Advertisement

Neighbour Recognition Through Volatile-Mediated Interactions

Chapter
Part of the Signaling and Communication in Plants book series (SIGCOMM)

Abstract

Plants constitutively emit a wide array of volatile organic compounds (VOCs) and, upon biotic and abiotic stress, release a more complex and more diverse VOC blend. These VOCs mediate multiple ecological interactions between plants and their associated community members, including plant–plant communication or neighbour recognition. Albeit initially discredited, the concept of VOCs mediating plant–plant communication is now well accepted. In general, plants perceive and respond to VOCs emanating from their neighbours with physiological, biochemical or phenotypic changes that may convey resistance to abiotic and biotic stress. However, the mechanisms underpinning this process, the ecological and evolutionary relevance as well as the circumstances under which this process occurs remain largely obscure. In particular, there is very scarce information on whether and how global change, which has increasingly been shown to change VOC emission patterns and alter VOC atmospheric lifetimes, can disrupt VOC-mediated plant–plant communication. This chapter updates our current knowledge about these aspects and, through synthesising them, intends to point out gaps in existing research, in particular the need for further studies in a changing environment.

Keywords

Plant Communication Lima Bean Herbivore Attack Undamaged Plant Hexenyl Acetate 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Ali M, Sugimoto K, Ramadan A, Arimura G (2013) Memory of plant communications for priming anti-herbivore responses. Sci Rep 3:1872PubMedPubMedCentralGoogle Scholar
  2. Ameye M, Audenaert K, De Zutter N, Steppe K, Van Meulebroek L, Vanhaecke L, De Vleesschauwer D, Haesaert G, Smagghe G (2015) Priming of wheat with the green leaf volatile Z-3-hexenyl acetate enhances defense against Fusarium graminearum but boosts deoxynivalenol production. Plant Physiol 167:1671–1684PubMedPubMedCentralCrossRefGoogle Scholar
  3. Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W, Takabayashi J (2000a) Herbivory-induced volatiles elicit defence genes in lima bean leaves. Nature 406:512–515PubMedCrossRefGoogle Scholar
  4. Arimura G, Tashiro K, Kuhara S, Nishioka T, Ozawa R, Takabayashi J (2000b) Gene responses in bean leaves induced by herbivory and by herbivore-induced volatiles. Biochem Biophys Res Commun 277:305–310PubMedCrossRefGoogle Scholar
  5. Arimura G, Muroi A, Nishihara M (2012) Plant–plant–plant communications, mediated by (E)-β-ocimene emitted from transgenic tobacco plants, prime indirect defense responses of lima beans. J Plant Interact 7:193–196CrossRefGoogle Scholar
  6. Asai N, Nishioka T, Takabayashi J, Furuichi T (2009) Plant volatiles regulate the activities of Ca2+-permeable channels and promote cytoplasmic calcium transients in Arabidopsis leaf cells. Plant Signal Behav 4:294–300PubMedPubMedCentralCrossRefGoogle Scholar
  7. Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Science 221:277–279PubMedCrossRefGoogle Scholar
  8. Balmer A, Pastor V, Gamir J, Flors V, Mauch-Mani B (2015) The ‘prime-ome’: towards a holistic approach to priming. Trends Plant Sci 20:443–452PubMedCrossRefGoogle Scholar
  9. Barton KE, Koricheva J (2010) The ontogeny of plant defense and herbivory: characterizing general patterns using meta-analysis. Am Nat 175:481–493PubMedCrossRefGoogle Scholar
