Feeding on prey increases photosynthetic efficiency in the carnivorous sundew Drosera capensis
Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
24201141
PubMed Central
PMC3864725
DOI
10.1093/aob/mct254
PII: mct254
Knihovny.cz E-zdroje
- Klíčová slova
- Carnivorous plant, Drosera capensis, cape sundew, cost/benefit, digestive enzymes, fruit flies, nitrogen, phosphorus, photosynthesis, sundew,
- MeSH
- chlorofyl a MeSH
- chlorofyl analýza MeSH
- Drosera fyziologie MeSH
- Drosophila melanogaster MeSH
- dusík metabolismus MeSH
- enzymy metabolismus MeSH
- fosfor metabolismus MeSH
- fotosyntéza fyziologie MeSH
- listy rostlin fyziologie MeSH
- masožravci * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- chlorofyl a MeSH
- chlorofyl MeSH
- dusík MeSH
- enzymy MeSH
- fosfor MeSH
UNLABELLED: BACKROUND AND AIMS: It has been suggested that the rate of net photosynthesis (AN) of carnivorous plants increases in response to prey capture and nutrient uptake; however, data confirming the benefit from carnivory in terms of increased AN are scarce and unclear. The principal aim of our study was to investigate the photosynthetic benefit from prey capture in the carnivorous sundew Drosera capensis. METHODS: Prey attraction experiments were performed, with measurements and visualization of enzyme activities, elemental analysis and pigment quantification together with simultaneous measurements of gas exchange and chlorophyll a fluorescence in D. capensis in response to feeding with fruit flies (Drosophila melanogaster). KEY RESULTS: Red coloration of tentacles did not act as a signal to attract fruit flies onto the traps. Phosphatase, phophodiesterase and protease activities were induced 24 h after prey capture. These activities are consistent with the depletion of phosphorus and nitrogen from digested prey and a significant increase in their content in leaf tissue after 10 weeks. Mechanical stimulation of tentacle glands alone was not sufficient to induce proteolytic activity. Activities of β-D-glucosidases and N-acetyl-β-D-glucosaminidases in the tentacle mucilage were not detected. The uptake of phosphorus from prey was more efficient than that of nitrogen and caused the foliar N:P ratio to decrease; the contents of other elements (K, Ca, Mg) decreased slightly in fed plants. Increased foliar N and P contents resulted in a significant increase in the aboveground plant biomass, the number of leaves and chlorophyll content as well as AN, maximum quantum yield (Fv/Fm) and effective photochemical quantum yield of photosystem II (ΦPSII). CONCLUSIONS: According to the stoichiometric relationships among different nutrients, the growth of unfed D. capensis plants was P-limited. This P-limitation was markedly alleviated by feeding on fruit flies and resulted in improved plant nutrient status and photosynthetic performance. This study supports the original cost/benefit model proposed by T. Givnish almost 30 years ago and underlines the importance of plant carnivory for increasing phosphorus, and thereby photosynthesis.
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Adamec L. Mineral nutrition of carnivorous plants – a review. Botanical Review. 1997;63:273–299.
Adamec L. Leaf absorption of mineral nutrients in carnivorous plants stimulates root nutrient uptake. New Phytologist. 2002;155:89–100. PubMed
Adamec L. Respiration and photosynthesis of bladders and leaves of aquatic Utricularia species. Plant Biology. 2006;8:765–769. PubMed
Adamec L. The influence of prey capture on photosynthetic rate in two aquatic carnivorous plant species. Aquatic Botany. 2008;89:66–70.
Adamec L. Dark respiration of leaves and traps of terrestrial carnivorous plants: are there greater energetic costs in traps? Central European Journal of Biology. 2010;5:121–124.
Adamec L. Ecophysiological look at plant carnivory: why are plants carnivorous? In: Seckbach J, Dubinski Z, editors. All flesh is grass. Plant-animal interrelationships. Cellular origin, life in extreme habitats and astrobiology. Vol. 16. Dordrecht: Springer Science + Business Media; 2011a. pp. 455–489.
Adamec L. By which mechanism does prey capture enhance plant growth in aquatic carnivorous plants: stimulation of shoot apex? Fundamental and Applied Limnology. 2011b;178:171–176.
Adamec L, Sirová D, Vrba J, Rejmánková E. Enzyme production in the traps of aquatic Utricularia species. Biologia. 2010;65:273–278.
