Skip to main content

Advertisement

SpringerLink
Log in

Enhanced Tolerance to Cold in Common Bean Treated with Biostimulant

Verbesserte Kältetoleranz bei mit Biostimulans behandelten Bohnen

  • Original Article / Originalbeitrag
  • Published:
Gesunde Pflanzen Aims and scope Submit manuscript

An Erratum to this article was published on 07 January 2021

This article has been updated

Abstract

Plants exposed to suboptimal temperatures suffer damage to physiological processes, growth, development and yield. Acting as enhancers of physiological and metabolic performance of plants, biostimulants have been used to mitigate crop damage caused by abiotic stresses. This study aimed to determine which formulation and dosage of FH Attivus® biostimulant have the best effects on the development of bean plants exposed to suboptimal temperatures (<20 °C). The experiment was conducted in a greenhouse under suboptimal temperatures in a randomized block design with four replications and ten treatments, consisting of three formulations and dosages of the biostimulant, applied at V4 stage, besides a control without biostimulant application. Growth, physiological and biochemical variables were evaluated. The application of biostimulant made bean plants more tolerant to low temperatures by maintaining CO2 net assimilation rate (A) and increasing the activity of antioxidant enzymes. The relative chlorophyll content (SPAD index), PSII effective quantum yield of linear electron flux (ϕPSII), apparent electron transport rate (ETR) and photochemical extinction coefficient (qP) were higher in all treatments compared to the control, as well as the lowest values of A and ETR were observed in the control. In addition, the activities of all evaluated antioxidant enzymes were superior to the control at the lowest dosages of formulation 2, and at all dosages of formulation 3, indicating, in these treatments, greater protection of cells against oxidative damage. The use of biostimulant is, therefore, a management that makes plants less susceptible to low temperatures in the growing environment.

Zusammenfassung

Pflanzen, die suboptimalen Temperaturen ausgesetzt sind, erleiden Schäden bezüglich physiologischer Prozesse, Wachstum, Entwicklung und Ertrag. Biostimulanzien, die als Verstärker der physiologischen und metabolischen Leistung von Pflanzen wirken, wurden verwendet, um Ernteschäden zu mildern, die durch abiotischen Stress verursacht werden. Ziel dieser Studie war es festzustellen, welche Formulierung und Dosierung von FH Attivus® Biostimulans die besten Auswirkungen auf die Entwicklung von Bohnenpflanzen hat, die suboptimalen Temperaturen (<20 °C) ausgesetzt sind. Das Experiment wurde in einem Gewächshaus unter suboptimalen Temperaturen durchgeführt, in einem randomisierten Blockdesign mit vier Wiederholungen und zehn Behandlungen, bestehend aus drei Formulierungen und Dosierungen des Biostimulans, angewendet im Stadium V4, neben einer Kontrolle ohne Biostimulans-Anwendung. Wachstum, physiologische und biochemische Variablen wurden ausgewertet. Die Anwendung von Biostimulanzien machte Bohnenpflanzen toleranter gegenüber niedrigen Temperaturen, indem die CO2-Nettoassimilationsrate (A) aufrechterhalten und die Aktivität von antioxidativen Enzymen erhöht wurde. Der relative Chlorophyllgehalt (SPAD-Index), die PSII-effektive Quantenausbeute des linearen Elektronenflusses (ϕPSII), die scheinbare Elektronentransportrate (ETR) und der photochemische Extinktionskoeffizient (qP) waren bei allen Behandlungen höher als bei der Kontrolle; die niedrigsten Werte von A und ETR wurden bei der Kontrolle beobachtet. Zusätzlich waren die Aktivitäten aller bewerteten antioxidativen Enzyme der Kontrolle bei den niedrigsten Dosierungen der Formulierung 2 und bei allen Dosierungen der Formulierung 3 überlegen, was anzeigt, dass bei diesen Behandlungen die Zellen besser vor oxidativen Schäden geschützt sind. Die Verwendung von Biostimulanzien ist daher ein Vorgehen, das Pflanzen weniger anfällig für niedrige Temperaturen in der Wachstumsumgebung macht.