  10. Blande JD, Holopainen JK, Li T (2010) Air pollution impedes plant-to-plant communication by volatiles. Ecol Lett 13:1172–1181PubMedCrossRefGoogle Scholar
  11. Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37:1892–1904PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bruce TJA, Matthes MC, Chamberlain K, Woodcock CM, Mohib A, Webster B, Smart LE, Birkett MA, Pickett JA, Napier JA (2008) cis-jasmone induces Arabidopsis genes that affect the chemical ecology of multitrophic interactions with aphids and their parasitoids. Proc Natl Acad Sci USA 105:4553–4558PubMedPubMedCentralCrossRefGoogle Scholar
  13. Cascone P, Iodice L, Maffei ME, Bossi S, Arimura G, Guerrieri E (2015) Tobacco overexpressing β-ocimene induces direct and indirect responses against aphids in receiver tomato plants. J Plant Physiol 173:28–32PubMedCrossRefGoogle Scholar
  14. Castelyn HD, Appelgryn JJ, Mafa MS, Pretorius ZA, Visser B (2015) Volatiles emitted by leaf rust infected wheat induce a defence response in exposed uninfected wheat seedlings. Australas Plant Pathol 44:245–254CrossRefGoogle Scholar
  15. Dahlin I, Vucetic A, Ninkovic V (2015) Changed host plant volatile emissions induced by chemical interaction between unattacked plants reduce aphid plant acceptance with intermorph variation. J Pest Sci 88:249–257CrossRefGoogle Scholar
  16. Das A, Lee SH, Hyun TK, Kim SW, Kim JY (2013) Plant volatiles as method of communication. Plant Biotechnol Rep 7:9–26CrossRefGoogle Scholar
  17. De Wit M, Kegge W, Evers JB, Vergeer-van Eijk MH, Gankema P, Voesenek LACJ, Pierik R (2012) Plant neighbor detection through touching leaf tips precedes phytochrome signals. Proc Natl Acad Sci USA 109:14705–14710PubMedPubMedCentralCrossRefGoogle Scholar
  18. Delaney KJ, Wawrzyniak M, Lemańczyk G, Wrzesińska D, Piesik D (2013) Synthetic cis-jasmone exposure induces wheat and barley volatiles that repel the pest cereal leaf beetle, Oulema melanopus L. J Chem Ecol 39:620–629PubMedCrossRefGoogle Scholar
  19. Desurmont GA, Hajek A, Agrawal AA (2014) Seasonal decline in plant defence is associated with relaxed offensive oviposition behaviour in the viburnum leaf beetle Pyrrhalta viburni. Ecol Entomol 39:589–594CrossRefGoogle Scholar
  20. Dorokhov YL, Komarova TV, Petrunia IV, Frolova OY, Pozdyshev DV, Gleba YY (2012) Airborne signals from a wounded leaf facilitate viral spreading and induce antibacterial resistance in neighboring plants. PLoS Pathog 8:e1002640PubMedPubMedCentralCrossRefGoogle Scholar
  21. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32PubMedCrossRefGoogle Scholar
  22. Engelberth J, Alborn H, Schmelz E, Tumlinson J (2004) Airborne signals prime plants against insect herbivore attack. Proc Natl Acad Sci USA 101:1781–1785PubMedPubMedCentralCrossRefGoogle Scholar
  23. Engelberth J, Contreras CF, Dalvi C, Li T, Engelberth M (2013) Early transcriptome analyses of Z-3-hexenol-treated Zea mays revealed distinct transcriptional networks and anti-herbivore defense potential of green leaf volatiles. PLoS One 8:e77465PubMedPubMedCentralCrossRefGoogle Scholar
  24. Erb M, Veyrat N, Robert CAM, Xu H, Frey M, Ton J, Turlings TCJ (2015) Indole is an essential herbivore-induced volatile priming signaling maize. Nat Commun 6:6273PubMedPubMedCentralCrossRefGoogle Scholar
