Full text loading...
Review Article
Free
On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet
- Rainer Hedrich1, and Kenji Fukushima1
- Vol. 72:133-153 (Volume publication date June 2021) https://doi.org/10.1146/annurev-arplant-080620-010429
- First published as a Review in Advance on January 12, 2021
-
Copyright © 2021 by Annual Reviews. All rights reserved
Abstract
Charles Darwin recognized that carnivorous plants thrive in nutrient-poor soil by capturing animals. Although the concept of botanical carnivory has been known for nearly 150 years, its molecular mechanisms and evolutionary origins have not been well understood until recently. In the last decade, technical advances have fueled the genome and transcriptome sequencings of active and passive hunters, leading to a better understanding of the traits associated with the carnivorous syndrome, from trap leaf development and prey digestion to nutrient absorption, exemplified, for example, by the Venus flytrap (Dionaea muscipula), pitcher plant (Cephalotus follicularis), and bladderwort (Utricularia gibba). The repurposing of defense-related genes is an important trend in the evolution of plant carnivory. In this review, using the Venus flytrap as a representative of the carnivorous plants, we summarize the molecular mechanisms underlying their ability to attract, trap, and digest prey and discuss the origins of plant carnivory in relation to their genomic evolution.
Article metrics loading...
Literature Cited
- 1.Adamec L. 2003. Ecophysiological characterization of dormancy states in turions of the aquatic carnivorous plant Aldrovanda vesiculosa. Biol. Plant. 47:3395–402
- 2.Adlassnig W, Koller-Peroutka M, Bauer S, Koshkin E, Lendl T, Lichtscheidl IK. 2012. Endocytotic uptake of nutrients in carnivorous plants. Plant J 71:2303–13
- 3.Adlassnig W, Peroutka M, Lambers H, Lichtscheidl IK. 2005. The roots of carnivorous plants. Plant Soil 274:1127–40
- 4.Basu D, Haswell ES. 2017. Plant mechanosensitive ion channels: an ocean of possibilities. Curr. Opin. Plant Biol. 40:43–48
- 5.Bauer U, Bohn HF, Federle W. 2008. Harmless nectar source or deadly trap: Nepenthes pitchers are activated by rain, condensation and nectar. Proc. R. Soc. B 275: 1632.259–65
- 6.Bauer U, Scharmann M, Skepper J, Federle W. 2013. ‘Insect aquaplaning’ on a superhydrophilic hairy surface: how Heliamphora nutans Benth. pitcher plants capture prey. Proc. R. Soc. B 280: 1753.20122569
- 7.Bemm F, Becker D, Larisch C, Kreuzer I, Escalante-Perez M et al. 2016. Venus flytrap carnivorous lifestyle builds on herbivore defense strategies. Genome Res 26:812–25Provides unequivocal evidence that carnivory evolved by rewiring the herbivore defense gene set.
- 8.Bennett KF, Ellison AM. 2009. Nectar, not colour, may lure insects to their death. Biol. Lett. 5:4469–72
- 9.Blehová A, Švubová R, Lukačová Z, Moravčíková J, Matušíková I. 2015. Transformation of sundew: pitfalls and promises. Plant Cell Tissue Organ Cult 120:2681–87
- 10.Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K et al. 2016. The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Curr. Biol. 26:3286–95Shows that Dionaea plants are able to count to five.
