Skip to main content
SpringerLink
Log in

Physiological and biochemical responses of soybean to white mold affected by manganese phosphite and fluazinam

  • Original Article
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

Abstract

White mold, caused by Sclerotinia sclerotiorum, is one of the most important diseases affecting soybean and its control has been difficult to achieve. This study aimed to investigate the potential of manganese (Mn) phosphite and fluazinam in protecting soybean plants against S. sclerotiorum infection by examining the photosynthetic performance (leaf gas exchange and chlorophyll (Chl) a fluorescence parameters), activities of defense enzymes [chitinase (CHI), β-1,3-glucanase (GLU), phenylalanine ammonia-lyase (PAL), and polyphenol oxidase (PPO)] as well as those related to the antioxidant metabolism (superoxide dismutase (SOD), catalase (CAT), peroxidase (POX), and ascorbate peroxidase (APX)) and the concentrations of hydrogen peroxide (H2O2), superoxide (O2−), and malondialdehyde (MDA). White mold development was completely inhibited by fluazinam. Soybean metabolism was not changed by fluazinam. White mold severity was significantly reduced on plants sprayed with Mn phosphite, which showed a better photosynthetic performance than the non-sprayed plants. Mycelial growth of S. sclerotiorum was inhibited by Mn phosphite. Activities of CAT, POX, and SOD decreased while CHI, GLU, and PAL activities increased at 96 hai for Mn phosphite-sprayed plants compared to non-sprayed plants. In conclusion, Mn phosphite affected white mold development and pathogen-induced physiological impairments in soybean leaflets due to its dual mode of action.

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Araujo L, Valdebenito-Sanhueza RM, Stadnik MJ (2010) Avaliação de formulações de fosfito de potássio sobre Colletotrichum gloeosporioides in vitro e no controle pós-infeccional da mancha foliar de Glomerella em macieira. Trop Plant Pathol 35:54–59

    Article  Google Scholar 

  • Araujo L, Bispo WMS, Rios VS, Fernandes SA, Rodrigues FA (2015) Induction of the phenylpropanoid pathway by acibenzolar-S-methyl and potassium phosphite increases mango resistance to Ceratocystis fimbriata infection. Plant Dis 99:447–459

    Article  CAS  PubMed  Google Scholar 

  • Bae YS, Knudsen GR (2007) Effect of sclerotial distribution pattern of Sclerotinia sclerotiorum on biocontrol efficacy of Trichoderma harzianum. Appl Soil Ecol 35:21–24

    Article  Google Scholar 

  • Bateman DF, Beer SV (1965) Simultaneous production and synergistic action of oxalic acid and polygalacturonase during pathogenesis by Sclerotium rolfsii. Phytopathology 55:204–211

    CAS  PubMed  Google Scholar 

  • Bermúdez-Cardona MB, Wordell Filho JA, Rodrigues FA (2015) Leaf gas exchange and chlorophyll a fluorescence in maize leaves infected with Stenocarpella macrospora. Phytopathology 105:26–34

    Article  PubMed  CAS  Google Scholar 

  • Bock CH, Brenneman TB, Hotchkiss MW, Wood BW (2013) Evaluation of a phosphite fungicide to control pecan scab in the southeastern USA. Crop Prot 36:58–64

    Article  CAS  Google Scholar 

  • Boland GJ, Hall R (1987) Evaluating soybeans cultivars for resistance to Sclerotinia sclerotiorum under field conditions. Plant Dis 71:934–936

    Article  Google Scholar 

  • Brackmann A, Giehl RFH, Sestari I, Steffens CA (2004) Fosfitos para o controle de podridões pós-colheita em maçãs ‘Fuji’ durante o armazenamento refrigerado. Cienc Rural 34:1039–1042

    Article  Google Scholar 

  • Bradford MN (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bu JW, Yao G, Gao HY, Jia YJ, Zhang LT, Cheng DD, Wang X (2009) Inhibition mechanism of photosynthesis in cucumber leaves infected by Sclerotinia sclerotiorum (Lib.) de Bary. Acta Phytopathol Sinc 39:613–621

    Google Scholar 

  • Cakmak I, Horst WJ (1991) Effect of aluminum on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83:463–468

    Article  CAS  Google Scholar 

  • Carmona MA, Simonetti E, Ravotti ME, Scandiani MM, Luque AG, Formento NA, Sautua FJ (2017) In vitro antifungal/fungistatic activity of manganese phosphite against soybean soil-borne pathogens. Phyton Int J Exp Bot 85:265–269

    Google Scholar 

  • Cerqueira A, Alves A, Berenguer H, Correia B, Gómez-Cadenas A, Diez JJ, Monteiro P, Pinto G (2017) Phosphite shifts physiological and hormonal profile of Monterey pine and delays Fusarium circinatum progression. Plant Physiol Biochem 114:88–99

