Plant Cognition and Behavior: From Environmental Awareness to Synaptic Circuits Navigating Root Apices

  • František BaluškaEmail author
  • Stefano Mancuso
Part of the Signaling and Communication in Plants book series (SIGCOMM)


Plants emerge as cognitive and intelligent organisms which coevolve with humans since the first flowering plants recognized primates as potential frugivores. Later, when humans started to settle down and initiated the agriculture, our coevolution with crop plants entered a new phase which allowed evolution of our civilization. Here we summarize recent advances in our understanding of plants relying, similarly as animals and humans, on learning and cognition to use their plant-specific behavior for survival. Although plants as such are sessile, their organs move actively and use these movements for active manipulation of their environment, both abiotic and biotic. Moreover, the major strategy of flowering plants is to control their animal pollinators and seed dispersers by providing them with food enriched not only with nutritive but also with manipulative and addictive compounds. There are several examples of cognitive supremacy of plants over animals.


  1. Abel S (2017) Phosphate scouting by root tips. Curr Opin Plant Biol 39:168–177CrossRefPubMedGoogle Scholar
  2. Akiyama K, Hayashi H (2006) Strigolactones: chemical signals for fungal symbionts and parasitic weeds in plant roots. Ann Bot 97:925–931PubMedCentralPubMedCrossRefGoogle Scholar
  3. Alpi A, Amrhein N, Bertl A, Blatt MR, Blumwald E, Cervone F, Dainty J, De Michelis MI, Epstein E, Galston AW, Goldsmith MH, Hawes C, Hell R, Hetherington A, Hofte H, Juergens G, Leaver CJ, Moroni A, Murphy A, Oparka K, Perata P, Quader H, Rausch T, Ritzenthaler C, Rivetta A, Robinson DG, Sanders D, Scheres B, Schumacher K, Sentenac H, Slayman CL, Soave C, Somerville C, Taiz L, Thiel G, Wagner R (2007) Plant neurobiology: no brain, no gain? Trends Plant Sci 12:135–136PubMedCentralPubMedCrossRefGoogle Scholar
  4. Appel HM, Cocroft RB (2014) Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–1266PubMedCentralPubMedCrossRefGoogle Scholar
  5. Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32:666–681CrossRefPubMedGoogle Scholar
  6. Ballaré CL, Pierik R (2017) The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ 40:2530–2543CrossRefPubMedGoogle Scholar
  7. Baluška F (2010) Recent surprising similarities between plant cells and neurons. Plant Signal Behav 5:87–89PubMedCentralPubMedCrossRefGoogle Scholar
  8. Baluška F, Hasenstein KH (1997) Root cytoskeleton: its role in perception of and response to gravity. Planta 203:S69–S78CrossRefPubMedGoogle Scholar
  9. Baluška F, Hlavacka A (2005) Plant formins come to age: something special about cross-walls. New Phytol 168:499–503CrossRefPubMedGoogle Scholar
  10. Baluška F, Levin M (2016) On having no head: cognition throughout biological systems. Front Psychol 7:902PubMedCentralPubMedCrossRefGoogle Scholar
  11. Baluška F, Lyons S (2018a) Symbiotic origin of eukaryotic nucleus—from Cell Body to Neo-Energide. In: Sahi VP, Baluška F (eds) Concepts in cell biology: history and evolution. Springer, Berlin. (In press)Google Scholar
  12. Baluška F, Lyons S (2018b) Energide-cell body as smallest unit of eukaryotic life. Ann Bot. (In press)Google Scholar
  13. Baluška F, Mancuso S (2007) Plant neurobiology as a paradigm shift not only in the plant sciences. Plant Signal Behav 2:205–207PubMedCentralPubMedCrossRefGoogle Scholar
  14. Baluška F, Mancuso S (2009a) Plant neurobiology: from sensory biology, via plant communication, to social plant behaviour. Cogn Process 10(Suppl. 1):3–7CrossRefGoogle Scholar
  15. Baluška F, Mancuso S (2009b) Deep evolutionary origins of neurobiology: turning the essence of ‘neural’ upside-down. Commun Integr Biol 2:60–65PubMedCentralPubMedCrossRefGoogle Scholar
  16. Baluška F, Mancuso S (2009c) Plants and animals: convergent evolution in action? In: Baluška F (ed) Plant-environment interactions: from sensory plant biology to active plant behavior. Springer, Berlin, pp 285–301CrossRefGoogle Scholar
  17. Baluška F, Mancuso S (2013) Root apex transition zone as oscillatory zone. Front Plant Sci 4:354PubMedCentralPubMedCrossRefGoogle Scholar
  18. Baluška F, Mancuso S (2016) Vision in plants via plant-specific ocelli? Trends Plant Sci 21:727–730CrossRefPubMedGoogle Scholar
  19. Baluška F, Mancuso S (2017) Plant ocelli for visually guided plant behavior. Trends Plant Sci 22:5–6CrossRefPubMedGoogle Scholar
  20. Baluška F, Vitha S, Barlow PW, Volkmann D (1997) Rearrangements of F-actin arrays in growing cells of intact maize root apex tissues: a major developmental switch occurs in the postmitotic transition region. Eur J Cell Biol 72:113–121PubMedGoogle Scholar
  21. Baluška F, Hlavačka A, Šamaj J, Palme K, Robinson DG, Matoh T, McCurdy DW, Menzel D, Volkmann D (2002) F-actin-dependent endocytosis of cell wall pectins in meristematic root cells: insights from brefeldin A-induced compartments. Plant Physiol 130:422–431PubMedCentralPubMedCrossRefGoogle Scholar
  22. Baluška F, Šamaj J, Menzel D (2003) Polar transport of auxin: carrier-mediated flux across the plasma membrane or neurotransmitter-like secretion? Trends Cell Biol 13:282–285CrossRefPubMedGoogle Scholar
  23. Baluška F, Mancuso S, Volkmann D, Barlow PW (2004a) Root apices as plant command centres: the unique ‘brain-like’ status of the root apex transition zone. Biologia 59(Suppl. 13):9–17Google Scholar
  24. Baluška F, Volkmann D, Barlow PW (2004b) Cell bodies in a cage. Nature 428:371CrossRefPubMedGoogle Scholar
  25. Baluška F, Volkmann D, Menzel D (2005a) Plant synapses: actin-based adhesion domains for cell-to-cell communication. Trends Plant Sci 10:106–111CrossRefPubMedGoogle Scholar
  26. Baluška F, Liners F, Hlavačka A, Schlicht M, Van Cutsem P, McCurdy D, Menzel D (2005b) Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 225:141–155CrossRefPubMedGoogle Scholar
  27. Baluška F, Barlow PW, Volkmann D, Mancuso S (2007) Gravity related paradoxes in plants: plant neurobiology provides the means for their resolution. In: Witzany G (ed) Biosemiotics in transdisciplinary context, Proceedings of the Gathering in Biosemiotics 6, Salzburg 2006. Umweb, HelsinkyGoogle Scholar
  28. Baluška F, Schlicht M, Volkmann D, Mancuso S (2008) Vesicular secretion of auxin: evidences and implications. Plant Signal Behav 3:254–256PubMedCentralPubMedCrossRefGoogle Scholar
  29. Baluška F, Schlicht M, Wan Y-L, Burbach C, Volkmann D (2009a) Intracellular domains and polarity in root apices: from synaptic domains to plant neurobiology. Nova Acta Leopold 96:103–122Google Scholar
  30. Baluška F, Mancuso S, Volkmann D, Barlow PW (2009b) The ‘root-brain’ hypothesis of Charles and Francis Darwin: revival after more than 125 years. Plant Signal Behav 4:1121–1127PubMedCentralPubMedCrossRefGoogle Scholar
  31. Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signalling—response nexus in the root. Trends Plant Sci 15:402–408CrossRefPubMedGoogle Scholar
  32. Baluška F, Volkmann D, Menzel D, Barlow PW (2012) Strasburger’s legacy to mitosis and cytokinesis and its relevance for the Cell Theory. Protoplasma 249:1151–1162CrossRefPubMedGoogle Scholar
  33. Baluška F, Yokawa K, Mancuso S, Baverstock K (2016) Understanding of anesthesia—why consciousness is essential for life and not based on genes. Commun Integr Biol 9:e1238118PubMedCentralPubMedCrossRefGoogle Scholar
  34. Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, Teulon JM, Creff A, Bissler M, Brouchoud C, Hagège A, Müller J, Chiarenza S, Javot H, Becuwe-Linka N, David P, Péret B, Delannoy E, Thibaud MC, Armengaud J, Abel S, Pellequer JL, Nussaume L, Desnos T (2017) Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nat Commun 8:15300PubMedCentralPubMedCrossRefGoogle Scholar