- 11.Bohn HF, Federle W 2004. Insect aquaplaning: Nepenthes pitcher plants capture prey with the peristome, a fully wettable water-lubricated anisotropic surface. PNAS 101:3914138–43
- 12.Braam J. 1992. Regulated expression of the calmodulin-related TCH genes in cultured Arabidopsis cells: induction by calcium and heat shock. PNAS 89:83213–16
- 13.Burr D, Ross J. 2008. A visual sense of number. Curr. Biol. 18:6425–28
- 14.Burri JT, Saikia E, Läubli NF, Vogler H, Wittel FK et al. 2020. A single touch can provide sufficient mechanical stimulation to trigger Venus flytrap closure. PLOS Biol 18:7e3000740
- 15.Carvunis A-R, Rolland T, Wapinski I, Calderwood MA, Yildirim MA et al. 2012. Proto-genes and de novo gene birth. Nature 487:7407370–74
- 16.Chase MW, Christenhusz MJM, Fay MF, Byng JW, Judd WS et al.Angiosperm Phylogeny Group 2016. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG IV. Bot. J. Linn. Soc. 181:11–20
- 17.Chauvin A, Caldelari D, Wolfender J-L, Farmer EE. 2013. Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol 197:2566–75
- 18.Chng W-BA, Hietakangas V, Lemaitre B. 2017. Physiological adaptations to sugar intake: new paradigms from Drosophila melanogaster. Trends Endocrinol. Metab. 28:2131–42
- 19.Clark MD, Contreras GF, Shen R, Perozo E. 2020. Electromechanical coupling in the hyperpolarization-activated K+ channel KAT1. Nature 583:7814145–49
- 20.Darwin C. 1875. Insectivorous Plants New York: D. Appleton Co.
- 21.Dayal A, Ng SFJ, Grabner M. 2019. Ca2+-activated Cl− channel TMEM16A/ANO1 identified in zebrafish skeletal muscle is crucial for action potential acceleration. Nat. Commun. 10:1115
- 22.Deng Z, Maksaev G, Schlegel AM, Zhang J, Rau M et al. 2020. Structural mechanism for gating of a eukaryotic mechanosensitive channel of small conductance. Nat. Commun. 11:13690
- 23.Di Giusto B, Bessière J-M, Guéroult M, Lim LBL, Marshall DJ et al. 2010. Flower-scent mimicry masks a deadly trap in the carnivorous plant Nepenthes rafflesiana. J. Ecol. 98:4845–56
- 24.Ellison AM, Adamec L 2018. Carnivorous Plants: Physiology, Ecology, and Evolution Oxford, UK: Oxford Univ. Press
- 25.Ellison AM, Adamec L 2018. Introduction: What is a carnivorous plant?. Carnivorous Plants: Physiology, Ecology, and Evolution AM Ellison, L Adamec 3–6 Oxford, UK: Oxford Univ. Press
- 26.Ellison AM, Gotelli NJ 2002. Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. PNAS 99:74409–12
- 27.Escalante-Pérez M, Krol E, Stange A, Geiger D, Al-Rasheid KAS et al. 2011. A special pair of phytohormones controls excitability, slow closure, and external stomach formation in the Venus flytrap. PNAS 108:3715492–97Shows that jasmonate and ABA control the Dionaea hunting cycle.
- 28.Escalante-Pérez M, Scherzer S, Al-Rasheid KAS, Döttinger C, Neher E, Hedrich R. 2014. Mechano-stimulation triggers turgor changes associated with trap closure in the Darwin plant Dionaea muscipula. Mol. Plant 7:4744–46
- 29.Fabricant A, Iwata GZ, Scherzer S, Bougas L, Rolfs K et al. 2021. Action potentials induce biomagnetic fields in Venus flytrap plants. Sci. Rep. 11:1438
- 30.Farmer EE, Gao Y-Q, Lenzoni G, Wolfender J-L, Wu Q. 2020. Wound- and mechanostimulated electrical signals control hormone responses. New Phytol 227:41037–50
- 31.Farmer EE, Gasperini D, Acosta IF. 2014. The squeeze cell hypothesis for the activation of jasmonate synthesis in response to wounding. New Phytol 204:2282–88
- 32.Feigenson L, Dehaene S, Spelke E. 2004. Core systems of number. Trends Cogn. Sci. 8:7307–14
- 33.Förster S, Schmidt LK, Kopic E, Anschütz U, Huang S et al. 2019. Wounding-induced stomatal closure requires jasmonate-mediated activation of GORK K+ channels by a Ca2+ sensor-kinase CBL1-CIPK5 complex. Dev. Cell 48:187–99.e6
- 34.Forterre Y, Skotheim JM, Dumais J, Mahadevan L. 2005. How the Venus flytrap snaps. Nature 433:7024421–25
- 35.Fromm J. 1991. Control of phloem unloading by action potentials in Mimosa. Physiol. Plant. 83:3529–33
- 36.Fukushima K, Fang X, Alvarez-Ponce D, Cai H, Carretero-Paulet L et al. 2017. Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nat. Ecol. Evol. 1:30059Reported common evolutionary trends of genes encoding digestive enzymes in separate carnivorous lineages.
