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

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Abstract

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.

Abstract

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.

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Abbreviations

A N :

Net photosynthesis

F0/Fm/Fv :

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

g s :

Stomatal conductance

PCA:

Principal component analyses

VOC:

Volatile organic compound

WUE:

Water use efficiency

References

  • Adams RP (1995) Identification of essential oil components by gas cromatography and mass spectroscopy. Allured Publishing Corp, Illinois

    Google Scholar 

  • 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 73:3–9

    CAS  Google Scholar 

  • 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 220:666–683

    PubMed  Google Scholar 

  • 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:e0170161

    PubMed  PubMed Central  Google Scholar 

  • Baldwin IT (2010) Plant volatiles. Curr Biol 20:392–397

    Google Scholar 

  • Baldwin IT, Schultz JC (1983) Rapid changes in tree leaf chemistry induced by damage: evidence for communication between plants. Sci 221:277–279

    CAS  Google Scholar 

  • 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 271:1–8

    CAS  PubMed  Google Scholar 

  • 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 147:463–468

    Google Scholar 

  • 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 100:6843–6848

    PubMed  Google Scholar 

  • Bouché N, Lacombe B, Fromm H (2003b) GABA signaling: a conserved and ubiquitous mechanism. Trends Cell Biol 13:607–610

    PubMed  Google Scholar 

  • 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 450:280–284

    CAS  PubMed  Google Scholar 

  • 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 147:261–270

    CAS  Google Scholar 

  • 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 153:54–62

    CAS  Google Scholar 

  • Ceccanti C, Landi M, Benvenuti S, Pardossi A, Guidi L (2018) Mediterranean wild edible plants: weeds or “new functional crops”? Molecules 23:2299

    PubMed Central  Google Scholar 

  • Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560

    CAS  PubMed  Google Scholar 

  • 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 66:11197–11208

    CAS  PubMed  Google Scholar 

  • 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 74:3119–3147

    CAS  PubMed  Google Scholar 

  • Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175

    CAS  PubMed  Google Scholar 

  • Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198:16–32

    CAS  PubMed  Google Scholar 

  • 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 7:363–368

    CAS  Google Scholar 

  • Erb M (2018) Volatiles as inducers and suppressors of plant defense and immunity-origins, specificity, perception and signaling. Curr Opin Plant Biol 44:117–121

    CAS  PubMed  Google Scholar 

  • Fincheira P, Quiroz A (2018) Microbial volatiles as plant growth inducers. Microbiol Res 208:63–75

    CAS  PubMed  Google Scholar 

  • Forieri I, Hildebrandt U, Rostas M (2016) Salinity stress effects on direct and indirect defence metabolites in maize. Environ Exp Bot 122:68–77

    CAS  Google Scholar 

  • 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 96:1228–1236

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 43:4488–4496

    CAS  PubMed  Google Scholar 

  • 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 117–136

    Google Scholar 

  • 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 58:2873–2885

    CAS  PubMed  Google Scholar 

  • 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 29:67–75

    Google Scholar 

  • Jones JB (1998) Plant nutrition manual. CRC Press, Boca Raton

    Google Scholar 

  • Kathiresan A, Tung P, Chinnappa CC, Reid DM (1997) Gamma-aminobutyric acid stimulates ethylene biosynthesis in sunflower. Plant Physiol 115:129–135

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kegge W, Pierik R (2010) Biogenic volatile organic compounds and plant competition. Trends Plant Sci 15:126–132

    CAS  PubMed  Google Scholar 

  • Kessler A, Halitschke R, Poveda K (2011) Herbivory-mediated pollinator limitation: negative impacts of induced volatiles on plant–pollinator interactions. Ecology 92:1769–1780

    PubMed  Google Scholar 

  • Kinnersley AM, Turano FJ (2000) Gamma aminobutyric acid (GABA) and plant responses to stress. Crit Rev Plant Sci 19:479–509

    CAS  Google Scholar 

  • Lähdesmäki P (1968) The amount of γ-amino butyric acid and the activity of glutamic decarboxylase in aging leaves. Physiol Plant 21:1322–1327

