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Physiological and biophysical alterations in maize plants caused by Colletotrichum graminicola infection verified by OJIP study

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Abstract

Anthracnose caused by Colletotrichum graminicola (Ces.) Wils is among the most aggressive maize diseases worldwide, considerably hindering crop productivity. To investigate the responses underlying the host–pathogen interaction involved in anthracnose infection, we conducted two field experiments in some of the main grain producing areas of the State of Tocantins, in Brazil. Four maize hybrids (with differential tolerance to C. graminicola) were sown in February and March, 2017. Chlorophyll fluorescence measures were performed according to the OJIP protocol; additionally, SPAD readings were conducted and productivity components were assessed. Inoculation with the fungus spore suspension affected the response curve of the chlorophyll fluorescence transient, SPAD index, and productivity components. Anthracnose stalk rot caused 20–25% reduction in grain weight, 6–8% reduction in maize ear size, and 20–23% reduction in ear weight. Furthermore, plants experiencing C. graminicola rot showed reduced SPAD index and a 24–34% reduction in the activity indicator of PSII (PITotal). These changes in the photosynthetic apparatus were successfully observed via chlorophyll fluorescence measurements.

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Data availability

Raw data were generated at Embrapa. Derived data supporting the findings of this study are available from the corresponding author Costa, R.V. on request.

References

  • Aucique-Pérez C, Rodrigues F, Moreira W, DaMatta F (2014) Leaf gas exchange and chlorophyll a fluorescence in wheat plants supplied with silicon and infected with Pyricularia oryzae. Phytopathology 104:143–149

    Article  Google Scholar 

  • Baghbani F, Lotfi R, Moharramnejad S, Bandehagh A, Roostaei M, Rastogi A, Kalaji HM (2019) Impact of Fusarium verticillioides on chlorophyll fluorescence parameters of two maize lines. European Journal of Plant Pathology 154:337–346

    Article  CAS  Google Scholar 

  • Bandara YMAY, Weerasooriya DK, Tesso TT, Little CR (2016) Stalk rot fungi affect leaf greenness (SPAD) of grain sorghum in a genotype- and growth stage-specific manner. Plant Disease 100:2062–2068

    Article  CAS  PubMed  Google Scholar 

  • Bandara AY, Weerasooriya DK, Tesso TT, Little CR (2019) Stalk rot resistant sorghum genotypes are resilient to pathogen-mediated photosystem II quantum yield retardation. Crop Protection 124: 104852

  • Bastiaans L (1991) Ratio between virtual and visual lesion size as a measure to describe reduction in leaf photosynthesis of rice due to leaf blast. Phytopathology 81:611–615

    Article  Google Scholar 

  • Bauriegel E, Giebel A, Geyer M, Schmidt U, Herppich WB (2011) Early detection of Fusarium infection in wheat using hyper-spectral imaging. Computers and Electronics in Agriculture 75:304–312

    Article  Google Scholar 

  • Bergstrom GC, Nicholson RL (1999) The biology of corn anthracnose: knowledge to exploit for improved management. Phytopathology 83:596–608

    CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Costa RV, Simon J, Cota LV, Silva DD, Almeida REM, Lanza FE, Lago BC, Pereira AA, Campos LJM, Figueiredo JEF (2019) Yield losses in off-season corn crop due to stalk rot disease. Pesquisa Agropecuária Brasileira 54:e00283

    Article  Google Scholar 

  • Cota LV, da Costa RV, Silva DD, Casela CR, Parreira DF (2012) Quantification of yield losses due to anthracnose stalk rot on corn in Brazilian conditions. Journal of Phytopathology 160:680–684

    Article  Google Scholar 

  • Gatch E, Munkvold G (2002) Fungal species composition in maize stalks in relation to European corn borer injury and transgenic insect protection plant disease. Plant Disease 86:1156–1162

    Article  CAS  PubMed  Google Scholar 

  • Jedmowski C, Ashoub A, Brüggemann W (2013) Reactions of Egyptian landraces of Hordeum vulgare and Sorghum bicolor to drought stress evaluated by the OJIP fluorescence transient analysis. Acta Physiol Plant 35:345–354

    Article  Google Scholar 

  • Jirak-Peterson JC, Esker PD (2011) Tillage crop rotation and hybrid effects on residue and corn anthracnose occurrence in Wisconsin. Plant Disease 95:601–610

    Article  PubMed  Google Scholar 

  • Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102

    Article  Google Scholar 

  • Keller NP, Bergstrom GC, Carruthers RI (1986) Potential yield reductions in maize associated with an anthracnose/European corn borer pest complex in New York. Phytopathology 76:586–589

    Article  CAS  Google Scholar 

  • Krause GH (1988) Photo-inhibition of photosynthesis. An evaluation of damaging and protective mechanisms. Physiol Plant 74:566–574