  25. Farmer EE (2001) Surface-to-air signals. Nature 411:854–856PubMedCrossRefGoogle Scholar
  26. Farmer EE, Ryan CA (1990) Interplant communication: airborne methyl jasmonate induces synthesis of proteinase inhibitors in plant leaves. Proc Natl Acad Sci USA 87:7713–7716PubMedPubMedCentralCrossRefGoogle Scholar
  27. Farré-Armengol G, Peñuelas J, Li T, Yli-Pirilä P, Filella I, Llusia J, Blande JD (2016) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol 209:152–160PubMedCrossRefGoogle Scholar
  28. Frost CJ, Mescher MC, Dervinis C, Davis JM, Carlson JE, De Moraes CM (2008) Priming defense genes and metabolites in hybrid poplar by the green leaf volatile cis-3-hexenyl acetate. New Phytol 180:722–733PubMedCrossRefGoogle Scholar
  29. Gagliano M, Renton M (2013) Love thy neighbour facilitation through an alternative signalling modality in plants. BMC Ecol 13:19PubMedPubMedCentralCrossRefGoogle Scholar
  30. Girling RD, Lusebrink I, Farthing E, Newman TA, Poppy GM (2013) Diesel exhaust rapidly degrades floral odours used by honeybees. Sci Rep 3:2779PubMedPubMedCentralCrossRefGoogle Scholar
  31. Girón-Calva PS, Molina-Torres J, Heil M (2012) Volatile dose and exposure time impact perception in neighboring plants. J Chem Ecol 38:226–228PubMedCrossRefGoogle Scholar
  32. Glinwood R, Ninkovic V, Pettersson J, Ahmed A (2004) Barley exposed to aerial allelopathy from thistles (Cirsium spp.) becomes less acceptable to aphids. Ecol Entomol 29:188–195CrossRefGoogle Scholar
  33. Glinwood R, Ahmed A, Qvarfordt E, Ninkovic V, Pettersson J (2009) Airborne interactions between undamaged plants of different cultivars affect insect herbivores and natural enemies. Arthropod Plant Interact 3:215–224CrossRefGoogle Scholar
  34. Glinwood R, Ninkovic V, Pettersson J (2011) Chemical interaction between undamaged plants—effects on herbivores and natural enemies. Phytochemistry 72:1683–1689PubMedCrossRefGoogle Scholar
  35. Godard KA, White R, Bohlmann J (2008) Monoterpene-induced molecular responses in Arabidopsis thaliana. Phytochemistry 69:1838–1849PubMedCrossRefGoogle Scholar
  36. Heil M (2014) Herbivore-induced plant volatiles: targets, perception and unanswered questions. New Phytol 204:297–306CrossRefGoogle Scholar
  37. Heil M, Adame-Álvarez RM (2010) Short signalling distances make plant communication a soliloquy. Biol Lett 6:843–845PubMedPubMedCentralCrossRefGoogle Scholar
  38. Heil M, Karban R (2009) Explaining evolution of plant communication by airborne signals. Trends Ecol Evol 25:137–144CrossRefGoogle Scholar
  39. Heil M, Kost C (2006) Priming of indirect defences. Ecol Lett 9:813–817PubMedCrossRefGoogle Scholar
  40. Heil M, Silva Bueno C (2007) Within-plant signaling by volatiles lead to induction and priming of an indirect plant defense in nature. Proc Natl Acad Sci USA 104:5467–5472PubMedPubMedCentralCrossRefGoogle Scholar
  41. Hughes K, Pearse J, Grof-Tisza P, Karban R (2015) Individual-level differences in generalist caterpillar responses to a plant–plant cue. Ecol Entomol. doi: 10.1111/een.12224 Google Scholar
  42. Johnson D, Gilbert L (2015) Interplant signalling through hyphal networks. New Phytol 205:1448–1453PubMedCrossRefGoogle Scholar
  43. Kaiser B, Vogg G, Fürst UB, Albert M (2015) Parasitic plants of the genus Cuscuta and their interaction with susceptible and resistant host plants. Front Plant Sci 6:45PubMedPubMedCentralCrossRefGoogle Scholar
