1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 72, 2021
  5. Article

Annual Review of Plant Biology

Volume 72, 2021

On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet

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 (), pitcher plant (), and bladderwort (). 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.

Keyword(s): action potential, calcium, carnivorous plants, evolution, hunting cycle, jasmonate
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-080620-010429
2021-06-17
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-080620-010429.html?itemId=/content/journals/10.1146/annurev-arplant-080620-010429&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Adamec L. 2003. Ecophysiological characterization of dormancy states in turions of the aquatic carnivorous plant Aldrovanda vesiculosa. Biol. Plant. 47:3395–402
     [Google Scholar]
  2. 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
     [Google Scholar]
  3. 3. 
    Adlassnig W, Peroutka M, Lambers H, Lichtscheidl IK. 2005. The roots of carnivorous plants. Plant Soil 274:1127–40
     [Google Scholar]
  4. 4. 
    Basu D, Haswell ES. 2017. Plant mechanosensitive ion channels: an ocean of possibilities. Curr. Opin. Plant Biol. 40:43–48
     [Google Scholar]
  5. 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
     [Google Scholar]
  6. 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
     [Google Scholar]
  7. 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.
     [Google Scholar]
  8. 8. 
    Bennett KF, Ellison AM. 2009. Nectar, not colour, may lure insects to their death. Biol. Lett. 5:4469–72
     [Google Scholar]
  9. 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
     [Google Scholar]
  10. 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.
     [Google Scholar]
  11. 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
     [Google Scholar]
  12. 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
     [Google Scholar]
  13. 13. 
    Burr D, Ross J. 2008. A visual sense of number. Curr. Biol. 18:6425–28
     [Google Scholar]
  14. 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
     [Google Scholar]
  15. 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
     [Google Scholar]
  16. 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
     [Google Scholar]
  17. 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
     [Google Scholar]
  18. 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
     [Google Scholar]
  19. 19. 
    Clark MD, Contreras GF, Shen R, Perozo E. 2020. Electromechanical coupling in the hyperpolarization-activated K+ channel KAT1. Nature 583:7814145–49
     [Google Scholar]
  20. 20. 
    Darwin C. 1875. Insectivorous Plants New York: D. Appleton Co.
  21. 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
     [Google Scholar]
  22. 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
     [Google Scholar]
  23. 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
     [Google Scholar]
  24. 24. 
    Ellison AM, Adamec L 2018. Carnivorous Plants: Physiology, Ecology, and Evolution Oxford, UK: Oxford Univ. Press
  25. 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
     [Google Scholar]
  26. 26. 
    Ellison AM, Gotelli NJ 2002. Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. PNAS 99:74409–12
     [Google Scholar]
  27. 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.
     [Google Scholar]
  28. 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
     [Google Scholar]
  29. 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
     [Google Scholar]
  30. 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
     [Google Scholar]
  31. 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
     [Google Scholar]
  32. 32. 
    Feigenson L, Dehaene S, Spelke E. 2004. Core systems of number. Trends Cogn. Sci. 8:7307–14
     [Google Scholar]
  33. 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
     [Google Scholar]
  34. 34. 
    Forterre Y, Skotheim JM, Dumais J, Mahadevan L. 2005. How the Venus flytrap snaps. Nature 433:7024421–25
     [Google Scholar]
  35. 35. 
    Fromm J. 1991. Control of phloem unloading by action potentials in Mimosa. Physiol. Plant. 83:3529–33
     [Google Scholar]
  36. 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.
     [Google Scholar]
  37. 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.
     [Google Scholar]
  38. 38. 
    Fukushima K, Hasebe M. 2014. Adaxial-abaxial polarity: the developmental basis of leaf shape diversity. Genesis 52:11–18
     [Google Scholar]
  39. 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
     [Google Scholar]
  40. 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
     [Google Scholar]
  41. 41. 
    Gaume L, Forterre Y. 2007. A viscoelastic deadly fluid in carnivorous pitcher plants. PLOS ONE 2:11e1185
     [Google Scholar]
  42. 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
     [Google Scholar]
  43. 43. 
    Gowda DC, Reuter G, Schauer R. 1982. Structural features of an acidic polysaccharide from the mucin of Drosera binata. Phytochemistry 21:92297–300
     [Google Scholar]
  44. 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
     [Google Scholar]
  45. 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
     [Google Scholar]
  46. 46. 
    Guo X, Liu D, Chong K 2018. Cold signaling in plants: insights into mechanisms and regulation. J. Integr. Plant Biol. 60:9745–56
     [Google Scholar]
  47. 47. 
    Hedrich R. 2012. Ion channels in plants. Physiol. Rev. 92:41777–811
     [Google Scholar]
  48. 48. 
    Hedrich R, Geiger D. 2017. Biology of SLAC1-type anion channels—from nutrient uptake to stomatal closure. New Phytol 216:146–61
     [Google Scholar]
  49. 49. 
    Hedrich R, Neher E. 2018. Venus flytrap: how an excitable, carnivorous plant works. Trends Plant Sci 23:3220–34
     [Google Scholar]
  50. 50. 
    Hedrich R, Salvador-Recatalà V, Dreyer I. 2016. Electrical wiring and long-distance plant communication. Trends Plant Sci 21:5376–87
     [Google Scholar]
  51. 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
     [Google Scholar]
  52. 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
     [Google Scholar]
  53. 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
     [Google Scholar]
  54. 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.
     [Google Scholar]
  55. 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
     [Google Scholar]
  56. 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
     [Google Scholar]
  57. 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
     [Google Scholar]
  58. 58. 
    Joel DM, Juniper BE, Dafni A. 1985. Ultraviolet patterns in the traps of carnivorous plants. New Phytol 101:4585–93
     [Google Scholar]
  59. 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
     [Google Scholar]
