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Lachancea thermotolerans acts as a resistance inducer in soybean infected with Meloidogyne incognita

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Abstract

The worldwide interest in sustainable agriculture has contributed to the development of alternative methods for the control of plant pests and diseases. This study aimed to assess the efficiency of Lachancea thermotolerans CCMA 0763 and its metabolites in controlling Meloidogyne incognita in soybean and their effects on plant defense enzymes and glyceollin synthesis. The following treatments were applied as foliar spray 4 days before nematode inoculation: fermentation broth, broth filtrate, yeast cells, sugarcane juice, acibenzolar-S-methyl (ASM). An inoculated untreated control and an absolute control were also included. The same treatments were used in the glyceollin assay. For analysis of resistance induction, the treatments were fermentation broth, broth filtrate, yeast cells, ASM, and water (control). Fermentation broth and yeast cells reduced total nematode number, population density and reproduction factor. Yeast-based treatments and ASM enhanced glyceollin synthesis compared with sugarcane juice and water. Peroxidase activity was highest at 4 and 10 days after treatment in plants treated with yeast-based treatmentss. Broth filtrate and yeast cells increased polyphenol oxidase activity at 4 days after treatment. Phenylalanine ammonia-lyase and glucanase activities were not influenced by treatment. L. thermotolerans stimulated phytoalexin synthesis in soybean cotyledons and defense enzyme activity in soybean roots, showing potential as a biopesticide.

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References

  • Abbasi, M. W., Ahmed, N., Zaki, M. J., Shuakat, S. S., & Khan, D. (2014). Potential of Bacillus species against Meloidogyne javanica parasitizing eggplant (Solanum melongena L.) and induced biochemical changes. Plant and Soil, 375(1–2), 159–173.

    Article  CAS  Google Scholar 

  • Adam, M., Heuer, H., & Hallmann, J. (2014). Bacterial antagonists of fungal pathogens also control root-knot nematodes by induced systemic resistance of tomato plants. PLoS One, 9(2), 1–8.

    Article  Google Scholar 

  • Aguilar-Uscanga, B., & François, J. M. (2003). A study of the yeast cell wall composition and structure in response to growth conditions and mode of cultivation. Letters in Applied Microbiology, 37(3), 268–274.

    Article  CAS  PubMed  Google Scholar 

  • Balasubramanian, V., Vashisht, D., Cletus, J., & Sakthivel, N. (2012). Plant β-1,3-glucanases: Their biological functions and transgenic expression against phytopathogenic fungi. Biotechnology Letters, 34(11), 1983–1990.

    Article  CAS  PubMed  Google Scholar 

  • Boneti, J. I. S., & Ferraz, S. (1981). Modificação do método de Hussey e Barker para extração de ovos de Meloidogyne exigua de raízes de cafeeiro. Fitopatologia Brasileira, 6, 553.

    Google Scholar 

  • Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72(1–2), 248–254.

    Article  CAS  PubMed  Google Scholar 

  • Carneiro, R. M. D. G., & Almeida, M. R. A. (2001). Técnica de eletroforese usada no estudo de enzimas dos nematoides das galhas para a identificação de espécies. Nematologia Brasileira, 1(25), 25–44.

  • Côté, F., Roberts, K. A., & Hahn, M. G. (2000). Identification of high-affinity binding sites for the hepta-β-glucoside elicitor in membranes of the model legumes Medicago truncatula and Lotus japonicus. Planta, 211(4), 596–605.

    Article  PubMed  Google Scholar 

  • Chan, Z., Qin, G., Xu, X., Li, B., & Tian, S. (2007). Proteome approach to characterize proteins induced by antagonist yeast and salicylic acid in peach fruit. Journal of Proteome Research, 6(5), 1677–1688.

  • Chin, S., Behm, C. A., & Mathesius, U. (2018). Functions of flavonoids in plant–nematode interactions. Plants, 7(4), 1–17.

    Article  Google Scholar 

  • Chinnasri, B., Sipes, B. S., & Schmitt, D. P. (2003). Effects of acibenzolar-S-methyl application to Rotylenchulus reniformis and Meloidogyne javanica. Journal of Nematology, 35(1), 110–114.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Duangmal, K., & Owusu Apenten, R. K. (1999). A comparative study of polyphenoloxidases from taro (Colocasia esculenta) and potato (Solanum tuberosum var. romano). Food Chemistry, 64(3), 351–359.