  35. Baracchi D, Marples A, Jenkins AJ, Leitch AR, Chittka L (2017) Nicotine in floral nectar pharmacologically influences bumblebee learning of floral features. Sci Rep 7:1951PubMedCentralPubMedCrossRefGoogle Scholar
  36. Barber CN, Huganir RL, Raben DM (2017) Phosphatidic acid-producing enzymes regulating the synaptic vesicle cycle: role for PLD? Adv Biol Regul (In press)Google Scholar
  37. Barlow PW (1995) Gravity perception in plants—a multiplicity of systems derived by evolution. Plant Cell Environ 18:951–962CrossRefPubMedGoogle Scholar
  38. Barlow PW (2006) Charles Darwin and the plant root apex: closing a gap in living systems theory as applied to plants. In: Baluška F, Mancuso S, Volkmann D (eds) Communication in plants: neuronal aspect of plant life. Springer, Berlin, pp 37–51CrossRefGoogle Scholar
  39. Barlow SE, Wright GA, Ma C, Barberis M, Farrell IW, Marr EC, Brankin A, Pavlik BM, Stevenson PC (2017) Distasteful nectar deters floral robbery. Curr Biol 27:2552–2558CrossRefPubMedGoogle Scholar
  40. Barrada A, Montané MH, Robaglia C, Menand B (2015) Spatial regulation of root growth: placing the plant TOR pathway in a developmental perspective. Int J Mol Sci 16:19671–19697PubMedCentralPubMedCrossRefGoogle Scholar
  41. Bateman RM (1991) Palaeoecology. In: Cleal CJ (ed) Plant fossils in geological investigation: the Palaeozoic. Ellis Horwood, Chichester, pp 34–116Google Scholar
  42. Bateman RM, Crane PR, DiMichele WA, Kenrick P, Rowe NP, Speck T, Stein WE (1998) Early evolution of land plants: phylogeny, physiology and ecology of the primary terrestrial radiation. Annu Rev Ecol Syst 29:263–292CrossRefGoogle Scholar
  43. Bauer U, Di Giusto B, Skepper J, Grafe TU, Federle W (2012) With a flick of the lid: a novel trapping mechanism in Nepenthes gracilis pitcher plants. PLoS One 7:e38951PubMedCentralPubMedCrossRefGoogle Scholar
  44. Bellot A, Guivernau B, Tajes M, Bosch-Morató M, Valls-Comamala V, Muñoz FJ (2014) The structure and function of actin cytoskeleton in mature glutamatergic dendritic spines. Brain Res 1573:1–16CrossRefPubMedGoogle Scholar
  45. Bender RL, Fekete ML, Klinkenberg PM, Hampton M, Bauer B, Malecha M, Lindgren K, Maki JA, Perera MA, Nikolau BJ, Carter CJ (2013) PIN6 is required for nectary auxin response and short stamen development. Plant J 74:893–890CrossRefPubMedGoogle Scholar
  46. Besserer A, Puech-Pagès V, Kiefer P, Gomez-Roldan V, Jauneau A, Roy S, Portais JC, Roux C, Bécard G, Séjalon-Delmas N (2006) Strigolactones stimulate arbuscular mycorrhizal fungi by activating mitochondria. PLoS Biol 4:e226PubMedCentralPubMedCrossRefGoogle Scholar
  47. Bhatt MV, Khandelwal A, Dudley SA (2011) Kin recognition, not competitive interactions, predicts root allocation in young Cakile edentula seedling pairs. New Phytol 189:1135–1142CrossRefPubMedGoogle Scholar
  48. Białasek M, Górecka M, Mittler R, Karpiński S (2017) Evidence for the involvement of electrical, calcium and ROS signaling in the systemic regulation of non-photochemical quenching and photosynthesis. Plant Cell Physiol 58:207–215PubMedCentralPubMedCrossRefGoogle Scholar
  49. Biedrzycki ML, Bais HP (2010) Kin recognition: another biological function for root secretions. Plant Signal Behav 5:401–402CrossRefPubMedGoogle Scholar
  50. Biedrzycki ML, Jilany TA, Dudley SA, Bais HP (2010) Root exudates mediate kin recognition in plants. Commun Integr Biol 3:28–35PubMedCentralPubMedCrossRefGoogle Scholar
  51. Biegler R (2017) Insufficient evidence for habituation in Mimosa pudica. Response to Gagliano et al. (2014). Oecologia (In press)Google Scholar
  52. Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R, Al-Rasheid KA, Rennenberg H, Shabala S, Neher E, Hedrich R (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Curr Biol 26:286–295PubMedCentralPubMedCrossRefGoogle Scholar
  53. Bonhomme V, Pelloux-Prayer H, Jousselin E, Forterre Y, Labat JJ, Gaume L (2011) Slippery or sticky? Functional diversity in the trapping strategy of Nepenthes carnivorous plants. New Phytol 191:545–554CrossRefPubMedGoogle Scholar
  54. Brenner E, Stahlberg R, Mancuso S, Vivanco J, Baluška F, Van Volkenburgh E (2006) Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11:413–419PubMedCentralPubMedCrossRefGoogle Scholar
  55. Brenner ED, Stahlberg R, Mancuso S, Baluška F, Van Volkenburgh E (2007) Response to Alpi et al: plant neurobiology: the gain is more than the name. Trends Plant Sci 12:285–286PubMedCentralPubMedCrossRefGoogle Scholar
  56. Broderbauer D, Weber A, Diaz A (2013) The design of trapping devices in pollination traps of the genus Arum (Araceae) is related to insect type. Bot J Linn Soc 172:385–397PubMedCentralPubMedCrossRefGoogle Scholar
  57. Buell CR, Last RL (2010) Twenty-first century plant biology: impacts of the Arabidopsis genome on plant biology and agriculture. Plant Physiol 154:497–500PubMedCentralPubMedCrossRefGoogle Scholar
  58. Bulgarelli D, Rott M, Schlaeppi K, van Themaat EVL, Ahmadinejad N, Assenza F, Rauf P, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95CrossRefPubMedGoogle Scholar
  59. Burbach C, Markus K, Zhang Y, Schlicht M, Baluška F (2012) Photophobic behavior of maize roots. Plant Signal Behav 7:874–878PubMedCentralPubMedCrossRefGoogle Scholar
  60. Busch W, Benfey PN (2010) Information processing without brains—the power of intercellular regulators in plants. Development 137:1215–1226PubMedCentralPubMedCrossRefGoogle Scholar
  61. Calvo P (2017) What is it like to be a plant? J Conscious Stud 24:205–227Google Scholar
  62. Calvo P, Friston K (2017) Predicting green: really radical (plant) predictive processing. J R Soc Interface 14:20170096PubMedCentralPubMedCrossRefGoogle Scholar
  63. Calvo P, Keijzer FA (2011) Plants: adaptive behavior, root brains and minimal cognition. Adapt Behav 19:155–171CrossRefGoogle Scholar
  64. Calvo P, Baluška F, Sims A (2016) “Feature Detection” vs. “Predictive Coding” Models of plant behavior. Front Psychol 7:1505PubMedCentralPubMedGoogle Scholar
  65. Calvo P, Sahi VP, Trewavas A (2017) Are plants sentient? Plant Cell Environ 40:2858–2869CrossRefPubMedGoogle Scholar
  66. Cao Y, Tanaka K, Nguyen CT, Stacey G (2014) Extracellular ATP is a central signaling molecule in plant stress responses. Curr Opin Plant Biol 20:82–87CrossRefPubMedGoogle Scholar
  67. Carvalhais LC, Dennis PG, Badri DV, Kidd BN, Vivanco JM, Schenk PM (2015) Linking jasmonic acid signaling, root exudates, and rhizosphere microbiomes. Mol Plant-Microbe Interact 28:1049–1058CrossRefPubMedGoogle Scholar
  68. Cazzonelli CI, Vanstraelen M, Simon S, Yin K, Carron-Arthur A, Nisar N, Tarle G, Cuttriss AJ, Searle IR, Benkova E, Mathesius U, Masle J, Friml J, Pogson BJ (2013) Role of the Arabidopsis PIN6 auxin transporter in auxin homeostasis and auxin-mediated development. PLoS One 8:e70069PubMedCentralPubMedCrossRefGoogle Scholar
  69. Chen R, Hilson P, Sedbrook J, Rosen E, Caspar T, Masson PH (1998) The Arabidopsis thaliana AGRAVITROPIC 1 gene encodes a component of the polar auxin transport efflux carrier. Proc Natl Acad Sci U S A 95:15112–15117PubMedCentralPubMedCrossRefGoogle Scholar
  70. Chen BJ, During HJ, Anten NP (2012) Detect thy neighbor: identity recognition at the root level in plants. Plant Sci 195:157–167CrossRefPubMedGoogle Scholar
  71. Chiu SL, Diering GH, Ye B, Takamiya K, Chen CM, Jiang Y, Niranjan T, Schwartz CE, Wang T, Huganir RL (2017) GRASP1 regulates synaptic plasticity and learning through endosomal recycling of AMPA receptors. Neuron 93:1405–1419PubMedCentralPubMedCrossRefGoogle Scholar
  72. Choi J, Tanaka K, Cao Y, Qi Y, Qiu J, Liang Y, Lee SY, Stacey G (2014a) Identification of a plant receptor for extracellular ATP. Science 343:290–294CrossRefPubMedGoogle Scholar