  44. Karban R (2001) Communication between sagebrush and wild tobacco in the field. Biochem Syst Ecol 29:995–1005CrossRefGoogle Scholar
  45. Karban R (2007) Associational resistance for mule’s ears with sagebrush neighbors. Plant Ecol 191:295–303CrossRefGoogle Scholar
  46. Karban R (2008) Plant behaviour and communication. Ecol Lett 11:727–739PubMedCrossRefGoogle Scholar
  47. Karban R, Maron J (2002) The fitness consequences of interspecific eavesdropping between plants. Ecology 83:1209–1213CrossRefGoogle Scholar
  48. Karban R, Shiojiri K (2009) Self-recognition affects plant communication and defense. Ecol Lett 12:502–506PubMedCrossRefGoogle Scholar
  49. Karban R, Baldwin IT, Baxter KJ, Laue G, Felton GW (2000) Communication between plants: induced resistance in wild tobacco plants following clipping of neighboring sagebrush. Oecologia 125:66–71CrossRefGoogle Scholar
  50. Karban R, Maron J, Felton GW, Ervin G, Eichenseer H (2003) Herbivore damage to sagebrush induces resistance in wild tobacco: evidence for eavesdropping between plants. Oikos 100:325–332CrossRefGoogle Scholar
  51. Karban R, Huntzinger M, McCall AC (2004) The specificity of eavesdropping on sagebrush by other plants. Ecology 85:1846–1852CrossRefGoogle Scholar
  52. Karban R, Shiojiri K, Huntzinger M, McCall AC (2006) Damage-induced resistance in sagebrush: volatiles are key to intra- and interplant communication. Ecology 87:922–930PubMedCrossRefGoogle Scholar
  53. Karban R, Shiojiri K, Ishizaki S (2010) An air transfer experiment confirms the role of volatile cues in communication between plants. Am Nat 176:381–384PubMedCrossRefGoogle Scholar
  54. Karban R, Ishizaki S, Shiojiri K (2012) Long-term demographic consequences of eavesdropping for sagebrush. J Ecol 100:932–938CrossRefGoogle Scholar
  55. Karban R, Shiojiri K, Ishizaki S, Wetzel WC, Evans RY (2013) Kin recognition affects plant communication and defence. Proc R Soc B 280:20123062PubMedPubMedCentralCrossRefGoogle Scholar
  56. Karban R, Wetzel WC, Shiojiri K, Ishizaki S, Ramirez SR, Blande JD (2014a) Deciphering the language of plant communication: volatile chemotypes of sagebrush. New Phytol 204:380–385PubMedCrossRefGoogle Scholar
  57. Karban R, Yang LH, Edwards KF (2014b) Volatile communication between plants that affects herbivory: a meta-analysis. Ecol Lett 17:44–52PubMedCrossRefGoogle Scholar
  58. Kegge W, Weldegergis BT, Soler R, Vergeer-Van Eijk MV, Dicke M, Voesenek LA, Pierik R (2013) Canopy light cues affect emission of constitutive and methyl jasmonate-induced volatile organic compounds in Arabidopsis thaliana. New Phytol 200:861–874PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 neighbouring plants. Ann Bot 115:961–970PubMedPubMedCentralCrossRefGoogle Scholar
  60. Kessler A (2015) The information landscape of plant constitutive and induced secondary metabolite production. Curr Opin Insect Sci 8:47–53CrossRefGoogle Scholar
  61. Kessler A, Halitschke R, Diezel C, Baldwin IT (2006) Priming of plant defense responses in nature by airborne signaling between Artemisia tridentata and Nicotiana attenuata. Oecologia 148:280–292PubMedCrossRefGoogle Scholar
  62. Kikuta Y, Ueda H, Nakayama K, Katsuda Y, Ozawa R, Takabayashi J, Hatanaka A, Matsuda K (2011) Specific regulation of pyrethrin biosynthesis in Chrysanthemum cinerariaefolium by a blend of volatiles emitted from artificially damaged conspecific plants. Plant Cell Physiol 52:588–596PubMedCrossRefGoogle Scholar