    Article  CAS  Google Scholar 

  • Krause GH, Weis E (1991) Chlorophyll fluorescence and photosynthesis: the basics. Annu Rev Plant Physiol Plant Mol Biol 42:313–349

    Article  CAS  Google Scholar 

  • Kuckenberg J, Tartachnyk I, Noga G (2009) Temporal and spatial changes of chlorophyll fluorescence as a basis for early and precise detection of leaf rust and powdery mildew infections in wheat leaves. Precision Agriculture 10:34–44

    Article  Google Scholar 

  • Lazár D (2006) The polyphasic chlorophyll a fluorescence rise measured under high intensity of exciting light. Functional Plant Biology 33:9–30

    Article  PubMed  Google Scholar 

  • Lichtenthaler HK (1988) In vivo chlorophyll fluorescence as a tool for stress detection in plants. Kluwer Academic Publishers Dordrecht, The Netherlands, pp 129–142

    Google Scholar 

  • Martinazzo EG, Ramm A, Bacarin MA (2012) The chlorophyll a fluorescence as an indicator of the temperature stress in the leaves of Prunus persica. Brazilian of Journal Plant Physiology 24:237–246

    Article  CAS  Google Scholar 

  • Martínez-Ferri E, Zumaquero A, Ariza MT, Barcelo A, Pilego C (2016) Nondestructive detection of white root rot disease in avocado rootstocks by leaf chlorophyll fluorescence. Plant Disease 100:49–58

    Article  PubMed  Google Scholar 

  • Maxwell K, Johnson GN (2000) Chlorophyll fluorescence: a practical guide. J Exp Bot 51:659–688

    Article  CAS  Google Scholar 

  • Mueller DS, Wise KA, Sisson AJ, Allen TW, Bergstrom GC, Bissonnette KM, Bradley CA, Byamukama E, Chilvers MI, Collins AA, Esker PD (2020) Corn yield loss estimates due to diseases in the United States and Ontario, Canada, from 2016 to 2019. Plant Health Progress 21(4):238–247

    Article  Google Scholar 

  • Murchie EH, Lawson T (2013) Chlorophyll fluorescence analysis: a guide to good practice and understanding some new applications. J Exp Bot 64:3983–3998

    Article  CAS  Google Scholar 

  • Nicoli A, Zambolim L, da Costa RV, Guimarães LJM, Lanza FE, da Silva DD, Cota LV (2015) Identification of sources of resistance to anthracnose stalk rot in maize. Ciência Rural 46:1885–1890

    Article  Google Scholar 

  • O’Neill PM, Shanahan JF, Schepers JS (2006) Use of chlorophyll fluorescence assessments to differentiate corn hybrid response to variable water conditions. Crop Science 46:681–687

    Article  CAS  Google Scholar 

  • Pan X, Zhang D, Chen X, Li L, Mu G, Li L, Song W (2010) Sb uptake and photosynthesis of Zea mays growing in soil watered with Sb mine drainage: an OJIP chlorophyll fluorescence study. Pol J Environ Stud 19:981–987

    CAS  Google Scholar 

  • Parreira DF, Zambolim L, Costa RV, Silva D (2016) A method for Colletotrichum graminicola inoculation in maize stalks. Revista Brasileira de Milho e Sorgo 15:53–64

    Article  Google Scholar 

  • R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/. Accessed 15 Jan 2021

  • Rios JA, Rios VS, Aucique-Pérez CE, Cruz MFA, Morais LE, DaMatta FM, Rodrigues FA (2017) Alteration of photosynthetic performance and source-sink relationships in wheat plants infected by Pyricularia oryazae. Plant Pathology 66:1496–1507

    Article  CAS  Google Scholar 

  • Rolfe SA, Scholes JD (2010) Chlorophyll fluorescence imaging of plant-pathogen interactions. Photoplasma 247:163–175

    Article  CAS  Google Scholar 

  • Sarkar RK, Panda D (2009) Distinction and characterisation of submergence tolerant and sensitive rice cultivars, probed by the fluorescence OJIP rise kinetics. Functional Plant Biology 36:222–233

    Article  CAS  PubMed  Google Scholar 

  • Silva MDA, Jifon JL, da Silva JAG, dos Santos CM, Sharma V (2014) Relationships between physiological traits and productivity of sugarcane in response to water deficit. The Journal of Agricultural Science 152:104–118

    Article  Google Scholar 

  • Simko I, Jimenez-Berni JA, Sirault XR (2016) Phenomic approaches and tools for phytopathologists. Phytopathology 107:6–17

    Article  PubMed  Google Scholar 

  • Srinivasarao C, Shanker AK, Kundu S, Reddy S (2016) Chlorophyll fluorescence induction kinetics and yield responses in rainfed crops with variable potassium nutrition in K deficient semi-arid alfisols. J Photochem Photobiol B Biol 160:86–95

