Advertisement

Physiological effects of strobilurin and carboxamides on plants: an overview

  • 93 Accesses

Abstract

Usually, fungicides are used to control and prevent diseases, however, a group of fungicides called strobilurins has brought about a new possibility of use for these products: the physiological effects. This group of fungicides modifies the plant physiology, through changes in metabolism and growth, which increases crop yield. Another group of fungicides, which also reveal physiological effects, is carboxamides. However, there are still only a few publications in scientific journals regarding the effects of the molecules of this group, since they were just introduced in the market recently. The carboxamides when applied together with or alternately to strobilurins potentiate their action. Both are systemic fungicides that operate preventively and have a little curative effect, but the preventive application of these products yields benefits, in addition to protecting the plant by increasing production through its physiological benefits. The physiological effects detected when applying strobilurins or carboxamides in healthy plants are due to the increase in net photosynthesis (true photosynthesis minus dark respiration and photorespiration), as it temporarily reduces plant respiration, which led to less carbon dioxide loss and, consequently, generates more energy for the plant. Besides, the increase in antioxidant enzymes provokes increased tolerance to stress. It also results in higher activity of nitrate reductase and a better hormonal balance, increasing the synthesis of indolyl acetic acid (IAA) and abscisic acid (ABA), as well as reduced ethylene production, delayed senescence and prolonged photosynthetic efficiency, known as "green effect". These effects, together, increase productivity and fruit quality.

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

Access options

Buy single article

Instant unlimited access to the full article PDF.

US$ 39.95

Price includes VAT for USA

Subscribe to journal

Immediate online access to all issues from 2019. Subscription will auto renew annually.

US$ 99

This is the net price. Taxes to be calculated in checkout.

References

  1. Ajigboye OO, Murchie E, Ray RV (2014) Foliar application of isopyrazam and epoxiconazole improves photosystem II efficiency, biomass and yield in winter wheat. Pestic Biochem Physiol 114:52–60. https://doi.org/10.1016/j.pestbp.2014.07.003

  2. Amaro ACE, Ramos ARP, Macedo AC, Ono EO, Rodrigues JD (2018) Effects of the fungicides azoxystrobin, pyraclostrobin and boscalid on the physiology of Japanese cucumber. Sci Hortic (Amsterdam) 228:66–75. https://doi.org/10.1016/j.scienta.2017.10.016

  3. Avenot HF, Michailides TJ (2010) Progress in understanding molecular mechanisms and evolution of resistance to succinate dehydrogenase inhibiting (SDHI) fungicides in phytopathogenic fungi. Crop Prot 29:643–651. https://doi.org/10.1016/j.cropro.2010.02.019

  4. Bahia K-H, Pascal L, Dong-Woo L, Elisabeth D, Fevzi D (2011) Recent advances in cytochrome bc 1: inter monomer electronic communication? FEBS Lett 586:617–621. https://doi.org/10.1016/j.febslet.2011.08.032

  5. Balba H (2007) Review of strobilurin fungicide chemicals. J Environ Sci Heal Part B 42:441–451. https://doi.org/10.1080/03601230701316465

  6. Barbosa KA, Fagan EB, Casaroli D, de Carvalho CS, Teixeira WF (2011) Aplicação de estrobilurina na cultura do milho: alterações fisiológicas e bromatológicas. Rev do Cent Univ Patos Minas 2:20–29

  7. Bartett DW, Clough JM, Godfrey CRA, Godwin JR, Hall AA, Heaney SP, Maund SJ (2001) Understanding the strobilurin fungicides. Pestic Outlook 12:143–148. https://doi.org/10.1039/B106300F

  8. Bartlett DW, Clough JM, Godwin JR, Hall AA, Hamer M, Parr-Dobrzanski B (2002) The strobilurin fungicides. Pest Manag Sci 58:649–662. https://doi.org/10.1002/ps.520

