The potential of endophytic bacteria isolated from Tagetes sp. to control Meloidogyne spp. infection on tomato plants
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Abstract. Munif A, Nursalim M, Pradana AP. 2021. The potential of endophytic bacteria isolated from Tagetes sp. to control Meloidogyne spp. infection on tomato plants. Biodiversitas 22: 3229-3236. The root-knot nematode (Meloidogyne spp.) is one of the plant-parasitic nematodes that cause economical loss in the vegetable plantations in the world. The endophytic bacteria may act as a potential biological agent to control the plant-parasitic nematodes. The aim of this study was to explore the endophytic bacteria from Tagetes sp., which had a potential to control Meloidogyne spp. and act as growth promoter for tomato plants. The endophytic bacteria were isolated from the roots and stems of Tagetes sp. and tissues were cultured on the tryptic soy agar (TSA) media. The endophytic bacterial isolates were selected using hypersensitive and blood agar tests to identify their biological safety. The selected endophytic bacteria were also assessed for growth promoter test in the tomato plants. The selected endophytic bacteria were assessed in vitro against the Meloidogyne spp. juvenile 2 and their effectiveness in suppressing the root-knot nematodes on tomato plants in greenhouse. The results showed that total of 184 endophytic bacterial isolates were successfully isolated from the roots and stem of Tagetes sp. In hypersensitive and hemolytic tests, 78 and 36 isolates showed negative responses, respectively. Of the 36 isolates tested, it was found that 14 of them were able to promote the growth of tomato seedlings. In in vitro test, 14 endophytic bacteria showed 73-93% mortality rate of Meloidogyne spp J2. The results at greenhouse showed that 3 bacterial isolates, namely, AL21, AL44, and AL53 suppress the number of root-knot nematodes up to 50-74% and improve tomato plant growth by 32%. These results indicate that endophytic bacteria isolated from Tagetes sp. have the potential to act as biocontrol agents of parasitic nematodes and a plant growth promoter.
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References
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Anjum R, Afzal M, Baber R, Khan MAJ, Kanwal W, Sajid W, Raheel A. 2019. Endophytes: as potential biocontrol agent—review and future prospects. J Agric Sci 11: 113-125.
Asyiah IN, Mudakir I, Hoesain M, Pradana AP, Djunaidy A, Sari RF. 2020. Consortium of endophytic bacteria and rhizobacteria effectively suppresses the population of Pratylenchus coffeae and promotes the growth of Robusta coffee. Biodiversitas 21(10): 4702-4708.
Balint?Kurti P. 2019. The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20(8): 1163-1178.
Chebotar V, Malfanova N, Shcherbakov A, Ahtemova G, Borisov AY, Lugtenberg B, Tikhonovich I. 2015. Endophytic bacteria in microbial preparations that improve plant development. Appl Biochem Microbiol 51(3): 271-277.
Elling AA. 2013. Major emerging problems with minor Meloidogyne species. Phytopathology 103(11): 1092-1102.
Ferreira MJ, Silva H, Cunha A. 2019. Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: A review. Pedosphere 29(4): 409-420.
Firdous J, Lathif NA, Mona R, Muhamad N. 2019. Endophytic bacteria and their potential application in agriculture: a review. Indian J Agric Res 53(1): 1-7.
Frank AC, Saldierna Guzmán JP, Shay JE. 2017. Transmission of bacterial endophytes. Microorganisms 5(4): 70.
Gupta M, Kiran S, Gulati A, Singh B, Tewari R. 2012. Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiol Res 167(6): 358-363.
Hanawi MJ. 2016. Tagetes erecta with native isolates of Paecilomyces lilacinus and Trichoderma hamatum in controlling root-knot nematode Meloidogyne javanica on tomato. Int J Appl or Innovation Eng Manage 5(1): 81-88.
Hariprasad P, Divakara S, Niranjana S. 2011. Isolation and characterization of chitinolytic rhizobacteria for the management of Fusarium wilt in tomato. Crop Protn 30(12): 1606-1612.
