1932

Abstract

Communication occurs when a sender emits a cue perceived by a receiver that changes the receiver's behavior. Plants perceive information regarding light, water, other nutrients, touch, herbivores, pathogens, mycorrhizae, and nitrogen-fixing bacteria. Plants also emit cues perceived by other plants, beneficial microbes, herbivores, enemies of herbivores, pollinators, and seed dispersers. Individuals responding to light cues experienced increased fitness. Evidence for benefits of responding to cues involving herbivores and pathogens is more limited. The benefits of emitting cues are also less clear, particularly for plant–plant communication. Reliance on multiple or dosage-dependent cues can reduce inappropriate responses, and plants often remember past cues. Plants have multiple needs and prioritize conflicting cues such that the risk of abiotic stress is treated as greater than that of shading, which is in turn treated as greater than that of consumption. Plants can distinguish self from nonself and kin from strangers. They can identify the species of competitor or consumer and respond appropriately. Cues involving mutualists often contain highly specific information.

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2021-11-03
2024-06-21
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Literature Cited

  1. Acevedo FE, Rivera-Vega LJ, Chung SH, Ray S, Felton GW 2015. Cues from chewing insects: the intersection of DAMPs, HAMPs, MAMPs and effectors. Curr. Opin. Plant Biol. 26:80–86
    [Google Scholar]
  2. Agrawal AA. 1998. Induced responses to herbivory and increased plant performance. Science 279:1201–2
    [Google Scholar]
  3. Agrawal AA, Kearney EE, Hastings AP, Ramsey TE. 2012. Attenuation of the jasmonate burst, plant defensive traits, and resistance to specialist monarch caterpillars on shaded common milkweed (Asclepias syriaca). J. Chem. Ecol. 38:893–901
    [Google Scholar]
  4. Akiyama K, Matsuzaki K, Hayashi H. 2005. Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature 435:824–27
    [Google Scholar]
  5. Al-Babili S, Bouwmeester HJ 2015. Strigolactones, a novel carotenoid-derived plant hormone. Annu. Rev. Plant Biol. 66:161–86
    [Google Scholar]
  6. Alpi A, Amrhein N, Bertl A, Blatt MR, Blumwald E et al. 2007. Plant neurobiology: no brain, no gain?. Trends Plant Sci 12:135–36
    [Google Scholar]
  7. Amo L, Dicke M, Visser ME. 2016. Are naïve birds attracted to herbivore induced plant defences?. Behaviour 153:353–66
    [Google Scholar]
  8. Appel HM, Cocroft RB. 2014. Plants respond to leaf vibrations caused by insect herbivore chewing. Oecologia 175:1257–66
    [Google Scholar]
  9. Appel HM, Fescemyer H, Ehlting J, Weston D, Rehrig E et al. 2014. Transcriptional responses of Arabidopsis thaliana to chewing and sucking insect herbivores. Front. Plant Sci. 5:565
    [Google Scholar]
  10. Babikova Z, Gilbert L, Bruce TJA, Birkett M, Caulfield JC et al. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16:835–43
    [Google Scholar]
  11. Baldwin IT. 1998. Jasmonate-induced responses are costly but benefit plants under attack in native populations. PNAS 95:8113–18
    [Google Scholar]
  12. Ballare CL. 2009. Illuminated behaviour: phytochrome as a key regulator of light foraging and plant anti-herbivore defence. Plant Cell Environ 32:713–25
    [Google Scholar]
  13. Ballare CL. 2014. Light regulation of plant defense. Annu. Rev. Plant Biol. 65:335–63
    [Google Scholar]
  14. Ballare CL, Austin AT. 2019. Recalculating growth and defense strategies under competition: key roles of photoreceptors and jasmonates. J. Exp. Bot. 70:3425–34
    [Google Scholar]
  15. Ballare CL, Pierik R. 2017. The shade-avoidance syndrome: multiple signals and ecological consequences. Plant Cell Environ 40:2530–43
    [Google Scholar]
  16. Ballare CL, Scopel AL, Sanchez RA. 1990. Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247:329–32
    [Google Scholar]
  17. Bartelheimer M, Steinlein T, Beyschlag W. 2006. Aggregative root placement: a feature during interspecific competition in inland sand-dune habitats. Plant Soil 280:101–14
    [Google Scholar]
  18. Barton KE, Koricheva J. 2010. The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am. Nat. 175:481–93
    [Google Scholar]
  19. Baskin CC, Baskin JM. 2014. Seeds. Ecology, Biogeography, and Evolution of Dormancy and Germination Burlington, MA: Elsevier Science, 2nd ed..