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

Access this article

Log in via an institution

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

Similar content being viewed by others

Change history

References

  • Albertos P, Wagner K, Poppenberger B (2018) Cold stress signalling in female reproductive tissues. Plant Cell Environ 42:846–853

    PubMed  Google Scholar 

  • Albrecht LP, Braccini AL, Scapim CA, Ávila MR, Albrecht AJP, Barbosa MC (2010) Qualidade das sementes de soja produzidas sob manejo com biorregulador. Rev Bras Sementes 32:39–48

    Google Scholar 

  • Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase, and glutathione reductase during acclimation to chilling in mesocotylus of maize seedlings. Plant Physiol 109:1247–1257

    CAS  PubMed  PubMed Central  Google Scholar 

  • Anjum AS, Ashraf U, Tanveer M, Khan I, Hussain S, Shahzad B, Zohaib A, Abbas F, Saleem MF, Ali I, Wang LC (2017) Drought induced changes in growth, osmolyte accumulation and antioxidant metabolism of three maize hybrids. Front Plant Sci 8:69

    PubMed  PubMed Central  Google Scholar 

  • Ashraf M, Harris PJC (2013) Photosynthesis under stressful environments: an overview. Photosynt 51:163–190

    CAS  Google Scholar 

  • Balouchi H (2010) Screening wheat parents of mapping population for heat and drought tolerance, detection of wheat genetic variation. Int J Biol Life Sci 7:62–72

    Google Scholar 

  • Bhering LL (2017) Rbio: a tool for biometric and statistical analysis using the R platform. Crop Breed Appl Biotechnol 17:187–190

    Google Scholar 

  • Bilger W, Schereiber U, Bock M (1995) Determination of the quantum efficiency of photosystem II and of non-photochemical quenching of chlorophyll fluorescence in the field. Oecol 102:425–432

    Google Scholar 

  • Bloom AJ, Zwieniecki MA, Passioura JВ, Randall LВ, Holbrook NM, Clair DAST (2004) Water relations under root chilling in a sensitive and tolerant tomato species. Plant Cell Environ 27:971–979

    Google Scholar 

  • Bulgari R, Cocetta G, Trivellini A, Vernieri P, Ferrante A (2015) Biostimulants and crop responses: a review. Biol Agric Hortic 31:1–17

    Google Scholar 

  • Bulgari R, Franzoni G, Ferrante A (2019) Biostimulants application in horticultural crops under abiotic stress conditions. Agronomy 9:306

    CAS  Google Scholar 

  • Canellas LP, Façanha AR (2004) Chemical nature of soil humified fractions and their bioactivity. Pesq agropec bras 39:233–240

    Google Scholar 

  • Canellas LP, Olivares FL, Aguiar NO, Jones DL, Nebbioso A, Mazzei P, Piccolo A (2015) Humic and fulvic acids as biostimulants in horticulture. Sci Hortic 196:15–27

    CAS  Google Scholar 

  • Canellas LP, Olivares FL, Okorokova-Façanha AL, Façanha AR (2002) Humic acids isolated from earthworm compost enhance root elongation, lateral root emergence, and plasma membrane H+-ATPase activity in maize roots. Plant Physiol 130:1951–1957

    CAS  PubMed  PubMed Central  Google Scholar 

  • Canellas LP, Teixeira JLRL, Dobbss LB, Silva CA, Medici LO, Zandonadi DB, Façanha AR (2008) Humic acids crossinteractions with root and organic acids. Ann Appl Biol 153:157–166

    CAS  Google Scholar 

  • Chance B, Maehley AC (1955) Assay of catalases and peroxidases. Method Enzymol 2:764–775

    Google Scholar 

  • Cornelissen JHC, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, Steege H, Morgan HD, Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plan functional traits worldwide. Aust J Bot 51:335–380