  73. Choi J, Tanaka K, Liang Y, Cao Y, Lee SY, Stacey G (2014b) Extracellular ATP, a danger signal, is recognized by DORN1 in Arabidopsis. Biochem J 463:429–437CrossRefPubMedGoogle Scholar
  74. Chowdhury MEK, Lim H, Bae H (2014) Update on the effects of sound wave on plants. Res Plant Dis 20:1–7CrossRefGoogle Scholar
  75. Contreras-Cornejo HA, López-Bucio JS, Méndez-Bravo A, Macías-Rodríguez L, Ramos-Vega M, Guevara-García ÁA, López-Bucio J (2015) Mitogen-activated protein Kinase 6 and ethylene and auxin signaling pathways are involved in Arabidopsis root-system architecture alterations by Trichoderma atroviride. Mol Plant-Microbe Interact 28:701–710CrossRefPubMedGoogle Scholar
  76. Couvillon MJ, Al Toufailia H, Butterfield TM, Schrell F, Ratnieks FLW, Schürch R (2015) Caffeinated forage tricks honeybees into increasing foraging and recruitment behaviors. Curr Biol 25:2815–2818CrossRefPubMedGoogle Scholar
  77. Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends Ecol Evol 20:487–494CrossRefPubMedGoogle Scholar
  78. Crepet WL, Niklas KJ (2009) Darwin's second ‘abominable mystery’: why are there so many angiosperm species? Am J Bot 96:366–381CrossRefPubMedGoogle Scholar
  79. Cvrčková F, Žárský V, Markoš A (2016) Plant studies may lead us to rethink the concept of behavior. Front Psychol 7:622PubMedCentralPubMedCrossRefGoogle Scholar
  80. Darwin C (1880) Power of movements in plants. John Murray, LondonCrossRefGoogle Scholar
  81. Daspute AA, Sadhukhan A, Tokizawa M, Kobayashi Y, Panda SK, Koyama H (2017) Transcriptional regulation of aluminum-tolerance genes in higher plants: clarifying the underlying molecular mechanisms. Front Plant Sci 8:1358PubMedCentralPubMedCrossRefGoogle Scholar
  82. De Luca PA, Vallejo-Marin M (2013) What’s the ‘buzz’ about? The ecology and evolutionary significance of buzz-pollination. Curr Opin Plant Biol 16:429–435CrossRefPubMedGoogle Scholar
  83. de Wit M, Keuskamp DH, Bongers FJ, Hornitschek P, Gommers CMM, Reinen E, Martínez-Cerón C, Fankhauser C, Pierik R (2016) Integration of phytochrome and cryptochrome signals determines plant growth during competition for light. Curr Biol 26:3320–3326CrossRefPubMedGoogle Scholar
  84. Degenhardt J, Hiltpold I, Köllner TG, Frey M, Gierl A, Gershenzon J, Hibbard BE, Ellersieck MR, Turlings TC (2009) Restoring a maize root signal that attracts insect-killing nematodes to control a major pest. Proc Natl Acad Sci U S A 106:13213–13218PubMedCentralPubMedCrossRefGoogle Scholar
  85. Dhonukshe P, Baluška F, Schlicht M, Hlavačka A, Šamaj J, Friml J, Gadella TWJ Jr (2006) Endocytosis of cell surface material mediates cell plate formation during plant cytokinesis. Dev Cell 10:137–150CrossRefPubMedGoogle Scholar
  86. Dhonukshe P, Grigoriev I, Fischer R, Tominaga M, Robinson DG, Hasek J, Paciorek T, Petrásek J, Seifertová D, Tejos R, Meisel LA, Zazímalová E, Gadella TW Jr, Stierhof YD, Ueda T, Oiwa K, Akhmanova A, Brock R, Spang A, Friml J (2008) Auxin transport inhibitors impair vesicle motility and actin cytoskeleton dynamics in diverse eukaryotes. Proc Natl Acad Sci U S A 105:4489–4494PubMedCentralPubMedCrossRefGoogle Scholar
  87. Ditengou FA, Gomes D, Nziengui H, Kochersperger P, Lasok H, Medeiros V, Paponov IA, Nagy SK, Nádai TV, Mészáros T, Barnabás B, Ditengou BI, Rapp K, Qi L, Li X, Becker C, Li C, Dóczi R, Palme K (2017) Characterization of auxin transporter PIN6 plasma membrane targeting reveals a function for PIN6 in plant bolting. New Phytol. (In press)CrossRefPubMedGoogle Scholar
  88. Dittmer HJ (1937) A quantitative study of the roots and root hairs of a winter rye plant (Secale cereale). Am J Bot 24:417–420CrossRefGoogle Scholar
  89. Dolan L (1998) Pointing roots in the right direction: the role of auxin transport in response to gravity. Genes Dev 12:2091–2095CrossRefPubMedGoogle Scholar
  90. Dubos C, Huggins D, Grant GH, Knight MR, Campbell MM (2003) A role for glycine in the gating of plant NMDA-like receptors. Plant J 35:800–810CrossRefPubMedGoogle Scholar
  91. Eggenberger K, Sanyal P, Hundt S, Wadhwani P, Ulrich AS, Nick P (2017) Challenge integrity: the cell-penetrating peptide BP100 interferes with the auxin-actin oscillator. Plant Cell Physiol 58:71–85PubMedGoogle Scholar
  92. Estabrook EM, Yoder JI (1998) Plant-plant communications: rhizosphere signaling between parasitic angiosperms and their hosts. Plant Physiol 116:1–7PubMedCentralPubMedCrossRefGoogle Scholar
  93. Eysholdt-Derzsó E, Sauter M (2017) Root bending is antagonistically affected by hypoxia and ERF-mediated transcription via auxin signaling. Plant Physiol 175:412–423PubMedCentralPubMedCrossRefGoogle Scholar
  94. Falik O, de Kroon H, Novoplansky A (2006) Physiologically-mediated self/non-self root discrimination in Trifolium repens has mixed effects on plant performance. Plant Signal Behav 1:116–121PubMedCentralPubMedCrossRefGoogle Scholar
  95. Fan W, Lou HQ, Yang JL, Zheng SJ (2016) The roles of STOP1-like transcription factors in aluminum and proton tolerance. Plant Signal Behav 11:e1131371CrossRefPubMedGoogle Scholar
  96. Fasano J, Massa G, Gilroy S (2002) Ionic signaling in plant responses to gravity and touch. J Plant Growth Regul 21:71–88CrossRefPubMedGoogle Scholar
  97. Foo E, Yoneyama K, Hugill C, Quittenden LJ, Reid JB (2013) Strigolactones: internal and external signals in plant symbioses? Plant Signal Behav 8:e23168PubMedCentralPubMedCrossRefGoogle Scholar
  98. Frederickson ME, Gordon DM (2007) The devil to pay: a cost of mutualism with Myrmelachista schumanni ants in ‘devil’s gardens’ is increased herbivory on Duroia hirsuta trees. Proc Biol Sci 274:1117–1123PubMedCentralPubMedCrossRefGoogle Scholar
  99. Frederickson ME, Greene MJ, Gordon DM (2005) ‘Devil’s gardens’ bedevilled by ants. Nature 437:495–496CrossRefPubMedGoogle Scholar
  100. Friedman WE (2009) The meaning of Darwin’s ‘abominable mystery’. Am J Bot 96:5–21CrossRefPubMedGoogle Scholar
  101. Fuller S (2003) Kuhn versus Popper—the struggle for the soul of science. Columbia University Press, New YorkGoogle Scholar
  102. Gagliano M (2013) Green symphonies: a call for studies on acoustic communication in plants. Behav Ecol 24:789–796CrossRefPubMedGoogle Scholar
  103. Gagliano M (2017) The mind of plants: thinking the unthinkable. Commun Integr Biol 10:e1288333PubMedCentralPubMedCrossRefGoogle Scholar
  104. Gagliano M, Mancuso S, Robert D (2012) Towards understanding plant bioacoustics. Trends Plant Sci 17:323–325CrossRefPubMedGoogle Scholar
  105. Gagliano M, Vyazovskiy VV, Borbély AA, Grimonprez M, Depczynski M (2016) Learning by association in plants. Sci Rep 6:38427PubMedCentralPubMedCrossRefGoogle Scholar
  106. Gagliano M, Grimonprez M, Depczynski M, Renton M (2017a) Tuned in: plant roots use sound to locate water. Oecologia 184:151–160PubMedCentralPubMedCrossRefGoogle Scholar
  107. Gagliano M, Abramson CI, Depczynski M (2017b) Plants learn and remember: lets get used to it. Oecologia. (In press)CrossRefPubMedGoogle Scholar
  108. Galen C, Rabenold JJ, Liscum E (2007a) Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. New Phytol 173:91–99CrossRefPubMedGoogle Scholar
  109. Galen C, Rabenold JJ, Liscum E (2007b) Light-sensing in roots. Plant Signal Behav 2:106–108PubMedCentralPubMedCrossRefGoogle Scholar
  110. Galloway AF, Pedersen MJ, Merry B, Marcus SE, Blacker J, Benning LG, Field KJ, Knox JP (2017) Xyloglucan is released by plants and promotes soil particle aggregation. New Phytol. (In press)PubMedCentralPubMedCrossRefGoogle Scholar
  111. Galvan-Ampudia CS, Testerink C (2011) Salt stress signals shape the plant root. Curr Opin Plant Biol 14:296–302CrossRefPubMedGoogle Scholar
