Jansen, Marcel A. K.

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Carnivorous plants and UV-radiation: a captivating story?

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Title Carnivorous plants and UV-radiation: a captivating story?Author(s) Jansen, Marcel A. K.Publication date 2017Original citation Jansen, M. (2017) “Carnivorous plants and UV-radiation; a captivatingstory?”, UV4Plants Bulletin, 2017(1), pp. 11-16. doi:10.19232/uv4pb.2017.1.12Type of publication Article (peer-reviewed)Link to publisher'sversionhttp://bulletin.uv4plants.org/index.php/uv4pbulletin/article/view/33http://dx.doi.org/10.19232/uv4pb.2017.1.12Access to the full text of the published version may require asubscription.Rights © 2017, the author. This work is licensed under a CreativeCommons Attribution-ShareAlike 4.0 International License.Authors, or their employers, will retain ownership of copyright.However, original publication in the Bulletin should be always citedupon republication in unaltered or altered form. The UV4PlantsBulletin contents will be published under one of the CreativeCommons Licenses, by default CC BY-SA 4.0, but at the request ofthe authors, other more restrictive (CC BY-ND 4.0, CC BY-NC 4.0)or less restrictive (CC BY 4.0) licenses can be used for individualarticles. https://creativecommons.org/https://creativecommons.org/licenses/by-sa/4.0/Item downloadedfromhttp://hdl.handle.net/10468/5394Downloaded on 2018-08-23T19:31:53ZUV4Plants Bulletin, 2017, no. 1 OpinionCarnivorous plants and UV-radiation: a captivating story?Marcel A. K. Jansen, ORCID: 0000-0003-2014-5859School of Biological, Earth and Environmental Sciences, UCC, Cork, IrelandDOI: 10.19232/uv4pb.2017.1.12 © 2017 The Author, licensed under (CC BY-SA 3.0)Carnivorous plants are “diﬀerent”, and thisfascinates people. The “appetite” of carnivor-ous plants has, on occasion, taken on myth-ical proportions. In “The Day of the Trif-ﬁds” giant, man-eating plants go on a ram-page, while in “Ice Age 3: Dawn of the Dino-saurs” a carnivorous plant gobbled up an en-tire mammoth. On a slightly less violent note,we have observed that carnivorous plantson our University College Cork recruitmentstand help attract high school students dur-ing open days, giving us a chance to advert-ise our undergraduate degree in plant bio-logy. A psychologist could probably writea PhD thesis on the fascination of humanswith carnivorous plants. However, let me justsay that if you are interested in these plants,you are in good company. Back in 1875,Charles Darwin wrote “Insectivorous Plants”,a book focussing heavily on Drosera sp (sun-dew) (Fig. 1A). In fact, Charles Darwin was sofascinated by these carnivorous plants thathe once stated that “at this present moment,I care more about the Drosera than the originof all the species in the world” (Darwin 1860).I surmise that Charles Darwin’s interest incarnivorous plants was inspired by his fam-ily. In fact, Dr. Erasmus Darwin, his grand-father, was already investigating how thetentacles of Drosera species respond to stim-uli (Cheers 1992). Another carnivorous plantaﬁcionado was Joseph Hooker (of Benthamand Hooker taxonomic fame) who as directorof Kew Gardens, London, was able to collectcarnivorous species from across the world.Hooker studied the digestive system of car-nivorous plants and concluded that “a sub-stance, acting as a pepsin is given oﬀ fromthe inner wall of a pitcher [of a Nepenthessp], but chieﬂy after placing the animal mat-ter in the acid ﬂuid” (Cheers 1992). Takentogether, these early observations summar-ise the main characteristics of carnivorousplants: their ability to capture and digestprey (insects, arthropods, and even smallmammals) for the purpose of plant nourish-ment. In fact, there is not a lot else