  63. Kishimoto K, Matsui K, Ozawa R, Takabayashi J (2005) Volatile C6-aldehydes and allo-ocimene activate defense genes and induce resistance against Botrytis cinerea in Arabidopsis thaliana. Plant Cell Physiol 46:1093–1102PubMedCrossRefGoogle Scholar
  64. Kost C, Heil M (2006) Herbivore-induced plant volatiles induce an indirect defence in neighbouring plants. J Ecol 94:619–628CrossRefGoogle Scholar
  65. Lee K, Seo PJ (2014) Airborne signals from salt-stressed Arabidopsis plants trigger salinity tolerance in neighbouring plants. Plant Signal Behav 9:e28392PubMedPubMedCentralCrossRefGoogle Scholar
  66. Li T, Blande JD (2015) Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Glob Chang Biol 21:1993–2004PubMedCrossRefGoogle Scholar
  67. Li T, Holopainen JK, Kokko H, Tervahauta AI, Blande JD (2012) Herbivore-induced aspen volatiles temporally regulate two different indirect defences in neighbouring plants. Funct Ecol 26:176–1185CrossRefGoogle Scholar
  68. Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908PubMedCrossRefGoogle Scholar
  69. Muroi A, Ramadan A, Nishihara M, Yamamoto M, Ozawa R, Takabayashi J, Arimura G (2011) The composite effect of transgenic plant volatiles for acquired immunity to herbivory caused by inter-plant communications. PLoS One 6:e24594PubMedPubMedCentralCrossRefGoogle Scholar
  70. Ninkovic V (2003) Volatile communication between barley plants affects biomass allocation. J Exp Bot 54:1931–1939PubMedCrossRefGoogle Scholar
  71. Ninkovic V, Åhman I (2009) Aphid acceptance of Hordeum genotypes is affected by plant volatile exposure and is correlated with aphid growth. Euphytica 169:177–185CrossRefGoogle Scholar
  72. Ninkovic V, Olsson U, Pettersson J (2002) Mixing barley cultivars affects aphid host plant acceptance in field experiments. Entomol Exp Appl 102:177–182CrossRefGoogle Scholar
  73. Ninkovic V, Glinwood R, Dahlin I (2009) Weed–barley interactions affect plant acceptance by aphids in laboratory and field experiments. Entomol Exp Appl 133:38–45CrossRefGoogle Scholar
  74. Ninkovic V, Dahlin I, Vucetic A, Petrovic-Obradovic O, Glinwood R, Webster B (2013) Volatile exchange between undamaged plants—a new mechanism affecting insect orientation in intercropping. PLoS One 8:e69431PubMedPubMedCentralCrossRefGoogle Scholar
  75. Oluwafemi S, Dewhirst SY, Veyrat N, Powers S, Bruce TJA, Caulfield JC, Pickett JA, Birkett MA (2013) Priming of production in maize of volatile organic defence compounds by the natural plant activator cis-jasmone. PLoS One 8:e62299PubMedPubMedCentralCrossRefGoogle Scholar
  76. Pastor V, Luna E, Mauch-Mani B, Ton J, Flors V (2013) Primed plants do not forget. Environ Exp Bot 94:46–56CrossRefGoogle Scholar
  77. Pearse IS, Karban R (2013) Do plant–plant signals mediate herbivory consistently in multiple taxa and ecological contexts? J Plant Interact 8:203–206CrossRefGoogle Scholar
  78. Pearse IS, Porensky LM, Yang LH, Stanton ML, Karban R, Bhattacharyya L, Cox R, Dove K, Higgins A, Kamoroff C, Kirk T, Knight C, Koch R, Parker C, Rollins H, Tanner K (2012) Complex consequences of herbivory and interplant cues in three annual plants. PLoS One 7:e38105PubMedPubMedCentralCrossRefGoogle Scholar