    [Google Scholar]
  20. Biddington NL. 1986. The effects of mechanically-induced stress in plants—a review. Plant Growth Reg 4:103–23
    [Google Scholar]
  21. Biedrzycki ML, Jilany TA, Dudley SA, Bais HP. 2010. Root exudates mediate kin recognition in plants. Comm. Integr. Biol. 3:28–35
    [Google Scholar]
  22. Bloom AJ, Chapin FS, Mooney HA. 1985. Resource limitation in plants—an economic analogy. Annu. Rev. Ecol. Syst. 16:363–92
    [Google Scholar]
  23. Boehm T. 2006. Quality control in self/nonself discrimination. Cell 125:845–58
    [Google Scholar]
  24. Bonfante P, Genre A. 2015. Arbuscular mycorrhizal dialogues: Do you speak ‘plantish’ or ‘fungish’?. Trends Plant Sci 20:150–54
    [Google Scholar]
  25. Braam J. 2005. In touch: plant responses to mechanical stimuli. New Phytol 165:373–89
    [Google Scholar]
  26. Bradbury JW, Vehrencamp SL. 1998. Principles of Animal Communication Sunderland, MA: Sinauer
    [Google Scholar]
  27. Brenner ED, Stahlberg R, Mancuso S, Vivanco J, Baluska F, Van Volkenburgh E. 2006. Plant neurobiology: an integrated view of plant signaling. Trends Plant Sci 11:413–19
    [Google Scholar]
  28. Bricchi I, Leitner M, Foti M, Mithofer A, Boland W, Maffei ME. 2010. Robotic mechanical wounding (MecWorm) versus herbivore-induced responses: early signaling and volatile emission in Lima bean (Phaseolus lunatus L.). Planta 232:719–29
    [Google Scholar]
  29. Briggs WR, Christie JM. 2002. Phototropins 1 and 2: versatile plant blue-light receptors. Trends Plant Sci 7:204–10
    [Google Scholar]
  30. Bruce TJA, Wadhams LJ, Woodcock CM. 2005. Insect host location: a volatile situation. Trends Plant Sci 10:269–74
    [Google Scholar]
  31. Cahill JF, McNickle GG, Haag JJ, Lamb EG, Nyanumba SM, St Clair CC 2010. Plants integrate information about nutrients and neighbors. Science 328:1657
    [Google Scholar]
  32. Calvo P, Gagliano M, Souza GM, Trewavas A. 2020. Plants are intelligent, and here is how. Ann. Bot. 125:11–28
    [Google Scholar]
  33. Caparrotta S, Boni S, Taiti C, Palm E, Mancuso S, Pandolfi C. 2018. Induction of priming by salt stress in neighboring plants. Env. Exp. Bot. 147:261–70
    [Google Scholar]
  34. Casal JJ. 2013. Photoreceptor signaling networks in plant responses to shade. Annu. Rev. Plant Biol. 64:403–27
    [Google Scholar]
  35. Casal JJ, Questa JI. 2018. Light and temperature cues: multitasking receptors and transcriptional integrators. New Phytol 217:1029–34
    [Google Scholar]
  36. Chamovitz DA. 2018. Plants are intelligent; now what?. Nat. Plants 4:622–23
    [Google Scholar]
  37. Chehab EW, Chen Y, Henderson Z, Kim S, Braam J. 2012. Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests. Curr. Biol. 22:701–6
    [Google Scholar]
  38. Chen BJW, During HJ, Anten NPR. 2012. Detect thy neighbor: identity recognition at the root level in plants. Plant Sci 195:157–67
    [Google Scholar]
  39. Chester KS. 1933. The problem of acquired physiological immunity in plants. Q. Rev. Biol. 8:275–324
    [Google Scholar]
  40. Cipollini DF. 1997. Wind-induced mechanical stimulation increases pest resistance in common bean. Oecologia 111:84–90
    [Google Scholar]
  41. Cipollini DF, Walters D, Voelckel C. 2014. Costs of resistance in plants: from theory to evidence. In Annual Plant Reviews, Vol. 47: Insect-Plant Interactionsed. C Voelckel, G Janderpp. 263307 Chichester, UK: Wiley
    [Google Scholar]
  42. Clarke CR, Timko MP, Yoder JI, Axetel MJ, Westwood JH. 2019. Molecular dialog between parasitic plants and their hosts. Annu. Rev. Phytopath. 57:279–99
    [Google Scholar]
  43. Clarkson DT. 1985. Factors affecting mineral nutrient acquisition by plants. Annu. Rev. Plant Physiol. 36:77–115
    [Google Scholar]
  44. Coleman RA, Barker AM, Fenner M. 1999. Parasitism of the herbivore Pieris brassicae L. (Lep. Pieridae) by Cotesia glomerate L. (Hym. Braconidae) does not benefit the host plant by reduction of herbivory. J. Appl. Entom. 123:171–77
    [Google Scholar]
  45. Cook CE, Whichard LP, Turner B, Wall ME, Egley GH. 1966. Germination of witchweed (Striga lutea Lour.): isolation and properties of a potent stimulant. Science 154:1189–90
    [Google Scholar]
  46. Cook DE, Mesarich CH, Thomma BPHJ. 2015. Understanding plant immunity as a surveillance system to detect invasion. Annu. Rev. Phytopath. 53:541–63
    [Google Scholar]
  47. Crepy MA, Casal JJ. 2015. Photoreceptor-mediated kin recognition in plants. New Phytol 205:329–38
    [Google Scholar]
  48. Dani FR, Jones GR, Destri S, Spencer SH, Turilazzi S. 2001. Deciphering the recognition signature within a cuticular chemical profile of paper wasps. Anim. Behav. 62:165–71
    [Google Scholar]
  49. Darwin C 1865. On the Movements and Habits of Climbing Plants Cambridge, UK: Cambridge Univ. Press
    [Google Scholar]
