Skip to main content
Springer Nature Link
Log in

Soft mechanical stimulation induces a defense response against Botrytis cinerea in strawberry

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Genes associated with plant mechanical stimulation were found in strawberry genome. A soft mechanical stimulation (SMS) induces molecular and biochemical changes in strawberry plants, conferring protection against Botrytis cinerea.

Abstract

Plants have the capacity to induce a defense response after exposure to abiotic stresses acquiring resistance towards pathogens. It was reported that when leaves of Arabidopsis thaliana were wounded or treated with a soft mechanical stimulation (SMS), they could resist much better the attack of the fungal pathogen Botrytis cinerea, and this effect was accompanied by an oxidative burst and the expression of touch-inducible genes (TCH). However, no further work was carried out to better characterize the induced defense response. In this paper, we report that TCH genes were identified for first time in the genomes of the strawberry species Fragaria ananassa (e.g. FaTCH2, FaTCH3, FaTCH4 and FaCML39) and Fragaria vesca (e.g. FvTCH2, FvTCH3, FvTCH4 and FvCML39). Phylogenetic studies revealed that F. ananassa TCH genes exhibited high similarity with the orthologous of F. vesca and lower with A. thaliana ones. We also present evidence that after SMS treatment on strawberry leaves, plants activate a rapid oxidative burst, callose deposition, and the up-regulation of TCH genes as well as plant defense genes such as FaPR1, FaCHI2-2, FaCAT, FaACS1 and FaOGBG-5. The latter represents the first report showing that TCH- and defense-induced genes participate in SMS-induced resistance in plants, bringing a rational explanation why plants exposed to a SMS treatment acquired an enhance resistance toward B. cinerea.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

Abbreviations

dpi:

Days post infection

SMS:

Soft mechanical stimulation

dpSMS:

Days post SMS treatment

hpSMS:

Hours post SMS treatment

mpSMS:

Minutes post SMS treatment

ROS:

Reactive oxygen species

TCH:

Touch-inducible genes

References

  • Abeles FB, Morgan PW, Saltveit ME (1992) Ethylene in plant biology. Academic Press, San Diego

    Google Scholar 

  • Alvarez ME, Pennell RI, Meijer PJ, Ishikawa A, Dixon RA, Lamb C (1998) Reactive oxygen intermediates mediate a systemic signal network in the establishment of plant immunity. Cell 92:773–784

    Article  CAS  PubMed  Google Scholar 

  • Amil-Ruiz F, Blanco-Portales R, Munoz-Blanco J, Caballero JL (2011) The strawberry plant defense mechanism: a molecular review. Plant Cell Physiol 52:1873–1903

    Article  CAS  PubMed  Google Scholar 

  • Amil-Ruiz F, Garrido-Gala J, Blanco-Portales R, Folta KM, Muñoz-Blanco J, Caballero JL (2013) Identification and evaluation of superior reference genes for transcript normalization in strawberry plant defense responses. PLoS One 8:e70603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anten NPR, Casado-Garcia R, Nagashima H (2005) Effects of mechanical stress and plant density on mechanical characteristics, growth, and lifetime reproduction of tobacco plants. Am Nat 166:650–660

    Article  PubMed  Google Scholar 

  • Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol 90:109–116

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bender KW, Rosenbaum DM, Vanderbeld B, Ubaid M, Snedden WA (2013) The Arabidopsis calmodulin-like protein, CML39, functions during early seedling establishment. Plant J 76:634–647

    Article  CAS  PubMed  Google Scholar 

  • Beneloujaephajri E, Costa A, L’Haridon F, Metraux JP, Binda M (2013) Production of reactive oxygen species and wound-induced resistance in Arabidopsis thaliana against Botrytis cinerea are preceded and depend on a burst of calcium. BMC Plant Biol 13:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Benikhlef L, L’Haridon F, Abou-Mansour E, Serrano M, Binda M, Costa A, Lehman S, Métraux JP (2013) Perception of soft mechanical stress in Arabidopsis leaves activates disease resistance. BMC Plant Biol 13:133

    Article  PubMed  PubMed Central  Google Scholar 

  • Böhm J, Scherzer S, Krol E, Kreuzer I, von Meyer K, Lorey C, Mueller TD, Shabala L, Monte I, Solano R et al (2016) The Venus flytrap Dionaea muscipula counts prey-induced action potentials to induce sodium uptake. Curr Biol 26:286–295

    Article  PubMed  PubMed Central  Google Scholar 

  • Botella JR, Arteca RN, Frangos JA (1995) A mechanical straininduced 1-aminocyclopropane-1-carboxylic acid synthase gene. P Natl Acad Sci USA 92:1595–1598

