, 251:48 | Cite as

“Help is in the air”: volatiles from salt-stressed plants increase the reproductive success of receivers under salinity

  • Marco LandiEmail author
  • Fabrizio Araniti
  • Guido Flamini
  • Ermes Lo Piccolo
  • Alice Trivellini
  • Maria Rosa Abenavoli
  • Lucia Guidi
Original Article


Main conclusion

Salinity alters VOC profile in emitter sweet basil plants. Airborne signals by emitter plants promote earlier flowering of receivers and increase their reproductive success under salinity.


Airborne signals can prime neighboring plants against pathogen and/or herbivore attacks, whilst little is known about the possibility that volatile organic compounds (VOCs) emitted by stressed plants alert neighboring plants against abiotic stressors. Salt stress (50 mM NaCl) was imposed on Ocimum basilicum L. plants (emitters, namely NaCl), and a putative alerting-priming interaction was tested on neighboring basil plants (receivers, namely NaCl-S). Compared with the receivers, the NaCl plants exhibited reduced biomass, lower photosynthesis, and changes in the VOC profile, which are common early responses of plants to salinity. In contrast, NaCl-S plants had physiological parameters similar to those of nonsalted plants (C), but exhibited a different VOC fingerprint, which overlapped, for most compounds, with that of emitters. NaCl-S plants exposed later to NaCl treatment (namely NaCl-S + NaCl) exhibited changes in the VOC profile, earlier plant senescence, earlier flowering, and higher seed yield than C + NaCl plants. This experiment offers the evidence that (1) NaCl-triggered VOCs promote metabolic changes in NaCl-S plants, which, finally, increase reproductive success and (2) the differences in VOC profiles observed between emitters and receivers subjected to salinity raise the question whether the receivers are able to “propagate” the warning signal triggered by VOCs in neighboring companions.


Airborne signal Emitter Infochemical Plant–plant communication Receiver Salt stress 



Net photosynthesis


Minimal/maximal/variable chlorophyll fluorescence yield in dark-adapted leaves


Stomatal conductance


Principal component analyses


Volatile organic compound


Water use efficiency



This study in part was supported by the Italian Ministry of Education, University and Research (MIUR), project SIR-2014 cod. RBSI14L9CE (MEDANAT).

Supplementary material

425_2020_3344_MOESM1_ESM.docx (465 kb)
Figure S1 Score plot of metabolomics data (DOCX 464 kb)
425_2020_3344_MOESM2_ESM.docx (346 kb)
Figure S2 Score plot of volatile organic compounds (DOCX 345 kb)
425_2020_3344_MOESM3_ESM.docx (22 kb)
Supplementary file3 (DOCX 22 kb)
425_2020_3344_MOESM4_ESM.docx (24 kb)
Supplementary file4 (DOCX 24 kb)
425_2020_3344_MOESM5_ESM.docx (20 kb)
Supplementary file5 (DOCX 19 kb)
425_2020_3344_MOESM6_ESM.docx (14 kb)
Supplementary file6 (DOCX 14 kb)