  50. Darwin C 1876. The Effects of Cross and Self Fertilization in the Vegetable Kingdom London: John Murray
    [Google Scholar]
  51. Darwin C 1880. The Power of Movement in Plants London: John Murray
    [Google Scholar]
  52. Darwin C. 1893. Insectivorous Plants London: John Murray
    [Google Scholar]
  53. de Kroon H, Huber H, Stuefer JF, van Groenendael M. 2005. A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82
    [Google Scholar]
  54. de Kroon H, Visser EJW, Huber H, Mommer M, Hutchings MJ. 2009. A modular concept of plant foraging behaviour: the interplay between local responses and systemic control. Plant Cell Environ 32:704–12
    [Google Scholar]
  55. De Moraes CM, Lewis WJ, Pare PW, Alborn HT, Tumlinson JH. 1998. Herbivore-infested plants selectively attract parasitoids. Nature 393:570–73
    [Google Scholar]
  56. De Moraes CM, Mescher MC, Tumlinson JH. 2001. Caterpillar-induced nocturnal plant volatiles repel conspecific females. Nature 410:577–80
    [Google Scholar]
  57. de Wit M, Kegge W, Evers JB, Vergeer-van Eijk MH, Gankema P et al. 2012. Plant neighbor detection through touching leaf tips precedes phytochrome signals. PNAS 109:14705–10
    [Google Scholar]
  58. Delory BM, Delaplace P, Fauconnier M, du Jardin P. 2016. Root-emitted volatile organic compounds: Can they mediate belowground plant-plant interactions?. Plant Soil 402:1–26
    [Google Scholar]
  59. DeWitt TJ, Sih A, Wilson DS. 1998. Costs and limits of phenotypic plasticity. Trends Ecol. Evol. 13:77–81
    [Google Scholar]
  60. Dicke M, Sabelis MW. 1988. How plants obtain predatory mites as bodyguards. Neth. J. Zool. 38:148–65
    [Google Scholar]
  61. Dicke M, van Baarlen P, Wessels R, Dijkman H. 1993. Herbivory induces systemic production of plant volatiles that attract predators of the herbivore: extraction of endogenous elicitor. J. Chem. Ecol. 19:581–99
    [Google Scholar]
  62. Dicke M, van Poecke RMP 2002. Signalling plant-insect interactions: signal transduction in direct and indirect plant defence. Frontiers in Molecular Biology: Plant Signal Transduction D Scheel, C Wasternack 289–316 Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  63. Drew MC, Saker LR, Ashley TW. 1973. Nutrient supply and the growth of the seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. J. Exp. Bot. 24:1189–202
    [Google Scholar]
  64. Dudley SA, File AL. 2007. Kin recognition in an annual plant. Biol. Lett. 3:435–38
    [Google Scholar]
  65. Dudley SA, Schmitt J. 1996. Testing the adaptive plasticity hypothesis: density-dependent selection on manipulated stem length in Impatiens capensis. . Am. Nat. 147:445–65
    [Google Scholar]
  66. Duran-Flores D, Heil M. 2016. Sources of specificity in plant damaged-self recognition. Curr. Opin. Plant Biol. 32:77–87
    [Google Scholar]
  67. Edwards W. 1954. The theory of decision making. Psych. Bull. 51:380–417
    [Google Scholar]
  68. Egerton-Warburton LM, Querejeta JI, Allen MF. 2007. Common mycorrhizal networks provide a potential pathway for the transfer of hydraulically lifted water between plants. J. Exp. Bot. 58:1473–83
    [Google Scholar]
  69. Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH 2004. Airborne signals prime plants against insect herbivore attack. PNAS 101:1781–85
    [Google Scholar]
  70. Faegri K, van der Pijl L. 1979. The Principles of Pollination Ecology Oxford, UK: Pergamon Press, 3rd ed..
    [Google Scholar]
  71. Falik O, Reides P, Gersani M, Novoplansky A. 2003. Self/non-self discrimination in roots. J. Ecol. 91:525–31
    [Google Scholar]
  72. Falik O, Reides P, Gersani M, Novoplansky A. 2005. Root navigation by self inhibition. Plant Cell Environ 28:562–69
    [Google Scholar]
  73. Farmer EE, Ryan CA 1990. Interplant communication: Airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. PNAS 87:7713–16
    [Google Scholar]
  74. File AL, Klironomos J, Maherali H, Dudley SA. 2012a. Plant kin recognition enhances abundance of symbiotic microbial partner. PLOS ONE 7:e45648
    [Google Scholar]
  75. File AL, Murphy GP, Dudley SA. 2012b. Fitness consequences of plants growing with siblings: reconciling kin selection, niche partitioning and competitive ability. Proc. R. Soc. B 279:209–18
    [Google Scholar]
  76. Fitter A, Williamson L, Linkohr B, Leyser O. 2002. Root system architecture determines fitness in an Arabidopsis mutant in competition for immobile phosphate ions but not for nitrate ions. Proc. R. Soc. B. 269:2017–22
    [Google Scholar]
  77. Friedman J, Hart KS, den Bakker MC. 2017. Losing one's touch: evolution of the touch-sensitive stigma in the Mimulus guttatus species complex. Am. J. Bot. 104:335–41
    [Google Scholar]
  78. Friedrich T, Faivre L, Baeurle I, Schubert D. 2019. Chromatin-based mechanisms of temperature memory in plants. Plant Cell Env 42:762–70
    [Google Scholar]