  9. Berdugo CA, Steiner U, Dehne HW, Oerke EC (2012) Effect of bixafen on senescence and yield formation of wheat. Pestic Biochem Physiol 104:171–177. https://doi.org/10.1016/j.pestbp.2012.07.010

  10. Berkelmann-Loehnertz B, Dorn C, Baus-Reichel O, Griebel T (2001) Impact of strobilurins on grapevine physiology under greenhouse conditions. IOBC WPRS Bull 24:303–307

  11. Bertelsen JR, De Neergaard E, Smedegaard-Petersen V (2001) Fungicidal effects of azoxystrobin and epoxiconazole on phyllosphere fungi, senescence and yield of winter wheat. Plant Pathol 50:190–205. https://doi.org/10.1046/j.1365-3059.2001.00545.x

  12. Blandino M, Galeazzi M, Savoia W, Reyneri A (2012) Timing of azoxystrobin+propiconazole application on maize to control northern corn leaf blight and maximize grain yield. Field Crop Res 139:20–29. https://doi.org/10.1016/j.fcr.2012.09.014

  13. Bonasia A, Conversa G, Lazzizera C, Elia A (2013) Pre-harvest nitrogen and Azoxystrobin application enhances postharvest shelf-life in Butterhead lettuce. Postharvest Biol Technol 85:67–76. https://doi.org/10.1016/j.postharvbio.2013.04.012

  14. Bradley KW, Sweets LE (2008) Influence of Glyphosate and fungicide coapplications on weed control, spray penetration, soybean response, and yield in Glyphosate-resistant soybean. Agron J 100:1360–1365. https://doi.org/10.2134/agronj2007.0329

  15. Brosnan JT, Horvath BJ, Elmore MT, Breeden GK, Sorochan JC (2010) Greenhouse investigation of strobilurin fungicide applications on creeping bentgrass root characteristics under two irrigation regimes. Crop Sci 50:2605–2612. https://doi.org/10.2135/cropsci2010.02.0088

  16. Cantore V, Lechkar O, Karabulut E, Sellami MH, Albrizio R, Boari F, Stellacci AM, Todorovic M (2016) Combined effect of deficit irrigation and strobilurin application on yield, fruit quality and water use efficiency of “cherry” tomato (Solanum lycopersicum L.). Agric Water Manag 167:53–61. https://doi.org/10.1016/j.agwat.2015.12.024

  17. Cecchini G (2003) Function and structure of complex II of the respiratory chain. Annu Rev Biochem 72:77–109. https://doi.org/10.1146/annurev.biochem.72.121801.161700

  18. CONAB (2019) Acompanhamento da safra brasileira de grãos. Safra 2018/19. CONAB, Brasília, pp 1–145

  19. Debona D, Nascimento KJT, Gomes JGO, Aucique-Perez CE, Rodrigues FA (2016) Physiological changes promoted by a strobilurin fungicide in the rice-Bipolaris oryzae interaction. Pestic Biochem Physiol 130:8–16. https://doi.org/10.1016/j.pestbp.2015.12.006

  20. Diaz-Espejo A, Cuevas MV, Ribas-Carbo M, Flexas J, Martorell S, Fernandez JE (2012) The effect of strobilurins on leaf gas exchange, water use efficiency and ABA content in grapevine under field conditions. J Plant Physiol 169:379–386. https://doi.org/10.1016/j.jplph.2011.11.014

  21. Domínguez I, Ferreres F, Pascual del Riquelme F, Font R, Gil MI (2012) Influence of preharvest application of fungicides on the postharvest quality of tomato (Solanum lycopersicum L.). Postharvest Biol Technol 72:1–10. https://doi.org/10.1016/j.postharvbio.2012.04.010

  22. Dunne B (2005) Strobilurin use on cereals. Crop Prot 23:17–20

  23. Factor TL, Júnior SL, Purquerio LFV (2011) Secondary effects of fungicides in tomato seedlings production. Acta Hortic 923:269–275

