Skip to main content
Log in

Phloem Sugar Flux and Jasmonic Acid-Responsive Cell Wall Invertase Control Extrafloral Nectar Secretion in Ricinus communis

  • Published:
Journal of Chemical Ecology Aims and scope Submit manuscript

Abstract

Plants secrete extrafloral nectar (EFN) that attracts predators. The efficiency of the resulting anti-herbivore defense depends on the quantity and spatial distribution of EFN. Thus, according to the optimal defense hypothesis (ODH), plants should secrete EFN on the most valuable organs and when herbivore pressure is high. Ricinus communis plants secreted most EFN on the youngest (i.e., most valuable) leaves and after the simulation of herbivory via the application of jasmonic acid (JA). Here, we investigated the physiological mechanisms that might produce these seemingly adaptive spatiotemporal patterns. Cell wall invertase (CWIN; EC 3.2.1.26) was most active in the hours before peak EFN secretion, its decrease preceded the decrease in EFN secretion, and CWIN activity was inducible by JA. Thus, CWIN appears to be a central player in EFN secretion: its activation by JA is likely to cause the induction of EFN secretion after herbivory. Shading individual leaves decreased EFN secretion locally on these leaves with no effect on CWIN activity in the nectaries, which is likely to be because it decreased the content of sucrose, the substrate of CWIN, in the phloem. Our results demonstrate how the interplay of two physiological processes can cause ecologically relevant spatiotemporal patterns in a plant defense trait.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Appel HM, Arnold TM, Schultz JC (2012) Effects of jasmonic acid, branching and girdling on carbon and nitrogen transport in poplar. New Phytol 195:419–426

    Article  CAS  PubMed  Google Scholar 

  • Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593

    Article  Google Scholar 

  • Arnold T, Appel HM, Patel V, Stocum E, Kavalier A, Schultz JC (2004) Carbohydrate translocation determines the phenolic content of Populus foliage: a test of the sink–source model of plant defense. New Phytol 164:157–164

    Article  CAS  Google Scholar 

  • Baker DA, Hall JL, Thorpe JR (1978) A study of the extrafloral nectaries of Ricinus communis. New Phytol 81:129–137

    Article  CAS  Google Scholar 

  • Bixenmann RJ, Coley PD, Kursar TA (2011) Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant-plant mutualism? Oecologia 165:417–425

    Article  CAS  PubMed  Google Scholar 

  • Bogatek R, Côme D, Corbineau F, Ranjan R, Lewak S (2002) Jasmonic acid affects dormancy and sugar catabolism in germinating apple embryos. Plant Physiol Biochem 40:167–173

    CAS  Google Scholar 

  • Bruinsma M, Ildema H, van Loon JJA, Dicke M (2008) Differential effects of jasmonic acid treatment of Brassica nigra on the attraction of pollinators, parasitoids, and butterflies. Entomol Exp Appl 128:109–116

    Article  CAS  Google Scholar 

  • Castrillon-Arbelaez P, Martinez-Gallardo N, Arnaut H, Tiessen A, Delano-Frier J (2012) Metabolic and enzymatic changes associated with carbon mobilization, utilization and replenishment triggered in grain amaranth (Amaranthus cruentus) in response to partial defoliation by mechanical injury or insect herbivory. BMC Plant Biol 12:163

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Chamberlain SA, Holland JN (2009) Quantitative synthesis of context dependency in ant-plant protection mutualisms. Ecology 90:2384–2392

    Article  PubMed  Google Scholar 

  • Claussen W, Loveys BR, Hawker JS (1985) Comparative investigations on the distribution of sucrose synthase activity and invertase activity within growing, mature and old leaves of some C3 and C4 plant species. Physiol Plant 65:275–280

    Article  CAS  Google Scholar 

  • Escalante-Pérez M, Jaborsky M, Lautner S, Fromm J, Müller T, Dittrich M, Kunert M, Boland W, Hedrich R, Ache P (2012) Poplar extrafloral nectaries: two types, two strategies of indirect defenses against herbivores. Plant Physiol 159:1176–1191

    Article  PubMed Central  PubMed  Google Scholar 

  • Gaffal KP (2012) How common is the ability of extrafloral nectaries to produce nectar droplets, to secrete nectar during the night and to store starch? Plant Biol 14:691–695

    Article  Google Scholar 

  • González-Teuber M, Heil M (2009) Nectar chemistry is tailored for both attraction of mutualists and protection from exploiters. Plant Signal Behav 4:809–813

    Article  PubMed Central  PubMed  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 (2008) Indirect defence via tritrophic interactions. New Phytol 178:41–61

    Article  CAS  PubMed  Google Scholar 

  • Heil M (2011) Nectar: generation, regulation and ecological functions. Trends Plant Sci 16:191–200