    Article  CAS  PubMed  Google Scholar 

  • Chaitanya KSK, Naithani SC (1994) Role of superoxide lipid peroxidation and superoxide dismutase in membrane perturbation during loss of viability in seeds of Shorea robusta Gaertn.f. New Phytol 126:623–627

    Article  CAS  Google Scholar 

  • Christensen TH, 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  Google Scholar 

  • Clark RB (1975) Characterization of phosphates in intact maize roots. J Agric Food Chem 23:458–460

    Article  CAS  PubMed  Google Scholar 

  • Conrath U, Pieterse CMJ, Mauch-Mani B (2002) Priming in plant-pathogen interactions. Trends Plant Sci 7:210–216

    Article  CAS  PubMed  Google Scholar 

  • Costa BHG, Resende MLV, Monteiro ACA, Junior PMR, Botelho DMS, Silva BM (2018) Potassium phosphites in the protection of common bean plants against anthracnose and biochemical defence responses. J Phytopathol 166:95–102

    Article  CAS  Google Scholar 

  • Dalio RJD, Fleischmann F, Humez M, Oswald W (2014) Phosphite protects Fagus sylvatica seedlings towards Phytophthora plurivora via local toxicity, priming and facilitation of pathogen recognition. PLoS One 9:e87860

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Daniel R, Guest D (2006) Defense responses induced by potassium phosphonate in Phytophthora palmivora-challenged Arabidopsis thaliana. Physiol Mol Plant Pathol 67:194–201

    Article  CAS  Google Scholar 

  • Debona D, Rodrigues FA, Rios JA, Martins SC, Pereira LF, DaMatta FM (2014) Limitations to photosynthesis in leaves of wheat plants infected by Pyricularia oryzae. Phytopathology 104:34–39

    Article  CAS  PubMed  Google Scholar 

  • Debona D, Nascimento KJT, Gomes JGO, Aucique-Pérez CE, Rodrigues FA (2016) Physiological changes promoted by a strobilurin fungicide in the rice-Bipolaris oryzae interaction. Pest Biochem Physiol 10:8–16

    Article  CAS  Google Scholar 

  • Dianese AL, Blum LEB, Dutra JB, Lopes LF (2009) Aplicação de fosfito de potássio, cálcio ou magnésio para a redução da podridão-do-pé do mamoeiro em casa de vegetação. Cienc Rural 29:2309–2314

    Article  Google Scholar 

  • Doke N, Miura Y, Sanchez LM, Park HJ, Noritake T, Yoshioka H, Kawakita K (1996) The oxidative burst protects plants against pathogen attack: mechanism and role as an emergency signal for plant biodefence. Gene 179:45–51

    Article  CAS  PubMed  Google Scholar 

  • Fagundes-Nacarath IRF, Debona D, Brás VV, Silveira PR, Rodrigues FA (2018) Phosphites attenuate Sclerotinia sclerotiorum-induced physiological impairments in common bean. Acta Physiol Plant 40:198

    Article  CAS  Google Scholar 

  • Fehr WR, Caviness CE, Burmood DT, Pennington JS (1971) Stage of development descriptions for soybeans, Glycine max (L.) Merrill. Crop Sci 11:929–931

    Article  Google Scholar 

  • Fortunato AA, Debona D, Bernadeli AMA, Rodrigues FA (2015a) Changes in the antioxidant system in soybean leaves infected by Corynespora cassiicola. Phytopathology 105:1050–1058

    Article  CAS  PubMed  Google Scholar 

  • Fortunato AA, Debona D, Bernardeli AMA, Rodrigues FA (2015b) Defence-related enzymes in soybean resistance to target spot. J Phytopathol 163:731–742

    Article  CAS  Google Scholar 

  • Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220

    Article  CAS  PubMed  Google Scholar 

  • Guimarães RL, Stotz HU (2004) Oxalate production by Sclerotinia sclerotiorum deregulates guard cells during infection. Plant Physiol 136:3703–3711

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Guo X, Stotz H (2010) ABA signaling inhibits oxalate-induced production of reactive oxygen species and protects against Sclerotinia sclerotiorum in Arabidopsis thaliana. Eur J Plant Pathol 128:7–19

    Article  CAS  Google Scholar 

  • Guo Z, Miyoshi H, Kimyoji T, Haga T, Fujita T (1991) Uncoupling activity of a newly developed fungicide, fluazinam [3-chloro-N-(3-chloro-2,6-dinitro-4-trifluoromethylphenyl)-5-trifluoromethyl-2-pyridinamine]. Biochim Biophys Acta Bioenerg 1056:89–92