- 37.Fukushima K, Fujita H, Yamaguchi T, Kawaguchi M, Tsukaya H, Hasebe M. 2015. Oriented cell division shapes carnivorous pitcher leaves of Sarracenia purpurea. Nat. Commun. 6:16450Established the importance of adaxial–abaxial polarity and cell layer–specific oriented cell division in the pitcher leaf development of Sarracenia.
- 38.Fukushima K, Hasebe M. 2014. Adaxial-abaxial polarity: the developmental basis of leaf shape diversity. Genesis 52:11–18
- 39.Fukushima K, Imamura K, Nagano K, Hoshi Y. 2011. Contrasting patterns of the 5S and 45S rDNA evolutions in the Byblis liniflora complex (Byblidaceae). J. Plant Res. 124:2231–44
- 40.Gao P, Loeffler TS, Honsel A, Kruse J, Krol E et al. 2015. Integration of trap- and root-derived nitrogen nutrition of carnivorous Dionaea muscipula. New Phytol 205:31320–29
- 41.Gaume L, Forterre Y. 2007. A viscoelastic deadly fluid in carnivorous pitcher plants. PLOS ONE 2:11e1185
- 42.Gorb E, Haas K, Henrich A, Enders S, Barbakadze N, Gorb S. 2005. Composite structure of the crystalline epicuticular wax layer of the slippery zone in the pitchers of the carnivorous plant Nepenthes alata and its effect on insect attachment. J. Exp. Biol. 208:244651–62
- 43.Gowda DC, Reuter G, Schauer R. 1982. Structural features of an acidic polysaccharide from the mucin of Drosera binata. Phytochemistry 21:92297–300
- 44.Green S, Green TL, Heslop-Harrison Y. 1979. Seasonal heterophylly and leaf gland features in Triphyophyllum (Dioncophyllaceae), a new carnivorous plant genus. Bot. J. Linn. Soc. 78:299–116
- 45.Guerringue Y, Thomine S, Frachisse J-M. 2018. Sensing and transducing forces in plants with MSL10 and DEK1 mechanosensors. FEBS Lett 592:121968–79
- 46.Guo X, Liu D, Chong K 2018. Cold signaling in plants: insights into mechanisms and regulation. J. Integr. Plant Biol. 60:9745–56
- 47.Hedrich R. 2012. Ion channels in plants. Physiol. Rev. 92:41777–811
- 48.Hedrich R, Geiger D. 2017. Biology of SLAC1-type anion channels—from nutrient uptake to stomatal closure. New Phytol 216:146–61
- 49.Hedrich R, Neher E. 2018. Venus flytrap: how an excitable, carnivorous plant works. Trends Plant Sci 23:3220–34
- 50.Hedrich R, Salvador-Recatalà V, Dreyer I. 2016. Electrical wiring and long-distance plant communication. Trends Plant Sci 21:5376–87
- 51.Henarejos-Escudero P, Guadarrama-Flores B, García-Carmona F, Gandía-Herrero F. 2018. Digestive glands extraction and precise pigment analysis support the exclusion of the carnivorous plant Dionaea muscipula Ellis from the Caryophyllales order. Plant Sci 274:342–48
- 52.Heubl G, Bringmann G, Meimberg H. 2006. Molecular phylogeny and character evolution of carnivorous plant families in Caryophyllales—revisited. Plant Biol 8:6821–30
- 53.Hirsikorpi M, Kämäräinen T, Teeri T, Hohtola A. 2002. Agrobacterium-mediated transformation of round leaved sundew (Drosera rotundifolia L.). Plant Sci 162:4537–42
- 54.Ibarra-Laclette E, Lyons E, Hernández-Guzmán G, Pérez-Torres CA, Carretero-Paulet L et al. 2013. Architecture and evolution of a minute plant genome. Nature 498:745294–98The first report of a sequenced carnivorous plant genome.