    Article  CAS  Google Scholar 

  • El-Beltagi, H. S., Farahat, A. A., Alsayed, A. A., & Mahfoud, N. A. (2012). Response of antioxidant substances and enzymes activities as a defense mechanism against root-knot nematode infection. Notulae Botanicae Horti Agrobotanici, 40(1), 132–142.

    Article  CAS  Google Scholar 

  • Ferreira, D. F. (2011). Sisvar: A computer statistical analysis system. Ciência e Agrotecnologia, 35(6), 1039–1042.

    Article  Google Scholar 

  • Ferreira-Saab, M., Formey, D., Torres, M., Aragón, W., Padilla, E. A., Tromas, A., Sohlenkamp, C., Schwan-Estrada, K. R. F., & Serrano, M. (2018). Compounds released by the biocontrol yeast Hanseniaspora opuntiae protect plants against Corynespora cassiicola and Botrytis cinerea. Frontiers in Microbiology, 9(1596), 1–12.

    Google Scholar 

  • Fialho, M. B., Bessi, R., Inomoto, M. M., & Pascholati, S. F. (2012). Nematicidal effect of volatile organic compounds (VOCs) on the plant-parasitic nematode Meloidogyne javanica. Summa Phytopathologica, 38(2), 152–154.

    Article  Google Scholar 

  • Freimoser, F. M., Rueda-Mejia, M. P., Tilocca, B., & Migheli, Q. (2019). Biocontrol yeasts: Mechanisms and applications. World Journal of Microbiology and Biotechnology, 35(10), 1–19.

    Article  Google Scholar 

  • Gao, H., Qi, G., Yin, R., Zhang, H., Li, C., & Zhao, X. (2016). Bacillus cereus strain S2 shows high nematicidal activity against Meloidogyne incognita by producing sphingosine. Scientific Reports, 6(28756), 1–11.

    Google Scholar 

  • Garcia-Brugger, A., Lamotte, O., Vandelle, E., Bourque, S., Lecourieux, D., Poinssot, B., Wendehenne, D., & Pugin, A. (2006). Early signaling events induced by elicitors of plant defenses. Molecular Plant-Microbe Interactions, 19(7), 711–724.

    Article  CAS  PubMed  Google Scholar 

  • Hashem, M., & Abo-Elyousr, K. A. (2011). Management of the root-knot nematode Meloidogyne incognita on tomato with combinations of different biocontrol organisms. Crop Protection, 30(3), 285–292.

    Article  Google Scholar 

  • Hernandes, I., Brito, O. D. C., Cardoso, M. R., Ferreira, J. C. A., Puerari, H. H., & Dias-Arieira, C. R. (2017). Acibenzolar-S-methyl on Meloidogyne javanica control in lettuce. Acta Agriculturae Scandinavica, Section B – Soil & Plant Science, 67(7), 660–664.

    CAS  Google Scholar 

  • Hussey, R. S., & Barker, K. R. (1973). A comparison of methods of collecting inocula of Meloidogyne spp. including a new technique. Plant Disease Reporter 57, 1025–1028.

  • Jaouannet, M., Magliano, M., Arguel, M. J., Gourgues, M., Evangelist, E., Abad, P., & Rosso, M. N. (2013). The root-knot nematode calreticulin mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions, 26(1), 97–105.

    Article  CAS  PubMed  Google Scholar 

  • Kaplan, D. T., Keen, N. T., & Thomason, I. J. (1980a). Association of glyceollin with the incompatible response of soybean roots to Meloidogyne incognita. Physiology of Plant Pathology, 16(3), 309–318.

    Article  CAS  Google Scholar 

  • Kaplan, D. T., Keen, N. T., & Thomason, I. J. (1980b). Studies on the mode of action of glyceollin in soybean incompatibility to the root knot nematode, Meloidogyne incognita. Physiology of Plant Pathology, 16(3), 319–325.

    Article  CAS  Google Scholar 

  • Karajeh, M. R. (2014). Enhancement of tomato growth, yield and resistance to the root-knot nematode (Meloidogyne javanica) after the field application of Saccharomyces cerevisiae. Hellenic Plant Protection Journal, 7(1), 35–41.