  79. Pearse IS, Hughes K, Shiojiri K, Ishizaki S, Karban R (2013) Interplant volatile signaling in willows: revisiting the original talking trees. Oecologia 172:869–875PubMedCrossRefGoogle Scholar
  80. Pettersson J, Ninkovic V, Ahmed E (1999) Volatiles from different barley cultivars affect aphid acceptance of neighbouring plants. Acta Agric Scand Sect B-Soil Plant Sci 49:152–157Google Scholar
  81. Pierik R, de Wit M (2014) Shade avoidance: phytochrome signalling and other aboveground neighbour detection cues. J Exp Bot 65:2815–2824PubMedCrossRefGoogle Scholar
  82. Pierik R, Ballaré CL, Dicke M (2014) Ecology of plant volatiles: taking a plant community perspective. Plant Cell Environ 37:1845–1853PubMedCrossRefGoogle Scholar
  83. Piesik D, Lemńczyk G, Skoczek A, Lamparski R, Bocianowski J, Kotwica K, Delaney KJ (2011) Fusarium infection in maize: volatile induction of infected and neighboring uninfected plants has the potential to attract a pest cereal leaf beetle, Oulema melanopus. J Plant Physiol 168:1534–1542PubMedCrossRefGoogle Scholar
  84. Piesik D, Pańka D, Jeske M, Wenda-Piesik A, Delaney KJ, Weaver DK (2013) Volatile induction of infected and neighbouring uninfected plants potentially influence attraction/repellence of a cereal herbivore. J Appl Entomol 137:296–309CrossRefGoogle Scholar
  85. Pinto DM, Blande JD, Nykänen R, Dong W-X, Nerg A-M, Holopainen JK (2007) Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J Chem Ecol 33:683–694PubMedCrossRefGoogle Scholar
  86. Quintana-Rodriguez E, Morales-Vargas AT, Molina-Torres J, Adame-Alvarez RM, Acosta-Gallegos JA, Heil M (2015) Plant volatiles cause direct, induced and associational resistance in common bean to the fungal pathogen Colletotrichum lindemuthianum. J Ecol 103:250–260CrossRefGoogle Scholar
  87. Rhoades DF (1983) Responses of alder and willow to attack by tent caterpillars and webworms: evidence for pheromonal sensitivity of willows. In: Hedin PA (ed) Plant resistance to insects. American Chemical Society, Washington, DC, pp 55–68CrossRefGoogle Scholar
  88. Runyon JB, Mescher MC, De Moraes CM (2006) Volatile chemical cues guide host location and host selection by parasitic plants. Science 313:1964–1967PubMedCrossRefGoogle Scholar
  89. Ruther J, Kleier (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222PubMedCrossRefGoogle Scholar
  90. Scala A, Allmann S, Mirabella R, Haring MA, Schuurink RC (2013) Green leaf volatiles: a plant’s multifunctional weapon against herbivores and pathogens. Int J Mol Sci 14:17781–17811PubMedPubMedCentralCrossRefGoogle Scholar
  91. Shiojiri K, Karban R (2006) Plant age, communication and resistance to herbivores: young sagebrush plants are better emitters and receivers. Oecologia 149:214–220PubMedCrossRefGoogle Scholar
  92. Shiojiri K, Karban R (2008a) Seasonality of herbivory and communication between individuals of sagebrush. Arthropod Plant Interact 2:87–92CrossRefGoogle Scholar
  93. Shiojiri K, Karban R (2008b) Vascular systemic induced resistance for Artemisia cana and volatile communication for Artemisia douglasiana. Am Midl Nat 159:468–477CrossRefGoogle Scholar
  94. Shiojiri K, Karban R, Ishizaki S (2009) Volatile communication among sagebrush branches affects herbivory: timing of active cues. Arthropod Plant Interact 3:99–104CrossRefGoogle Scholar
  95. Shiojiri K, Ozawa R, Matsui K, Sabelis M, Takabayashi J (2012) Intermittent exposure to traces of green leaf volatiles triggers a plant response. Sci Rep 2:378PubMedPubMedCentralCrossRefGoogle Scholar