  112. Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA, Brunoud G, Haring MA, Munnik T, Vernoux T, Testerink C (2013) Halotropism is a response of plant roots to avoid a saline environment. Curr Biol 23:2044–2050CrossRefPubMedGoogle Scholar
  113. Gardiner J (2012) Insights into plant consciousness from neuroscience, physics and mathematics: a role for quasicrystals? Plant Signal Behav 7:1049–1055PubMedCentralPubMedCrossRefGoogle Scholar
  114. Gaskett AC, Winnick CG, Herberstein ME (2008) Orchid sexual deceit provokes ejaculation. Am Nat 171:E206–E212CrossRefPubMedGoogle Scholar
  115. Giehl RFH, von Wirén N (2014) Root nutrient foraging. Plant Physiol 166:509–517PubMedCentralPubMedCrossRefGoogle Scholar
  116. Gilroy S, Białasek M, Suzuki N, Górecka M, Devireddy AR, Karpiński S, Mittler R (2016) ROS, calcium, and electric signals: key mediators of rapid systemic signaling in plants. Plant Physiol 171:1606–1615PubMedCentralPubMedCrossRefGoogle Scholar
  117. Godfrey-Smith P (1996) Precis of complexity and the function of mind in nature. Adapt Behav 4:453–465CrossRefGoogle Scholar
  118. Golomb L, Abu-Abied M, Belausov E, Sadot E (2008) Different subcellular localizations and functions of Arabidopsis myosin VIII. BMC Plant Biol 8:3PubMedCentralPubMedCrossRefGoogle Scholar
  119. González AP, Chrtek J, Dobrev PI, Dumalasová V, Fehrer J, Mráz P, Latzel V (2016) Stress-induced memory alters growth of clonal offspring of white clover (Trifolium repens). Am J Bot 103:1567–1574CrossRefPubMedGoogle Scholar
  120. González-Teuber M, Kaltenpoth M, Boland W (2014) Mutualistic ants as an indirect defence against leaf pathogens. New Phytol 202:640–650CrossRefPubMedGoogle Scholar
  121. Grasso DA, Pandolfi C, Bazihizina N, Nocentini D, Nepi M, Mancuso S (2015) Extrafloral-nectar-based partner manipulation in plant-ant relationships. AoB Plants 7:plv002PubMedCentralPubMedCrossRefGoogle Scholar
  122. Grémiaux A, Yokawa K, Mancuso S, Baluška F (2014) Plant anesthesia supports similarities between animals and plants: Claude Bernard’s forgotten studies. Plant Signal Behav 9:e27886PubMedCentralPubMedCrossRefGoogle Scholar
  123. Gruntman M, Novoplansky A (2004) Physiologically mediated self/non-self discrimination in roots. Proc Natl Acad Sci U S A 101:3863–3867PubMedCentralPubMedCrossRefGoogle Scholar
  124. Gu Y, Huganir RL (2016) Identification of the SNARE complex mediating the exocytosis of NMDA receptors. Proc Natl Acad Sci U S A 113:12280–12285PubMedCentralPubMedCrossRefGoogle Scholar
  125. Gu Y, Chiu SL, Liu B, Wu PH, Delannoy M, Lin DT, Wirtz D, Huganir RL (2016) Differential vesicular sorting of AMPA and GABAA receptors. Proc Natl Acad Sci U S A 113:E922–E931PubMedCentralPubMedCrossRefGoogle Scholar
  126. Gundel PE, Pierik R, Mommer L, Ballaré CL (2014) Competing neighbors: light perception and root function. Oecologia 176:1–10CrossRefPubMedGoogle Scholar
  127. Haberlandt T-H (1900) Über die Perception des geotropischen Reizes. Ber Dtsch Bot Ges 18:261–272Google Scholar
  128. Hahn A, Firn R, Edelmann HG (2006) Interacting signal transduction chains in gravity-stimulated maize roots. Signal Transduct 6:449–455CrossRefGoogle Scholar
  129. Hahn A, Zimmermann R, Wanke D, Harter K, Edelmann HG (2008) The root cap determines ethylene-dependent growth and development in maize roots. Mol Plant 1:359–367CrossRefPubMedGoogle Scholar
  130. Hedrich R, Salvador-Recatalà V, Dreyer I (2016) Electrical wiring and long-distance plant communication. Trends Plant Sci 21:376–387CrossRefPubMedPubMedCentralGoogle Scholar
  131. Henning T, Weigend M (2013a) Total control—pollen presentation and floral longevity in Loasaceae (blazing star family) are modulated by light, temperature and pollinator visitation rates. PLoS One 7:e41121CrossRefGoogle Scholar
  132. Henning T, Weigend M (2013b) Beautiful, complicated—and intelligent? Novel aspects of the thigmonastic stamen movement in Loasaceae. Plant Signal Behav 8:e24605PubMedCentralPubMedCrossRefGoogle Scholar
  133. Hodge A (2009) Root decisions. Plant Cell Environ 32:628–640PubMedCrossRefGoogle Scholar
  134. Hoffland E, Findenegg GR, Nelemans JA (1989) Solubilization of rock phosphate by rape. II. Local root exudation of organic acids as a response to P-starvation. Plant Soil 113:161–165CrossRefGoogle Scholar
  135. Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619–629PubMedCentralPubMedCrossRefGoogle Scholar
  136. Huang X, Maisch J, Nick P (2017) Sensory role of actin in auxin-dependent responses of tobacco BY-2. J Plant Physiol 218:6–15PubMedCrossRefGoogle Scholar
  137. Irwin RE, Cook D, Richardson LL, Manson JS, Gardner DR (2014) Secondary compounds in floral rewards of toxic rangeland plants: impacts on pollinators. J Agric Food Chem 62:7335–7344PubMedCrossRefGoogle Scholar
  138. Jásik J, Boggetti B, Baluška F, Volkmann D, Gensch T, Rutten T, Altmann T, Schmelzer E (2013) PIN2 turnover in Arabidopsis root epidermal cells explored by the photoconvertible protein Dendra2. PLoS One 8:e61403PubMedCentralPubMedCrossRefGoogle Scholar
  139. Jásik J, Bokor B, Stuchlík S, Mičieta K, Turňa J, Schmelzer E (2016) Effects of auxins on PIN-FORMED2 (PIN2) dynamics are not mediated by inhibiting PIN2 endocytosis. Plant Physiol 172:1019–1031PubMedCentralPubMedGoogle Scholar
  140. Jersáková J, Johnson SD, Kindlmann P (2006) Mechanisms and evolution of deceptive pollination in orchids. Biol Rev Camb Philos Soc 81:219–235PubMedCrossRefGoogle Scholar
  141. Karban R (2008) Plant behavior and communication. Ecol Lett 11:727–739PubMedCrossRefGoogle Scholar
  142. Karban R (2015) Plant sensing and communication. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  143. Karpiński S, Szechyńska-Hebda M (2010) Secret life of plants: from memory to intelligence. Plant Signal Behav 5:1391–1394PubMedCentralPubMedCrossRefGoogle Scholar
  144. Karpinski S, Reynolds H, Karpinska B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657CrossRefPubMedGoogle Scholar
  145. Kawa D, Julkowska MM, Sommerfeld HM, Ter Horst A, Haring MA, Testerink C (2016) Phosphate-dependent root system architecture responses to salt stress. Plant Physiol 172:690–706PubMedCentralPubMedGoogle Scholar
  146. Keijzer FA (2017) Evolutionary convergence and biologically embodied cognition. Interface Focus 7:20160123CrossRefPubMedPubMedCentralGoogle Scholar
  147. Keijzer FA, van Duijn M, Lyon P (2013) What nervous systems do: early evolution, input–output, and the skin brain thesis. Adapt Behav 21:67–85CrossRefGoogle Scholar
  148. Kent Peters N, Long SR (1988) Alfalfa root exudates and compounds which promote or inhibit induction of Rhizobium meliloti nodulation genes. Plant Physiol 88:396–400CrossRefGoogle Scholar
  149. Kessler D, Baldwin IT (2007) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–354CrossRefPubMedGoogle Scholar
  150. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202CrossRefPubMedGoogle Scholar
  151. Kessler D, Diezel C, Baldwin IT (2010) Changing pollinators as a means of escaping herbivores. Curr Biol 20:237–242CrossRefPubMedGoogle Scholar
  152. Knee EM, Gong FC, Gao M, Teplitski M, Jones AR, Foxworthy A, Mort AJ, Bauer WD (2001) Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol Plant-Microbe Interact 14:775–784CrossRefPubMedGoogle Scholar
  153. Kobayashi Y, Kobayashi Y, Sugimoto M, Lakshmanan V, Iuchi S, Kobayashi M, Bais HP, Koyama H (2013a) Characterization of the complex regulation of AtALMT1 expression in response to phytohormones and other inducers. Plant Physiol 162:732–740PubMedCentralPubMedCrossRefGoogle Scholar
  154. Kobayashi Y, Lakshmanan V, Kobayashi Y, Asai M, Iuchi S, Kobayashi M, Bais HP, Koyama H (2013b) Overexpression of AtALMT1 in the Arabidopsis thaliana ecotype Columbia results in enhanced Al-activated malate excretion and beneficial bacterium recruitment. Plant Signal Behav 8:e25565PubMedCentralPubMedCrossRefGoogle Scholar