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Koch T, Hilpert A, Fiala B, Boland W, Linsenmair KE (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 U S A 98:1083–1088

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heil M, Greiner S, Meimberg H, Krüger R, Noyer J-L, Heubl G, Linsenmair KE, Boland W (2004) Evolutionary change from induced to constitutive expression of an indirect plant resistance. Nature 430:205–208

    Article  CAS  PubMed  Google Scholar 

  • Heil M, Büchler R, Boland W (2005) Quantification of invertase activity in ants under field conditions. J Chem Ecol 30:431–437

    Article  Google Scholar 

  • Heil M, Barajas-Barron A, Orona-Tamayo D, Wielsch N, Svatos A (2014) Partner manipulation stabilises a horizontally transmitted mutualism. Ecol Lett 17:185–192

    Article  PubMed  Google Scholar 

  • Herbers K, Meuwly P, Frommer WB, Metraux J-P, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holland JN, Chamberlain SA, Horn KC (2009) Optimal defence theory predicts investment in extrafloral nectar resources in an ant-plant mutualism. J Ecol 97:89–96

    Article  Google Scholar 

  • Kaplan I, Halitschke R, Kessler A, Rehill BJ, Sardanelli S, Denno RF (2008) Physiological integration of roots and shoots in plant defense strategies links above-and belowground herbivory. Ecol Lett 11:841–851

    Article  PubMed  Google Scholar 

  • Koricheva J, Romero GQ (2012) You get what you pay for: reward-specific trade-offs among direct and ant-mediated defences in plants. Biol Lett 8:628–630

    Article  PubMed Central  PubMed  Google Scholar 

  • Landgraf R, Schaarschmidt S, Hause B (2013) Repeated leaf wounding alters the colonization of Medicago truncatula roots by beneficial and pathogenic microorganisms. Plant Cell Environ 35:1344–1357

    Article  Google Scholar 

  • Lohaus G, Burba M, Heldt HW (1994) Comparison of the contents of sucrose and amino acids in the leaves, phloem sap and taproots of high and low sugar-producing hybrids of sugar beet (Beta vulgaris L.). J Exp Bot 45:1097–1101

    Article  CAS  Google Scholar 

  • Lunn JE, Hatch MD (1995) Primary partitioning and storage of photosynthate in sucrose and starch in leaves of C4 plants. Planta 197:385–391

    Article  CAS  Google Scholar 

  • Lüttge U (2013) Green nectaries: the role of photosynthesis in secretion. J Linn Soc Bot 173:1–11

    Article  Google Scholar 

  • Martin T, Frommer WB, Salanoubat M, Willmitzer L (1993) Expression of an Arabidopsis sucrose synthase gene indicates a role in metabolization of sucrose both during phloem loading and in sink organs. Plant J 4:367–377

    Article  CAS  PubMed  Google Scholar 

  • McKey D (1974) Adaptive patterns in alkaloid physiology. Am Nat 108:305–320

    Article  Google Scholar 

  • McKey D (1979) The distribution of secondary compounds within plants. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, New York, pp 55–133

    Google Scholar 

  • Nichol P, Hall JL (1988) Characteristics of nectar secretion by the extrafloral nectaries of Ricinus communis. J Exp Bot 39:573–586

    Article  CAS  Google Scholar 

  • Ohyama A, Nishimura S, Hirai M (1998) Cloning of cDNA for a cell wall-bound acid invertase from tomato (Lycopersicon esculentum) and expression of soluble and cell wall-bound invertases in plants and wounded leaves of L. esculentum and L. peruvianum. Genes Gen Syst 73:149–157

    Article  CAS  Google Scholar 

  • Orona-Tamayo D, Wielsch N, Escalante-Pérez M, Svatos A, Molina-Torres J, Muck A, Ramirez-Chávez E, Ádame-Alvarez R-M, Heil M (2013) Short-term proteomic dynamics reveal metabolic factory for active extrafloral nectar secretion by Acacia cornigera ant-plants. Plant J 73:546–554

    Article  CAS  PubMed  Google Scholar 

  • Pharr DM, Sox HN (1984) Changes in carbohydrate and enzyme levels during the sink to source transition of leaves of Cucumis sativus L., a stachyose translocator. Plant Sci Lett 35:187–193

    Article  CAS  Google Scholar 

  • Radhika V, Kost C, Bartram S, Heil M, Boland W (2008) Testing the optimal defence hypothesis for two indirect defences: extrafloral nectar and volatile organic compounds. Planta 228:449–457

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Radhika V, Kost C, Boland W, Heil M (2010a) The role of jasmonates in floral nectar secretion. PLoS One 5:e9265