  79. Friesen ML, Porter SS, Stark SC, von Wettberg EJ, Sach JL et al. 2011. Microbially mediated plant functional traits. Annu. Rev. Ecol. Evol. Syst. 42:23–46
    [Google Scholar]
  80. Fujii S, Kubo KI, Takayama S. 2016. Non-self and self-recognition models in plant self-incompatibility. Nat. Plants 2:16130
    [Google Scholar]
  81. Fukano Y, Yamawo A. 2015. Self-discrimination in the tendrils of the vine Cayratia japonica is mediated by physiological connection. Proc. R. Soc. B 282:20151379
    [Google Scholar]
  82. Galen C. 1999. Why do flowers vary?. BioScience 49:631–40
    [Google Scholar]
  83. Galen C, Huddle J, Liscum E. 2004. An experimental test of the adaptive evolution of phototropins: blue-light photoreceptors controlling phototropism in Arabidopsis thaliana. . Evolution 20:354–68
    [Google Scholar]
  84. Geervliet JBF, Ariens S, Dicke M, Vet LEM. 1998. Long-distance assessment of patch profitability through volatile infochemicals by the parasitoids Cotesia glomerata and C. rubecula (Hymenoptera: Braconidae). Biol. Control 11:113–21
    [Google Scholar]
  85. Gegear RJ, Laverty TM. 2005. Flower constancy in bumblebees: a test of the trait variability hypothesis. Anim. Behav. 69:939–49
    [Google Scholar]
  86. Gersani M, Brown JS, O'Brien EE, Maina GM, Abramsky Z 2001. Tragedy of the commons as a result of root competition. J. Ecol. 89:660–69
    [Google Scholar]
  87. Gilbert L, Johnson D 2017. Plant-plant communication through common mycorrhizal networks. Adv. Bot. Res. 82:83–97
    [Google Scholar]
  88. Gleason HA. 1917. The structure and development of the plant association. Bull. Torrey Bot. Club 43:463–81
    [Google Scholar]
  89. Goh CH, Nam HG, Park YS 2003. Stress memory in plants: a negative regulation of stomatal response and transient induction of rd22 gene to light in abscisic acid-entrained Arabidopsis plants. Plant J 36:240–55
    [Google Scholar]
  90. Gruntman M, Novoplansky A 2004. Physiologically mediated self/non-self discrimination in roots. PNAS 101:3863–67
    [Google Scholar]
  91. Gundel PE, Pierik R, Mommer L, Ballare CL. 2014. Competing neighbors: light perception and root function. Oecologia 176:1–10
    [Google Scholar]
  92. Halitschke R, Stenberg JA, Kessler D, Kessler A, Baldwin IT. 2008. Shared signals: ‘Alarm calls’ from plants increase apparency to herbivores and their enemies in nature. Ecol. Lett. 11:24–34
    [Google Scholar]
  93. Hall DE, MacGregor KB, Nijsse J, Bown AW. 2004. Footsteps from insect larvae damage leaf surfaces and initiate rapid responses. Eur. J. Plant Path. 110:441–47
    [Google Scholar]
  94. Hamilton WD. 1964a. The genetical evolution of social behavior. I. J. Theor. Biol 7:116
    [Google Scholar]
  95. Hamilton WD 1964b. The genetical evolution of social behavior. II. J. Theor. Biol 7:1752
    [Google Scholar]
  96. Hansen DM, Van der Niet T, Johnson SD. 2012. Floral signposts: testing the significance of visual ‘nectar guides’ for pollinator behavior and plant fitness. Proc. R. Soc. B 279:634–39
    [Google Scholar]
  97. Harder LD, Aizen MA. 2010. Floral adaptation and diversification under pollen limitation. Phil. Trans. R. Soc. B 365:529–43
    [Google Scholar]
  98. Hassanien RHE, Hou TZ, Li YF, Li BM. 2014. Advances in effects of sound waves on plants. J. Integr. Agr. 13:335–48
    [Google Scholar]
  99. Hayes S, Pantazopoulou CK, van Gelderen K, Reinin E, Tween AL et al. 2019. Soil salinity limits plant shade avoidance. Curr. Biol. 29:1669–76
    [Google Scholar]
  100. Heil M. 2004. Direct defense or ecological costs: responses of herbivorous beetles to volatiles released by wild lima bean (Phaseolus lunatus). J. Chem. Ecol. 30:1289–95
    [Google Scholar]
  101. Heil M, Adame-Alvarez RM. 2010. Short signaling distances make plant communication a soliloquy. Biol. Lett. 6:843–45
    [Google Scholar]
  102. Helms AM, De Moraes CM, Tooker JF, Mescher MC 2013. Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory. PNAS 110:199–204
    [Google Scholar]
  103. Henning T, Mittelbach M, Ismail SA, Acuna-Castillo RH, Weigend M. 2018. A case of behavioural diversification in male floral function—the evolution of thigmonastic pollen presentation. Sci. Rep. 8:14018
    [Google Scholar]
  104. Herrera CM. 2009. Multiplicity in Unity Chicago: Univ. Chicago Press
    [Google Scholar]
  105. Hess L, de Kroon H. 2007. Effects of rooting volume and nutrient availability as an alternative explanation for root self/non-self discrimination. J. Ecol. 95:241–51
    [Google Scholar]
  106. Hilborn R, Mangel M. 1997. The Ecological Detective. Confronting Models with Data Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  107. Hilker M, Fatouros NE. 2016. Resisting the onset of herbivore attack: Plants perceive and respond to insect eggs. Curr. Opin. Plant Biol. 32:9–16
    [Google Scholar]