    Article  CAS  Google Scholar 

  • Braam J (2005) In touch: plant responses to mechanical stimuli. New Phytol 165:373–389

    Article  PubMed  Google Scholar 

  • Braam J, Davis RW (1990) Rain-, wind-, and touch-induced expression of calmodulin and calmodulin-related genes in Arabidopsis. Cell 60:357–364

    Article  CAS  PubMed  Google Scholar 

  • Chalfoun NR, Grellet-Bournonville CF, Martínez-Zamora MG, Díaz-Perales A, Castagnaro AP, Díaz-Ricci JC (2013) Purification and characterization of AsES protein: a subtilisin secreted by Acremonium strictum is a novel plant defense elicitor. J Biol Chem 288:14098–14113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chassot C, Buchala A, Schoonbeek H, Metraux JP, Lamotte O (2008) Wounding of Arabidopsis leaves causes a powerful but transient protection against Botrytis infection. Plant J 55:555–567

    Article  CAS  PubMed  Google Scholar 

  • Choquer M, Fournier E, Kunz C, Levis C, Pradier JM, Simon A, Viaud M (2007) Botrytis cinerea virulence factors: new insights into a necrotrophic and polyphageous pathogen. FEMS Microbiol Lett 277:1–10

    Article  CAS  PubMed  Google Scholar 

  • Conrath U (2006) Systemic acquired resistance. Plant Signal Behav 1:179–184

    Article  PubMed  PubMed Central  Google Scholar 

  • Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J et al (2012) The top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430

    Article  PubMed  Google Scholar 

  • Di Rienzo JA, Gonzalez LA, Tablada EM (2009) fgStatistics—user manual. Electronic Edition, Argentina

  • Di Rienzo JA (2011) fgStatistics. Statistical software for the analysis of experiments of functional genomics. http://sites.google.com/site/fgStatistics/

  • Di Rienzo JA, Casanoves F, Balzarini MG, Gonzalez L, Tablada M, Robledo CW (2013) InfoStat versión 2013. Grupo InfoStat, FCA, Universidad Nacional de Córdoba, Argentina. http://www.infostat.com.ar

  • Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato-tuber tissues to infection with an incompatible race of Phytophthora-infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357

    Article  CAS  Google Scholar 

  • Eggert D, Naumann M, Reimer R, Voigt CA (2014) Nanoscale glucan polymer network causes pathogen resistance. Sci Rep 4:4159

    Article  PubMed  PubMed Central  Google Scholar 

  • Ellinger D, Naumann M, Falter C, Zwikowics C, Jamrow T, Manisseri C, Somerville SC, Voigt CA (2013) Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol 161:1433–1444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foyer CH, Rasool B, Davey JW, Hancock RD (2016) Cross-tolerance to biotic and abiotic stresses in plants: a focus on resistance to aphid infestation. J Exp Bot 67:2025–2037

    Article  CAS  PubMed  Google Scholar 

  • Francia D, Demaria D, Calderini O, Ferraris L, Valentino D, Arcioni S, Tamietti G, Cardinale F (2007) Wounding induces resistance to pathogens with different lifestyles in tomato: role of ethylene in cross-protection. Plant Cell Environ 30:1357–1365

    Article  CAS  PubMed  Google Scholar 

  • Fujikawa Y, Nakanishi T, Kawakami H, Yamasaki K, Sato MH, Tsuji H, Matsuoka M, Kato N (2014) Split luciferase complementation assay to detect regulated protein-protein interactions in rice protoplasts in a large-scale format. Rice 7:11

    Article  PubMed  PubMed Central  Google Scholar 

  • García T, Gutiérrez J, Veloso J, Gago-Fuentes R, Díaz J (2015) Wounding induces local resistance but systemic susceptibility to Botrytis cinerea in pepper plants. J Plant Physiol 176:202–209

    Article  PubMed  Google Scholar 

  • Govrin EM, Levine A (2000) The hypersensitive response facilitates plant infection by the necrotrophic pathogen Botrytis cinerea. Curr Biol 10:751–757

    Article  CAS  PubMed  Google Scholar 

  • Graham MY, Weidner J, Wheeler K, Pelow MJ, Graham TL (2003) Induced expression of pathogenesis-related protein genes in soybean by wounding and the Phytophthora sojae cell wall glucan elicitor. Physiol Mol Plant P 63:141–149