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Heffer Link V, Johnson KB (2007) White mold: the plant health instructor. http://www.apsnet.org/edcenter/intropp/lessons/fungi/ascomycetes/Pages/WhiteMold.aspx. Accessed 9 June 2018

  • Hegedus DD, Rimmer SR (2005) Sclerotinia sclerotiorum: when to be or not to be a pathogen? FEMS Microbiol Lett 251:177–184

    Article  CAS  PubMed  Google Scholar 

  • Kim HS, Diers BW (2014) Inheritance of partial resistance to Sclerotinia stem rot in soybean. Crop Sci 40:55–61

    Article  Google Scholar 

  • Klughammer C, Schreiber U (2008) Complementary PSII quantum yield calculated from simple fluorescence parameters measured by PAM fluorometry and saturation pulse method. PAM Appl Notes 1:27–35

    Google Scholar 

  • Lehner MS, Paula Junior TJ, Silva RA, Vieira RF, Carneiro JES, Schnabel G, Mizubuti ESG (2015) Fungicide sensitivity of Sclerotinia sclerotiorum: a thorough assessment using discriminatory dose, EC50, high-resolution melting analysis, and description of new point mutation associated with thiophanate-methyl resistance. Plant Dis 99:1537–1543

    Article  CAS  PubMed  Google Scholar 

  • Lehner MS, Pethybridge SJ, Meyer MC, Del Ponte EM (2017) Meta-analytic modelling of the incidence-yield and incidence-sclerotial production relationships in soybean white mould epidemics. Plant Pathol 66:460–468

    Article  Google Scholar 

  • Lobato MC, Olivieri FP, Daleo GR, Andreu AB (2010) Antimicrobial activity of phosphites against different potato pathogens. J Plant Dis Protec 117:102–109

    Article  CAS  Google Scholar 

  • Machinandiarena MF, Lobato MC, Feldman ML, Daleo GR, Andreu AB (2012) Potassium phosphite primes defense responses in potato against Phytophthora infestans. J Plant Physiol 149:1417–1424

    Article  CAS  Google Scholar 

  • Malenčić DL, Kiprovski B, Popović M, Prvulović D, Miladinović J, Djordjević V (2010) Changes in antioxidant systems in soybean as affected by Sclerotinia sclerotiorum (Lib.) de Bary. Plant Physiol Biochem 48:903–908

    Article  PubMed  CAS  Google Scholar 

  • Mandal S, Mitra A, Mallick N (2008) Biochemical characterization of oxidative burst during interaction between Solanum lycopersicum and Fusarium oxysporum f. sp. lycopersici. Physiol Mol Plant Pathol 72:56–61

    Article  CAS  Google Scholar 

  • McCrearya CM, Depuydta D, Vynb RJ, Gillars CL (2016) Fungicide efficacy of dry bean white mold [Sclerotinia sclerotiorum(Lib.) de Bary, causal organism] and economic analysis at moderate to high disease pressure. Crop Prot 82:75–81

    Article  CAS  Google Scholar 

  • Meyer MC, Campos HD, Godoy CV, Utiamada CM (2014) Ensaios cooperativos de controle químico de mofo branco na cultura da soja: safras 2009 a 2012. https://www.infoteca.cnptia.embrapa.br/bitstream/doc/985018/1/Ensaioscooperativosdecontrolequimicodemofobranconaculturadasojasafras2009a2012.pdf. Accessed 15 July 2018

  • Mueller DS, Dorrance AE, Derksen RC, Ozkan E, Kurle JE, Grau CR, Gaska JM, Hartman GL, Bradley CA, Pedersen WL (2002) Efficacy of fungicides on Sclerotinia sclerotiorum and their potential for control of Sclerotinia stem rot on soybean. Plant Dis 86:26–31

    Article  CAS  PubMed  Google Scholar 

  • Mueller DS, Bradley C, Chilvers M, Esker P, Malvick D, Peltier A, Sisson A, Wise K (2015) White mold: Soybean Disease Management. Crop Protection Network, 1005: [http://www.ncsrp.com/pdf_doc/WhiteMold_CPN1005_2015.pdf. Accessed 10 June 2018

  • Nascimento KJT, Araujo L, Resende RS, Schurt DA, Silva WL, Rodrigues FA (2016) Silicon, acibenzolar-S-methyl and potassium phosphite in the control of brown spot in rice. Bragantia 75:212–221

    Article  CAS  Google Scholar 

  • Nojosa GBA, Resende MLV, Barguil BM, Moraes SRG, Vilas Boas CH (2009) Efeito de indutores de resistência em cafeeiro contra a mancha de Phoma. Summa Phytopathol 35:60–62

    Article  Google Scholar 

  • Panicker S, Gangadharam K (1999) Controlling downy mildew of maize caused by Peronosclerospora sorghi by foliar sprays of phosphonic acid compounds. Crop Protec 18:115–118