thatthe diﬀerent taxa of carnivorous plants share.The nearly 600 species of carnivorous plantsthat occur across nine families and diﬀer-ent taxa are not necessarily closely related.Indeed, there is strong evidence that car-nivory in plants has evolved independentlyon at least nine separate occasions (Givnish2014). Their trapping structures are highlydiverse, and these include the sticky leavesand/or responsive tentacles (like those ob-served by Erasmus Darwin), pitfall traps orpitchers with digestive juices (as studied byJoseph Hooker), hinged-trapping leaves in Di-onaea sp (Venus ﬂy trap) and bladder-trapsin Utricularia sp (bladderwort). In general,there is good understanding of the actualmechanical responses involved in capturingprey as well as the subsequent digestive pro-cesses involved in extracting nutrients fromthe prey. What is typically less clear iswhy any insect (or other prey) would ven-ture near the trapping-structure of a carni-vorous plant. Secreted nectar, scent and trap©2017 by the authors 115 M. A. K. Jansen: Carnivorous plants and UV-radiationFigure 5.1: Drosera rotundifolia plants in visible light (A) and under UV radiation (B) showing reﬂect-ance of tentacles. Copyright O. Holovachov (http://www.holovachov.com).shape and colour are often listed as key at-tractants for insects (Joel et al. 1985), with insome cases ﬂowers emitting diﬀerent scentsas the trapping-structure to avoid potentialpollinator-prey conﬂicts (Ho et al. 2016). Yet,it has also been suggested that UV-radiationplays a role in prey attraction (Joel et al.1985). In fact, in 2012/2013 several ma-jor news outlets reported that “These Carni-vorous Plants Glow Under Ultraviolet Lightto Attract Prey” (Smithsonian.com, Decem-ber 11, 2013), “Carnivorous Plants Glow toAttract Prey” (National Geographic, February25, 2013), and “Carnivorous plant speciesglow blue to lure prey” (BBC Nature, February19, 2013). These stories referred to strongUV-induced ﬂuorescence, which was reputedto attract prey, and an example of which isshown in ﬁgure 2. Here, I will explore theevidence for a role of UV-radiation in attract-ing prey, and identify some of the gaps inour understanding of this putative role of UV-radiation.It has long been known that ﬂoral patternsof UV-reﬂection or absorbance play a keyrole in pollination biology (Brock et al. 2016;Cronin and Bok 2016). Such ﬂoral UV pat-terns are common. Indeed, the UV4Plantsbulletin (Issue 1, 2016) displayed a photo-graph which showed UV-patterns in dan-delion ﬂowers. These patterns are thoughtto contribute to attracting or deterring ofspeciﬁc insects, serve as plant-species spe-ciﬁc markers and/or as orientation cues. Joelet al. (1985) noted the conceptual similar-ities between ﬂowers attracting pollinatorsand carnivorous plants attracting prey. Us-ing UV-photography, Joel et al. (1985) sur-veyed UV-patterns in the trapping structuresof carnivorous plants. The authors tooktheir photos under natural sunlight condi-tions using ﬁlters that transmit between 305and 385 nm. Their study showed that vari-ous carnivorous plants have “conspicuousUV patterns” on or near their traps. Thepitchers of Heliamphora display a clear UV-reﬂecting entrance to the beaker-structure.In contrast, Sarracenia pitchers contain UV-absorbing nectar, while in Drosophyllum spe-cies the old leaves are UV-reﬂecting, whilstthe young, carnivorous leaves in the centreof the plant are UV-absorbing and appear12 ©2017 by the authorsUV4Plants Bulletin, 2017, no. 1Figure 5.2: Blue ﬂuorescence emitted by the rim of a Nepenthes alata beaker. Copyright O. Holo-vachov (http://www.holovachov.com).as a relatively dark environment. A recentphotograph of UV-reﬂectance in Drosera ro-tundifolia by Oleksandr Holovachov showsreﬂectance of tentacles (Figure 1B). Kurupet al. (2013) took the study of UV-patternsa step further by scanning the ﬂuorescenceof trapping structures using a densitometer.Kurup et al. (2013) focussed on blue ﬂuor-escence, following excitation with 366 nmradiation. In this context it is worth point-ing out that the technology used by Joelet al. (1985) showed reﬂectance and absorb-ance in the UV-B and UV-A part of the spec-trum, while Kurup et al. (2013) measured UV-induced blue ﬂuorescence. Not surprisingly,diﬀerent UV-patterns were noted by the twogroups. Thus, technology plays a key role inwhat UV-pattern is observed, and this is a ma-jor consideration when interpreting the liter-ature. Kurup et al. (2013) explored the blueﬂuorescence of Nepenthes sp peristomes (thering of tissue that surrounds the entrance tothe digestive tube). The authors stated that“The peristomes ofNepenthes species ﬂashedlike well-designed blue ﬂuorescent tracks”.The markings in or near traps have beenhypothesised to have a functional role inprey capture (Joel et al. 1985; Kurup et al.2013). Moran, Clarke, Greenwood, et al.(2012) showed that an insectivorous speciesof Nepenthes displayed a distinct colour pat-tern compared to a closely related speciesthat harvests tree-shrew excreta. Light doesplay a role in creating this pattern. Shadingexperiments by Moran, Clarke, and Gowen(2012), showed that reductions in visible andUV light resulted in a substantial decrease inthe capture of Drosophila by Nepenthes ar-istolochioides pitchers. However, these res-ults were interpreted in the context of light©2017 by the authors 135 M. A. K. Jansen: Carnivorous plants and UV-radiation(of all wavelengths) transmitted through thetranslucent pitcher, rather than as a speciﬁcrole for UV-patterns. Kurup et al. (2013) ex-perimentally tested whether UV-induced blueﬂuorescence has a functional role in prey cap-ture. The authors found that removal ofthe peristome (rim) from Nepenthes pitchersled to a dramatic decrease in captured prey.Masking the peristome with acetone-extractshad a similar negative eﬀect on prey cap-ture. These results might be interpreted assupporting a role of UV-induced ﬂuorescencein prey-capture (which is exactly what popu-lar scientiﬁc journals did), but are far fromconclusive. Clearly, excising tissue will notjust remove UV-induced ﬂuorescence, butalso cells that are important for the pro-duction of nectar and scent, while causingmassive tissue disruption. Similarly, acetone-extracts will have multiple eﬀects on cellsand tissues. Furthermore, basic photobiolo-gical questions should be asked concerningUV-induced blue ﬂuorescence. How realisticis it that the sensitivity of the insect eye issuch that it can perceive small changes inUV induced blue ﬂuorescence, against a back-ground of solar blue radiation? In this con-text, it is also important to be aware of thebackground of blue autoﬂuorescence emit-ted by cell-wall-bound ferulic acid and otherplant secondary metabolites following excit-ation with UV wavelengths (Buschmann etal. 2000; Garcıá-Plazaola et al. 2015). Thus,although pictures of UV-induced blue ﬂuor-escence look great, doubts remain concern-ing the functional role of such ﬂuorescence.In fact, these doubts also apply to the com-mon UV-induced blue ﬂuorescence in, for ex-ample, ﬂowers. Holovachov (2015) statesthat “despite considerable research eﬀorts,the function of ultraviolet-induced visibleﬂuorescence in the world of plants remainspoorly understood”, and indeed is unlikely toplay a key role in the interactions between in-sects and plants.Phenomena such as UV-reﬂectance, andUV-absorbance are more likely candidates forattracting insect prey. Both UV-reﬂectance,and UV-absorbance are known to be involvedin the well characterised process of pollin-ator