    Article  CAS  Google Scholar 

  • Grellet-Bournonville CF, Martinez-Zamora MG, Castagnaro AP, Díaz-Ricci JC (2012) Temporal accumulation of salicylic acid activates the defense response against Colletotrichum in strawberry. Plant Physiol Biochem 54:10–16

    Article  CAS  PubMed  Google Scholar 

  • Guerrero-Molina MF, Lovaisa NC, Salazar SM, Martinez-Zamora MG, Diaz-Ricci JC, Pedraza RO (2014) Physiological, structural and molecular traits activated in strawberry plants after inoculation with the plant growth-promoting bacterium Azospirillum brasilense REC3. Plant Biol 17:766–773

    Article  PubMed  Google Scholar 

  • Guidarelli M, Carbone F, Mourgues F, Perrotta G, Rosati C, Bertolinia P, Baraldia E (2011) Colletotrichum acutatum interactions with unripe and ripe strawberry fruits and differential responses at histological and transcriptional levels. Plant Pathol 60:685–697

    Article  Google Scholar 

  • Gus-Mayer S, Naton B, Hahlbrock K, Schmelzer E (1998) Local mechanical stimulation induces components of the pathogen defense response in parsley. Proc Natl Acad Sci USA 95:8398–8403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hael-Conrad V, Abou-Mansour E, Díaz-Ricci JC, Métraux JP, Serrano M (2015) The novel elicitor AsES triggers a defense response against Botrytis cinerea in Arabidopsis thaliana. Plant Sci 241:120–127

    Article  CAS  PubMed  Google Scholar 

  • Hael-Conrad V, Perato SM, Arias ME, Martinez-Zamora MG, Di-Peto PLA, Martos GG, Castagnaro AP, Diaz-Ricci JC, Chalfoun NR (2017) The elicitor protein AsES induces a SAR response accompanied by systemic microbursts and micro-HRs in Fragaria ananassa. Mol Plant Microbe Interact. doi:10.1094/MPMI-05-17-0121-FI

    PubMed  Google Scholar 

  • Heller J, Tudzynski P (2011) Reactive oxygen species in phytopathogenic fungi: signaling, development, and disease. Annu Rev Phytopathol 49:369–390

    Article  CAS  PubMed  Google Scholar 

  • Hirakawa H, Shirasawa K, Kosugi S, Tashiro K, Nakayama S, Yamada M, Kohara M, Watanabe A, Kishida Y, Fujishiro T et al (2014) Dissection of the octoploid strawberry genome by deep sequencing of the genomes of Fragaria species. DNA Res 21:169–181

    Article  CAS  PubMed  Google Scholar 

  • Iida H (2014) Mugifumi, a beneficial farm work of adding mechanical stress by treading to wheat and barley seedlings. Front Plant Sci 5:453

    Article  PubMed  PubMed Central  Google Scholar 

  • Jaffe MJ, Huberman M, Johnson J, Telewski FW (1985) Thigmomorphogenesis: the induction of callose formation and ethylene evolution by mechanical perturbation in bean stems. Physiol Plantarum 64:271–279

    Article  CAS  Google Scholar 

  • Kim JT, Min JY, Kim HT (2006) Response to fungicides of Colletotrichum species isolated from infected tissues of several crops. Res Plant Dis 12:32–39

    Article  Google Scholar 

  • Kumar S, Tamura K, Jakobsen IB, Nei M (2001) MEGA2: Molecular evolutionary genetics analysis software. Bioinformatics. 17:1244–1245

    Article  CAS  PubMed  Google Scholar 

  • Laloi C, Apel K, Danon A (2004) Reactive oxygen signalling: the latest news. Curr Opin Plant Biol 7:323–328

    Article  CAS  PubMed  Google Scholar 

  • Lee D, Polisensky DH, Braam J (2005) Genome-wide identification of touch- and darkness-regulated Arabidopsis genes: a focus on calmodulin-like and XTH genes. N Phytology 165:429–444

    Article  CAS  Google Scholar 

  • Lehmann S, Serrano M, L’Haridon F, Tjamos SE, Metraux JP (2015) Reactive oxygen species and plant resistance to fungal pathogens. Phytochemistry 112:54–62

    Article  CAS  PubMed  Google Scholar 

  • Mamaní A, Filippone MP, Grellet C, Welin B, Castagnaro AP, Díaz-Ricci JC (2012) Pathogen-induced accumulation of an ellagitannin elicits plant defense response. Mol Plant Microbe Interact 25:1430–1439