- 55.Iosip A-L, Böhm J, Scherzer S, Al-Rasheid KAS, Dreyer Iet al 2020. The Venus flytrap trigger hair–specific potassium KDM1 can reestablish the K+ gradient required for hapto-electric signaling. PLOS Biol1812e3000964
- 56.Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:7161463–67
- 57.Jiao Y, Leebens-Mack J, Ayyampalayam S, Bowers JE, McKain MR et al. 2012. A genome triplication associated with early diversification of the core eudicots. Genome Biol 13:1R3
- 58.Joel DM, Juniper BE, Dafni A. 1985. Ultraviolet patterns in the traps of carnivorous plants. New Phytol 101:4585–93
- 59.Jungnickel KEJ, Parker JL, Newstead S. 2018. Structural basis for amino acid transport by the CAT family of SLC7 transporters. Nat. Commun. 9:1550
- 60.Jürgens A, El-Sayed AM, Suckling DM. 2009. Do carnivorous plants use volatiles for attracting prey insects?. Funct. Ecol. 23:5875–87
- 60a.Kocáb O, Jakšová J, Novák O, Petřík I, Lenobel Ret al 2020. Jasmonate-independent regulation of digestive enzyme activity in the carnivorous butterwort Pinguicula × Tina. J. Exp. Bot 71:123749–58
- 61.Koller-Peroutka M, Krammer S, Pavlik A, Edlinger M, Lang I, Adlassnig W 2019. Endocytosis and digestion in carnivorous pitcher plants of the family Sarraceniaceae. Plants 8:10367
- 62.Krausko M, Perutka Z, Šebela M, Šamajová O, Šamaj J et al. 2017. The role of electrical and jasmonate signalling in the recognition of captured prey in the carnivorous sundew plant Drosera capensis. New Phytol 213:41818–35
- 63.Kreuzwieser J, Scheerer U, Kruse J, Burzlaff T, Honsel A et al. 2014. The Venus flytrap attracts insects by the release of volatile organic compounds. J. Exp. Bot. 65:2755–66
- 64.Lan T, Renner T, Ibarra-Laclette E, Farr KM, Chang T-H et al. 2017. Long-read sequencing uncovers the adaptive topography of a carnivorous plant genome. PNAS 114:221E4435–41
- 65.Lee KJI, Bushell C, Koide Y, Fozard JA, Piao C et al. 2019. Shaping of a three-dimensional carnivorous trap through modulation of a planar growth mechanism. PLOS Biol 17:10e3000427
- 66.Leebens-Mack JH, Barker MS, Carpenter EJ, Deyholos MK, Gitzendanner MA et al. 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:7780679–85
- 67.Levchenko V, Konrad KR, Dietrich P, Roelfsema MRG, Hedrich R 2005. Cytosolic abscisic acid activates guard cell anion channels without preceding Ca2+ signals. PNAS 102:114203–8
- 68.Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:54941151–55
- 69.Malmberg RL, Rogers WL, Alabady MS. 2018. A carnivorous plant genetic map: pitcher/insect-capture QTL on a genetic linkage map of Sarracenia. Life Sci. Alliance 1:6e201800146
- 70.Masi E, Ciszak M, Colzi I, Adamec L, Mancuso S. 2016. Resting electrical network activity in traps of the aquatic carnivorous plants of the genera Aldrovanda and Utricularia. Sci. Rep. 6:124989
- 71.Mazza CA, Izaguirre MM, Curiale J, Ballaré CL. 2010. A look into the invisible: ultraviolet-B sensitivity in an insect (Caliothrips phaseoli) revealed through a behavioural action spectrum. Proc. R. Soc. B 277: 1680.367–73
- 72.Miguel S, Nisse E, Biteau F, Rottloff S, Mignard B et al. 2019. Assessing carnivorous plants for the production of recombinant proteins. Front. Plant Sci. 10:793
- 73.Monte I, Ishida S, Zamarreño AM, Hamberg M, Franco-Zorrilla JM et al. 2018. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nat. Chem. Biol. 14:5480–88