Adlassnig W, Koller-Peroutka M, Bauer S, Koshkin E, Lendl T, Lichtscheidl IK. Endocytotic uptake of nutrients in carnivorous plants. Plant Journal. 2012;71:303–313. PubMed
Amagase S, Mori M, Nakayama S. Digestive enzymes in insectivorous plants IV. Enzymatic digestion of insects by Nepenthes secretion and Drosera peltata extract: proteolytic and chitinolytic activities. Journal of Biochemistry. 1972;72:765–767. PubMed
Bennett KF, Ellison AM. Nectar, not colour, may lure insects to their death. Biology Letters. 2009;5:469–472. PubMed PMC
Brearley FQ, Mansur M. Nutrient stoichiometry of Nepenthes species from a Bornean peat swamp forest. Carnivorous Plant Newsletter. 2012;41:105–108.
Briscoe AD, Chittka L. The evolution of color vision in insects. Annual Review of Entomology. 2001;46:471–510. PubMed
Brunner F, Stintzi A, Fritig B, Legrand M. Substrate specifities of tobacco chitinases. Plant Journal. 1998;14:225–234. PubMed
Butler JL, Ellison AM. Nitrogen cycling dynamics in the carnivorous northern pitcher plant, Sarracenia purpurea. Functional Ecology. 2007;21:835–843.
Chandler GE, Anderson JW. Studies on the origin of some hydrolytic enzymes associated with the leaves and tentacles of Drosera species and their role in heterotrophic nutrition. New Phytologist. 1976a;77:51–62.
Chandler GE, Anderson JW. Studies of the nutrition and growth of Drosera species with reference to the carnivorous habit. New Phytologist. 1976b;76:129–141.
Clancy FG, Coffey MD. Acid phosphatase and protease release by the insectivorous plant Drosera rotundifolia. Canadian Journal of Botany. 1977;55:480–488.
Darwin C. Insectivorous plants. London: John Murray; 1875.
Dixon KW, Pate JS, Bailey WJ. Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves. Australian Journal of Botany. 1980;28:283–297.
Di Giusto B, Bessière J-M, Guéroult M, et al. Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. Journal of Ecology. 2010;98:845–856.
Eilenberg H, Pnini-Cohen S, Schuster S, Movtchan A, Zilberstein A. Isolation and characterization of chitinase genes from pitchers of the carnivorous plant Nepenthes khasiana. Journal of Experimental Botany. 2006;57:2775–2784. PubMed
Ellison AM. Nutrient limitation and stoichiometry of carnivorous plants. Plant Biology. 2006;8:740–747. PubMed
Ellison AM, Adamec L. Ecophysiological traits of terrestrial and aquatic carnivorous plants: are the costs and benefits the same? Oikos. 2011;120:1721–1731.
Ellison AM, Gotelli NJ. Evolutionary ecology of carnivorous plants. Trends in Ecology & Evolution. 2001;16:623–629.
Ellison AM, Gotelli NJ. Energetics and the evolution of carnivorous plants – Darwin's ‘most wonderful plants in the world. Journal of Experimental Botany. 2009;60:19–42. PubMed
Farnsworth EJ, Ellison AM. Prey availability directly affects physiology, growth, nutrient allocation and scaling relationships among leaf traits in 10 carnivorous plant species. Journal of Ecology. 2008;96:213–221.
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD. Carnivory in the bromeliad Brocchinia reducta with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient poor habitats. American Naturalist. 1984;124:479–497.
Hatano N, Hamada T. Proteomic analysis of secreted protein induced by a component of prey in pitcher fluid of the carnivorous plant Nepenthes alata. Journal of Proteomics. 2012;75:4844–4852. PubMed
He J, Zain A. Photosynthesis and nitrogen metabolism of Nepenthes alata in response to inorganic NO3− and organic prey N in the greenhouse. International Scholarly Research Network Botany. 2012 ID 263270.
Heslop-Harrison Y. Enzyme release in carnivorous plants. In: Dingle JT, Dean RT, editors. Lysosomes in biology and pathology. Amsterdam: North-Holland; 1975. pp. 527–578.