    Article  PubMed  Google Scholar 

  • Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trends Plant Sci 17:9–15

    Article  CAS  PubMed  Google Scholar 

  • Markovic D, Nikolic N, Glinwood R, Seisenbaeva G, Ninkovic V (2016) Plant responses to brief touching: a mechanism for early neighbour detection? PLoS One 11:e0165742

    Article  PubMed  PubMed Central  Google Scholar 

  • Martinez-Zamora MG, Grellet-Bournonville C, Castagnaro AP, Díaz Ricci JC (2012) Identification and characterization of a novel Class I endo-β-1,3-glucanase regulated by salicylic acid, ethylene and fungal pathogens in strawberry. Funct Plant Biol 39:412–420

    Article  Google Scholar 

  • Martos GG (2015) Estudio de la inducción de la respuesta de defensa contra patógenos fúngicos en frutilla mediada por una proteína inductora. PhD thesis, Universidad Nacional de Tucumán, Tucumán, Argentina

  • Martos GG, Teran MM, Díaz-Ricci JC (2015) The defence elicitor AsES causes a rapid and transient membrane depolarization, a triphasic oxidative burst and the accumulation of nitric oxide. Plant Physiol Biochem 97:443–450

    Article  CAS  PubMed  Google Scholar 

  • McCormack E, Braam J (2003) Calmodulins and related potential calcium sensors of Arabidopsis. New Phytol 159:585–598

    Article  CAS  Google Scholar 

  • McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389

    Article  CAS  PubMed  Google Scholar 

  • Mercado JA, Trainotti L, Jiménez-Bermúdez L, Santiago-Doménech N, Posé S, Donolli R, Barceló M, Casadoro G, Pliego-Alfaro F, Quesada MA (2010) Evaluation of the role of the endo-β-(1,4)-glucanase gene FaEG3 in strawberry fruit softening. Postharvest Biol Technol 55:8–14

    Article  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  CAS  PubMed  Google Scholar 

  • Mittler R (2016) ROS are good. Trends Plant Sci 22:11–19

    Article  PubMed  Google Scholar 

  • Mittler R, Herr EH, Orvar BL, van Camp W, Wilikens H, Inzé D, Ellis BE (1999) Transgenic tobacco plants with reduced capability to detoxify reactive oxygen intermediates are hyperresponsive to pathogen infection. Proc Natl Acad Sci USA 96:14165–14170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Nürnberger T, Brunner F, Kemmerling B, Piater L (2004) Innate immunity in plants and animals: striking similarities and obvious differences. Immunol Rev 198:249–266

    Article  PubMed  Google Scholar 

  • O’Brien JA, Daudi A, Finch P, Butt VS, Whitelegg JP, Souda P, Ausubel FM, Bolwell G (2012) A Peroxidase-dependent apoplastic oxidative burst in cultured Arabidopsis cells functions in MAMP-elicited defense. Plant Physiol 158:2013–2027

    Article  PubMed  PubMed Central  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real time RT-PCR. Nucleic Acids Res 29:45

    Article  Google Scholar 

  • Ramakers C, Ruijter JM, Deprez RHL, Moorman AF (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339:62–66

    Article  CAS  PubMed  Google Scholar 

  • Rose JKC, Braam J, Fry SC, Nishitani K (2002) The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: current perspectives and a new unifying nomenclature. Plant Cell Physiol 43:1421–1435

    Article  CAS  PubMed  Google Scholar 

  • Saidi I, Ammar S, Demont-Caulet N, Thévenin J, Lapierre C, Bouzid S, Jouanin L (2010) Thigmomorphogenesis in Solanum lycopersicum. Plant Signal 5:122–125

    Article  CAS  Google Scholar 

  • Salazar SM, Castagnaro AP, Arias ME, Chalfoun NR, Tonello U, Díaz-Ricci JC (2007) Induction of a defense response in strawberry mediated by an avirulent strain of Colletotrichum. Eur J Plant Pathol 117:109–122

    Article  Google Scholar 

  • Scurfield G (1973) Reaction wood: its structure and function. Science 179:647–655

    Article  CAS  PubMed  Google Scholar 

  • Solovyev VV (2007) Statistical approaches in eukaryotic gene prediction. In: Balding D, Canning C, Bishop M (eds) Handbook of statistical genetics. Wiley-Interscience

  • Thomma BPHJ, Eggermont K, Penninckx IAMA, Mauch-Mani B, Vogelsang R, Cammue BPA, Broekaert WF (1998) Separate jasmonate-dependent and salicylate-dependent defense-response pathways in Arabidopsis are essential for resistance to distinct microbial pathogens. Proc Natl Acad Sci USA 95:15107–15111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thordal-Christensen H, Zhang Z, Wei Y, Collinge DB (1997) Subcellular localization of H2O2 in plants H2O2 accumulation in papillae and hypersensitive response during the barley—powdery mildew interaction. Plant J 11:1187–1194