- 74.Monte I, Kneeshaw S, Franco-Zorrilla JM, Chini A, Zamarreño AM et al. 2020. An ancient COI1-independent function for reactive electrophilic oxylipins in thermotolerance. Curr. Biol. 30:6962–971.e3
- 75.Moran JA, Booth WE, Charles JK. 1999. Aspects of pitcher morphology and spectral characteristics of six Bornean Nepenthes pitcher plant species: implications for prey capture. Ann. Bot. 83:5521–28
- 76.Murthy SE, Dubin AE, Whitwam T, Jojoa-Cruz S, Cahalan SM et al. 2018. OSCA/TMEM63 are an evolutionarily conserved family of mechanically activated ion channels. eLife 7:e41844
- 77.Nakamura Y, Reichelt M, Mayer VE, Mithöfer A. 2013. Jasmonates trigger prey-induced formation of ‘outer stomach’ in carnivorous sundew plants. Proc. R. Soc. B 280: 1759.20130228
- 78.Nieder A. 2005. Counting on neurons: the neurobiology of numerical competence. Nat. Rev. Neurosci. 6:3177–90
- 79.Oikawa T, Ishimaru Y, Munemasa S, Takeuchi Y, Washiyama K et al. 2018. Ion channels regulate nyctinastic leaf opening in Samanea saman. Curr. Biol. 28:142230–38.e7
- 80.Oldroyd GED, Leyser O. 2020. A plant's diet, surviving in a variable nutrient environment. Science 368:6486eaba0196
- 81.Oropeza-Aburto A, Cervantes-Pérez SA, VA Albert, Herrera-Estrella L. 2020. Agrobacterium tumefaciens mediated transformation of the aquatic carnivorous plant Utricularia gibba. Plant Methods 16:150
- 82.Palfalvi G, Hackl T, Terhoeven N, Shibata TF, Nishiyama T et al. 2020. Genomes of the Venus flytrap and close relatives unveil the roots of plant carnivory. Curr. Biol. 30:122312–20.e5
- 83.Panchy N, Lehti-Shiu M, Shiu S-H. 2016. Evolution of gene duplication in plants. Plant Physiol 171:42294–316
- 84.Paszota P, Escalante-Perez M, Thomsen LR, Risor MW, Dembski A et al. 2014. Secreted major Venus flytrap chitinase enables digestion of Arthropod prey. Biochim. Biophys. Acta Proteins Proteom. 2:374–83
- 85.Pavlovič A, Jakšová J, Novák O. 2017. Triggering a false alarm: Wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol 216:3927–38
- 86.Pavlovič A, Mithöfer A. 2019. Jasmonate signalling in carnivorous plants: copycat of plant defence mechanisms. J. Exp. Bot. 70:133379–89
- 87.Pica P, Lemer C, Izard V, Dehaene S. 2004. Exact and approximate arithmetic in an Amazonian indigene group. Science 306:5695499–503
- 88.Polisensky DH, Braam J. 1996. Cold-shock regulation of the Arabidopsis TCH genes and the effects of modulating intracellular calcium levels. Plant Physiol 111:41271–79
- 89.Poppinga S, Bauer U, Speck T, Volkov AG 2018. Motile traps. Carnivorous Plants: Physiology, Ecology, and Evolution AM Ellison, L Adamec 180–92 Oxford, UK: Oxford Univ. Press
- 90.Poppinga S, Hartmeyer SRH, Seidel R, Masselter T, Hartmeyer I, Speck T. 2012. Catapulting tentacles in a sticky carnivorous plant. PLOS ONE 7:9e45735
- 90a.Procko C, Murthy SE, Keenan WT, Mousavi SAR, Dabi Tet al 2020. Stretch-activated ion channels identified in the touch-sensitive structures of carnivorous Droseraceae plants. bioRxiv 2020.12.15.422915. https://doi.org/10.1101/2020.12.15.422915
- 91.Raghavan M, Fee D, Barkhaus PE. 2019. Generation and propagation of the action potential. Handb. Clin. Neurol. 160:3–22
- 92.Ranade SS, Syeda R, Patapoutian A. 2015. Mechanically activated ion channels. Neuron 87:61162–79