  96. Shulaev V, Silverman P, Raskin I (1997) Airborne signalling by methyl salicylate in plant pathogen resistance. Nature 385:718–721CrossRefGoogle Scholar
  97. Tamogami S, Rakwal R, Agrawal GK (2008) Interplant communication: airborne methyl jasmonate is essentially converted into JA and JA–Ile activating jasmonate signaling pathway and VOCs emission. Biochem Biophys Res Commun 376:723–727PubMedCrossRefGoogle Scholar
  98. Ton J, D'Alessandro M, Jourdie V, Jakab G, Karlen D, Held M, Mauch-Mani B, Turlings TCJ (2007) Priming by airborne signals boosts direct and indirect resistance in maize. Plant J 49:16–26PubMedCrossRefGoogle Scholar
  99. Ueda H, Kikuta Y, Matsuda K (2012) Plant communication mediated by individual or blended VOCs? Plant Signal Behav 7:222–226PubMedPubMedCentralCrossRefGoogle Scholar
  100. Ul Hassan MN, Zainal Z, Ismail I (2015) Green leaf volatiles: biosynthesis, biological functions and their applications in biotechnology. Plant Biotechnol J 13:727–739PubMedCrossRefGoogle Scholar
  101. Underwood N, Inouye BD, Hambäck PA (2014) A conceptual framework for associational effects: when do neighbors matter and how would we know? Q Rev Biol 89:1–19PubMedCrossRefGoogle Scholar
  102. von Dahl CC, Hävecker M, Schlögl R, Baldwin IT (2006) Caterpillar-elicited methanol emission: a new signal in plant-herbivore interactions? Plant J 46:948–960CrossRefGoogle Scholar
  103. von Dahl CC, Winz RA, Halitschke R, Kühnemann F, Gase K, Baldwin IT (2007) Tuning the herbivore-induced ethylene burst: the role of transcript accumulation and ethylene perception in Nicotiana attenuate. Plant J 51:293–307CrossRefGoogle Scholar
  104. Vucetic A, Dahlin I, Petrovic-Obradovic O, Glinwood R, Webster B, Ninkovic V (2014) Volatile interaction between undamaged plants affects tritrophic interactions through changed plant volatile emission. Plant Signal Behav 9:e29517PubMedCentralCrossRefGoogle Scholar
  105. Yamauchi Y, Kunishima M, Mizutani M, Sugimoto Y (2015) Reactive short-chain leaf volatiles act as powerful inducers of abiotic stress-related gene expression. Sci Rep 5:8030PubMedPubMedCentralCrossRefGoogle Scholar
  106. Yao YL, Danna CH, Zemp FJ, Titov V, Ciftci ON, Przybylski R, Ausubel FM, Kovalchuk I (2011) UV-C-irradiated Arabidopsis and tobacco emit volatiles that trigger genomic instability in neighbouring plants. Plant Cell 23:3824–3852CrossRefGoogle Scholar
  107. Yao YL, Danna CH, Ausubel FM, Kovalchuk I (2012) Perception of volatiles produced by UV-C-irradiated plants alters the response to viral infection in naïve neighboring plants. Plant Signal Behav 7:741–745PubMedPubMedCentralCrossRefGoogle Scholar
  108. Yi HS, Heil M, Adame-Alvarez RM, Ballhorn DJ, Ryu CM (2009) Airborne induction and priming of plant defenses against a bacterial pathogen. Plant Physiol 151:2152–2161PubMedPubMedCentralCrossRefGoogle Scholar
  109. Yoneya K, Takabayashi J (2014) Plant–plant communication mediated by airborne signals: ecological and plant physiological perspectives. Plant Biotechnol 31:409–416CrossRefGoogle Scholar
  110. Zebelo SA, Matsui K, Ozawa R, Maffei ME (2012) Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci 196:93–100PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Environmental and Biological SciencesUniversity of Eastern FinlandKuopioFinland

Personalised recommendations