Ichiishi S, Nagamitsu T, Kondo Y, Iwashina T, Kondo K, Tagashira N. Effects of macro-components and sucrose in the medium on in vitro red-color pigmentation in Dionaea muscipula Ellis and Drosera spathulata Labill. Plant Biotechnology. 1999;16:235–238.
Ishisaki K, Arai S, Hamada T, Honda Y. Biochemical characterization of a recombinant plant class III chitinase from the pitcher of the carnivorous plant Nepenthes alata. Carbohydrate Research. 2012;361:170–174. PubMed
Juniper BE, Robins RJ, Joel DM. The carnivorous plants. London: Academic Press; 1989.
Jürgens A, El-Sayed AM, Suckling DM. Do carnivorous plants use volatiles for attracting prey insects? Functional Ecology. 2009;23:875–887.
Karagatzides JD, Ellison AM. Construction costs, payback times, and the leaf economics of carnivorous plants. American Journal of Botany. 2009;96:1612–1619. PubMed
Karlsson PS, Pate JS. Contrasting effects of supplementary feeding of insects or mineral nutrients on the growth and nitrogen and phosphorus economy of pygmy species of Drosera. Oecologia. 1992;92:8–13. PubMed
Kováčik J, Klejdus B, Štork F, Hedbavny J. Prey-induced changes in the accumulation of amino acids and phenolic metabolites in the leaves of Drosera capensis L. Amino Acids. 2012;42:1277–1285. PubMed
Król E, Płachno BJ, Adamec L, Stolarz M, Dziubińska H, Trębacz K. Quite a few reasons for calling carnivores ‘the most wonderful plants in the world. Annals of Botany. 2012;109:47–64. PubMed PMC
Laakkonen L, Jobson RW, Albert VA. A new model for the evolution of carnivory in the bladderwort plant (Utricularia): adaptive changes in cytochrome c oxidase (COX) provide respiratory power. Plant Biology. 2006;8:569–593. PubMed
Libantová J, Kämäräinen T, Moravčíková J, Matušíková I, Salaj J. Detection of chitinolytic enzymes with different substrate specificity in tissue of intact sundew (Drosera rotundifolia L.) Molecular Biology Reports. 2009;36:851–856. PubMed
Lichtenthaler HK. Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology. 1987;148:350–382.
Matušíková I, Salaj J, Moravčíková J, Mlynárová L, Nap JP, Libantová J. Tentacles of in vitro-grown round-leaf sundew (Drosera rotundifolia L.) show induction of chitinase activity upon mimicking the presence of prey. Planta. 2005;222:1020–1027. PubMed
Maxwell K, Johnson GN. Chlorophyll fluorescence – a practical guide. Journal of Experimental Botany. 2000;51:659–668. PubMed
McNally SF, Stewart A, Wilson UE. The stimulation of acid phosphatase activity in the stalked gland of Drosera rotundifolia. Annals of Botany. 1988;61:289–292.
Méndez M, Karlsson PS. Costs and benefits of carnivory in plants: insights from the photosynthetic performance of four carnivorous plants in a subarctic environment. Oikos. 1999;86:105–112.
Millett J, Jones RI, Waldron S. The contribution of insect prey to the total nitrogen content of sundews (Drosera spp.) determined in situ by stable isotope analysis. New Phytologist. 2003;158:527–534. PubMed
Moran JA, Moran AJ. Foliar reflectance and vector analysis reveal nutrient stress in prey-deprived pitcher plants (Nepenthes rafflesiana) International Journal of Plant Sciences. 1998;159:996–1001.
Moran JA, Booth WE, Charles JK. Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture. Annals of Botany. 1999;83:521–528.
Moran JA, Clarke CH, Gowen BE. The use of light in prey capture by the tropical pitcher plant Nepenthes aristolochioides. Plant Signaling & Behavior. 2012;7:957–960. PubMed PMC
Nakamura Y, Reichelt M, Mayer VE, Mithöfer A. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proceedings of the Royal Society B: Biological Sciences. 2013;280:20130228. PubMed PMC
Olde Venterink H, Pieterse NM, Belgers JDM, Wassen MJ, De Ruiter PC. N, P and K budgets along nutrient availability and productivity gradients in wetlands. Ecological Applications. 2002;12:1010–1026.
Olde Venterink H, Wassen MJ, Verkroost AWM, De Ruiter PC. Species richness-productivity patterns differ between N-, P-, and K-limited wetlands. Ecology. 2003;84:2191–2199.