- 93.Renner T, Lan T, Farr KM, Ibarra-Laclette E, Herrera-Esrella L et al. 2018. Carnivorous plant genomes. Carnivorous Plants: Physiology, Ecology, and Evolution A Ellison, L Adamec 135–52 Oxford, UK: Oxford Univ. Press
- 94.Reyer A, Häßler M, Scherzer S, Huang S, Pedersen J et al. 2020. Channelrhodopsin-mediated optogenetics highlights a central role of depolarization-dependent plant proton pumps. PNAS 117:20920–25
- 95.Rice A, Glick L, Abadi S, Einhorn M, Kopelman NM et al. 2015. The Chromosome Counts Database (CCDB)—a community resource of plant chromosome numbers. New Phytol 206:119–26
- 96.Rivadavia F, Kondo K, Kato M, Hasebe M. 2003. Phylogeny of the sundews, Drosera (Droseraceae), based on chloroplast rbcL and nuclear 18S ribosomal DNA sequences. Am. J. Bot. 90:1123–30
- 97.Roper SD. 2015. The taste of table salt.. Pflügers Arch 467:3457–63
- 98.Sachse R, Westermeier A, Mylo M, Nadasdi J, Bischoff M et al. 2020. Snapping mechanics of the Venus flytrap (Dionaea muscipula). PNAS 117:2716035–42
- 99.Sadowski E-M, Seyfullah LJ, Sadowski F, Fleischmann A, Behling H, Schmidt AR 2015. Carnivorous leaves from Baltic amber. PNAS 112:1190–95
- 100.Schäfer N, Maierhofer T, Herrmann J, Jørgensen ME, Lind C et al. 2018. A tandem amino acid residue motif in guard cell SLAC1 anion channel of grasses allows for the control of stomatal aperture by nitrate. Curr. Biol. 28:91370–1379.e5
- 101.Scherzer S, Böhm J, Krol E, Shabala L, Kreuzer I et al. 2015. Calcium sensor kinase activates potassium uptake systems in gland cells of Venus flytraps. PNAS 112:237309–14
- 102.Scherzer S, Federle W, Al-Rasheid KAS, Hedrich R. 2019. Venus flytrap trigger hairs are micronewton mechano-sensors that can detect small insect prey. Nat. Plants 5:7670–75This study documents that flytrap sensory hairs can sense prey with a body weight as small as a mosquito.
- 103.Scherzer S, Krol E, Kreuzer I, Kruse J, Karl F et al. 2013. The Dionaea muscipula ammonium channel DmAMT1 provides NH4+ uptake associated with Venus flytrap's prey digestion. Curr. Biol. 23:171649–57This study addresses the molecular nature, function, and regulation of prey-derived ammonium uptake in the Venus flytrap.
- 104.Scherzer S, Shabala L, Hedrich B, Fromm J, Bauer H et al. 2017. Insect haptoelectrical stimulation of Venus flytrap triggers exocytosis in gland cells. PNAS 114:184822–27
- 105.Scholz I, Bückins M, Dolge L, Erlinghagen T, Weth A et al. 2010. Slippery surfaces of pitcher plants: Nepenthes wax crystals minimize insect attachment via microscopic surface roughness. J. Exp. Biol. 213:71115–25
- 106.Schulze WX, Sanggaard KW, Kreuzer I, Knudsen AD, Bemm F et al. 2012. The protein composition of the digestive fluid from the Venus flytrap sheds light on prey digestion mechanisms. Mol. Cell. Proteom. 11:111306–19
- 107.Smith SA, Brown JW, Yang Y, Bruenn R, Drummond CP et al. 2018. Disparity, diversity, and duplications in the Caryophyllales. New Phytol 217:2836–54
- 108.Soucy SM, Huang J, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:8472–82
- 109.Suda H, Mano H, Toyota M, Fukushima K, Mimura T et al. 2020. Calcium dynamics during trap closure visualized in transgenic Venus flytrap. Nat. Plants 6:1219–24This article documents that the Venus flytrap's memory and counting are based on a calcium clock.