Johnstone IL. 1994. The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. Bioessays 16(3): 171-178.
Kalliora C, Mamoulakis C, Vasilopoulos E, Stamatiades GA, Kalafati L, Barouni R, Karakousi T, Abdollahi M, Tsatsakis A. 2018. Association of pesticide exposure with human congenital abnormalities. Toxicol Appl Pharmacol 346: 58-75.
Kandel SL, Joubert PM, Doty SL. 2017. Bacterial endophyte colonization and distribution within plants. Microorganisms 5(4): 77.
Kaur T, Jasrotia S, Ohri P, Manhas RK. 2016. Evaluation of in vitro and in vivo nematicidal potential of a multifunctional streptomycete, Streptomyces hydrogenans strain DH16 against Meloidogyne incognita. Microbiol Res 192: 247-252.
Khan Z, Doty SL. 2009. Characterization of bacterial endophytes of sweet potato plants. Plant and Soil 322(1): 197-207.
Klement Z, Goodman R. 1967. The hypersensitive reaction to infection by bacterial plant pathogens. Annu Rev Phytopathol 5(1): 17-44.
Kumar V, Kumari A, Angmo K, Bhalla TC. 2017. Isolation and characterization of lactic acid bacteria from traditional pickles of Himachal Pradesh, India. J Food Sci Technol 54(7): 1945-1952.
Le B, Yang SH. 2019. Microbial chitinases: properties, current state and biotechnological applications. World Jo Microb Biot 35(9): 1-12.
Luc M, Sikora RA, Bridge J. 2005. Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Cabi.
Marahatta SP, Wang K-H, Sipes BS, Hooks CR. 2012. Effects of Tagetes patula on active and inactive stages of root-knot nematodes. J Nematol 44(1): 26.
Mardhiana M, Pradana AP, Adiwena M, Santoso D, Wijaya R, Murtilaksono A. 2017. Use of endophytic bacteria from roots of Cyperus rotundus for biocontrol of Meloidogyne incognita. Biodiversitas 18(4): 1308-1315.
Mika A, Boenisch MJ, Hopff D, Lüthje S. 2010. Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors. J Exp Bot 61(3): 831-841.
Miliute I, Buzaite O, Baniulis D, Stanys V. 2015. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agriculture 102(4): 465-478.
Munif A, Herliyana EN, Pradana AP. 2019. Endophytic bacterial consortium originated from forestry plant roots and their nematicidal activity against Meloidogyne incognita infestation in greenhouse. Acta Univ Agric et Silvic 67(5): 1171-1182.
Mustafa S, Kabir S, Shabbir U, Batool R. 2019. Plant growth promoting rhizobacteria in sustainable agriculture: from theoretical to pragmatic approach. Symbiosis 78(2): 115-123.
Ntalli NG, Caboni P. 2012. Botanical nematicides: a review. J Agric Food Chem. 60(40): 9929-9940.
O’Brien PA. 2017. Biological control of plant diseases. Australas Plant Path 46(4): 293-304.
Pavithra G, Bindal S, Rana M, Srivastava S. 2020. Role of endophytic microbes against plant pathogens: a review. Asian J Plant Sci 19(1): 54-62.
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA. 2014. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52: 347-375.
Podolich O, Ardanov P, Zaets I, Pirttilä AM, Kozyrovska N. 2015. Reviving of the endophytic bacterial community as a putative mechanism of plant resistance. Plant and Soil 388(1): 367-377.
Príncipe A, Alvarez F, Castro MG, Zachi L, Fischer SE, Mori GB, Jofré E. 2007. Biocontrol and PGPR features in native strains isolated from saline soils of Argentina. Curr Microbiol 55(4): 314-322.
Ralmi NHAA, Khandaker MM, Mat N. 2016. Occurrence and control of root knot nematode in crops: a review. Aust J Crop Sci 11(12): 1649-1654.