    Google Scholar 

  • Craigie JS (2011) Seaweed extract stimuli in plant science and agriculture. J Appl Phycol 23:371–393

    CAS  Google Scholar 

  • Di Stasio E, Van Oosten MJ, Silletti S, Raimondi G, Dell’Aversana E, Carillo P, Maggio A (2018) Ascophyllum nodosum-based algal extracts act as enhancers of growth, fruit quality, and adaptation to stress in salinized tomato plants. J Appl Phycol 30:2675–2686

    Google Scholar 

  • Fracheboud Y, Jompuk C, Ribaut JM, Stamp P, Leipner J (2004) Genetic analysis of cold-tolerance of photosynthesis in maize. Plant Mol Biol 56(2):241–253

    CAS  PubMed  Google Scholar 

  • Friesen PC, Sage RF (2016) Photosynthetic responses to chilling in a chilling-tolerant and chilling-sensitive Miscanthus hybrid. Plant Cell Environ 39:1420–1431

    CAS  PubMed  Google Scholar 

  • Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92

    CAS  Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiol 59:309–314

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gogoi N, Farooq M, Barthakur S, Baroowa B, Paul S, Bharadwaj N, Ramanjulu S (2018) Thermal stress impacts on reproductive development and grain yield in grain legumes. J Plant Biol 61:265–291

    CAS  Google Scholar 

  • Gomes-Junior RA, Moldes CA, Delite FS, Pompeu GB, Gratão PL, Mazzafera P, Lea PJ, Azevedo RA (2006) Antioxidant metabolism of coffee cell suspension cultures in response to cadmium. Chemosphere 65:1330–1337

    CAS  PubMed  Google Scholar 

  • Goñi O, Quille P, O’Connell S (2018) Ascophyllum nodosum extract biostimulants and their role in enhancing tolerance to drought stress in tomato plants. Plant Physiol Biochem 126:63–73

    PubMed  Google Scholar 

  • Gusta LV, Wisniewski M (2013) Understanding plant cold hardiness: an opinion. Physiol Plantarum 147:4–14

    CAS  Google Scholar 

  • Hao L, Guo L, Li R, Cheng Y, Huang L, Zhou H, Xu M, Li F, Zhang X, Zheng Y (2019) Responses of photosynthesis to high temperature stress associated with changes in leaf structure and biochemistry of blueberry (Vaccinium corymbosum L.). Sci Hortic 246:251–264

    CAS  Google Scholar 

  • Hatami E, Shokouhian AA, Ghanbari AR, Naseri LA (2018) Alleviating salt stress in almond rootstocks using of humic acid. Sci Hortic 237:296–302

    CAS  Google Scholar 

  • Havir EA, Mchale NA (1987) Biochemical and developmental characterization of multiple forms of catalase in tobacco leaves. Plant Physiol 84:450–455

    CAS  PubMed  PubMed Central  Google Scholar 

  • Heath RL, Packer L (1968) Photoperoxidation in isolated chloroplast: I. Kinetics and stoichiometry of fatty acid peroxidation. Arch Biochem Biophys 125:189–198

    CAS  PubMed  Google Scholar 

  • Heinemann AB, Ramirez-Villegas J, Souza TLPO, Didonet AD, di Stefano JG, Boote KJ, Jarvis A (2016) Drought impact on rainfed common bean production areas in Brazil. Agric Forest Meteorol 225:57–74

    Google Scholar 

  • Hojati M, Modarres-Sanavy SAM, Karimi M, Ghanati F (2011) Responses of growth and antioxidant systems in Carthamus tinctorius L. under water deficit stress. Acta Physiol Plant 33:105–112

    Google Scholar 

  • Hu T, Wang Y, Wang Q, Dang N, Wang L, Liu C, Zhu J, Zhan X (2019) The tomato 2‑oxoglutarate-dependent dioxygenase gene SlF3HL is critical for chilling stress tolerance. Hortic Res 6:45