  24. Fagan EB, Dourado Neto D, Vivian R, Franco RB, Yeda MP, Massignam LF, de Oliveira RF, Martins KV (2010) Efeito da aplicação de piraclostrobina na taxa fotossintética, respiração, atividade da enzima nitrato redutase e produtividade de grãos de soja. Bragantia 69:771–777. https://doi.org/10.1590/S0006-87052010000400001

  25. Glaab J, Kaiser WM (1999) Increased nitrate reductase activity in leaf tissue after application of the fungicide Kresoxim-methyl. Planta 207:442–448. https://doi.org/10.1007/s004250050503

  26. Glättli A, Grote T, Stammler G (2011) SDH-inhibitors: history, biological performance and molecular mode of action. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Rossel PE, Lyr H (eds) Modern fungicides and antifungal compounds VI. 16th International Reinhardsbrunn Symposium, Friedrichroda, Germany, April 25–29, 2010. Deutsche Phytomedizinische Gesellschaft eV Selbstverlag, pp. 159–169.

  27. Grossmann K, Retzlaff G (1997) Bioregulatory Effects of the Fungicidal Strobilurin Kresoxim-methyl in Wheat (Triticum aestivum). Pestic Sci 50:11–20. https://doi.org/10.1002/(SICI)1096-9063(199705)50:1%3c11:AID-PS556%3e3.0.CO;2-8

  28. Grossmann K, Kwiatkowski J, Caspar G (1999) Regulation of phytohormone levels, leaf senescence and transpiration by the strobilurin kresoxim-methyl in wheat (Triticum aestivum). J Plant Physiol 154:805–808. https://doi.org/10.1016/S0176-1617(99)80262-4

  29. Horsefield R, Yankovskaya V, Sexton G, Whittingham W, Shiomi K, Omura S, Byrne B, Cecchini G, Iwata S (2006) Structural and computational analysis of the quinone-binding site of complex II (succinate-ubiquinone oxidoreductase): a mechanism of electron transfer and proton conduction during ubiquinone reduction. J Biol Chem 281:7309–7316. https://doi.org/10.1074/jbc.M508173200

  30. Hörtensteiner S, Kräutler B (2011) Chlorophyll breakdown in higher plants. Biochim Biophys Acta Bioenerg 1807:977–988. https://doi.org/10.1016/j.bbabio.2010.12.007

  31. Huang S, Millar AH (2013) Succinate dehydrogenase: the complex roles of a simple enzyme. Curr Opin Plant Biol 16:344–349. https://doi.org/10.1016/j.pbi.2013.02.007

  32. Inagaki MN, Mori M, Nachit MM (2009) Effect of a strobilurin-class fungicide on water use in synthetic bread wheat genotypes grown under increasing water deficit conditions. Cereal Res Commun 37:513–519. https://doi.org/10.2307/23789995

  33. Ishikawa S, Hare MC, Kettlewell PS (2012) Effects of strobilurin fungicide programmes and fertilizer nitrogen rates on winter wheat: leaf area, dry matter yield and nitrogen yield. J Agric Sci 150:427–441. https://doi.org/10.1017/S0021859611000724

  34. Jabs T, Pfirrmann J, Schäfer S, Wu YX (2002) Anti-oxidative and anti-senescence effects of the strobilurin pyraclostrobin in plants: a new strategy to cope with environmental stress in cereals. In: The BCPC Conference: Pests and Diseases, Volumes 1 and 2.In: Proceedings of an International Conference Held at the Brighton Hilton Metropole Hotel, Brighton, UK, 18–21 November 2002. British Crop Protection Council, pp. 941–946.