Osunkoya OO, Daud SD, Di-Giusto B, Wimmer FL, Holige TM. Construction costs and physico-chemical properties of the assimilatory organs of Nepenthes species in northern Borneo. Annals of Botany. 2007;99:895–906. PubMed PMC
Pavlovič A, Masarovičová E, Hudák J. Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. Annals of Botany. 2007;100:527–536. PubMed PMC
Pavlovič A, Singerová L, Demko V, Hudák J. Feeding enhances photosynthetic efficiency in the carnivorous pitcher plant Nepenthes talangensis. Annals of Botany. 2009;104:307–314. PubMed PMC
Pavlovič A, Demko V, Hudák J. Trap closure and prey retention in Venus flytrap (Dionaea muscipula) temporarily reduces photosynthesis and stimulates respiration. Annals of Botany. 2010;105:37–44. PubMed PMC
Pavlovič A, Slováková Ľ, Pandolfi C, Mancuso S. On the mechanism underlying photosynthetic limitation upon trigger hair irritation in the carnivorous plant Venus flytrap (Dionaea muscipula Ellis) Journal of Experimental Botany. 2011a;62:1991–2000. PubMed PMC
Pavlovič A, Slováková Ľ, Šantrůček J. Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria. Plant Cell and Environment. 2011b;34:1865–1873. PubMed
Peroutka M, Adlassnig W, Lendl T, Pranjić K, Lichtscheidl IK. Functional biology of carnivorous plants. In: Teixeira da Silva JA, editor. Floriculture, Ornamental and Plant Biotechnology. V. Global Science Books; 2008. pp. 266–286.
Rischer H, Hamm A, Bringmann G. Nepenthes insignis uses a C2-portion of the carbon skeleton of L-alanine acquired via its carnivorous organs, to build up the allelochemical plumbagin. Phytochemistry. 2002;59:603–609. PubMed
Rost K, Schauer R. Physical and chemical properties of the mucin secreted by Drosera capensis. Phytochemistry. 1977;16:1365–1368.
Rottloff S, Stieber R, Maischak H, Turini FG, Heubl G, Mithöfer A. Functional characterization of a class III acid endochitinase from the traps of the carnivorous pitcher plant genus. Nepenthes. Journal of Experimental Botany. 2011;62:4639–4647. PubMed PMC
Schaefer HM, Ruxton GD. Fatal attraction: carnivorous plants roll out the red carpet to lure insects. Biology Letters. 2008;4:153–155. PubMed PMC
Schulze ED, Gebauer G, Schulze W, Pate JS. The utilization of nitrogen from insect capture by different growth forms of Drosera from Southwest Australia. Oecologia. 1991;87:240–246. PubMed
Schulze W, Schulze ED. Insect capture and growth of the insectivorous Drosera rotundifolia L. Oecologia. 1990;82:427–429. PubMed
Schulze W, Frommer WB, Ward JM. Transporters for ammonium, amino acids and peptides are expressed in pitchers of the carnivorous plant Nepenthes. Plant Journal. 1999;17:637–646. PubMed
Sirová D, Adamec L, Vrba J. Enzymatic activities in traps of four aquatic species of the carnivorous genus Utricularia. New Phytologist. 2003;159:669–675. PubMed
Takahashi K, Suzuki T, Nishii W, Kubota K, Shibata C, Isobe T, Dohmae N. A cysteine endopeptidase (‘dionain’) is involved in the digestive fluid of Dionaea muscipula (Venus's fly-trap) Bioscience, Biotechnology & Biochemistry. 2011;75:346–348. PubMed
Takahashi K, Nishii W, Shibata C. The digestive fluid of Drosera indica contains a cysteine endopeptidase (‘droserain’) similar to dionain from Dionaea muscipula. Carnivorous Plant Newsletter. 2012;41:132–134.
Thorén LM, Tuomi J, Kämäräinen T, Laine K. Resource availability affects investment in carnivory in Drosera rotundifolia. New Phytologist. 2003;159:507–511. PubMed
Wakefield AE, Gotelli NJ, Wittman SE, Ellison AM. Prey addition alters nutrient stoichiometry of the carnivorous plant Sarracenia purpurea. Ecology. 2005;86:1737–1743.
A novel insight into the cost-benefit model for the evolution of botanical carnivory