    PubMed  PubMed Central  Google Scholar 

  • Hussain HA, Hussain S, Khaliq A, Ashraf U, Anjum SA, Men S, Wang L (2018) Chilling and Drought Stresses in Crop Plants: Implications, Cross Talk, and Potential Management Opportunities. Front Plant Sci 9

  • du Jardin P (2015) Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic 196:3–14

    Google Scholar 

  • Jithesh MN, Shukla PS, Kant P, Joshi J, Critchley AT, Prithiviraj B (2019) Physiological and transcriptomics analyses reveal that Ascophyllum nodosum extracts induce salinity tolerance in Arabidopsis by regulating the expression of stress responsive genes. J Plant Growth Regul 38:463–478

    CAS  Google Scholar 

  • Jouyban Z, Hasanzade R, Sharafi S (2013) Chilling stress in plants. Int J Agric Crop Sci 5:2961–2968

    Google Scholar 

  • Kar M, Mishra D (1976) Catalase; peroxidase; and polyphenoloxidase activities during rice leaf senensence. Plant Physiol 57:315–319

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karami-Moalem S, Maali-Amiri R, Kazemi-Shahandashti S (2018) Effect of cold stress on oxidative damage and mitochondrial respiratory properties in chickpea. Plant Physiol Biochem 122:31–39

    CAS  PubMed  Google Scholar 

  • Li X, Wei J, Scott ER, Liu J, Guo S, Li Y, Zhang L, Han W (2018) Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. Molecules 23:165

    PubMed Central  Google Scholar 

  • Liu C, Liu Y, Gui K, Fan D, Li G, Zheng Y, Yu L, Yang R (2011) Effect of drought on pigments; osmotic adjustment and antioxidant enzymes in six woody plant species in karst habitats of southwestern China. Environ Exp Bot 71:174–183

    CAS  Google Scholar 

  • Liu C, Yang X, Yan Z, Fan Y, Feng G, Liu D (2019) Analysis of differential gene expression in cold–tolerant vs. cold–sensitive varieties of snap bean (Phaseolus vulgaris L.) in response to low temperature stress. Genes Genom. https://doi.org/10.1007/s13258-019-00870-2

    Article  Google Scholar 

  • Mathobo R, Marais D, Steyn JM (2017) The effect of drought stress on yield; leaf gaseous exchange and chlorophyll fluorescence of dry beans (Phaseolus vulgaris L.). Agric Water Manag 80:118–125

    Google Scholar 

  • Miura K, Furumoto T (2013) Cold signaling and cold response in plants. Int J Mol Sci 14:5312–5337

    CAS  PubMed  PubMed Central  Google Scholar 

  • Moreira R, Sineiro J, Chenlo F, Arufe S, Díaz-Varela D (2017) Aqueous extracts of Ascophyllum nodosum obtained by ultrasound-assisted extraction: effects of drying temperature of seaweed on the properties of extracts. J Appl Phycol 29:3191–3200

    CAS  Google Scholar 

  • Nair P, Kandasamy S, Zhang J, Ji X, Kirby C, Benkel B, Hodges MD, Critchley AT, Hiltz D, Prithiviraj B (2012) Transcriptional and metabolomic analysis of Ascophyllum nodosum mediated freezing tolerance in Arabidopsis thaliana. BMC Genomics 13:643

    CAS  PubMed  PubMed Central  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-especific peroxidase en spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Van Oosten MJ, Pepe O, De Pascale S, Silletti S, Maggio A (2017) The role of biostimulants and bioeffectors as alleviators of abiotic stress in crop plants. Chem Biol Technol Agric 4:5

    Google Scholar 

  • Pandy P, Srivastava K, Rajpoot R, Rani A, Pandey AK, Dubey RS (2016) Water deficit and aluminum interactive effects on generation of reactive oxygen species and responses of antioxidative enzymes in the seedlings of two rice cultivars differing in stress tolerance. Environ Sci Pollut Res 23:1516–1528