  35. Jadoski CJ, Rodrigues JD, Soratto RP, dos Santos CM, Ribeiro E (2015) Ação fisiológica da piraclostrobina na assimilação de CO2 e enzimas antioxidantes em planta de feijão condicionado em diferentes tensões de água no solo. Irriga 20:319. https://doi.org/10.15809/irriga.2015v20n2p319

  36. Jørgensen LN, Olesen JE (2002) Fungicide treatments affect yield and moisture content of grain and straw in winter wheat. Crop Prot 21:1023–1032. https://doi.org/10.1016/S0261-2194(02)00086-8

  37. Joshi J, Sharma S, Guruprasad KN (2014) Foliar application of pyraclostrobin fungicide enhances the growth, rhizobial-nodule formation and nitrogenase activity in soybean (var. JS-335). Pestic Biochem Physiol 114:61–66. https://doi.org/10.1016/j.pestbp.2014.07.002

  38. Kaneko I, Ishii H (2009) Effect of azoxystrobin on activities of antioxidant enzymes and alternative oxidase in wheat head blight pathogens Fusarium graminearum and Microdochium nivale. J Gen Plant Pathol 75:388–398. https://doi.org/10.1007/s10327-009-0178-9

  39. Kildea S, Dunne B, Mullins E, Cooke LR, Mercer PC, O’Sullivan E (2010) Pyraclostrobin reduces germ tube growth of QoI-resistant Mycosphaerella graminicola pycnidiospores and the severity of septoria tritici blotch on winter wheat. Plant Pathol 59:1091–1098. https://doi.org/10.1111/j.1365-3059.2010.02348.x

  40. Köhle H, Grossmann K, Jabs T, Gerhard M, Kaiser W, Glaab J, Conrath U, Seehaus K, Herms S (2002) Physiological effects of the strobilurin fungicide F 500 on plants. In: Dehne HW, Gisi U, Kuck KH, Russell PE (eds) Modern fungicides and antifungal compounds III. Springer, Germany, pp 61–74

  41. Kozlowski LA, Simões DFM, Souza CD, Tentro M (2009) Efeito fisiológico de estrobilurina F 500® no crescimento e rendimento do feijoeiro. Rev Acadêmica Ciência Agrária e Ambient 7:41–54

  42. Leadbeater, AJ (2014) Plant health management: fungicides and antibiotics. In: Van Alfen NK (ed) Encyclopedia of agriculture and food systems, 2nd ed, Elsevier, Amsterdam, pp 408–424

  43. Lima JD, da Silva MW, da Silva SHM-G (2012) Respostas fisiológicas em mudas de banananeira tratadas com estrobilurinas. Semin Ciências Agrárias 33:77–86. https://doi.org/10.5433/1679-0359.2012v33n1p77

  44. Macedo AC, Amaro ACE, Ramos ARP, Ono EO, Rodrigues JD (2017) Strobilurin and boscalid in the quality of net melon fruits. Semin Agrar 38(2):543–550. https://doi.org/10.5433/1679-0359.2017v38n2p543

  45. McCreary CM, Depuydt D, Vyn RJ, Gillard 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

  46. McDougall P (2010) The cost of new agrochemical product discovery, development and registration in 1995, 2000 and 2005–8. European Crop Protection Association and Crop Life America, Brussels

  47. Mizutani A, Miki N, Yukioka H, Tamura H, Masuko M (1996) A possible mechanism of control of rice blast disease by a novel alkoxyiminoacetamide fungicide, SSF126. Phytopathology 86:295–300

  48. Mori C, Costamilan LM (2004) Ferrugem da soja: estimativas de custo de controle, em Passo Fundo RS. Embrapa Trigo, Passo Fundo

  49. Nason MA, Farrar J, Bartlett D (2007) Strobilurin fungicides induce changes in photosynthetic gas exchange that do not improve water use efficiency of plants grown under conditions of water stress. Pest Manag Sci 63:1191–1200. https://doi.org/10.1002/ps.1443

  50. Nelson KA, Meinhart CG (2011) Foliar boron and pyraclostrobin effects on corn yield. Agron J 103:1352–1358. https://doi.org/10.2134/agronj2011.0090