  1. Adams RP (1995) Identification of essential oil components by gas cromatography and mass spectroscopy. Allured Publishing Corp, IllinoisGoogle Scholar
  2. Agati G, Cerovic ZG, Pinelli P, Tattini M (2011) Light-induced accumulation of ortho-dihydroxylated flavonoids as non-destructively monitored by chlorophyll fluorescence excitation techniques. Environ Exp Bot 73:3–9CrossRefGoogle Scholar
  3. Ameye M, Allmann S, Verwaeren J, Smagghe G, Haesaert G, Schuurink RC, Audenaert K (2017) Green leaf volatile production by plants: a meta-analysis. New Phytol 220:666–683PubMedCrossRefPubMedCentralGoogle Scholar
  4. Araniti F, Lupini A, Sunseri F, Abenavoli MR (2017) Allelopathic potential of Dittrichia voscosa (L.) W. Greuter mediated by VOCs: a physiologycal and metabolomic approach. PLoS One 12:e0170161PubMedPubMedCentralCrossRefGoogle Scholar
  5. Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397CrossRefGoogle Scholar
  6. Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Sci 221:277–279CrossRefGoogle Scholar
  7. Bibbiani S, Colzi I, Taiti C, Guidi Nissim W, Papini A, Mancuso S, Gonnelli C (2018) Smelling the metal: volatile organic compound emission under Zn excess in the mint Tetradenia riparia. Plant Sci 271:1–8PubMedCrossRefPubMedCentralGoogle Scholar
  8. Bolarín MC, Santa-Cruz A, Cayuela E, Pérez-Alfocea F (1995) Short-term solute changes in leaves and roots of cultivated and wild tomato seedlings under salinity. J Plant Physiol 147:463–468CrossRefGoogle Scholar
  9. Bouché N, Fait A, Bouchez D, Moller SG, Fromm H (2003a) Mitochondrial succinic-semialdehyde dehydrogenase of the γ-aminobutyrate shunt is required to restrict levels of reactive oxygen intermediates in plants. Proc Nat Acad Sci USA 100:6843–6848PubMedCrossRefPubMedCentralGoogle Scholar
  10. Bouché N, Lacombe B, Fromm H (2003b) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol 13:607–610PubMedCrossRefGoogle Scholar
  11. Breitkreuz KE, Shelp BJ, Fischer WN, Schwacke R, Rentsch D (1999) Identification and characterization of GABA, proline and quaternary ammonium compound transporters from Arabidopsis thaliana. FEBS Lett 450:280–284PubMedCrossRefPubMedCentralGoogle Scholar
  12. Caparrotta S, Boni S, Taiti C, Palm E, Mancuso S, Pandolfi C (2018) Induction of priming by salt stress in neighboring plants. Environ Exp Bot 147:261–270CrossRefGoogle Scholar
  13. Catola S, Centritto M, Cascone P, Ranieri A, Loreto F, Calamai L, Balestrini R, Guerrieri E (2018) Effects of single or combined water deficit and aphid attack on tomato volatile organic compound (VOC) emission and plant–plant communication. Environ Exp Bot 153:54–62CrossRefGoogle Scholar
  14. Ceccanti C, Landi M, Benvenuti S, Pardossi A, Guidi L (2018) Mediterranean wild edible plants: weeds or “new functional crops”? Molecules 23:2299PubMedCentralCrossRefGoogle Scholar
  15. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560PubMedCrossRefPubMedCentralGoogle Scholar
  16. Cofer TM, Seidl-Adams I, Tumlinson JH (2018) From acetoin to (Z)-3-hexen-1-ol: the diversity of volatile organic compounds that induce plant responses. J Agric Food Chem 66:11197–11208PubMedCrossRefPubMedCentralGoogle Scholar
  17. Covarrubias AA, Cuevas-Velazquez CL, Romero-Pérez PS, Rendón-Luna DF, Chater CCC (2017) Structural disorder in plant proteins: where plasticity meets sessility. Cell Mol Life Sci 74:3119–3147PubMedCrossRefPubMedCentralGoogle Scholar
  18. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefPubMedCentralGoogle Scholar
  19. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32PubMedCrossRefPubMedCentralGoogle Scholar
  20. El-Bassiouny HM, Bekheta MA (2005) Effect of salt stress on relative water content, lipid peroxidation, polyamines amino acids and ethylene of two wheat cultivars. Int J Agric Biol 7:363–368Google Scholar