    Article  CAS  Google Scholar 

  • Torres MA (2010) ROS in biotic interactions. Physiol Plantarum 138:414–429

    Article  CAS  Google Scholar 

  • Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Jones JDG, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Loon LC (1997) Induced resistance in plants and the role of pathogenesis-related proteins. Eur J Plant Pathol 103:753–765

    Article  Google Scholar 

  • van Kan JA (2006) Licensed to kill: the lifestyle of a necrotrophic plant pathogen. Trends Plant Sci 11:247–253

    Article  PubMed  Google Scholar 

  • Van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Van Loon LC, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Walters DR, Cowley T, Weber H (2006) Rapid accumulation of trihydroxy oxylipins and resistance to the bean rust pathogen Uromyces fabae following wounding in Vicia faba. Ann Bot 97:779–784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:131–151

    Article  Google Scholar 

  • Wang SL, Liu CP, Liang TW (2012) Fermented and enzymatic production of chitin/chitosan oligosaccharides by extracellular chitinases from Bacillus cereus TKU027. Carbohydr Polym 90:1305–1313

    Article  CAS  PubMed  Google Scholar 

  • Willekens H, Chamnongpol S, Davey M, Schraudner M, Langebartels C, Van Montagu M, Inzé D, Van Camp W (1997) Catalase is a sink for H2O2 and is indispensable for stress defence in C-3 plants. EMBO J 16:4806–4816

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Williamson B, Tudzynski B, Tudzynski P, van Kan JAL (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580

    Article  CAS  PubMed  Google Scholar 

  • Wilson BF, Archer RR (1977) Reaction wood—induction and mechanical action. Ann Rev Plant Physiol 28:23–43

    Article  Google Scholar 

  • Xu W, Purugganan MM, Polisensky DH, Antosiewicz DM, Fry SC, Braam J (1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7:1555–1567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yahraus T, Chandra S, Legendre L, Low PS (1995) Evidence for a mechanically induced oxidative burst. Plant Physiol 109:1259–1266

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao HC, Zhao H, Wang JB, Wang BC, Wang YN (2005) Stress stimulation induced resistance of plant. Coll Surf B Biointerfaces 43:174–178

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This paper was partially supported with grants of the Universidad Nacionál de Tucumán (PIUNT 26/D544), and Agencia Nacionál de Promoción Científica y Tecnológica (PICT 2013–2075). Authors are grateful to Banco de Germoplasma (BGA) from Universidad Nacionál de Tucumán (UNT) and Ing. Cecilia Lemme for providing strawberry plants.

Author information

Author notes

  1. Rodrigo Hernán Tomas-Grau and Fernando José Requena-Serra contributed equally to this work.

Authors and Affiliations

  1. Instituto Superior de Investigaciones Biológicas (INSIBIO), CONICET-UNT, and Instituto de Química Biológica “Dr. Bernabé Bloj”, Facultad de Bioquímica, Química y Farmacia, UNT, Chacabuco 461, T4000ILI, San Miguel de Tucumán, Argentina

    Rodrigo Hernán Tomas-Grau, Fernando José Requena-Serra, Verónica Hael-Conrad, Martín Gustavo Martínez-Zamora, María Fernanda Guerrero-Molina & Juan Carlos Díaz-Ricci

Authors
  1. Rodrigo Hernán Tomas-Grau
    View author publications

    Search author on:PubMed Google Scholar

  2. Fernando José Requena-Serra
    View author publications

    Search author on:PubMed Google Scholar

  3. Verónica Hael-Conrad
    View author publications

    Search author on:PubMed Google Scholar

  4. Martín Gustavo Martínez-Zamora
    View author publications

    Search author on:PubMed Google Scholar

  5. María Fernanda Guerrero-Molina
    View author publications

    Search author on:PubMed Google Scholar

  6. Juan Carlos Díaz-Ricci
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Juan Carlos Díaz-Ricci.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Eugenio Benvenuto.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 69 KB)

Supplementary material 2 (DOCX 334 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tomas-Grau, R.H., Requena-Serra, F.J., Hael-Conrad, V. et al. Soft mechanical stimulation induces a defense response against Botrytis cinerea in strawberry. Plant Cell Rep 37, 239–250 (2018). https://doi.org/10.1007/s00299-017-2226-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-017-2226-9

Keywords