  51. Nwankno AJ, Gordon SL, Verrall SR, Brennan RM, Hancock RD (2012) Treatment with fungicides influences phytochemical quality of blackcurrant juice. Ann Appl Biol 160:86–96. https://doi.org/10.1111/j.1744-7348.2011.00523.x

  52. Pedersen M, Wegner C, Phansak P, Sarath G, Gaussoin R, Schlegel V (2017) Monitoring wheat mitochondrial compositional and respiratory changes using Fourier transform mid-infrared spectroscopy in response to agrochemical treatments. Spectrochim Acta Part A Mol Biomol Spectrosc 173:727–732. https://doi.org/10.1016/j.saa.2016.10.025

  53. Ramos ARP, Amaro ACE, Macedo AC, Sugawara GSA, Evangelista RM, Rodrigues JD, Ono EO (2013) Fruit quality of tomato “giuliana” treated with products with physiological effects. Semin Agrar 34(6):3543–3552. https://doi.org/10.5433/1679-0359.2013v34n6Supl1p3543

  54. Ruske RE, Gooding MJ, Jones SA (2003) The effects of triazole and strobilurin fungicide programmes on nitrogen uptake, partitioning, remobilization and grain N accumulation in winter wheat cultivars. J Agric Sci 140:395–407. https://doi.org/10.1017/S0021859603003228

  55. Sarwat M, Naqvi AR, Ahmad P, Ashraf M, Akram NA (2013) Phytohormones and microRNAs as sensors and regulators of leaf senescence: assigning macro roles to small molecules. Biotechnol Adv 31:1153–1171. https://doi.org/10.1016/j.biotechadv.2013.02.003

  56. Sauter H, Steglich W, Anke T (1999) Strobilurins: evolution of a new class of active substances. Angew Chemie Int Ed 38:1328–1349

  57. Schnabel G, Crisosto CH (2008) Seasonal applications of a pyraclostrobin and boscalid mixture do not impact same-year peach fruit quality attributes. Horttechnology 18:678–684

  58. Semar M, Strobel D, Strathmann S, Groeger U (2011) Xemium®-the BASF fungicide innovation. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Rossel PE, Lyr H (eds) Modern Fungicides and Antifungal Compounds VI. 16th International Reinhardsbrunn Symposium, Friedrichroda, Germany, April 25–29, 2010. Deutsche Phytomedizinische Gesellschaft eV Selbstverlag, pp. 63–68.

  59. Silva FDL, Balardin RS, Debona D, Corte GD, Tormen NR, Domingues L (2009) Efeito fisiológico do tratamento de sementes de soja com fungicidas e inseticidas, in: XVIII Congresso de Iniciação Científica.

  60. Sirtoli LF, Rodrigues JD, Goto R (2011) Efeito fisiológico do fungicida boscalida na atividade da nitrato redutase e nas características fitotécnias de pepineiro japonês enxertado e não enxertado. Sci Agrar Parana 10:58–69

  61. Soares LH, Fagan EB, Casaroli D, Andrade DM, Soares AL, Martins KV, Rocha FJ (2011) Aplicação de diferentes estrobilurinas na cultura da soja. Rev. da FZVA 18(1):78–97

  62. Stammler G, Speakman J (2006) Microtiter method to test the sensitivity of Botrytis cinerea to boscalid. J Phytopathol 154:508–510. https://doi.org/10.1111/j.1439-0434.2006.01139.x

  63. Stammler G, Benzinger G, Speakman J (2007a) A rapid and reliable method for monitoring the sensitivity of sclerotinia sclerotiorum to boscalid. J Phytopathol 155:746–748. https://doi.org/10.1111/j.1439-0434.2007.01294.x