  21. Erb M (2018) Volatiles as inducers and suppressors of plant defense and immunity-origins, specificity, perception and signaling. Curr Opin Plant Biol 44:117–121PubMedCrossRefPubMedCentralGoogle Scholar
  22. Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75PubMedCrossRefPubMedCentralGoogle Scholar
  23. Forieri I, Hildebrandt U, Rostas M (2016) Salinity stress effects on direct and indirect defence metabolites in maize. Environ Exp Bot 122:68–77CrossRefGoogle Scholar
  24. Fougere F, Le Rudulier D, Streeter JG (1991) Effects of salt stress on amino acid, organic acid and carbohydrate composition of roots, bacteroids, and cytosol of alfa alfa (Medicago sativa L.). Plant Physiol 96:1228–1236PubMedPubMedCentralCrossRefGoogle Scholar
  25. Goulas Y, Cerovic ZG, Cartelat A, Moya I (2004) Dualex: a new instrument for field measurements of epidermal ultraviolet absorbance by chlorophyll fluorescence. Appl Opt 43:4488–4496PubMedCrossRefPubMedCentralGoogle Scholar
  26. Guerrieri E (2016) Who’s listening to talking plants? In: Ginwood R, Blande J (eds) Deciphering chemical language of plant communication. Signaling and communication in plants series. Springer, Basel, pp 117–136CrossRefGoogle Scholar
  27. Hoeberichts FA, Van Doorn WG, Vorst O, Hall RD, Van Wordragen MF (2007) Sucrose prevents up-regulation of senescence-associated genes in carnation petals. J Exp Bot 58:2873–2885PubMedCrossRefPubMedCentralGoogle Scholar
  28. Jalali F, Zafari D, Salari H (2017) Volatile organic compounds of some Trichoderma spp. increase growth and induce salt tolerance in Arabidopsis thaliana. Fungal Ecol 29:67–75CrossRefGoogle Scholar
  29. Jones JB (1998) Plant nutrition manual. CRC Press, Boca RatonGoogle Scholar
  30. Kathiresan A, Tung P, Chinnappa CC, Reid DM (1997) Gamma-aminobutyric acid stimulates ethylene biosynthesis in sunflower. Plant Physiol 115:129–135PubMedPubMedCentralCrossRefGoogle Scholar
  31. Kegge W, Pierik R (2010) Biogenic volatile organic compounds and plant competition. Trends Plant Sci 15:126–132PubMedCrossRefPubMedCentralGoogle Scholar
  32. Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780PubMedCrossRefPubMedCentralGoogle Scholar
  33. Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509CrossRefGoogle Scholar
  34. Lähdesmäki P (1968) The amount of γ-amino butyric acid and the activity of glutamic decarboxylase in aging leaves. Physiol Plant 21:1322–1327CrossRefGoogle Scholar
  35. Landi M, Remorini D, Pardossi A, Guidi L (2013) Sweet basil (Ocimum basilicum) with green or purple leaves: which differences occur in photosynthesis under boron toxicity? J Plant Nutr Soil Sci 176:942–951CrossRefGoogle Scholar
  36. Lee K, Seo PJ (2014) Airborne signals from salt-stressed Arabidopsis plants trigger salinity tolerance in neighboring plants. Plant Signal Behav 9:e28392PubMedPubMedCentralCrossRefGoogle Scholar
  37. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–Vis spectroscopy. Curr Prot Food Anal Chem 1:F4–8Google Scholar
  38. Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166PubMedCrossRefGoogle Scholar
  39. Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908PubMedCrossRefPubMedCentralGoogle Scholar
  40. Lusebrink I, Evenden ML, Blanchet FG, Cooke JEK, Erbilgin N (2011) Effect of water stress and fungal inoculation on monoterpene emission from an historical and a new pine host of the mountain pine beetle. J Chem Ecol 37:1013–1026PubMedCrossRefPubMedCentralGoogle Scholar
  41. Masclaux C, Valadier MH, Brugière N, Morot-Gaudry JF, Hirel B (2000) Characterization of the sink/source transition in tobacco (Nicotiana tabacum L.) shoots in relation to nitrogen management and leaf senescence. Planta 211:510–518PubMedCrossRefPubMedCentralGoogle Scholar
  42. Matsui K (2016) A portion of plant airborne communication is endorsed by uptake and metabolism of volatile organic compounds. Curr Opin Plant Biol 32:24–30PubMedCrossRefPubMedCentralGoogle Scholar