  108. Hoballah ME, Turlings TCJ. 2005. The role of fresh versus old leaf damage in the attraction of parasitic wasps to herbivore-induced maize volatiles. J. Chem Ecol. 31:2003–18
    [Google Scholar]
  109. Hoeksema JD, Bever JD, Chakraborty S, Bala CV, Gardes M et al. 2018. Evolutionary history of plant hosts and fungal symbionts predicts the strength of mycorrhizal mutualism. Commun. Biol. 1:116
    [Google Scholar]
  110. Holopainen JK, Blande JD. 2013. Where do herbivore-induced plant volatiles go?. Front. Plant Sci. 4:185
    [Google Scholar]
  111. Holzapfel C, Alpert P. 2003. Root cooperation in a clonal plant: Connected strawberries segregate roots. Oecologia 134:22–27
    [Google Scholar]
  112. Horiuchi J, Arimura G, Ozawa R, Shimoda T, Takabayashi J, Nishioka T. 2003. A comparison of the responses of Tetranychus urticae (Acari: Tetranychus) and Phytoseiulus persimilis (Acari: Phytoseiidae) to volatiles emitted from lima bean leaves with different levels of damage made by T. urticae or Spodoptera exigua (Lepidoptera: Noctuidae). Appl. Ent. Zool. 38:109–16
    [Google Scholar]
  113. Huber H, Kane NC, Heschel MS, von Wettberg EJ, Banta J et al. 2004. Frequency and microenvironmental pattern of selection on plant shade-avoidance traits in a natural population of Impatiens capensis. . Am. Nat. 163:548–63
    [Google Scholar]
  114. Huber-Sannwald E, Pyke DA, Caldwell MM. 1996. Morphological plasticity following species-specific recognition and competition in two perennial grasses. Am. J. Bot. 83:919–31
    [Google Scholar]
  115. Izaguirre MM, Mazza CA, Astigueta MS, Ciarla AM, Ballare CL. 2013. No time for candy: Passionfruit (Passiflora edulis) plants down-regulate damage-induced extra floral nectar production in response to light signals of competition. Oecologia 173:213–21
    [Google Scholar]
  116. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444:323–29
    [Google Scholar]
  117. Junker RR, Parachnowitsch AL. 2015. Working towards a holistic view on flower traits—how floral scents mediate plant-animal interactions in concert with other floral characters. J. Indian Inst. Sci. 95:43–67
    [Google Scholar]
  118. Kalske A, Shiojiri K, Uesugi A, Sakata U, Morrell K, Kessler A. 2019. Insect herbivory selects for volatile-mediated plant-plant communication. Curr. Biol. 29:3128–33
    [Google Scholar]
  119. Kant MR, Jonckheere W, Knegt B, Lemos F, Liu J et al. 2015. Mechanisms and ecological consequences of plant defence induction and suppression in herbivore communities. Ann. Bot. 115:1015–51
    [Google Scholar]
  120. Karban R, Brody AK, Schnathorst WC. 1989. Crowding and a plant's ability to defend itself against herbivores and diseases. Am. Nat. 134:749–60
    [Google Scholar]
  121. Karban R, Maron J. 2002. The fitness consequences of interspecific eavesdropping between plants. Ecology 83:1209–13
    [Google Scholar]
  122. Karban R, Orrock JL. 2018. A judgment and decision-making model for plant behavior. Ecology 99:190919
    [Google Scholar]
  123. Karban R, Orrock JL, Preisser EL, Sih A. 2016a. A comparison of plants and animals in their responses to risk of consumption. Curr. Opin. Plant Biol. 32:1–8
    [Google Scholar]
  124. Karban R, Shiojiri K. 2009. Self-recognition affects plant communication and defense. Ecol. Lett. 12:502–6
    [Google Scholar]
  125. Karban R, Shiojiri K, Huntzinger M, McCall AC. 2006. Damage-induced resistance in sagebrush: Volatiles are key to intra- and interplant communication. Ecology 87:922–30
    [Google Scholar]
  126. Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evan RY. 2013. Kin recognition affects plant communication and defence. Proc. R. Soc. B 280:20123062
    [Google Scholar]
  127. Karban R, Yang LH, Edwards KF. 2014a. Volatile communication between plants that affects herbivory: a meta-analysis. Ecol. Lett. 17:44–52
    [Google Scholar]
  128. Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD. 2014b. Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytol 204:380–85
    [Google Scholar]
  129. Karban R, Wetzel WC, Shiojiri K, Pezzola E, Blande JD. 2016b. Geographic dialects in volatile communication between sagebrush individuals. Ecology 97:2917–24
    [Google Scholar]
  130. Kegge W, Ninkovic V, Glinwood R, Welschen RAM, Voesenek LACJ, Pierik R. 2015. Red:far-red light conditions affect the emission of volatile organic compounds from barley (Hordeum vulgare), leading to altered biomass allocation in neighboring plants. Ann. Bot. 115:961–70
    [Google Scholar]
  131. Keller MM, Jaillais Y, Pedmale UV, Moreno JE, Chory J, Ballare CL. 2011. Cryptochrome 1 and phytochrome B control shade-avoidance responses in Arabidopsis via partially independent hormonal cascades. Plant J 67:195–207
    [Google Scholar]
  132. Kessler A, Baldwin IT. 2001. Defensive function of herbivore-induced plant volatile emissions in nature. Science 291:2141–44