  155. Koch H, Stevenson PC (2017) Do linden trees kill bees? Reviewing the causes of bee deaths on silver linden (Tilia tomentosa). Biol Lett 13:20170484PubMedCrossRefPubMedCentralGoogle Scholar
  156. Köhler A, Pirk CW, Nicolson SW (2012) Honeybees and nectar nicotine: deterrence and reduced survival versus potential health benefits. J Insect Physiol 58:286–292PubMedCrossRefGoogle Scholar
  157. Koltai H (2015) Cellular events of strigolactone signalling and their crosstalk with auxin in roots. J Exp Bot 66:4855–4861PubMedCrossRefGoogle Scholar
  158. Koncz C (2006) Dedication: George P. Rédei—Arabidopsis geneticist and polymath. Plant Breed Rev 26:1–33Google Scholar
  159. Konings H (1995) Gravitropism of roots: an evaluation of progress during the last three decades. Acta Bot Neerl 44:195–223CrossRefGoogle Scholar
  160. Kuhn TS (1962, 2012) The structure of scientific revolutions. University of Chicago Press, ChicagoGoogle Scholar
  161. Kumar AS, Bais HP (2012) Wired to the roots: impact of root-beneficial microbe interactions on aboveground plant physiology and protection. Plant Signal Behav 7:1598–1604PubMedCentralPubMedCrossRefGoogle Scholar
  162. Kumar M, Pandya-Kumar N, Dam A, Haor H, Mayzlish-Gati E, Belausov E, Wininger S, Abu-Abied M, McErlean CS, Bromhead LJ, Prandi C, Kapulnik Y, Koltai H (2015) Arabidopsis response to low-phosphate conditions includes active changes in actin filaments and PIN2 polarization and is dependent on strigolactone signalling. J Exp Bot 66:1499–2510PubMedCentralPubMedCrossRefGoogle Scholar
  163. Kutschera U, Niklas KJ (2009) Evolutionary plant physiology: Charles Darwin’s forgotten synthesis. Naturwissenschaften 96:1339–1354PubMedCentralPubMedCrossRefGoogle Scholar
  164. Lakshmanan V, Castaneda R, Rudrappa T, Bais HP (2013) Root transcriptome analysis of Arabidopsis thaliana exposed to beneficial Bacillus subtilis FB17 rhizobacteria revealed genes for bacterial recruitment and plant defense independent of malate efflux. Planta 238:657–668PubMedCrossRefGoogle Scholar
  165. Lapsansky ER, Milroy AM, Andales MJ, Vivanco JM (2016) Soil memory as a potential mechanism for encouraging sustainable plant health and productivity. Curr Opin Biotechnol 38:137–142PubMedCrossRefGoogle Scholar
  166. Lee HJ, Ha JH, Kim SG, Choi HK, Kim ZH, Han YJ, Kim JI, Oh Y, Fragoso V, Shin K, Hyeon T, Choi HG, Oh KH, Baldwin IT, Park CM (2016a) Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Sci Signal 9:ra106PubMedCrossRefGoogle Scholar
  167. Lee HJ, Ha JH, Park CM (2016b) Underground roots monitor aboveground environment by sensing stem-piped light. Commun Integr Biol 9:e1261769PubMedCentralPubMedCrossRefGoogle Scholar
  168. Lee HJ, Park YJ, Ha JH, Baldwin IT, Park CM (2017) Multiple routes of light signaling during root photomorphogenesis. Trends Plant Sci 22:803–812PubMedCrossRefGoogle Scholar
  169. Lei W, Myers KR, Rui Y, Hladyshau S, Tsygankov D, Zheng JQ (2017) Phosphoinositide-dependent enrichment of actin monomers in dendritic spines regulates synapse development and plasticity. J Cell Biol 216:2551–2564PubMedCentralPubMedCrossRefGoogle Scholar
  170. Lev-Yadun S (2016a) Plants are not sitting ducks waiting for herbivores to eat them. Plant Signal Behav 11:e1179419PubMedCentralPubMedCrossRefGoogle Scholar
  171. Lev-Yadun S (2016b) Does the whistling thorn acacia (Acacia drepanolobium) use auditory aposematism to deter mammalian herbivores? Plant Signal Behav 11:e1207035PubMedCentralPubMedCrossRefGoogle Scholar
  172. Lev-Yadun S (2017) Do carrots outsmart rabbits? Trends Ecol Evol 32:227–228CrossRefGoogle Scholar
  173. Li X, Zhang W (2008) Salt-avoidance tropism in Arabidopsis thaliana. Plant Signal Behav 3:351–353PubMedCentralPubMedCrossRefGoogle Scholar
  174. Liu Y, Lai N, Gao K, Chen F, Yuan L, Mi G (2013) Ammonium inhibits primary root growth by reducing the length of meristem and elongation zone and decreasing elemental expansion rate in the root apex in Arabidopsis thaliana. PLoS One 8:e61031PubMedCentralPubMedCrossRefGoogle Scholar
  175. Liu JT, Hu LS, Liu YL, Chen RS, Cheng Z, Chen SJ, Amatore C, Huang WH, Huo KF (2014) Real-time monitoring of auxin vesicular exocytotic efflux from single plant protoplasts by amperometry at microelectrodes decorated with nanowires. Angew Chem Int Ed Eng 53:2643–2647CrossRefGoogle Scholar
  176. López-Bucio JS, Dubrovsky JG, Raya-González J, Ugartechea-Chirino Y, López-Bucio J, de Luna-Valdez LA, Ramos-Vega M, León P, Guevara-García AA (2014) Arabidopsis thaliana mitogen-activated protein kinase 6 is involved in seed formation and modulation of primary and lateral root development. J Exp Bot 65:169–183CrossRefPubMedGoogle Scholar
  177. López-Ráez JA, Shirasu K, Foo E (2017) Strigolactones in plant interactions with beneficial and detrimental organisms: the Yin and Yang. Trends Plant Sci 22:527–537CrossRefPubMedGoogle Scholar
  178. Luschnig C, Vert G (2014) The dynamics of plant plasma membrane proteins: PINs and beyond. Development 141:2924–2938CrossRefPubMedGoogle Scholar
  179. Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev 12:2175–2187PubMedCentralPubMedCrossRefGoogle Scholar
  180. Lyon P (2006) The biogenic approach to cognition. Cogn Process 7:11–29CrossRefPubMedGoogle Scholar
  181. Lyon P (2015) The cognitive cell: bacterial behavior reconsidered. Front Microbiol 6:264PubMedCentralPubMedCrossRefGoogle Scholar
  182. Mancuso S, Marras AM, Volker M, Baluška F (2005) Non-invasive and continuous recordings of auxin fluxes in intact root apex with a carbon-nanotube-modified and self-referencing microelectrode. Anal Biochem 341:344–351CrossRefPubMedGoogle Scholar
  183. Mancuso S, Marras AM, Mugnai S, Schlicht M, Zarsky V, Li G, Song L, Hue HW, Baluška F (2007) Phospholipase Dζ2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244PubMedCentralPubMedCrossRefGoogle Scholar
  184. Manoli A, Begheldo M, Genre A, Lanfranco L, Trevisan S, Quaggiotti S (2014) NO homeostasis is a key regulator of early nitrate perception and root elongation in maize. J Exp Bot 65:185–200CrossRefPubMedGoogle Scholar
  185. Manoli A, Trevisan S, Voigt B, Yokawa K, Baluška F, Quaggiotti S (2016) Nitric oxide-mediated maize root apex responses to nitrate are regulated by auxin and strigolactones. Front Plant Sci 6:1269PubMedCentralPubMedCrossRefGoogle Scholar
  186. Marder M (2012) Plant intentionality and the phenomenological framework of plant intelligence. Plant Signal Behav 7:1365–1372PubMedCentralPubMedCrossRefGoogle Scholar
  187. Marder M (2013) Plant intelligence and attention. Plant Signal Behav 8:e23902PubMedCentralPubMedCrossRefGoogle Scholar
  188. Margulis L, Sagan D (1995) What is life? Simon & Schuster, New YorkGoogle Scholar
  189. Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluška F, Arecchi FT, Mancuso S (2009) Spatio-temporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci U S A 106:4048–4053PubMedCentralPubMedCrossRefGoogle Scholar
  190. Mayer VE, Frederickson ME, McKey D, Blatrix R (2014) Current issues in the evolutionary ecology of ant-plant symbioses. New Phytol 202:749–764CrossRefPubMedGoogle Scholar
  191. Mescher MC, De Moraes CM (2015) Role of plant sensory perception in plant-animal interactions. J Exp Bot 66:425–433CrossRefPubMedGoogle Scholar
  192. Mescher MC, Runyon JB, De Moraes CM (2006) Plant host finding by parasitic plants. A new perspective on plant-to-plant communication. Plant Signal Behav 1:284–286PubMedCentralPubMedCrossRefGoogle Scholar
  193. Metlen KL, Aschehoug ET, Callaway RM (2009) Plant behavioural ecology: dynamic plasticity in secondary metabolites. Plant Cell Environ 32:641–653CrossRefPubMedGoogle Scholar