    Google Scholar 

  • Pareek A, Khurana A, Sharma AK, Kumar R (2017) An overview of signaling regulons during cold stress tolerance in plants. Curr Genomics 18:498–511

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pask A, Pietragalla J, Mullan D, Reynolds M (2012) Physiological breeding II: a field guide to wheat phenotyping. CIMMYT, Texcoco

    Google Scholar 

  • Ploschuk EL, Bado LA, Salinas M, Wassner DF, Windauer LB, Insausti P (2014) Photosynthesis and fluorescence responses of Jatropha curcas to chilling and freezing stress during early vegetative stages. Environ Exp Bot 102:18–26

    CAS  Google Scholar 

  • Pokluda R, Sêkara A, Jezdinsk A, Kalisz A, Neugebauerová J, Grabowska A (2016) The physiological status and stress biomarker concentration of Coriandrum sativum L. plants subjected to chilling are modified by biostimulant application. Biol Agric Hortic 32:258–268

    Google Scholar 

  • Rayirath P, Benkel B, Hodges MD, Allan-Wojtas P, MacKinnon S, Critchley AT, Prithiviraj B (2009) Lipophilic components of the brown seaweed, Ascophyllum nodosum, enhance freezing tolerance in Arabidopsis thaliana. Planta 230:135–147

    CAS  PubMed  Google Scholar 

  • Rezende AA, Pacheco MTB, Silva VSN, Ferreira TAPC (2018) Nutritional and protein quality of dry Brazilian beans (Phaseolus vulgaris L.). Food Sci Technol 38:421–427

    Google Scholar 

  • Rihan HZ, Al-Issawi M, Fuller MP (2017) Advances in physiological and molecular aspects of plant cold tolerance. J Plant Interact 12:143–157

    CAS  Google Scholar 

  • Rooy SSB, Salekdeh GH, Ghabooli M, Gholami M, Karimi R (2017) Cold–induced physiological and biochemical responses of three grapevine cultivars differing in cold tolerance. Acta Physiol Plant 39:264

    Google Scholar 

  • Rouphael Y, Colla G (2018) Synergistic biostimulatory action: designing the next generation of plant biostimulants for sustainable agriculture. Front Plant Sci 9:1655

    PubMed  PubMed Central  Google Scholar 

  • Ruban AV, Johnson MP, Duffy CDP (2012) The photoprotective molecular switch in the photosystem II antenna. Biochem Biophys Acta 1817:167–181

    CAS  PubMed  Google Scholar 

  • Saeger JD, Praet SV, Vereecke D, Park J, Jacques S, Han T, Depuydt S (2019) Toward the molecular understanding of the action mechanism of Ascophyllum nodosum extracts on plants. J Appl Phycol. https://doi.org/10.1007/s10811-019-01903-9

    Article  Google Scholar 

  • Santaniello A, Scartazza A, Gresta F, Loreti E, Biasone A, Di Tommaso D, Piaggesi A, Perata P (2017) Ascophyllum nodosum seaweed extract alleviates drought stress in Arabidopsis by affecting photosynthetic performance and related gene expression. Front Plant Sci 8:1362

    PubMed  PubMed Central  Google Scholar 

  • Schreiber U, Klughammer C, Kolbowski J (2012) Assessment of wavelength-dependent parameters of photosynthetic electron transport with a new type of multi-color PAM chlorophyll fluorometer. Photos Res 113:127–144

    CAS  Google Scholar 

  • Shukla PS, Mantin EG, Adil M, Bajpai S, Critchley AT, Prithiviraj B (2019) Ascophyllum nodosum-based biostimulants: sustainable applications in agriculture for the stimulation of plant growth, stress tolerance, and disease management. Front Plant Sci 10:655

    PubMed  PubMed Central  Google Scholar 

  • Snider JL, Collins GD, Whitaker J, Perry CD, Chastain DR (2014) Electron transport through photosystem II is not limited by a wide range of water deficit conditions in field-grown Gossypium hirsutum. J Agron Crop Sci 200:77–82