    [Google Scholar]
  133. Kiers ET, Duhamel M, Beesetty Y, Mensah JA, Franken O et al. 2011. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 333:880–82
    [Google Scholar]
  134. Kiers ET, Rousseau RA, West SA, Denison RF. 2003. Host sanctions and the legume-rhizobium mutualism. Nature 425:78–81
    [Google Scholar]
  135. Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH. 2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–11
    [Google Scholar]
  136. Kong CH, Zhang SZ, Li YH, Xia ZC, Yang XF et al. 2018. Plant neighbor detection and allelochemical response are driven by root-secreted signaling chemicals. Nat. Commun. 9:3867
    [Google Scholar]
  137. Kurashige NS, Agrawal AA. 2005. Phenotypic plasticity to light competition and herbivory in Chenopodium album (Chenopodiaceae). Am. J. Bot. 92:21–26
    [Google Scholar]
  138. Landrein B, Ingram G. 2019. Connected through the force: mechanical signals in plant development. J. Exp. Bot. 70:3507–19
    [Google Scholar]
  139. Leonard AS, Papaj DR. 2011. ‘X’ marks the spot: the possible benefits of nectar guides to bees and plants. Funct. Ecol. 25:1293–301
    [Google Scholar]
  140. Leyser O, Oldroyd GED. 2020. A plant's diet, surviving in a variable nutrient environment. Science 368:eaba0196
    [Google Scholar]
  141. Linkosalo T, Lechowicz MJ. 2006. Twilight far-red treatment advances leaf bud burst of silver birch (Betula pendula). Tree Physiol 26:1249–56
    [Google Scholar]
  142. Lomascolo SB, Levey DJ, Kimball RT, Bolker BM, Alborn HT 2010. Dispersers shape fruit diversity in Ficus (Moraceae). PNAS 107:14668–72
    [Google Scholar]
  143. Mahall BE, Callaway RM 1991. Root communication among desert shrubs. PNAS 88:874–76
    [Google Scholar]
  144. Majetic CJ, Raguso RA, Ashman TL. 2009. The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. . Funct. Ecol. 23:480–87
    [Google Scholar]
  145. Mantyla E, Alessio GA, Blande JD, Heijari J, Holopainen JK et al. 2008. From plants to birds: higher avian predation rates in trees responding to insect herbivory. PLOS ONE 3:e2832
    [Google Scholar]
  146. Markovic D, Colzi I, Taiti C, Ray S, Scalone R et al. 2019. Airborne signals synchronize the defenses of neighboring plants in response to touch. J. Exp. Bot. 70:691–700
    [Google Scholar]
  147. Mauch-Mani B, Baccelli I, Luna E, Flors V. 2017. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68:485–512
    [Google Scholar]
  148. Maynard Smith J, Harper DGC 1995. Animal signals: models and terminology. . J. Theor. Biol. 177:305–11
    [Google Scholar]
  149. Mendelson TC, Fitzpatrick CL, Hauber ME, Pence CH, Rodriguez RL et al. 2016. Cognitive phenotypes and the evolution of animal decisions. Trends Ecol. Evol. 31:850–59
    [Google Scholar]
  150. Misra RC, Ghosh R, Bae H. 2016. Plant acoustics: in the search of a sound mechanism for sound signaling in plants. J. Exp. Bot. 67:4483–94
    [Google Scholar]
  151. Mithofer A, Wanner G, Boland W. 2005. Effects of feeding Spodoptera littoralis on lima bean leaves. II. Continuous mechanical wounding resembling insect feeding is sufficient to elicit herbivory-related volatile emission. Plant Physiol 137:1160–68
    [Google Scholar]
  152. Monshausen GB, Gilroy S. 2009. Feeling green: mechanosensing in plants. Trends Cell Biol 19:228–35
    [Google Scholar]
  153. Moreira X, Nell CS, Meza-Lopez MM, Rasmann S, Mooney KA. 2018. Specificity of plant–plant communication for Baccharis salicifolia sexes but not genotypes. Ecology 99:2731–39
    [Google Scholar]
  154. Moreno JE, Yi T, Chory J, Ballare CL 2009. Ecological modulation of plant defense via phytochrome control of jasmonate sensitivity. PNAS 106:4935–40
    [Google Scholar]
  155. Nagashima A, Higaki T, Koeduka T, Ishigami K, Hosokawa S et al. 2019. Transcriptional regulators involved in responses to volatile organic compounds in plants. J. Biol. Chem. 294:2256–66
    [Google Scholar]
  156. Nelson RJ. 1995. An Introduction to Behavioral Endocrinology Sunderland, MA: Sinauer
    [Google Scholar]
  157. Nibau C, Gibbs DJ, Coates JC. 2008. Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–604
    [Google Scholar]
  158. Nick P, Schafer E. 1988. Spatial memory during the tropism of maize (Zea mays L.) coleoptiles. Planta 175:380–88
    [Google Scholar]
  159. Novoplansky A. 2019. What plant roots know?. Semin. Cell Dev. Biol. 92:126–33
    [Google Scholar]
  160. Novoplansky A, Cohen D, Sachs T. 1990. How Portulaca seedlings avoid their neighbors. Oecologia 82:490–93
    [Google Scholar]
  161. Oldroyd GED. 2013. Speak, friend, and enter: signalling systems that promote beneficial symbiotic associations in plants. Nat. Rev. Microbiol. 11:252–63
    [Google Scholar]
  162. Orians C. 2005. Herbivores, vascular pathways, and systemic induction: facts and artifacts. J. Chem. Ecol. 31:2231–42