attraction in ﬂowers (Guldberg and At-satt 1975; Silberglied 1979). Unfortunately,the monitoring of UV reﬂectance and absorb-ance is often subject to technical limitations.UV-enabled cameras are equipped with ﬁltersthat transmit in the UV-range of the spec-trum, thus omitting the visible wavelengths.Yet, changes in UV absorbance and reﬂect-ance need to be interpreted in terms of thecontrast with other wavelength zones. Ex-ploring whether UV-radiation per se has arole in carnivory can be straightforward, forexample by comparing prey capture in thepresence or absence of UV-radiation. How-ever, interpreting the precise role of UV ra-diation is complex as any UV-eﬀect can bemediated either through the insect (i.e. vis-ion) or through the plant (i.e. absorbanceor reﬂectance). If the duration of the ex-periment is long enough, UV acclimation re-sponses will further modify the biochemicalmake-up of the plant, and therefore poten-tial UV-patterns. Clearly, prising apart thecomplex interaction between prey and carni-vorous plant will be highly complex. Never-theless, the application of the principles andterminology of photobiological research andUV-manipulation, as commonly practised inthe UV4Plants community, can potentiallycontribute to the understanding of the roleof UV radiation in prey capture. Exploringthe wavelength dependency of UV reﬂectanceand absorbance vis-á-vis insect vision canconsolidate the link between these processes;for instance, local excitation with UV laserscan trigger local UV-reﬂectance whilst avoid-ing a direct eﬀect on the insect. The use ofartiﬁcial “model traps” together with the ap-plication of UV-absorbing pigments can sim-ilarly be used to experimentally test attrac-tion traits. Nevertheless, it is unlikely thatsuch work will generate more than “correl-ations” between UV-exposure and prey cap-ture. Genetic manipulation is a more likely14 ©2017 by the authorsUV4Plants Bulletin, 2017, no. 1strategy to conclusively proof a role for UVradiation in prey capture. Manipulation ofUV-patterning through, for instance, breed-ing (Moyers et al. 2017), or manipulation ofthe spectral vision of the prey, for example ofthe model species Drosophila melanogaster(Feiler et al. 1992), are both realistic. Studiesusing genetically modiﬁed material shouldbe able to reveal the relative importanceof UV patterns, relative to other attractantssuch as secreted nectar, scent and trap shapeand colour.For now, UV-patterns exist, caused by UV-reﬂectance, UV-absorbance and UV-inducedblue ﬂuorescence. But although the story ofUV-and carnivorous plants may be captivat-ing, the truth about the functional role of UV-patterns is still to be captured!Acknowledgements The author wishes tothank reviewers for constructive comments.ReferencesBrock, M. T., L. K. Lucas, N. A. Anderson, M. J.Rubin, R. J. C. Markelz, M. F. Covington,U. K. Devisetty, C. Chapple, J. N. Maloof,and C. Weinig (2016). “Genetic architecture,biochemical underpinnings and ecologicalimpact of ﬂoral UV patterning”. In: Molecu-lar Ecology 25.5, pp. 1122–1140. doi: 10.1111/mec.13542.Buschmann, C., G. Langsdorf, and H.Lichtenthaler (2000). “Imaging of theblue, green, and red ﬂuorescence emissionof plants: an overview”. In: Photosynthet-ica 38.4, pp. 483–491. doi: 10.1023/a:1012440903014.Cheers, G. (1992). Guide to carnivorous plantsof the world. London: Angus & Robertson.isbn: 9780207161865.Cronin, T. W. and M. J. Bok (2016). “Photore-ception and vision in the ultraviolet”. In:The Journal of Experimental Biology 219.18,pp. 2790–2801. doi: 10 . 1242 / jeb .128769.Chap. I. STRUCTURE OF THE LEAVES.excellently adapted for the special purpose of catch-ing insects, so that the subject seemed well worthy ofinvestigation.The results have proved highly remarkable ; themore important ones being—firstly, the extraordinaryFig. 