    Article  PubMed Central  PubMed  Google Scholar 

  • Radhika V, Kost C, Mithöfer A, Boland W (2010b) Regulation of extrafloral nectar secretion by jasmonates in lima bean is light dependent. Proc Natl Acad Sci U S A 107:17228–17233

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 4–53

    Google Scholar 

  • Rogers WE, Siemann E, Lankau RA (2003) Damage induced production of extrafloral nectaries in native and invasive seedlings of Chinese tallow tree (Sapium sebiferum). Am Midl Nat 149:413–417

    Article  Google Scholar 

  • Roitsch T, González M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  PubMed  Google Scholar 

  • Rostás M, Eggert K (2008) Ontogenetic and spatio-temporal patterns of induced volatiles in Glycine max in the light of the optimal defence hypothesis. Chemoecology 18:29–38

    Article  Google Scholar 

  • Rosumek FB, Silveira FAO, Neves FD, Barbosa NPD, Diniz L, Oki Y, Pezzini F, Fernandes GW, Cornelissen T (2009) Ants on plants: a meta-analysis of the role of ants as plant biotic defenses. Oecologia 160:537–549

    Article  PubMed  Google Scholar 

  • Ruhlmann JM, Kram BW, Carter CJ (2010) CELL WALL INVERTASE 4 is required for nectar production in Arabidopsis. J Exp Bot 61:395–404

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Samarakoon AB, Rauser WE (1979) Carbohydrate levels and photoassimilate export from leaves of Phaseolus vulgaris exposed to excess cobalt, nickel, and zinc. Plant Physiol 63:1165–1169

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schaarschmidt S, González M-C, Roitsch T, Strack D, Sonnewald U, Hause B (2007) Regulation of arbuscular mycorrhization by carbon. The symbiotic interaction cannot be improved by increased carbon availability accomplished by root-specifically enhanced invertase activity. Plant Physiol 143:1827–1840

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schaffer AA, Sagee O, Goldschmidt EE, Goren R (1987) Invertase and sucrose synthase activity, carbohydrate status and endogenous IAA levels during citrus leaf development. Physiol Plant 69:151–155

    Article  CAS  Google Scholar 

  • Stephenson AG (1982) The role of the extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63:663–669

    Article  Google Scholar 

  • Sturm A, Chrispeels MJ (1990) cDNA cloning of carrot extracellular beta-fructosidase and its expression in response to wounding and bacterial infection. Plant Cell 2:1107–1119

    CAS  PubMed Central  PubMed  Google Scholar 

  • Turgeon R (1989) The sink-source transition in leaves. Annu Rev Plant Biol 40:119–138

    Article  Google Scholar 

  • Vassey TL (1989) Light/dark profiles of sucrose phosphate synthase, sucrose synthase, and acid invertase in leaves of sugar beets. Plant Physiol 89:347–351

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wäckers FL, Bonifay C (2004) How to be sweet? Extrafloral nectar allocation by Gossypium hirsutum fits optimal defense theory predictions. Ecology 85:1512–1518

    Article  Google Scholar 

  • Wäckers FL, Zuber D, Wunderlin R, Keller F (2001) The effect of herbivory on temporal and spatial dynamics of foliar nectar production in cotton and castor. Ann Bot 87:365–370

    Article  Google Scholar 

  • Weber MG, Keeler KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 111:1251–1261

    Article  PubMed Central  PubMed  Google Scholar 

  • Wooley SC, Donaldson JR, Gusse AC, Lindroth RL, Stevens MT (2007) Extrafloral nectaries in aspen (Populus tremuloides): heritable genetic variation and herbivore-induced expression. Ann Bot 100:1337–1346

    Article  PubMed Central  PubMed  Google Scholar 

  • Zangerl AR, Rutledge CE (1996) The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am Nat 147:599–608

    Article  Google Scholar 

  • Zhang L, Cohn NS, Mitchell JP (1996) Induction of a pea cell-wall invertase gene by wounding and its localized expression in phloem. Plant Physiol 112:1111–1117

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Antonio Cisneros for taking the photographs of R. communis, CINVESTAV-Irapuato for providing all field facilities and Caroline Woods as well as three anonymous referees for multiple valuable comments on an earlier version of this manuscript. CONACyT of México is gratefully acknowledged for financial support to DOT (grant: 191236) and MH (project grants: 129678 and 130656).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martin Heil.

Additional information

Cynthia Millán-Cañongo and Domancar Orona-Tamayo have contributed equally to this paper

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Millán-Cañongo, C., Orona-Tamayo, D. & Heil, M. Phloem Sugar Flux and Jasmonic Acid-Responsive Cell Wall Invertase Control Extrafloral Nectar Secretion in Ricinus communis . J Chem Ecol 40, 760–769 (2014). https://doi.org/10.1007/s10886-014-0476-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-014-0476-3

Keywords

Navigation