  64. Stammler G, Itoh M, Hino I, Watanabe A, Kojima K, Motoyoshi M, Koch A, Haden E (2007b) Efficacy of orysastrobin against blast and sheath blight in transplanted rice. J Pestic Sci 32:10–15. https://doi.org/10.1584/jpestics.G06-22

  65. Stammler G, Brix HD, Nave B, Gold R, Schoefl U (2008) Studies on the biological performance of boscalid and its mode of action. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Rossel PE, Lyr H (eds) Modern Fungicides and Antifungal Compounds V: 15th International Reinhardsbrunn Symposium, Friedrichroda, Germany, May 6–10, 2007. Deutsche Phytomedizinische Gesellschaft eV Verlag, pp. 45–51.

  66. Swoboda C, Pedersen P (2009) Effect of fungicide on soybean growth and yield. Agron J 101:352–356. https://doi.org/10.2134/agronj2008.0150

  67. Takahashi N, Sunohara Y, Fujiwara M, Matsumoto H (2017) Improved tolerance to transplanting injury and chilling stress in rice seedlings treated with orysastrobin. Plant Physiol Biochem 113:161–167. https://doi.org/10.1016/j.plaphy.2017.02.004

  68. Walter H (2011) New fungicides and new modes of action., in: modern fungicides and antifungal compounds VI. In: Dehne HW, Deising HB, Gisi U, Kuck KH, Rossel PE, Lyr H (eds) Modern Fungicides and Antifungal Compounds VI. 16th International Reinhardsbrunn Symposium, Friedrichroda, Germany, April 25–29, 2010. Deutsche Phytomedizinische Gesellschaft eV Selbstverlag, pp. 47–54.

  69. Wu Y-X, von Tiedemann A (2001) Physiological effects of azoxystrobin and epoxiconazole on senescence and the oxidative status of wheat. Pestic Biochem Physiol 71:1–10. https://doi.org/10.1006/pest.2001.2561

  70. Wu Y, von Tiedemann A (2002) Impact of fungicides on active oxygen species and antioxidant enzymes in spring barley (Hordeum vulgare L.) exposed to ozone. Environ Pollut 116:37–47. https://doi.org/10.1016/S0269-7491(01)00174-9

  71. Xia D, Esser L, Tang W-K, Zhou F, Zhou Y, Yu L, Yu C-A (2013) Structural analysis of cytochrome bc1 complexes: Implications to the mechanism of function. Biochim Biophys Acta Bioenerg 1827:1278–1294. https://doi.org/10.1016/j.bbabio.2012.11.008

  72. Yorinori JT, Nunes Junior J, Lazzarotto JJ (2004) Ferrugem "Asiática" da soja no Brasil: evolução, importância econômica e controle. Embrapa Soja, Londrina

  73. Ypema HL, Gold RE (1999) Kresoxim-methyl: modification of a naturally occurring compound to produce a new fungicide. Plant Dis 83:4–19. https://doi.org/10.1094/PDIS.1999.83.1.4

  74. Zhang Y-J, Zhang X, Chen C-J, Zhou M-G, Wang H-C (2010) Effects of fungicides JS399-19, azoxystrobin, tebuconazole, and carbendazim on the physiological and biochemical indices and grain yield of winter wheat. Pestic Biochem Physiol 98:151–157. https://doi.org/10.1016/j.pestbp.2010.04.007

Download references

Acknowledgements

The authors wish to thank the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP). Amanda C. E. Amaro was the recipient of FAPESP grant number 2008/56632–7.

Author information

Correspondence to Amanda Cristina Esteves Amaro.

Additional information

Publisher's Note

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

Communicated by P. Wojtaszek.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Amaro, A.C.E., Baron, D., Ono, E.O. et al. Physiological effects of strobilurin and carboxamides on plants: an overview. Acta Physiol Plant 42, 4 (2020). https://doi.org/10.1007/s11738-019-2991-x

Download citation

Keywords

  • Boscalid
  • Carboxamide
  • Pyraclostrobin
  • Strobilurin