    Article  CAS  Google Scholar 

  • Peruch LAM, Brunna ED (2008) Relação entre doses de calda bordalesa e de fosfito potássio na intensidade do míldio e na produtividade da videira cv. ‘Goethe’. Cienc Rural 38:2413–2418

    Article  CAS  Google Scholar 

  • Perveen K, Haseen A, Shukla PK (2010) Effect of Sclerotinia sclerotiorum on the disease development, growth, oil yield and biochemical changes in plants of Mentha arvensis. Saudi J Biol Sci 17:291–294

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinto KMS, Nascimento LC, Gomes ECS, Silva HF, Miranda JR (2012) Efficiency of resistance elicitors in the management of grapevine downy mildew Plasmopara viticola: epidemiological, biochemical and economic aspects. Eur J Plant Pathol 134:745–754

    Article  Google Scholar 

  • Rios JA, Rios VS, Aucique-Pérez CE, Cruz MFA, Morais LE, DaMatta FM, Rodrigues FA (2017) The photosynthetic performance and source-sink relationships are altered on wheat plants infected by Pyricularia oryzae. Plant Pathol 66:1496–1507

    Article  CAS  Google Scholar 

  • Ryals J, Uknes S, Wars E (1994) Systemic acquired resistance. Plant Physiol 104:1109–1112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simonetti E, Viso NP, Montecchia M, Zilli C, Balestrasse K, Carmona M (2015) Evaluation of native bacteria and manganese phosphite for alternative control of charcoal root rot of soybean. Microbiol Res 180:40–48

    Article  CAS  PubMed  Google Scholar 

  • Smillie R, Grant BR, Guest D (1989) The mode of action of phosphite: evidence for both direct and indirect modes of action on three Phytophthora spp. in plants. Phytopathology 79:921–926

    Article  CAS  Google Scholar 

  • Sumida CH, Canteri MG, Peitil DC, Tibolla F, Orsini IP, Araujo FA, Chagas DF, Calvos NS (2015) Chemical and biological control of Sclerotinia stem rot in the soybeans crop. Cienc Rural 45:760–766

    Article  CAS  Google Scholar 

  • Tariq VN, Jeffries P (1985) Changes occurring in chloroplasts of Phaseolus following infection by Sclerotinia: a cytochemical study. J Cell Sci 75:195–295

    Article  CAS  PubMed  Google Scholar 

  • Vallad GE, Goodman RM (2004) Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44:1920–1934

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB (2011) Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. Plos Pathog 7:e1002107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144:307–313

    Article  CAS  Google Scholar 

  • Xavier SA, Koga LJ, Barros DCM, Canteri MG, Lopes ION, Godoy CV (2015) Variação da sensibilidade de populações de Phakopsora pachyrhizi a fungicidas inibidores da desmetilação no Brasil. Summa Phytopathol 41:191–196

    Article  Google Scholar 

  • Yang XB, Lundeen P, Uphoff MD (1999) Soybean varietal response and yield loss caused by Sclerotinia sclerotiorum. Plant Dis 83:456–461

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Zhang Z, Gao H, Liu M, Fan X (2014) Mechanisms by which the infection of Sclerotinia sclerotiorum (Lib.) de Bary affects the photosynthetic performance in tobacco leaves. BMC Plant Biol 14:1–11

    Article  Google Scholar 

  • Zhou J, Sun A, Xing D (2013) Modulation of cellular redox status by thiamine-activated NADPH oxidase confers Arabidopsis resistance to Sclerotinia sclerotiorum. J Exp Bot 64:3261–3272

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Prof. Fabrício A. Rodrigues thanks the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq) for his research fellowship. This study was supported by grants from CAPES, CNPq, and FAPEMIG to Prof. Rodrigues. This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001.

Author information

Authors and Affiliations

  1. Laboratório da Interação Planta-Patógeno, Departamento de Fitopatologia, Universidade Federal de Viçosa, Viçosa, Minas Gerais State, 36570-900, Brazil

    M. I. C. Novaes, D. Debona, I. R. F. Fagundes-Nacarath, V. V. Brás & F. A. Rodrigues

Authors
  1. M. I. C. Novaes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. D. Debona
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. I. R. F. Fagundes-Nacarath
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. V. V. Brás
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. F. A. Rodrigues
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to F. A. Rodrigues.

Additional information

Communicated by E. Kuzniak-Gebarowska.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Novaes, M.I.C., Debona, D., Fagundes-Nacarath, I.R.F. et al. Physiological and biochemical responses of soybean to white mold affected by manganese phosphite and fluazinam. Acta Physiol Plant 41, 186 (2019). https://doi.org/10.1007/s11738-019-2976-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11738-019-2976-9

Keywords

Search

Navigation