alford HL, Forbes SM, Wallace G, Smith SM (2003) Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis. J Exp Bot 54:525–531

    Article  CAS  PubMed  Google Scholar 

  • Shuel RW (1959) Studies of nectar secretion in excised flowers. II. The influence of certain growth regulators and enzyme inhibitors. Can J Bot 37:1167–1180

    Article  Google Scholar 

  • Shuel RW (1964) Nectar secretion in excised flowers. III. The dual effect of indolyl-3-acetic acid. J Apicult Res 3:99–111

    CAS  Google Scholar 

  • Shuel RW (1978) Nectar secretion in excised flowers. V. Effects of indoleacetic acid and sugar supply on distribution of [14C]sucrose in flower tissues and nectar. Can J Bot 56:565–571

    Article  CAS  Google Scholar 

  • Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767

    Article  CAS  PubMed  Google Scholar 

  • Song JT, Seo HS, Song SI, Lee JS, Choi YD (2000) NTR1 encodes a floral nectary-specific gene in Brassica campestris L. ssp. pekinensis. Plant Mol Biol 42:647–655

    Article  CAS  PubMed  Google Scholar 

  • Stadler R, Truernit E, Gahrtz M, Sauer N (1999) The AtSUC1 sucrose carrier may represent the osmotic driving force for anther dehiscence and pollen tube growth in Arabidopsis. Plant J. 19:269–278

    Article  CAS  PubMed  Google Scholar 

  • Stuurman J, Hoballah ME, Broger L, Moore J, Basten C, Kuhlemeier C (2004) Dissection of floral pollination syndromes in petunia. Genetics 168:1585–1599

    Article  CAS  PubMed  Google Scholar 

  • Tholl D, Chen F, Petri J, Gershenzon J, Pichersky E (2005) Two sesquiterpene synthases are responsible for the complex mixture of sesquiterpenes emitted from Arabidopsis flowers. Plant J 42:757–771

    Article  CAS  PubMed  Google Scholar 

  • Thoma S, Hecht U, Kippers A, Botella J, Devries S, Somerville C (1994) Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol 105:35–45

    Article  CAS  PubMed  Google Scholar 

  • Tian GW, Mohanty A, Chary SN, Li S, Paap B, Drakakaki G, Kopec CD, Li J, Ehrhardt D, Jackson D, Rhee SY, Raikhel NV, Citovsky V (2004) High-throughput fluorescent tagging of full-length Arabidopsis gene products in planta. Plant Physiol 135:25–38

    Article  CAS  PubMed  Google Scholar 

  • Vesely V (1962) The economic effectiveness of bee pollination on winter rape (Brassica napus L., var. oleifera metz.). Min Zemedel Lesn a Vodniho Hospodar Ust Vedtach Inform Zemedel Ekon 8:659–673

    Google Scholar 

  • Vogel S (1969) Flowers offering fatty oil instead of nectar. Abstracts XIth International Botany Congress Seattle, WA

  • Vogel S (1998) Remarkable nectaries: structure, ecology, organophyletic perspectives IV. Miscellaneous cases. Flora 193:225–248

    Google Scholar 

  • Wang YS, Motes CM, Mohamalawari DR, Blancaflor EB (2004) Green fluorescent protein fusions to Arabidopsis fimbrin 1 for spatio-temporal imaging of F-actin dynamics in roots. Cell Motil Cytoskeleton 59:79–93

    Article  CAS  PubMed  Google Scholar 

  • Weber LG (1958) Nutrition and reproduction in the Australian sheep blowfly Lucilia cuprina. Aust J Zool 6:139–144

    Article  Google Scholar 

  • Weijers D, Friml J (2009) Snapshot: auxin signaling and transport. Cell 136:U1172–U1200

    Article  CAS  Google Scholar 

  • Wenzler M, Holscher D, Oerther T, Schneider B (2008) Nectar formation and floral nectary anatomy of Anigozanthos flavidus: a combined magnetic resonance imaging and spectroscopy study. J Exp Bot 59:3425–3434

    Article  CAS  PubMed  Google Scholar 

  • Wist TJ, Davis AR (2006) Floral nectar production and nectary anatomy and ultrastructure of Echinacea purpurea (Asteraceae). Ann Bot 97:177–193

    Article  PubMed  Google Scholar 

  • Wist TJ, Davis AR (2008) Floral structure and dynamics of nectar production in Echinacea pallida var. angustifolia (Asteraceae). Int J Plant Sci 169:708–722

    Article  Google Scholar 

  • Zhu J, Hu ZH (2002) Cytological studies on the development of sieve element and floral nectary tissue in Arabidopsis thaliana. Acta Bot Sin 44:9–14

    Google Scholar 

  • Zhu J, Hu Z, Muuml IM (1995) Ultrastructural investigations on floral nectary of Arabidopsis thaliana prepared by high pressure freezing and freeze substitution. Biol Cell 84:225

    Article  Google Scholar 

  • Zhu J, Hu ZH, Müller M (1997) Ultrastructure of the floral nectary of Arabidopsis thaliana L. prepared from high pressure freezing and freeze substitution. Acta Bot Sin 39:289–295

    Google Scholar 

Download references

Acknowledgments

We apologize to the authors of many relevant articles not discussed earlier in this article due to space constraints. Thanks are given Mr. Jeffery Ruhlmann for providing the laser-scanning confocal microscopy image utilized herein and to Dr. Art Davis, University of Saskatchewan, for providing invaluable critical feedback on the manuscript. Portions of this work were previously unpublished and supported by funds from the United States Department of Agriculture (2006-35301-16887 to C·C.) and the National Science Foundation (0820730 to C·C.).

Author information

Authors and Affiliations

  1. Department of Biology, University of Minnesota Duluth, 1035 Kirby Dr, 207 Swenson Science Building, Duluth, MN, 55812, USA

    Brian W. Kram & Clay J. Carter

Authors
  1. Brian W. Kram
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Clay J. Carter
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Clay J. Carter.

Additional information

Communicated by Scott Russell.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kram, B.W., Carter, C.J. Arabidopsisthaliana as a model for functional nectary analysis. Sex Plant Reprod 22, 235–246 (2009). https://doi.org/10.1007/s00497-009-0112-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00497-009-0112-5

Keywords

Search

Navigation