  194. Mettbach U, Strnad M, Mancuso S, Baluška F (2017) Immunogold-EM analysis reveal Brefeldin A-sensitive clusters of auxin in Arabidopsis root apex cells. Plant Signal Behav 10:e1327105Google Scholar
  195. Michard E, Lima PT, Borges F, Silva AC, Portes MT, Carvalho JE, Gilliham M, Liu LH, Obermeyer G, Feijó JA (2011) Glutamate receptor-like genes form Ca2+ channels in pollen tubes and are regulated by pistil D-serine. Science 332:434–437CrossRefPubMedGoogle Scholar
  196. Mishra RC, Ghosh R, Bae H (2016) Plant acoustics: in the search of a sound mechanism for sound signaling in plants. J Exp Bot 67:4483–4494CrossRefPubMedGoogle Scholar
  197. Mo M, Yokawa K, Wan Y, Baluška F (2015) How and why do root apices sense light under the soil surface? Front Plant Sci 6:775PubMedCentralPubMedGoogle Scholar
  198. Moni A, Lee AY, Briggs WR, Han IS (2015) The blue light receptor Phototropin 1 suppresses lateral root growth by controlling cell elongation. Plant Biol 17:34–40CrossRefPubMedGoogle Scholar
  199. Monshausen GB, Zieschang HE, Sievers A (1996) Differential proton secretion in the apical elongation zone caused by gravistimulation is induced by a signal from the root cap. Plant Cell Environ 19:1408–1414CrossRefPubMedGoogle Scholar
  200. Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, Raya-González J, Jiménez-Domínguez G, Chávez-Calvillo G, Rellán-Álvarez R, Herrera-Estrella L (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proc Natl Acad Sci U S A 114:E3563–E3572PubMedCentralPubMedCrossRefGoogle Scholar
  201. Morel J, Habib L, Plantureux S, Guckert A (1991) Influence of maize root mucilage on soil aggregate stability. Plant Soil 136:111–119CrossRefGoogle Scholar
  202. Müller A, Guan C, Gälweiler L, Tänzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K (1998) AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–6911PubMedCentralPubMedCrossRefGoogle Scholar
  203. Müller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Šamaj J (2010) Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-golgi network and plasma membrane. Plant J 61:234–248CrossRefPubMedGoogle Scholar
  204. Murphy GP, Dudley SA (2009) Kin recognition: competition and cooperation in Impatiens (Balsaminaceae). Am J Bot 96:1990–1996CrossRefPubMedGoogle Scholar
  205. Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X, Friml J, Scheres B, Fu Y, Yang Z (2012) ROP GTPase-dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLoS Biol 10:e1001299PubMedCentralPubMedCrossRefGoogle Scholar
  206. Nemec B (1900) Über die Art der Wahrnehmung des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18:241–245Google Scholar
  207. Nemec B (1902) Die Perception des Schwerkraftreizes bei den Pflanzen. Ber Dtsch Bot Ges 18:339–355Google Scholar
  208. Nepi M (2014) Beyond nectar sweetness: the hidden ecological role of non-protein amino acids in nectar. J Ecol 102:108–115CrossRefGoogle Scholar
  209. Nepi M (2017) New perspectives in nectar evolution and ecology: simple alimentary reward or a complex multiorganism interaction? Acta Agrobot 70 (In press)Google Scholar
  210. Ni M, Zhang L, Shi YF, Wang C, Lu Y, Pan J, Liu JZ (2017) Excessive cellular S-nitrosothiol impairs endocytosis of auxin efflux transporter PIN2. Front Plant Sci 8:1988PubMedCentralPubMedCrossRefGoogle Scholar
  211. Nick P (2010) Probing the actin-auxin oscillator. Plant Signal Behav 5:94–98PubMedCentralPubMedCrossRefGoogle Scholar
  212. Nisar N, Cuttriss AJ, Pogson BJ, Cazzonelli CI (2014) The promoter of the Arabidopsis PIN6 auxin transporter enabled strong expression in the vasculature of roots, leaves, floral stems and reproductive organs. Plant Signal Behav 9:e27898PubMedCentralPubMedCrossRefGoogle Scholar
  213. Nonaka A, Toyoda T, Miura Y, Hitora-Imamura N, Naka M, Eguchi M, Yamaguchi S, Ikegaya Y, Matsuki N, Nomura H (2014) Synaptic plasticity associated with a memory engram in the basolateral amygdala. J Neurosci 34:9305–9309CrossRefPubMedGoogle Scholar
  214. Novoplansky A (2009) Picking battles wisely: plant behaviour under competition. Plant Cell Environ 32:726–741CrossRefPubMedGoogle Scholar
  215. Oelschlägel B, Gorb S, Wanke S, Neinhuis C (2009) Structure and biomechanics of trapping flower trichomes and their role in the pollination biology of Aristolochia plants (Aristolochiaceae). New Phytol 184:988–1002CrossRefPubMedGoogle Scholar
  216. Orrock J, Connolly B, Kitchen A (2017) Induced defences in plants reduce herbivory by increasing cannibalism. Nat Ecol Evol 1:1205–1207CrossRefPubMedGoogle Scholar
  217. Ortiz-Ramírez C, Michard E, Simon AA, Damineli DSC, Hernández-Coronado M, Becker JD, Feijó JA (2017) GLUTAMATE RECEPTOR-LIKE channels are essential for chemotaxis and reproduction in mosses. Nature 549:91–95CrossRefPubMedGoogle Scholar
  218. Pandya-Kumar N, Shema R, Kumar M, Mayzlish-Gati E, Levy D, Zemach H, Belausov E, Wininger S, Abu-Abied M, Kapulnik Y, Koltai H (2014) Strigolactone analog GR24 triggers changes in PIN2 polarity, vesicle trafficking and actin filament architecture. New Phytol 202:1184–1196CrossRefPubMedGoogle Scholar
  219. Pantazopoulou CK, Bongers FJ, Küpers JJ, Reinen E, Das D, Evers JB, Anten NPR, Pierik R (2017) Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics. Proc Natl Acad Sci U S A 114:7450–7455PubMedCentralPubMedCrossRefGoogle Scholar
  220. Pavlovič A, Jakšová J, Novák O (2017) Triggering a false alarm: wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). New Phytol 216:927–938CrossRefPubMedGoogle Scholar
  221. Perrin RM, Young LS, Murthy UMN, Harrison BR, Wang Y, Will JL, Masson PH (2005) Gravity signal transduction in primary roots. Ann Bot 96:737–743PubMedCentralPubMedCrossRefGoogle Scholar
  222. Phillips RD, Scaccabarozzi D, Retter BA, Hayes C, Brown GR, Dixon KW, Peakall R (2014) Caught in the act: pollination of sexually deceptive trap-flowers by fungus gnats in Pterostylis (Orchidaceae). Ann Bot 113:629–641CrossRefPubMedGoogle Scholar
  223. Pierik R, de Wit M (2014) Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues. J Exp Bot 65:2815–2824CrossRefPubMedGoogle Scholar
  224. Pierik R, Testerink C (2014) The art of being flexible: how to escape from shade, salt, and drought. Plant Physiol 166:5–22PubMedCentralPubMedCrossRefGoogle Scholar
  225. Pierik R, De Wit M, Voesenek LACJ (2011) Growth-mediated stress escape: convergence of signal transduction pathways activated upon exposure to two different environmental stresses. New Phytol 189:122–134CrossRefPubMedGoogle Scholar
  226. Plieth C, Trewavas A (2002) Reorientation of seedlings in the Earth’s gravitational field induces cytosolic calcium transients. Plant Physiol 129:786–796PubMedCentralPubMedCrossRefGoogle Scholar
  227. Popper K (1994) All life is problem solving. Routledge, Taylor and Francis Group, AbingdonGoogle Scholar
  228. Price MB, Jelesko J, Okumoto S (2012) Glutamate receptor homologs in plants: functions and evolutionary origins. Front Plant Sci 3:235PubMedCentralPubMedCrossRefGoogle Scholar
  229. Pyke GH (2016) Floral nectar: pollinator attraction or manipulation? Trends Ecol Evol 31:339–341CrossRefPubMedGoogle Scholar
  230. Qu Y, Wang Q, Guo J, Wang P, Song P, Jia Q, Zhang X, Kudla J, Zhang W, Zhang Q (2017) Peroxisomal CuAOζ and its product H2O2 regulate the distribution of auxin and IBA-dependent lateral root development in Arabidopsis. J Exp Bot 68:4851–4867CrossRefPubMedGoogle Scholar
  231. Raghothama KG (1999) Phosphate acquisition. Annu Rev Plant Physiol Plant Mol Biol 50:665–693CrossRefPubMedGoogle Scholar
  232. Ramesh SA, Tyerman SD, Xu B, Bose J, Kaur S, Conn V, Domingos P, Ullah S, Wege S, Shabala S, Feijó JA, Ryan PR, Gilliham M (2015) GABA signalling modulates plant growth by directly regulating the activity of plant-specific anion transporters. Nat Commun 6:7879PubMedCentralPubMedCrossRefGoogle Scholar