  60. 60. 
    Jürgens A, El-Sayed AM, Suckling DM. 2009. Do carnivorous plants use volatiles for attracting prey insects?. Funct. Ecol. 23:5875–87
     [Google Scholar]
  61. 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
     [Google Scholar]
  62. 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
     [Google Scholar]
  63. 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
     [Google Scholar]
  64. 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
     [Google Scholar]
  65. 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
     [Google Scholar]
  66. 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
     [Google Scholar]
  67. 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
     [Google Scholar]
  68. 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
     [Google Scholar]
  69. 68. 
    Lynch M, Conery JS. 2000. The evolutionary fate and consequences of duplicate genes. Science 290:54941151–55
     [Google Scholar]
  70. 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
     [Google Scholar]
  71. 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
     [Google Scholar]
  72. 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
     [Google Scholar]
  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
     [Google Scholar]
  74. 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
     [Google Scholar]
  75. 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
     [Google Scholar]
  76. 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
     [Google Scholar]
  77. 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
     [Google Scholar]
  78. 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
     [Google Scholar]
  79. 78. 
    Nieder A. 2005. Counting on neurons: the neurobiology of numerical competence. Nat. Rev. Neurosci. 6:3177–90
     [Google Scholar]
  80. 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
     [Google Scholar]
  81. 80. 
    Oldroyd GED, Leyser O. 2020. A plant's diet, surviving in a variable nutrient environment. Science 368:6486eaba0196
     [Google Scholar]
  82. 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
     [Google Scholar]
  83. 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
     [Google Scholar]
  84. 83. 
    Panchy N, Lehti-Shiu M, Shiu S-H. 2016. Evolution of gene duplication in plants. Plant Physiol 171:42294–316
     [Google Scholar]
  85. 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
     [Google Scholar]
  86. 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
     [Google Scholar]
  87. 86. 
    Pavlovič A, Mithöfer A. 2019. Jasmonate signalling in carnivorous plants: copycat of plant defence mechanisms. J. Exp. Bot. 70:133379–89
     [Google Scholar]
  88. 87. 
    Pica P, Lemer C, Izard V, Dehaene S. 2004. Exact and approximate arithmetic in an Amazonian indigene group. Science 306:5695499–503
     [Google Scholar]
  89. 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
     [Google Scholar]
  90. 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
     [Google Scholar]
  91. 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
     [Google Scholar]
  92. 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
    [Crossref] [Google Scholar]
  93. 91. 
    Raghavan M, Fee D, Barkhaus PE. 2019. Generation and propagation of the action potential. Handb. Clin. Neurol. 160:3–22
     [Google Scholar]
  94. 92. 
    Ranade SS, Syeda R, Patapoutian A. 2015. Mechanically activated ion channels. Neuron 87:61162–79
     [Google Scholar]
  95. 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
     [Google Scholar]
  96. 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
     [Google Scholar]
  97. 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
     [Google Scholar]
  98. 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
     [Google Scholar]
  99. 97. 
    Roper SD. 2015. The taste of table salt.. Pflügers Arch 467:3457–63
     [Google Scholar]
  100. 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
     [Google Scholar]
  101. 99. 
    Sadowski E-M, Seyfullah LJ, Sadowski F, Fleischmann A, Behling H, Schmidt AR 2015. Carnivorous leaves from Baltic amber. PNAS 112:1190–95
     [Google Scholar]
  102. 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
     [Google Scholar]
  103. 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
     [Google Scholar]
  104. 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.
     [Google Scholar]
  105. 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.
     [Google Scholar]
  106. 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
     [Google Scholar]
  107. 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
     [Google Scholar]
  108. 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
     [Google Scholar]
  109. 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
     [Google Scholar]
  110. 108. 
    Soucy SM, Huang J, Gogarten JP. 2015. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16:8472–82
     [Google Scholar]
  111. 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.
     [Google Scholar]
  112. 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
     [Google Scholar]
  113. 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
     [Google Scholar]
  114. 112. 
    True JR, Carroll SB. 2002. Gene co-option in physiological and morphological evolution. Annu. Rev. Cell Dev. Biol. 18:53–80
     [Google Scholar]
  115. 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
     [Google Scholar]
  116. 114. 
    Van de Peer Y, Maere S, Meyer A. 2009. The evolutionary significance of ancient genome duplications. Nat. Rev. Genet. 10:10725–32
     [Google Scholar]
  117. 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
     [Google Scholar]
  118. 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
     [Google Scholar]
  119. 117. 
    Wasternack C, Feussner I. 2018. The oxylipin pathways: biochemistry and function. Annu. Rev. Plant Biol. 69:363–86
     [Google Scholar]
  120. 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.
     [Google Scholar]
  121. 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
     [Google Scholar]
  122. 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
     [Google Scholar]
  123. 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
     [Google Scholar]
/content/journals/10.1146/annurev-arplant-080620-010429
Loading
On the Origin of Carnivory: Molecular Physiology and Evolution of Plants on an Animal Diet
Annual Review of Plant Biology 72, 133 (2021); https://doi.org/10.1146/annurev-arplant-080620-010429
/content/journals/10.1146/annurev-arplant-080620-010429
/content/journals/10.1146/annurev-arplant-080620-010429
Loading

Data & Media loading...

Supplemental Material

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 Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error