Rosenblueth M, Martínez-Romero E. 2006. Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8): 827-837.
Santos MLd, Berlitz DL, Wiest SLF, Schünemann R, Knaak N, Fiuza LM. 2018. Benefits associated with the interaction of endophytic bacteria and plants. Braz Arch Biol Technol 61: : e18160431.
Shetty LJ, Sakr FM, Al-Obaidy K, Patel MJ, Shareef H. 2015. A brief review on medicinal plant Tagetes erecta Linn. J Appl Pharm Sci 5(3): 91-95.
Singh T, Prajapati A, Maru A, Chaudhary R, Patel D. 2019. Root-knot nematodes (Meloidogyne spp.) infecting pomegranate: a review. Agric Rev 40(4): 309-313.
Stoltzfus J, So R, Malarvithi P, Ladha J, De Bruijn F. 1997. Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant and Soil 194(1): 25-36.
Stroze CT, Baida FC, Balbi-Peña MI, Dias-Arieira CR, Santiago DC. 2019. Tagetes minuta propagation and interaction with Nematoide. J Agric Sci 11(1): 139-148.
Sturz AV, Christie BR, Nowak J. 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19(1): 1-30.
Subedi S, Thapa B, Shrestha J. 2020. Root-knot nematode (Meloidogyne incognita) and its management: a review. J Agric Nat Resour 3(2): 21-31.
Taghavi S, Van Der Lelie D, Hoffman A, Zhang Y-B, Walla MD, Vangronsveld J, Newman L, Monchy S. 2010. Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6(5): e1000943.
Vallad GE, Goodman RM. 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44(6): 1920-1934.
Vallet-Gely I, Novikov A, Augusto L, Liehl P, Bolbach G, Péchy-Tarr M, Cosson P, Keel C, Caroff M, Lemaitre B. 2010. Association of hemolytic activity of Pseudomonas entomophila, a versatile soil bacterium, with cyclic lipopeptide production. Appl Environ Microbiol 76(3): 910-921.
Verma P, Verma A. 2012. Evaluation of antibacterial activity of different parts of Tagetes erecta. Int J Pharm Life Sci 3(6): 1766-1768.
Verma SC, Ladha JK, Tripathi AK. 2001. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2-3): 127-141.
Win KT, Tanaka F, Okazaki K, Ohwaki Y. 2018. The ACC deaminase expressing endophyte Pseudomonas spp. enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance, and ionic balance in tomato plants. Plant Physiol Biochem 127: 599-607.
Wiratno W, Syakir M, Sucipto I, Pradana AP. 2019. Isolation and characterization of endophytic bacteria from roots of Piper nigrum and their activities against Fusarium oxysporum and Meloidogyne incognita. Biodiversitas 20(3): 682-687.
XU L-w, Juan C, QI H-y, SHI Y-p. 2012. Phytochemicals and their biological activities of plants in Tagetes L. Chin Herb Med 4(2): 103-117.
Yadav AN, Verma P, Singh B, Chauhan VS, Suman A, Saxena AK. 2017. Plant growth promoting bacteria: biodiversity and multifunctional attributes for sustainable agriculture. Adv Biotechnol Microbiol 5(5): 1-16.
Anjum R, Afzal M, Baber R, Khan MAJ, Kanwal W, Sajid W, Raheel A. 2019. Endophytes: as potential biocontrol agent—review and future prospects. J Agric Sci 11: 113-125.
Asyiah IN, Mudakir I, Hoesain M, Pradana AP, Djunaidy A, Sari RF. 2020. Consortium of endophytic bacteria and rhizobacteria effectively suppresses the population of Pratylenchus coffeae and promotes the growth of Robusta coffee. Biodiversitas 21(10): 4702-4708.
Balint?Kurti P. 2019. The plant hypersensitive response: concepts, control and consequences. Mol Plant Pathol 20(8): 1163-1178.