  233. Ramesh SA, Tyerman SD, Gilliham M, Xu B (2017) γ-Aminobutyric acid (GABA) signalling in plants. Cell Mol Life Sci 74:1577–1603CrossRefPubMedGoogle Scholar
  234. Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–737CrossRefPubMedGoogle Scholar
  235. Retzer K, Lacek J, Skokan R, Del Genio CI, Vosolsobě S, Laňková M, Malínská K, Konstantinova N, Zažímalová E, Napier RM, Petrášek J, Luschnig C (2017) Evolutionary conserved cysteines function as cis-acting regulators of Arabidopsis PIN-FORMED 2 distribution. Int J Mol Sci 18:E2274CrossRefPubMedGoogle Scholar
  236. Rodrigo-Moreno A, Bazihizina N, Azzarello E, Masi E, Tran D, Bouteau F, Baluška F, Mancuso S (2017) Root phonotropism: early signalling events following sound perception in Arabidopsis roots. Plant Sci 264:9–15CrossRefPubMedGoogle Scholar
  237. Rudrappa T, Czymmek KJ, Paré PW, Bais HP (2008) Root-secreted malic acid recruits beneficial soil bacteria. Plant Physiol 148:1547–1556PubMedCentralPubMedCrossRefGoogle Scholar
  238. Rumpel S, LeDoux J, Zador A, Malinow R (2005) Postsynaptic receptor trafficking underlying a form of associative learning. Science 308:83–88CrossRefPubMedGoogle Scholar
  239. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–2967CrossRefPubMedGoogle Scholar
  240. Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F (2005) The endocytic network in plants. Trends Cell Biol 15:425–433CrossRefPubMedGoogle Scholar
  241. Sattarzadeh A, Franzen R, Schmelzer E (2008) The Arabidopsis class VIII myosin ATM2 is involved in endocytosis. Cell Motil Cytoskeleton 65:457–468CrossRefPubMedGoogle Scholar
  242. Schiestl FP (2005) On the success of a swindle: pollination by deception in orchids. Naturwissenschaften 92:255–264CrossRefPubMedGoogle Scholar
  243. Schiestl FP (2010) Pollination: sexual mimicry abounds. Curr Biol 20:R1020–R1022CrossRefPubMedGoogle Scholar
  244. Schlicht M, Strnad M, Scanlon MJ, Mancuso S, Hochholdinger F, Palme K, Volkmann D, Menzel D, Baluška F (2006) Auxin immunolocalization implicates vesicular neurotransmitter-like mode of polar auxin transport in root apices. Plant Signal Behav 1:122–133PubMedCentralPubMedCrossRefGoogle Scholar
  245. Schlicht M, Šamajová O, Schachtschabel D, Mancuso S, Menzel D, Boland W, Baluška F (2008) Dorenone blocks polarized tip-growth of root hairs by interfering with the PIN2-mediated auxin transport network in the root apex. Plant J 55:709–717CrossRefPubMedGoogle Scholar
  246. Sekereš J, Pleskot R, Pejchar P, Žárský V, Potocký M (2015) The song of lipids and proteins: dynamic lipid-protein interfaces in the regulation of plant cell polarity at different scales. J Exp Bot 66:1587–1598CrossRefPubMedGoogle Scholar
  247. Sibaoka T (1991) Rapid plant movements triggered by action potentials. Bot Mag Tokyo 104:73–95CrossRefGoogle Scholar
  248. Sievers A, Behrens H, Buckhout T, Gradmann D (1984) Can a Ca2+ pump in the endoplasmic reticulum of the Lepidium root be the trigger for rapid changes in membrane potential after gravistimulation? J Plant Physiol 114:195–200PubMedGoogle Scholar
  249. Simon S, Skůpa P, Viaene T, Zwiewka M, Tejos R, Klíma P, Čarná M, Rolčík J, De Rycke R, Moreno I, Dobrev PI, Orellana A, Zažímalová E, Friml J (2016) PIN6 auxin transporter at endoplasmic reticulum and plasma membrane mediates auxin homeostasis and organogenesis in Arabidopsis. New Phytol 211:65–74CrossRefPubMedGoogle Scholar
  250. Sivaguru M, Baluška F, Volkmann D, Felle HH, Horst WJ (1999) Impacts of aluminum on the cytoskeleton of the maize root apex. Short-term effects on the distal part of the transition zone. Plant Physiol 119:1073–1082PubMedCentralPubMedCrossRefGoogle Scholar
  251. Sivaguru M, Pike S, Gassmann W, Baskin TI (2003) Aluminum rapidly depolymerizes cortical microtubules and depolarizes the plasma membrane: evidence that these responses are mediated by a glutamate receptor. Plant Cell Physiol 44:667–675CrossRefPubMedGoogle Scholar
  252. Smékalová V, Luptovčiak I, Komis G, Šamajová O, Ovečka M, Doskočilová A, Takáč T, Vadovič P, Novák O, Pechan T, Ziemann A, Košútová P, Šamaj J (2014) Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation. New Phytol 203:1175–1193PubMedCentralPubMedCrossRefGoogle Scholar
  253. Stahlberg R, Stephens NR, Cleland RE, Van Volkenburgh E (2006) Shade-induced action potentials in Helianthus annuus L. originate primarily from the epicotyl. Plant Signal Behav 1:15–22PubMedCentralPubMedCrossRefGoogle Scholar
  254. Stolarz M, Dziubinska H (2017) Osmotic and salt stresses modulate spontaneous and glutamate-induced action potentials and distinguish between growth and circumnutation in Helianthus annuus seedlings. Front Plant Sci 8:1766PubMedCentralPubMedCrossRefGoogle Scholar
  255. Sun F, Zhang W, Hu H, Li B, Wang Y, Zhao Y, Li K, Liu M, Li X (2008) Salt modulates gravity signaling pathway to regulate growth direction of primary roots in Arabidopsis. Plant Physiol 146:178–188PubMedCentralPubMedCrossRefGoogle Scholar
  256. Sun J, Chen Q, Qi L, Jiang H, Li S, Xu Y, Liu F, Zhou W, Pan J, Li X, Palme K, Li C (2011) Jasmonate modulates endocytosis and plasma membrane accumulation of the Arabidopsis PIN2 protein. New Phytol 191:360–375PubMedCrossRefGoogle Scholar
  257. Suzuki H, Yokawa K, Nakano S, Yoshida Y, Fabrissin I, Okamoto T, Baluška F, Koshiba T (2016) Root cap-dependent gravitropic U-turn of maize root requires light-induced auxin biosynthesis via the YUC pathway in the root apex. J Exp Bot 67:4581–4591PubMedCentralPubMedCrossRefGoogle Scholar
  258. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, Blanchet A, Nussaume L, Desnos T (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796PubMedCrossRefGoogle Scholar
  259. Sweeney C, Lakshmanan V, Bais HP (2017) Interplant above-ground signaling prompts upregulation of auxin promoter and malate transporter as part of defensive response in the neighboring plants. Front Plant Sci 8:595PubMedCentralPubMedCrossRefGoogle Scholar
  260. Szczuka A, Korczyńska J, Wnuk A, Symonowicz B, Gonzalez Szwacka A, Mazurkiewicz P, Kostowski W, Godzińska EJ (2013) The effects of serotonin, dopamine, octopamine and tyramine on behavior of workers of the ant Formica polyctena during dyadic aggression tests. Acta Neurobiol Exp. (Wars) 73:495–520Google Scholar
  261. Szechyńska-Hebda M, Kruk J, Górecka M, Karpińska B, Karpiński S (2010) Evidence for light wavelength-specific photoelectrophysiological signaling and memory of excess light episodes in Arabidopsis. Plant Cell 22:2201–2218PubMedCentralPubMedCrossRefGoogle Scholar
  262. Szechyńska-Hebda M, Lewandowska M, Karpiński S (2017) Electrical signaling, photosynthesis and systemic acquired acclimation. Front Physiol 8:684PubMedCentralPubMedCrossRefGoogle Scholar
  263. Takáč T, Vadovič P, Pechan T, Luptovčiak I, Šamajová O, Šamaj J (2016) Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6. Sci Rep 6:28306PubMedCentralPubMedCrossRefGoogle Scholar
  264. Tanaka K, Choi J, Cao Y, Stacey G (2014) Extracellular ATP acts as a damage-associated molecular pattern (DAMP) signal in plants. Front Plant Sci 5:446PubMedCentralPubMedCrossRefGoogle Scholar
  265. Tononi G, Cirelli C (2014) Sleep and the price of plasticity: from synaptic and cellular homeostasis to memory consolidation and integration. Neuron 81:12–34PubMedCentralPubMedCrossRefGoogle Scholar
  266. Trevisan S, Manoli A, Quaggiotti S (2014) NO signaling is a key component of the root growth response to nitrate in Zea mays L. Plant Signal Behav 9:e28290PubMedCentralPubMedCrossRefGoogle Scholar
  267. Trevisan S, Manoli A, Ravazzolo L, Botton A, Pivato M, Masi A, Quaggiotti S (2015) Nitrate sensing by the maize root apex transition zone: a merged transcriptomic and proteomic survey. J Exp Bot 66:3699–3715PubMedCentralPubMedCrossRefGoogle Scholar