    [Google Scholar]
  163. Orrock JL, Connolly BM, Choi WG, Guiden PW, Swanson SJ, Gilroy S. 2018. Plants eavesdrop on cues produced by snails and induce costly defenses that affect insect herbivores. Oecologia 186:703–10
    [Google Scholar]
  164. Orrock JL, Sih A, Ferrari MCO, Karban R, Preisser EL et al. 2015. Error management in plant allocation to herbivore defense. Trends Ecol. Evol. 30:441–45
    [Google Scholar]
  165. Pavlovic A, Jaksova J, Novak O. 2017. Triggering a false alarm: Wounding mimics prey capture in the carnivorous Venus flytrap (Dionaea muscipula). . New Phytol 216:927–38
    [Google Scholar]
  166. Pearcy RW, Sims DA 1994. Photosynthetic acclimation to changing light environments: scaling from the leaf to the whole plant. Exploitation of Environmental Heterogeneity by Plants MW Caldwell, RW Pearcy 145–74 San Diego: Academic
    [Google Scholar]
  167. Peiffer M, Tooker JF, Luthe D, Felton GW. 2009. Plants on early alert: glandular trichomes as sensors for insect herbivores. New Phytol 184:644–56
    [Google Scholar]
  168. Pierik R, Visser EJW, de Kroon H, Voesenek LACJ. 2003. Ethylene is required in tobacco to successfully compete with proximate neighbours. Plant Cell Environ 26:1229–34
    [Google Scholar]
  169. Pinto CF, Torrico-Bazoberry D, Penna M, Cossio-Rodriguez R, Cocroft R et al. 2019. Chemical responses of Nicotiana tabacum (Solanaceae) induced by vibrational signals of a generalist herbivore. J. Chem. Ecol. 45:708–14
    [Google Scholar]
  170. Poelman EH, Bruinsma M, Zhu F et al. 2012. Hyperparasitoids use herbivore-induced plant volatiles to locate their parasitoid host. PLOS Biol 10:e10001435
    [Google Scholar]
  171. Raguso RA. 2008. Wake up and smell the roses: the ecology and evolution of floral scent. Annu. Rev. Ecol. Evol. Syst. 39:549–69
    [Google Scholar]
  172. Rasmann S, Kollner TG, Degenhardt J, Hiltpold I, Toepfer S et al. 2005. Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434:732–37
    [Google Scholar]
  173. Ray S, Basu S, Rivera-Vega LJ, Acevedo FE, Louis J et al. 2016. Lessons from the far end: caterpillar frass–induced defenses in maize, rice, cabbage, and tomato. J. Chem. Ecol. 42:1130–41
    [Google Scholar]
  174. Rodriguez A, Alquezar B, Pena L. 2013. Fruit aromas in mature fleshy fruits as signals of readiness for predation and seed dispersal. New Phytol 197:36–48
    [Google Scholar]
  175. Sabelis MW, van de Baan HE. 1983. Location of distant spider mite colonies by phytoseiid predators: demonstration of specific kairomones emitted by Tetranychus urticae and Panonychus ulmi. Entomol. Exp. Appl. 33:303–14
    [Google Scholar]
  176. Schaefer HM, Ruxton GD. 2011. Plant–Animal Communication Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  177. Schaefer HM, Schmidt V, Winkler H. 2003. Testing the defence trade-off hypothesis: how contents of nutrients and secondary compounds affect fruit removal. Oikos 102:318–28
    [Google Scholar]
  178. Schenk HJ, Callaway RM, Mahall BE. 1999. Spatial root segregation: Are plants territorial?. Adv. Ecol. Res. 28:145–80
    [Google Scholar]
  179. Schiestl FP, Johnson SD. 2013. Pollinator-mediated evolution of floral signals. Trends Ecol. Evol. 28:307–15
    [Google Scholar]
  180. Schulz-Bohm K, Gerards S, Hundscheid M, Melenhorst J, de Boer W, Garbeva P. 2018. Calling from distance: attraction of soil bacteria by plant root volatiles. . ISME J 12:1252–62
    [Google Scholar]
  181. Schuman MC, Barthel K, Baldwin IT 2012. Herbivory-induced volatiles function as defenses increasing fitness of the native plant Nicotiana attenuata in nature. eLife 1:e00007
    [Google Scholar]
  182. Semchenko M, Saar S, Lepik A. 2014. Plant root exudates mediate neighbor recognition and trigger complex behavioural changes. New Phytol 204:631–37
    [Google Scholar]
  183. Shahid S, Kim G, Johnson NR, Wafula E, Wang F et al. 2018. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553:82–85
    [Google Scholar]
  184. Shemesh H, Arbiv A, Gersani M, Ovadia O, Novoplansky A. 2010. The effects of nutrient dynamics on root patch choice. PLOS ONE 5:e10824
    [Google Scholar]
  185. Shulaev V, Silverman P, Raskin I. 1997. Airborne signaling by methyl salicylate in plant pathogen resistance. Nature 385:718–21
    [Google Scholar]
  186. Simard SW, Beiler KJ, Bingham MA, Deslippec JR, Philip LJ, Testee FP. 2012. Mycorrhizal networks: mechanisms, ecology and modelling. Fungal Biol. Rev. 26:39–60
    [Google Scholar]
  187. Simard SW, Perry DA, Jones MD, Myrold DD, Durall DM, Molina R. 1997. Net transfer of carbon between ectomycorrhizal tree species in the field. Nature 388:579–82
    [Google Scholar]
  188. Simons P. 1992. The Action Plant Oxford, UK: Blackwell
    [Google Scholar]
  189. Smith H. 2000. Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–91
    [Google Scholar]