    Google Scholar 

  • 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 176:942–951

    CAS  Google Scholar 

  • Lee K, Seo PJ (2014) Airborne signals from salt-stressed Arabidopsis plants trigger salinity tolerance in neighboring plants. Plant Signal Behav 9:e28392

    PubMed  PubMed Central  Google Scholar 

  • Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV–Vis spectroscopy. Curr Prot Food Anal Chem 1:F4–8

    Google Scholar 

  • Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166

    CAS  PubMed  Google Scholar 

  • Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908

    PubMed  Google Scholar 

  • 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 37:1013–1026

    CAS  PubMed  Google Scholar 

  • 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 211:510–518

    CAS  PubMed  Google Scholar 

  • Matsui K (2016) A portion of plant airborne communication is endorsed by uptake and metabolism of volatile organic compounds. Curr Opin Plant Biol 32:24–30

    CAS  PubMed  Google Scholar 

  • 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 231:337–345

    CAS  PubMed  Google Scholar 

  • 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 395:375–389

    CAS  Google Scholar 

  • 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:e31971

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 151:613–622

    Google Scholar 

  • Qualley A, Dudareva N (2001) Plant volatiles. Wiley, Chichester

    Google Scholar 

  • 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 167:1159–1169

    CAS  Google Scholar 

  • 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 31:2217–2222

    CAS  PubMed  Google Scholar 

  • Shabala S, Munns R (2012) Salinity stress: Physiological constraints and adaptive mechanisms. In: Shabala S (ed) Plant stress physiology. CAB International, Oxford, pp 59–93

    Google Scholar 

  • Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52:407–436

    CAS  PubMed  Google Scholar 

  • Shelp BJ, Bown AW, McLean MD (1999) Metabolism and functions of gamma-aminobutyric acid. Trends Plant Sci 4:446–452

    CAS  PubMed  Google Scholar 

  • Sims JT, Kline JS (1991) Chemical fractionation and plant uptake of heavy metals in soils amended with co-composted sewage sludge. J Environ Qual 20:387–395

    CAS  Google Scholar 

  • 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 14:407–426

    CAS  Google Scholar 

  • 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 176:748–755

    CAS  Google Scholar 

  • Urano K, Maruyama K, Ogata Y et al (2009) Characterization of the ABA-regulated global responses to dehydration in Arabidopsis by metabolomics. Plant J 57:1065–1078

    CAS  PubMed  Google Scholar 

  • Xia J, Sinelnikov IV, Han B, Wishart DS (2015) MetaboAnalyst 3.0—making metabolomics more meaningful. Nucleic Acids Res 43:251–257

    Google Scholar 

  • Yoneya K, Takabayashi J (2014) Plant–plant communication mediated by airborne signals: ecological and plant physiological perspectives. Plant Biotechnol 31:409–416

    CAS  Google Scholar 

  • 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 24:323–331

    PubMed  Google Scholar 

Download references

Acknowledgements

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

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Authors and Affiliations

  1. Department of Agriculture, Food and Environment, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Marco Landi, Ermes Lo Piccolo & Lucia Guidi

  2. CIRSEC, Centre for Climatic Change Impact, University of Pisa, Via del Borghetto 80, 56124, Pisa, Italy

    Marco Landi & Lucia Guidi

  3. Department of Agraria, University ‘Mediterranea’ of Reggio Calabria, località Feo di Vito, 89122, Reggio Calabria, RC, Italy

    Fabrizio Araniti & Maria Rosa Abenavoli

  4. Department of Pharmacy, University of Pisa, Via Bonanno Pisano 6, 56126, Pisa, Italy

    Guido Flamini

  5. Institute of Life Sciences, Scuola Superiore Sant’Anna, Via Santa Cecilia 3, 56127, Pisa, Italy

    Alice Trivellini

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  1. Marco Landi
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Correspondence to Marco Landi.

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Landi, M., Araniti, F., Flamini, G. et al. “Help is in the air”: volatiles from salt-stressed plants increase the reproductive success of receivers under salinity. Planta 251, 48 (2020). https://doi.org/10.1007/s00425-020-03344-y

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