  43. Papadakis IE, Tsiantas PI, Tsaniklidis G, Landi M, Psychoyou M, Fasseas C (2018) Changes in sugar metabolism associated to stem bark thickening partially assist young tissues of Eriobotrya japonica seedlings under boron stress. J Plant Physiol 231:337–345PubMedCrossRefPubMedCentralGoogle Scholar
  44. Pardossi A, Romani M, Carmassi G, Guidi L, Landi M, Incrocci L, Maggini R, Puccinelli M, Vacca W, Ziliani M (2015) Boron accumulation and tolerance in sweet basil (Ocimum basilicum L.) with green or purple leaves. Plant Soil 395:375–389CrossRefGoogle Scholar
  45. Pareja M, Qvarfordt E, Webster B, Mayon P, Pickett J, Birkett M, Glinwood R (2012) Herbivory by a phloem-feeding insect inhibits floral volatile production. PLoS One 7:e31971PubMedPubMedCentralCrossRefGoogle Scholar
  46. Pompeiano A, Landi M, Meloni G, Vita F, Guglielminetti L, Guidi L (2017) Allocation pattern, ion partitioning, and chlorophyll a fluorescence in Arundo donax L. in responses to salinity stress. Plant Biosyst 151:613–622CrossRefGoogle Scholar
  47. Qualley A, Dudareva N (2001) Plant volatiles. Wiley, ChichesterGoogle Scholar
  48. Rai V, Vajpayee P, Singh SN, Mehrotra S (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169CrossRefGoogle Scholar
  49. Ruther J, Kleier S (2005) Plant–plant signaling: ethylene synergizes volatile emission in Zea mays induced by exposure to (Z)-3-hexen-1-ol. J Chem Ecol 31:2217–2222PubMedCrossRefPubMedCentralGoogle Scholar
  50. Shabala S, Munns R (2012) Salinity stress: Physiological constraints and adaptive mechanisms. In: Shabala S (ed) Plant stress physiology. CAB International, Oxford, pp 59–93CrossRefGoogle Scholar
  51. Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436PubMedCrossRefPubMedCentralGoogle Scholar
  52. Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452PubMedCrossRefPubMedCentralGoogle Scholar
  53. Sims JT, Kline JS (1991) Chemical fractionation and plant uptake of heavy metals in soils amended with co-composted sewage sludge. J Environ Qual 20:387–395CrossRefGoogle Scholar
  54. Singh M, Kumar J, Singh S, Singh VP, Prasad SM (2015) Roles of osmoprotectants in improving salinity and drought tolerance in plants: a review. Rev Environ Sci Biotech 14:407–426CrossRefGoogle Scholar
  55. Tarchoune I, Baâtour O, Harrathi J, Cioni PL, Lachaâl M, Flamini G, Ouerghi Z (2013) Essential oil and volatile emissions of basil (Ocimum basilicum) leaves exposed to NaCl or Na2SO4 salinity. J Plant Nutr Soil Sci 176:748–755Google Scholar
  56. Urano K, Maruyama K, Ogata Y et al (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078PubMedCrossRefPubMedCentralGoogle Scholar
  57. Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43:251–257CrossRefGoogle Scholar
  58. Yoneya K, Takabayashi J (2014) Plant–plant communication mediated by airborne signals: ecological and plant physiological perspectives. Plant Biotechnol 31:409–416CrossRefGoogle Scholar
  59. Yuan JS, Himanen SJ, Holopainen JK, Chen F, Stewart CN (2009) Smelling global climate change: mitigation of function for plant volatile organic compounds. Trends Ecol Evol 24:323–331PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2020

Authors and Affiliations

  • Marco Landi
    • 1
    • 2
    Email author
  • Fabrizio Araniti
    • 3
  • Guido Flamini
    • 4
  • Ermes Lo Piccolo
    • 1
  • Alice Trivellini
    • 5
  • Maria Rosa Abenavoli
    • 3
  • Lucia Guidi
    • 1
    • 2
  1. 1.Department of Agriculture, Food and EnvironmentUniversity of PisaPisaItaly
  2. 2.CIRSEC, Centre for Climatic Change ImpactUniversity of PisaPisaItaly
  3. 3.Department of AgrariaUniversity ‘Mediterranea’ of Reggio CalabriaReggio CalabriaItaly
  4. 4.Department of PharmacyUniversity of PisaPisaItaly
  5. 5.Institute of Life SciencesScuola Superiore Sant’AnnaPisaItaly

Personalised recommendations