  190. Smith SE, Read DJ. 2008. Mycorrhizal Symbiosis New York: Academic, 3rd ed..
    [Google Scholar]
  191. Song YY, Zeng RS, Xu JAF, Li J, Shen XA, Yihdego WG. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLOS ONE 5:e13324
    [Google Scholar]
  192. Sprengel CK 1996 (1793. Discovery of the secret of nature in the structure and fertilization of flowers, transl. P Haase. Floral Biology: Studies on Floral Evolution in Animal Pollinated Plants DG Lloyd, SCH Barrett 3–43 New York: Chapman and Hall (from German)
    [Google Scholar]
  193. Stowe KA, Marquis RJ, Hochwender CG, Simms EL. 2000. The evolutionary ecology of tolerance to consumer damage. Annu. Rev. Ecol. Syst. 31:565–95
    [Google Scholar]
  194. Strauss SY, Siemans DH, Decher MB, Mitchell-Olds T. 1999. Ecological costs of plant resistance to herbivores in the currency of pollination. Evolution 53:1105–13
    [Google Scholar]
  195. Stuefer JF, de Kroon H, During HJ. 1996. Exploitation of environmental heterogeneity by spatial division of labour in a clonal plant. Funct. Ecol. 10:328–34
    [Google Scholar]
  196. Sugimoto K, Matsui K, Iijima Y, Akakabe Y, Shoko M et al. 2014. Intake and transformation to a glycoside of (Z)-3-hexenol from infested neighbors reveals a mode of plant odor reception and defense. PNAS 111:7144–49
    [Google Scholar]
  197. Takabayashi J, Sabelis MW, Janssen A, Shiojiri K, van Wijk M. 2006. Can plants betray the presence of multiple herbivore species to predators and parasitoids? The role of learning in phytochemical information networks. Ecol. Res. 21:3–8
    [Google Scholar]
  198. Takabayashi J, Takahashi S, Dicke M, Posthumus MA. 1995. Developmental stage of herbivore Pseudaletia separata affects production of herbivore-induced synomone by corn plants. J. Chem. Ecol 21:273–87
    [Google Scholar]
  199. Terry LI, Roemer RB, Walter GH, Booth D. 2014. Thrips’ responses to thermogenic associated signals in a cycad pollination system: the interplay of temperature, light, humidity and cone volatiles. Funct. Ecol. 28:857–67
    [Google Scholar]
  200. Thaler JS, Humphrey PT, Whiteman NK. 2012. Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–70
    [Google Scholar]
  201. Tompkins P, Bird C. 1973. The Secret Life of Plants New York: Harper and Row
    [Google Scholar]
  202. Truitt CL, Wei HX, Pare PW. 2004. A plasma membrane protein from Zea mays binds with the herbivore elicitor volicitin. Plant Cell 16:523–32
    [Google Scholar]
  203. Turlings TCJ, Tumlinson JH 1992. Systemic release of chemical signals by herbivore-injured corn. PNAS 89:8399–402
    [Google Scholar]
  204. Valladares F, Niinemets U. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annu. Rev. Ecol. Evol. Syst. 39:237–57
    [Google Scholar]
  205. Van Hulten M, Pelser M, van Loon LC, Pieterse CMJ, Ton J 2006. Costs and benefits of priming for defense in Arabidopsis. . PNAS 103:5602–7
    [Google Scholar]
  206. Veits M, Khait I, Obolski U, Zinger E, Boonman A et al. 2019. Flowers respond to pollinator sound within minutes by increasing nectar sugar concentrations. Ecol. Lett. 22:1483–92
    [Google Scholar]
  207. Vet LEM, Dicke M. 1992. Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Ent. 37:141–72
    [Google Scholar]
  208. Weiss MR. 1991. Floral color changes as cues for pollinators. Nature 354:227–29
    [Google Scholar]
  209. Wester P, Lunau K. 2017. Plant-pollinator communication. Adv. Bot. Res. 82:225–57
    [Google Scholar]
  210. White J 1984. Plant metamerism. Perspectives in Plant Population Ecology R Dirzo, J Sarukhan 15–47 Sunderland, MA: Sinauer Press
    [Google Scholar]
  211. Willmer P. 2011. Pollination and Floral Ecology Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  212. Willson MF, Whelan CJ. 1990. The evolution of fruit color in fleshy-fruited plants. Am. Nat. 136:790–809
    [Google Scholar]
  213. Wright GA, Schiestl FP. 2009. The evolution of floral scent: the influence of olfactory learning by insect pollinators on the honest signaling of floral rewards. Funct. Ecol. 23:841–51
    [Google Scholar]
  214. Xuan W, Beeckman T, Xu G. 2017. Plant nitrogen nutrition: sensing and signaling. Curr. Opin. Plant Biol. 39:57–65
    [Google Scholar]
  215. Yamaguchi Y, Barona G, Ryan CA, Pearce G 2011. GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol 156:932–42
    [Google Scholar]
  216. Yi H-S, Heil M, Adame-Alvarez R-M, Ballhorn D, Ryu C-M. 2009. Airborne induction and priming of plant resistance to a bacterial pathogen. Plant Physiol 151:2152–61
    [Google Scholar]
  217. Yu X, Feng B, He P, Shan L. 2017. From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopath. 55:109–37
    [Google Scholar]
  218. Zamioudis C, Pieterse CMJ. 2012. Modulation of host immunity by beneficial microbes. Mol. Plant-Microbe Int. 25:139–50
    [Google Scholar]
  219. Zangerl AR, Rutledge CE. 1996. The probability of attack and patterns of constitutive and induced defense: a test of optimal defense theory. Am. Nat. 147:599–608
    [Google Scholar]
  220. Zhang PJ, Wei JN, Zhao C, Zhang YF, Li CY et al. 2019. Airborne host-plant manipulation by whiteflies via an inducible blend of plant volatiles. PNAS 116:7387–96
    [Google Scholar]
  221. Zipfel C, Oldroyd GED. 2017. Plant signalling in symbiosis and immunity. Nature 543:328–36
    [Google Scholar]
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