    Google Scholar 

  • Klarzynski, O., Plesse, B., Joubert, J. M., Yvin, J. C., Kopp, M., Kloareg, B., & Fritig, B. (2000). Linear β-1,3-glucans are elicitors of defense responses in tobacco. Plant Physiology, 124(3), 1027–1038.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lever, M. (1972). A new reaction for colorimetric determination of carbohydrates. Analytical Biochemistry, 47, 273–279.

    Article  CAS  PubMed  Google Scholar 

  • Limtong, S., & Koowadjanakul, N. (2012). Yeasts from phylloplane and their capability to produce indole-3-acetic acid. World Journal of Microbiology and Biotechnology, 28(12), 3323–3335.

    Article  CAS  PubMed  Google Scholar 

  • Liu, Q., Luo, L., & Zheng, L. (2018). Lignins: Biosynthesis and biological functions in plants. International Journal of Molecular Science, 19(1), 1–16.

    Google Scholar 

  • Llorens, E., Vicedo, B., López, M. M., Lapeña, L., Graham, J. H., & García-Agustín, P. (2015). Induced resistance in sweet orange against Xanthomonas citri subsp. citri by hexanoic acid. Crop Protection, 74(August), 77–84.

    Article  CAS  Google Scholar 

  • Lusso, M. F. G., & Pascholati, S. F. (1999). Activity and isoenzymatic pattern of soluble peroxidases in maize tissues after mechanical injury or fungal inoculation. Summa Phytopathologica, 25, 244–249.

    CAS  Google Scholar 

  • Medeiros, H. A., Resende, R. S., Ferreira, F. C., Freitas, L. G., & Rodrigues, F. A. (2015). Induction of resistance in tomato against Meloidogyne javanica by Pochonia chlamydosporia. Nematoda, 2, 1–7.

    Google Scholar 

  • Melillo, M. T., Leonetti, P., Bongiovanni, M., Castagnone-Sereno, P., & Bleve-Zacheo, T. (2006). Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato–root-knot nematode interactions. New Phytologist, 170(3), 501–512.

    Article  CAS  Google Scholar 

  • Melillo, M. T., Leonetti, P., & Veronico, P. (2014). Benzothiadiazole effect in the compatible tomato-Meloidogyne incognita interaction: Changes in giant cell development and priming of two root anionic peroxidases. Planta, 240(4), 841–854.

    Article  CAS  PubMed  Google Scholar 

  • Mioranza, T. M., Schwan-Estrada, K. R. F., Zubek, L., Miamoto, A., Hernandes, I., Rissato, B. B., Mizuno, M. S., Schwan, R. F., & Dias-Arieira, C. R. (2020). Effects of yeast fermentation broths on the Meloidogyne incognita population in soybean. Tropical Plant Pathology, 45(2), 112–121.

    Article  Google Scholar 

  • Molinari, S., & Baser, N. (2010). Induction of resistance to root-knot nematodes by SAR elicitors in tomato. Crop Protection, 29(11), 1354–1362.

    Article  CAS  Google Scholar 

  • Molinari, S., & Leonetti, P. (2019). Bio-control agents activate plant immune response and prime susceptible tomato against root-knot nematodes. PLoS One, 14(12), 1–17.

    Article  Google Scholar 

  • Nakamura, T., Murakami, T., Saotome, M., Tomita, K., Kitsuwa, T., & Meyers, S. P. (1991). Identification of indole-3-acetic acid in Pichia spartinae, an ascosporogenous yeast from Spartina alterniflora marshland environments. Mycologia, 83(5), 662–664.

    Article  CAS  Google Scholar 

  • Narusaka, M., Minami, T., Iwabuchi, C., Hamasaki, T., Takasaki, S., Kawamura, K., & Narusaka, Y. (2015). Yeast cell wall extract induces disease resistance against bacterial and fungal pathogens in Arabidopsis thaliana and brassica crop. PLoS One, 10(1), 1–14.

    Article  Google Scholar 

  • Nayak, D. K., & Pandey, R. K. (2016). Physiological and biochemical changes of susceptible and resistant brinjal cultivars induced by root-knot nematode, Meloidogyne incognita. Journal of Global Biosciences, 5(7), 4358–4368.