1.* -{Drosera rotundifoUa.)Leaf viewed from above ; enlarged four times.sensitiveness of the glands to slight pressure and tominute doses of certain nitrogenous fluids, as shownby the movements of the so-called hairs or tentacles;* The drawings of Drosera andDionsea, given in this vrork, weremade for me by my son GeorgeDarwin ; those of Aldrovanda, andof the several species of Utri-cnlaria, by my son Francis. Theyhave been excellently reproducedon wood by Mr. Cooper, 188Strand.Figure 5.3: Page 3 from the book Insectivorousplants (Darwin 1875).Darwin, C. (1860). Letter no. 2996. DarwinCorrespondence Project. url: http://www.darwinproject.ac.uk/DCP-LETT-2996(visited on 04/06/2017).– (1875). Insectivorous plants. London: JohnMurray. 462 pp.Feiler, R., R. Bjornson, K. Kirschfeld, D.Mismer, G. Rubin, D. Smith, M. Soco-lich, and C. Zuker (1992). “Ectopic expres-sion of ultraviolet-rhodopsins in the bluephotoreceptor cells of Drosophila: visualphysiology and photochemistry of trans-genic animals”. In: Journal of Neuroscience12, pp. 3862–3868. issn: 0270-6474.©2017 by the authors 155 M. A. K. Jansen: Carnivorous plants and UV-radiationGarcıá-Plazaola, J. I., B. Fernández-Marıń, S. O.Duke, A. Hernández, F. López-Arbeloa, andJ. M. Becerril (2015). “Autoﬂuorescence:Biological functions and technical applica-tions”. In: Plant Science 236, pp. 136–145.doi: 10.1016/j.plantsci.2015.03.010.Givnish, T. J. (2014). “New evidence on theorigin of carnivorous plants”. In: Proceed-ings of the National Academy of Sciences112.1, pp. 10–11. doi: 10 . 1073 / pnas .1422278112.Guldberg, L. D. and P. R. Atsatt (1975). “Fre-quency of Reﬂection and Absorption ofUltraviolet Light in Flowering Plants”. In:American Midland Naturalist 93.1, p. 35.doi: 10.2307/2424103.Ho, W., N. Kutz, J. Ng, and J. Riﬀell (2016).“Sexual selection drives ﬂoral scent di-versiﬁcation in carnivorous pitcher plants(NA Sarraceniaceae)”. In: bioRxiv. doi: 10.1101 / 079947. eprint: http : / / www .biorxiv.org/content/early/2016/10/12/079947.full.pdf.Holovachov, O. (2015). “Unseen beauty ofﬂowers – hidden signals or spectacular by-product?” In: Green Letters 19.3, pp. 329–331. doi: 10 . 1080 / 14688417 . 2015 .1078121.Joel, D. M., B. E. Juniper, and A. Dafni (1985).“Ultraviolet Patterns in the Traps of Carni-vorous Plants”. In: New Phytologist 101.4,pp. 585–593. doi: 10.1111/j.1469-8137.1985.tb02864.x.Kurup, R., A. J. Johnson, S. Sankar, A. A. Hus-sain, C. S. Kumar, and B. Sabulal (2013).“Fluorescent prey traps in carnivorousplants”. In: Plant Biology 15.3. Ed. by H.Rennenberg, pp. 611–615. doi: 10.1111/j.1438-8677.2012.00709.x.Moran, J. A., C. Clarke, and B. E. Gowen(2012). “The use of light in prey captureby the tropical pitcher plantNepenthes ar-istolochioides”. In: Plant Signaling & Beha-vior 7.8, pp. 957–960. doi: 10.4161/psb.20912.Moran, J. A., C. Clarke, M. Greenwood, andL. Chin (2012). “Tuning of color contrastsignals to visual sensitivity maxima of treeshrews by three Bornean highland Nepen-thes species”. In: Plant Signaling & Beha-vior 7.10, pp. 1267–1270. doi: 10.4161/psb.21661.Moyers, B. T., G. L. Owens, G. J. Baute, and L. H.Rieseberg (2017). “The genetic architectureof UV ﬂoral patterning in sunﬂower”. In:Annals of Botany 120.1, pp. 39–50. doi: 10.1093/aob/mcx038.Silberglied, R. E. (1979). “Communication inthe Ultraviolet”. In: Annual Review of Eco-logy and Systematics 10.1, pp. 373–398.doi: 10.1146/annurev.es.10.110179.002105.Editorial-board-reviewed article.Published on-line on 2017-10-09.Edited by: T. Matthew Robson16 ©2017 by the authors

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Carnivorous plants and UV-radiation: a captivating story?

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