- 110.Sun J, Bankston JR, Payandeh J, Hinds TR, Zagotta WN, Zheng N. 2014. Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507:749073–77
- 111.Toyota M, Spencer D, Sawai-Toyota S, Jiaqi W, Zhang T et al. 2018. Glutamate triggers long-distance, calcium-based plant defense signaling. Science 361:64071112–15
- 112.True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 18:53–80
- 113.Uchizono S, Itoh TQ, Kim H, Hamada N, Kwon JY, Tanimura T. 2017. Deciphering the genes for taste receptors for fructose in Drosophila. Mol. Cells 40:10731–36
- 114.Van de Peer Y, Maere S, Meyer A. 2009. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10:10725–32
- 115.Wang K, Yang Z, Qing D, Ren F, Liu S et al. 2018. Quantitative and functional posttranslational modification proteomics reveals that TREPH1 plays a role in plant touch-delayed bolting. PNAS 115:43E10265–74
- 116.Wang Y-Y, Cheng Y-H, Chen K-E, Tsay Y-F. 2018. Nitrate transport, signaling, and use efficiency. Annu. Rev. Plant Biol. 69:85–122
- 117.Wasternack C, Feussner I. 2018. The oxylipin pathways: biochemistry and function. Annu. Rev. Plant Biol. 69:363–86
- 118.Whitewoods CD, Gonçalves B, Cheng J, Cui M, Kennaway R et al. 2020. Evolution of carnivorous traps from planar leaves through simple shifts in gene expression. Science 367:91–96Established the importance of adaxial–abaxial and proximodistal polarities in the development of Utricularia’s suction traps.
- 119.Yang Y, Moore MJ, Brockington SF, Mikenas J, Olivieri J et al. 2018. Improved transcriptome sampling pinpoints 26 ancient and more recent polyploidy events in Caryophyllales, including two allopolyploidy events. New Phytol 217:2855–70
- 120.Yilamujiang A, Reichelt M, Mithöfer A. 2016. Slow food: Insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous Nepenthes plants. Ann. Bot. 118:2369–75
- 121.Yuan F, Yang H, Xue Y, Kong D, Ye R et al. 2014. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in Arabidopsis. Nature 514:7522367–71
Data & Media loading...
Supplementary Data
Download all Supplemental Material as a single PDF. Includes Supplemental Appendices 1-2, Supplemental Figure 1, Supplemental Tables 1-2, and Supplemental References. Revised Nov. 12, 2021.
- Article Type: Review Article
Most Read This Month
Most Cited Most Cited RSS feed
-
-
REACTIVE OXYGEN SPECIES: Metabolism, Oxidative Stress, and Signal Transduction
Klaus Apel, and Heribert HirtVol. 55 (2004), pp. 373–399
-
-
-
-
-
Carbon Isotope Discrimination and Photosynthesis
Vol. 40 (1989), pp. 503–537
-
-
-
-
-
ASCORBATE AND GLUTATHIONE: Keeping Active Oxygen Under Control
Vol. 49 (1998), pp. 249–279
-
-
-
-
-
PLANT CELLULAR AND MOLECULAR RESPONSES TO HIGH SALINITY
Vol. 51 (2000), pp. 463–499
-
-
-
Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo
Vol. 59 (2008), pp. 89–113
-
-
-
THE WATER-WATER CYCLE IN CHLOROPLASTS: Scavenging of Active Oxygens and Dissipation of Excess Photons
Vol. 50 (1999), pp. 601–639
-
-
-
Chlorophyll Fluorescence and Photosynthesis: The Basics
G H Krause, and E WeisVol. 42 (1991), pp. 313–349
-
- More Less