  • Ngadze, E., Icishahayo, D., Coutinho, T. A., & Van Der Waals, J. E. (2012). Role of polyphenol oxidase, peroxidase, phenylalanine ammonia lyase, chlorogenic acid, and total soluble phenols in resistance of potatoes to soft rot. Plant Disease, 96(2), 186–192.

    Article  CAS  PubMed  Google Scholar 

  • Oostenbrink, R. (1966). Major characteristics of the relation between nematodes and plants. Meded Land-Bouwhogeschool, 66(4), 46.

    Google Scholar 

  • Pascholati, S. F., & Dalio, R. J. D. (2018) Fisiologia do Parasitismo: Como as plantas se defendem dos patógenos. In: Amorim, L., Rezende, J. A. M., Filho, A. B. (Eds), Manual de Fitopatologia: princípios e conceitos. (pp.424-450). Ouro Fino – MG: Agronômica Ceres.

  • Passardi, F., Cosio, C., Penel, C., & Dunand, C. (2005). Peroxidases have more functions than a Swiss army knife. Plant Cell Report, 24(5), 255–265.

    Article  CAS  Google Scholar 

  • Phan, N. T., Waele, D. D., Lorieux, M., Xiong, L., & Bellafiore, S. (2018). A hypersensitivity-like response to Meloidogyne graminicola in rice (Oryza sativa). Phytopathology, 108(4), 521–528.

    Article  PubMed  Google Scholar 

  • Pretscher, J., Fischkal, T., Branscheidt, S., Jäger, L., Kahl, S., Schlander, M., Thines, E., & Claus, H. (2018). Yeasts from different habitats and their potential as biocontrol agents. Fermentation, 4(2), 1–17.

    Article  Google Scholar 

  • Puerari, H. H., Dias-Arieira, C. R., Dadazio, T. S., Mattei, D., Silva, T. R. B., & Ribeiro, R. C. F. (2013). Evaluation of acibenzolar-S-methyl for the control of Meloidogyne javanica and effects on the development of susceptible and resistant soybean. Tropical Plant Pathology, 38(1), 044–048.

    Article  Google Scholar 

  • Quiroga, M., Guerrero, C., Botella, M. A., Barceló, A., Amaya, I., Medina, M. I., Alonso, F. J., Forchetti, S. M., Tigier, H., & Valpuesta, V. (2000). A tomato peroxidase involved in the synthesis of lignin and suberin. Plant Physiology, 122(4), 1119–1127.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raasch-Fernandes, L. D., Bonaldo, S. M., Rodrigues, D. J., Vieira-Junior, G. M., Schwan-Estrada, K. R. F., Silva, C. R., Verçosa, A. G. A., Oliveira, D. L., & Debiasi, B. W. (2019). Induction of phytoalexins and proteins related to pathogenesis in plants treated with extracts of cutaneous secretions of southern Amazonian Bufonidae amphibians. PLoS One, 14(1), 1–22.

    Google Scholar 

  • Sahebani, N., & Hadavi, N. (2008). Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil Biology and Biochemistry, 40(8), 2016–2020.

    Article  CAS  Google Scholar 

  • Singh, R., & Chandrawat, K. S. (2017). Role of phytoalexins in plant disease resistance. International Journal of Current Microbiology and Applied Science, 6(1), 125–129.

    Article  CAS  Google Scholar 

  • Spadaro, D., & Droby, S. (2016). Development of biocontrol products for postharvest diseases of fruit: The importance of elucidating the mechanisms of action of yeast antagonists. Trends in Food Science & Technology, 47(January), 39–49.

    Article  CAS  Google Scholar 

  • Schisler, D. A., Janisiewicz, W. J., Boekhout, T., & Kurtzman, C. P. (2011) Chapter 4 - agriculturally important yeasts: Biological control of field and postharvest diseases using yeast antagonists, and yeasts as pathogens of plants. In: Kurtzman, C. P., Fell, J. W., Boekhout, T. (Eds), The Yeasts (Fifth Edition). (pp. 45–52). Elsevier Science.