    CAS  Google Scholar 

  • Sofo A, Scopa A, Nuzzaci M, Vitti A (2015) Ascorbate peroxidase and catalase activities and their genetic regulation in plants subjected to drought and salinity stresses. Int J Mol Sci 16:13561–13578

    CAS  PubMed  PubMed Central  Google Scholar 

  • Soliman MH, Alayafi AAM, Kelish AAE, Abu-Elsaoud AM (2018) Acetylsalicylic acid enhance tolerance of Phaseolus vulgaris L. to chilling stress, improving photosynthesis, antioxidants and expression of cold stress responsive genes. Bot Stud 59:6. https://doi.org/10.1186/s40529-018-0222-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wijewardana C, Henry WB, Hock MW, Reddy KR (2016) Growth and physiological trait variation among corn hybrids for cold tolerance. Can J Plant Sci 96:639–656

    CAS  Google Scholar 

  • Yakhin OI, Lubyanov AA, Yakhin IA, Brown PH (2017) Biostimulants in plant science: a global perspective. Front Plant Sci 7:2049

    PubMed  PubMed Central  Google Scholar 

  • Zandonadi DB, Santos MP, Dobbss LB, Olivares FL, Canellas LP, Binzel ML, Okorokova-Façanha AL, Façanha AR (2010) Nitric oxide mediates humic acids-induced root development and plasma membrane H+-ATPase activation. Planta 231:1025–1036

    CAS  PubMed  Google Scholar 

  • Zhang J, Liub J, Yangc C, Dud S, Yang W (2016) Photosynthetic performance of soybean plants to water deficit under high and low light intensity. S Afr J Bot 105:279–287

    CAS  Google Scholar 

  • Žydelis R, Weihermüller L, Herbst M, Klosterhalfen A, Lazauskas S (2018) A model study on the effect of water and cold stress on maize development under nemoral climate. Agric For Meteorol 263:169–179

    Google Scholar 

Download references

Acknowledgements

We thank the Coordination for the Improvement of Higher Education Personnel (CAPES) for doctoral scholarships granted to the first and second authors and for a master in science scholarship granted to the fourth author. Also to the National Council for Scientific and Technological Development (CNPq, Brazil) through “Productivity in Research” fellowship granted to the last author (Proc. 305952/2018-8).

Author information

Authors and Affiliations

  1. School of Agricultural Sciences, Laboratory of Ecophysiology Applied to Agriculture, Department of Crop Production, São Paulo State University (UNESP), Botucatu, Brazil

    Vanessa do Rosário Rosa, Anna Luiza Farias dos Santos, Mariana Peduti Vicentini Sab & Marcelo de Almeida Silva

  2. Federal Goianian Institute (IF Goiano), Laboratory of Ecophysiology and Crop Production, Rio Verde, Brazil

    Adinan Alves da Silva

  3. Fertilizantes Heringer S.A., Paulínia, Brazil

    Flávio Barcellos Cardoso & Mario Antonio Marin

Authors
  1. Vanessa do Rosário Rosa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anna Luiza Farias dos Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Adinan Alves da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mariana Peduti Vicentini Sab
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Flávio Barcellos Cardoso
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mario Antonio Marin
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcelo de Almeida Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Marcelo de Almeida Silva.

Ethics declarations

Conflict of interest

V. do Rosário Rosa, A.L. Farias dos Santos, A. Alves da Silva, M. Peduti Vicentini Sab, F. Barcellos Cardoso, M.A. Marin and M. de Almeida Silva declare that they have no competing interests.

Additional information

The original online version of this article was revised: There was an error in the author order. The correct order is given in the author line above.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

do Rosário Rosa, V., Farias dos Santos, A.L., Alves da Silva, A. et al. Enhanced Tolerance to Cold in Common Bean Treated with Biostimulant. Gesunde Pflanzen 73, 39–50 (2021). https://doi.org/10.1007/s10343-020-00526-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10343-020-00526-2

Keywords

Schlüsselwörter

Search

Navigation