  268. Trewavas A (2005) Plant intelligence. Naturwissenschaften 92:401–413CrossRefPubMedGoogle Scholar
  269. Trewavas A (2007) Response to Alpi et al.: Plant neurobiology—all metaphors have value. Trends Plant Sci 12:231–233CrossRefPubMedGoogle Scholar
  270. Trewavas AJ (2014) Plan behaviour and intelligence. Oxford University Press, OxfordCrossRefGoogle Scholar
  271. Trewavas A (2016) Intelligence, cognition, and language of green plants. Front Psychol 7:588PubMedCentralPubMedCrossRefGoogle Scholar
  272. Trewavas A (2017) The foundations of plant intelligence. Interface Focus 7:20160098PubMedCrossRefPubMedCentralGoogle Scholar
  273. Trewavas A, Baluška F (2011) The ubiquity of consciousness. EMBO Rep 12:1221–1225PubMedCentralPubMedCrossRefGoogle Scholar
  274. Tripathi D, Zhang T, Koo AJ, Stacey G, Tanaka K (2017) Extracellular ATP acts on jasmonate signaling to reinforce plant defense. Plant Physiol (In press)PubMedCrossRefPubMedCentralGoogle Scholar
  275. Tsai HH, Schmidt W (2017) Mobilization of iron by plant-borne coumarins. Trends Plant Sci 22:538–548CrossRefPubMedGoogle Scholar
  276. Tu-Sekine B, Goldschmidt H, Raben DM (2015) Diacylglycerol, phosphatidic acid, and their metabolic enzymes in synaptic vesicle recycling. Adv Biol Regul 57:147–152PubMedCrossRefGoogle Scholar
  277. Utsuno K, Shikanai T, Yamada Y, Hashimoto T (1998) AGR, an Agravitropic locus of Arabidopsis thaliana, encodes a novel, membrane-protein family member. Plant Cell Physiol 39:1111–1118PubMedCrossRefGoogle Scholar
  278. Valenzuela CE, Acevedo-Acevedo O, Miranda GS, Vergara-Barros P, Holuigue L, Figueroa CR, Figueroa PM (2016) Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. J Exp Bot 67:4209–4220PubMedCentralPubMedCrossRefGoogle Scholar
  279. Vallverdú J, Castro O, Mayne R, Talanov M, Levin M, Baluška B, Gunji Y, Dussutour A, Zenil H, Adamatzky A (2018) Slime mould: the fundamental mechanisms of biological cognition. Biosystems 165:57–70PubMedCrossRefGoogle Scholar
  280. van Duijn M (2017) Phylogenetic origins of biological cognition: convergent patterns in the early evolution of learning. Interface Focus 7:20160158PubMedCrossRefPubMedCentralGoogle Scholar
  281. Van Hoven W (1991) Mortalities in kudu (Tragelaphus strepsiceros) populations related to chemical defence in trees. J Afr Zool 105:141–146Google Scholar
  282. Van Loon LC (2016) The intelligent behavior of plants. Trends Plant Sci 21:286–294PubMedCrossRefGoogle Scholar
  283. Volkmann D, Mori T, Tirlapur UK, König K, Fujiwara T, Kendrick-Jones J, Baluška F (2003) Unconventional myosins of the plant-specific class VIII: endocytosis, cytokinesis, plasmodesmata/pit-fields, and cell-to-cell coupling. Cell Biol Int 27:289–291PubMedCrossRefGoogle Scholar
  284. Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiol 132:44–51PubMedCentralPubMedCrossRefGoogle Scholar
  285. Wan Y, Jasik J, Wang L, Hao H, Volkmann D, Menzel D, Mancuso S, Baluška F, Lin J (2012) The signal transducer NPH3 integrates the phototropin1 photosensor with PIN2-based polar auxin transport in Arabidopsis root phototropism. Plant Cell 24:551–565PubMedCentralPubMedCrossRefGoogle Scholar
  286. Waters MT, Gutjahr C, Bennett T, Nelson DC (2017) Strigolactone signaling and evolution. Annu Rev Plant Biol 68:291–322PubMedCrossRefGoogle Scholar
  287. Watt M, McCully ME, Canny MJ (1994) Formation and stabilization of rhizosheaths of Zea mays L.: effect of soil water content. Plant Physiol 106:179–186PubMedCentralPubMedCrossRefGoogle Scholar
  288. Weiland M, Mancuso S, Baluška F (2016) Signalling via glutamate and GLRs in Arabidopsis thaliana. Funct Plant Biol 43:1–25Google Scholar
  289. Wittmann M, Queisser G, Eder A, Wiegert JS, Bengtson CP, Hellwig A, Wittum G, Bading H (2009) Synaptic activity induces dramatic changes in the geometry of the cell nucleus: interplay between nuclear structure, histone H3 phosphorylation, and nuclear calcium signaling. J Neurosci 29:14687–14700PubMedCrossRefGoogle Scholar
  290. Wolverton C, Ishikawa H, Evans M (2002) The kinetics of root gravitropism: dual motor and sensors. J Plant Growth Regul 21:102–112PubMedCrossRefGoogle Scholar
  291. Xu W, Jia L, Baluška F, Ding G, Shi W, Ye N, Zhang J (2012) PIN2 is required for the adaptation of Arabidopsis roots to alkaline stress by modulating proton secretion. J Exp Bot 63:6105–6114PubMedCentralPubMedCrossRefGoogle Scholar
  292. Yan S, Zhang T, Dong S, McLamore ES, Wang N, Shan X, Shen Y, Wan Y (2016) MeJA affects root growth by modulation of transmembrane auxin flux in the transition zone. J Plant Growth Regul 35:256–265CrossRefGoogle Scholar
  293. Yan S, Jiao C, McLamore ES, Wang N, Yao H, Shen Y (2017) Insect herbivory of leaves affects the auxin flux along root apices in Arabidopsis thaliana. J Plant Growth Regul 36:846–854CrossRefGoogle Scholar
  294. Yang ZB, He C, Ma Y, Herde M, Ding Z (2017) Jasmonic acid enhances Al-induced root growth inhibition. Plant Physiol 173:1420–1433PubMedCrossRefGoogle Scholar
  295. Yasuda R (2017) Biophysics of biochemical signaling in dendritic spines: implications in synaptic plasticity. Biophys J 113:2152–2159CrossRefPubMedGoogle Scholar
  296. Yokawa K, Kagenishi T, Kawano T, Mancuso S, Baluška F (2011) Illumination of Arabidopsis roots induces immediate burst of ROS production. Plant Signal Behav 6:1457–1461CrossRefGoogle Scholar
  297. Yokawa K, Fassano R, Kagenishi T, Baluška F (2014) Light as stress factor to plant roots – case of root halotropism. Front Plant Sci 5:718PubMedCentralPubMedCrossRefGoogle Scholar
  298. Yokawa K, Baluška F (2015) C. elegans and Arabidopsis thaliana show similar behavior: ROS induce escape tropisms both in illuminated nematodes and roots. Plant Signal Behav 10:e1073870PubMedCentralPubMedCrossRefGoogle Scholar
  299. Yokawa K, Baluška F (2016) The TOR complex: an emergency switch for root behavior. Plant Cell Physiol 57:14–18CrossRefPubMedGoogle Scholar
  300. Yokawa K, Kagenishi T, Pavlovič A, Gall S, Weiland M, Mancuso S, Baluška F (2018) Anesthetics stop diverse plant organ movements, affect endocytic vesicle recycling, ROS homeostasis, and block action potentials in Venus Flytraps. Ann Bot (In press)Google Scholar
  301. Žárský V (2015) Signal transduction: GABA receptor found in plants. Nat Plants 1:15115CrossRefPubMedGoogle Scholar
  302. Zhu J, Geisler M (2015) Keeping it all together: auxin-actin crosstalk in plant development. J Exp Bot 66:4983–4998CrossRefPubMedGoogle Scholar
  303. Zhu J, Bailly A, Zwiewka M, Sovero V, Di Donato M, Ge P, Oehri J, Aryal B, Hao P, Linnert M, Burgardt NI, Lücke C, Weiwad M, Michel M, Weiergräber OH, Pollmann S, Azzarello E, Mancuso S, Ferro N, Fukao Y, Hoffmann C, Wedlich-Söldner R, Friml J, Thomas C, Geisler M (2017a) TWISTED DWARF1 mediates the action of auxin transport inhibitors on actin cytoskeleton dynamics. Plant Cell 28:930–948Google Scholar
  304. Zhu R, Dong X, Hao W, Gao W, Zhang W, Xia S, Liu T, Shang Z (2017b) Heterotrimeric G protein-regulated Ca2+ influx and PIN2 asymmetric distribution are involved in Arabidopsis thaliana roots’ avoidance response to extracellular ATP. Front Plant Sci 8:1522PubMedCentralPubMedCrossRefGoogle Scholar
  305. Zou N, Li B, Chen H, Su Y, Kronzucker HJ, Xiong L, Baluška F, Shi W (2013) GSA-1/ARG1 protects root gravitropism in Arabidopsis under ammonium stress. New Phytol 200:97–111CrossRefPubMedGoogle Scholar

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© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  1. 1.IZMB, University of BonnBonnGermany
  2. 2.LINV, University of FlorenceFlorenceItaly

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