  • Schwan-Estrada, K. R. F., Stangarlin, J. R., & Pascholati, S. F. (2008). Mecanismos bioquímicos de defesa vegetal. In S. F. PascholatI, B. Leite, J. R. Stangarlin, & P. Cia (Eds.), Interação Planta-Patógeno, fisiologia, bioquímica e biologia molecular (pp. 227–247). Piracicaba-SP: FEALQ.

    Google Scholar 

  • Stangarlin, J. R., Schulz, D. G., Franzener, G., Assi, L., Schwan-Estrada, K. R. F., & Kuhn, O. J. (2010). Indução de fitoalexinas em soja e sorgo por preparações de Saccharomyces boulardii. Arquivos do Instituto Biológico, 77(1), 91–98.

    Article  Google Scholar 

  • Stangarlin, J. R., Kuhn, O. J., Toledo, M. V., Portz, R. L., Schwan-Estrada, K. R. F., & Pascholati, S. F. (2011). A defesa vegetal contra fitopatógenos. Scientia Agraria Paranaensis, 10(1), 18–46.

    Google Scholar 

  • Sun, C., Fu, D., Lu, H., Zhang, J., Zheng, X., & Yu, T. (2018). Autoclaved yeast enhances the resistance against Penicillium expansum in postharvest pear fruit and its possible mechanisms of action. Biological Control, 119(April), 51–58.

    Article  CAS  Google Scholar 

  • Sundararaj, P., & Kathiresan, T. (2012). Induction of β-1,3-glucanase and chitinase activities in resistant and susceptible sugarcane clones inoculated with Pratylenchus zeae. International Journal of Nematology, 22(1), 47–56.

    Google Scholar 

  • Thakur, M., & Sohal, B. S. (2013). Role of elicitors in inducing resistance in plants against pathogen infection: A review. ISRN Biochemistry, 2013, 1–10.

    Article  Google Scholar 

  • Umesha, S. (2006). Note: Phenylalanine ammonia lyase activity in tomato seedlings and its relationship to bacterial canker disease resistance. Phytoparasitica, 34(1), 68–71.

    Article  CAS  Google Scholar 

  • Vogelsang, R., & Barz, W. (1993). Purification, characterization and differential hormonal regulation of a β-1,3-glucanase and chitinase from chickpea (Cicer arientinum L.). Planta, 189(1), 60–69.

    Article  CAS  PubMed  Google Scholar 

  • Walters, D. R., & Fountaine, J. M. (2009). Practical application of induced resistance to plant diseases: An appraisal of effectiveness under field conditions. Journal of Agricultural Science, 147(5), 523–535.

    Article  CAS  Google Scholar 

  • Walters, D., Walsh, D., Newton, A., & Lyon, G. (2005). Induced resistance for plant disease control: Maximizing the efficacy of resistance elicitors. Phytopathology, 95(12), 1368–1373.

    Article  CAS  PubMed  Google Scholar 

  • Ziegler, E., & Pontzen, R. (1982). Specific inhibition of glucan-elicited glyceolin accumulation in soybeans by an extracellular mannan-glycoprotein of Phytophthora megasperma f. sp. glycinea. Physiological Plant Pathology, 20(3), 321–331.

    Article  CAS  Google Scholar 

  • Zipor, G., & Oren-Shamir, M. (2013). Do vacuolar peroxidases act as plant caretakers? Plant Science, 199-200(February), 41–47.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, Y., Ye, W., & Kerns, J. (2014). First report and morphological and molecular characterization of Meloidogyne incognita from Radermachera sinica in China. Nematropica, 44(2), 118–129.

    Google Scholar 

  • Zhang, X., & Liu, C.-J. (2015). Multifaceted regulations of gateway enzyme phenylalanine ammonia-lyase in the biosynthesis of phenylpropanoids. Molecular Plant, 8(1), 17–27.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors are grateful to CAPES for the scholarship for the first author and to CNPq for the grants awarded to K.R.F. Schwan-Estrada and C.R. Dias-Arieira.

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Mioranza, T.M., Miamoto, A., Mattos, A.P. et al. Lachancea thermotolerans acts as a resistance inducer in soybean infected with Meloidogyne incognita. Eur J Plant Pathol 159, 511–523 (2021). https://doi.org/10.1007/s10658-020-02178-4

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