    Article  CAS  Google Scholar 

  • Stefanov D, Petkova V, Denev ID (2011) Screening for heat tolerance in common bean (Phaseolus vulgaris L) lines and cultivars using JIP-test. Scientia Horticulturae 128:1–6

    Article  Google Scholar 

  • Strasser BJ, Strasser RJ (1995) Measuring fast fluorescence transients to address environmental questions: the JIP-test. In: Mathis P (ed) Photosynthesis: from light to biosphere. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 977–980

    Google Scholar 

  • Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples, Cap. 25. In: Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanism, regulation and adaptation. Taylor and Francis, New York, NY, USA, pp 445–483

    Google Scholar 

  • Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In Chlorophyll a fluorescence. Springer, Dordrecht, pp. 321–362

  • Sukno SA, García VM, Shaw BD, Thon MR (2008) Root infection and systemic colonization of maize by Colletotrichum graminicola. Applied Environment Microbiology 74:823–832

    Article  CAS  Google Scholar 

  • Szareski VJ, Carvalho IR, Kehl K, Pelegrin AJ, Nardino M, Demari GH, Barbosa MH, Lautenchleger F, Smaniotto D, Aumonde TZ, Pedo T, Souza VQ (2018) Interrelations of characters and multivariate analysis in corn. J Agric Sci 10:187–194

    Article  Google Scholar 

  • Thwe AA, Kasemsap P (2014) Quantification of OJIP fluorescence transient in tomato plants under acute ozone stress. Kasetsart Journal: Natural Science 48:665–675

    Google Scholar 

  • Tůmová L, Tarkowská D, Řehořová K, Marková H, Kočová M, Rothová O, Čečetka P, Holá D (2018) Drought-tolerant and drought-sensitive genotypes of maize (Zea maysL.) differ in contents of endogenous brassinosteroids and their drought-induced changes. PloS One 13:e0197870

    Article  PubMed  PubMed Central  Google Scholar 

  • Venard C, Vaillancourt L (2007) Colonization of fiber cells by Colletotrichum graminicola in wounded maize stalks. Phytopathology 97:438–447

    Article  CAS  PubMed  Google Scholar 

  • Warzecha T, Skrzypek E, Adamski T, Surma M, Kaczmarek Z, Sutkowska A (2019) Chlorophyll a fluorescence parameters of hulled and hull-less barley (Hordeum vulgare L.) DH lines inoculated with Fusarium culmorum. The Plant Pathology Journal 35:112–124

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zivcak M, Brestic M, Oslovska K, Slamka P (2008) Performance index as a sensitive indicator of water stress in Triticum aestivum L. Plant Soil and Environment 54:133–139

    Article  Google Scholar 

Download references

Acknowledgements

The authors gratefully acknowledge the support provided by Embrapa, Fazenda Boa Esperança, and Fazenda Frigovale.

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Authors and Affiliations

  1. Embrapa Soja, Londrina, PR, 86001-970, Brazil

    Leonardo José Motta Campos

  2. Embrapa Pesca e Aquicultura, Palmas, TO, 77008-900, Brazil

    Rodrigo Estavam Munhoz de Almeida

  3. Embrapa Milho e Sorgo, Sete Lagoas, MG, 35701-970, Brazil

    Dagma Dionísia da Silva, Luciano Viana Cota & Rodrigo Veras da Costa

  4. Universidade Federal do Tocantins, Palmas, TO, 77001-090, Brazil

    Alessandra Maria Lima Naoe & Joênes Mucci Peluzio

  5. Faculdade Católica do Tocantins, Unidade II, Palmas, TO, 77000-000, Brazil

    Fernanda Pinheiro Bernardes

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  1. Leonardo José Motta Campos
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  2. Rodrigo Estavam Munhoz de Almeida
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  8. Rodrigo Veras da Costa
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Contributions

Conceptualization: Costa, R.V.; Campos, L.J.M.; Almeida, R.E.M.; Silva, D.D. Data acquisition: Costa, R.V.; Campos, L.J.M.; Bernardes, F.P. Data analysis: Campos, L.J.M.; Costa, R.V.; Cota, L.V.; Silva, D.D.; Peluzio, J.M. Design of methodology: Campos, L.J.M.; Costa, R.V.; Bernardes, F.P. Writing and editing: Costa, R.V.; Campos, L.J.M.; Almeida, R.E.M.; Cota, L.V.; Silva, D.D.; Naoe, A.M.L; Peluzio, J.M.

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Correspondence to Rodrigo Veras da Costa.

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Campos, L.J.M., de Almeida, R.E.M., da Silva, D.D. et al. Physiological and biophysical alterations in maize plants caused by Colletotrichum graminicola infection verified by OJIP study. Trop. plant pathol. 46, 674–683 (2021). https://doi.org/10.1007/s40858-021-00465-x

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