Chebotar V, Malfanova N, Shcherbakov A, Ahtemova G, Borisov AY, Lugtenberg B, Tikhonovich I. 2015. Endophytic bacteria in microbial preparations that improve plant development. Appl Biochem Microbiol 51(3): 271-277.
Elling AA. 2013. Major emerging problems with minor Meloidogyne species. Phytopathology 103(11): 1092-1102.
Ferreira MJ, Silva H, Cunha A. 2019. Siderophore-producing rhizobacteria as a promising tool for empowering plants to cope with iron limitation in saline soils: A review. Pedosphere 29(4): 409-420.
Firdous J, Lathif NA, Mona R, Muhamad N. 2019. Endophytic bacteria and their potential application in agriculture: a review. Indian J Agric Res 53(1): 1-7.
Frank AC, Saldierna Guzmán JP, Shay JE. 2017. Transmission of bacterial endophytes. Microorganisms 5(4): 70.
Gupta M, Kiran S, Gulati A, Singh B, Tewari R. 2012. Isolation and identification of phosphate solubilizing bacteria able to enhance the growth and aloin-A biosynthesis of Aloe barbadensis Miller. Microbiol Res 167(6): 358-363.
Hanawi MJ. 2016. Tagetes erecta with native isolates of Paecilomyces lilacinus and Trichoderma hamatum in controlling root-knot nematode Meloidogyne javanica on tomato. Int J Appl or Innovation Eng Manage 5(1): 81-88.
Hariprasad P, Divakara S, Niranjana S. 2011. Isolation and characterization of chitinolytic rhizobacteria for the management of Fusarium wilt in tomato. Crop Protn 30(12): 1606-1612.
Johnstone IL. 1994. The cuticle of the nematode Caenorhabditis elegans: a complex collagen structure. Bioessays 16(3): 171-178.
Kalliora C, Mamoulakis C, Vasilopoulos E, Stamatiades GA, Kalafati L, Barouni R, Karakousi T, Abdollahi M, Tsatsakis A. 2018. Association of pesticide exposure with human congenital abnormalities. Toxicol Appl Pharmacol 346: 58-75.
Kandel SL, Joubert PM, Doty SL. 2017. Bacterial endophyte colonization and distribution within plants. Microorganisms 5(4): 77.
Kaur T, Jasrotia S, Ohri P, Manhas RK. 2016. Evaluation of in vitro and in vivo nematicidal potential of a multifunctional streptomycete, Streptomyces hydrogenans strain DH16 against Meloidogyne incognita. Microbiol Res 192: 247-252.
Khan Z, Doty SL. 2009. Characterization of bacterial endophytes of sweet potato plants. Plant and Soil 322(1): 197-207.
Klement Z, Goodman R. 1967. The hypersensitive reaction to infection by bacterial plant pathogens. Annu Rev Phytopathol 5(1): 17-44.
Kumar V, Kumari A, Angmo K, Bhalla TC. 2017. Isolation and characterization of lactic acid bacteria from traditional pickles of Himachal Pradesh, India. J Food Sci Technol 54(7): 1945-1952.
Le B, Yang SH. 2019. Microbial chitinases: properties, current state and biotechnological applications. World Jo Microb Biot 35(9): 1-12.
Luc M, Sikora RA, Bridge J. 2005. Plant Parasitic Nematodes in Subtropical and Tropical Agriculture. Cabi.
Marahatta SP, Wang K-H, Sipes BS, Hooks CR. 2012. Effects of Tagetes patula on active and inactive stages of root-knot nematodes. J Nematol 44(1): 26.
Mardhiana M, Pradana AP, Adiwena M, Santoso D, Wijaya R, Murtilaksono A. 2017. Use of endophytic bacteria from roots of Cyperus rotundus for biocontrol of Meloidogyne incognita. Biodiversitas 18(4): 1308-1315.
Mika A, Boenisch MJ, Hopff D, Lüthje S. 2010. Membrane-bound guaiacol peroxidases from maize (Zea mays L.) roots are regulated by methyl jasmonate, salicylic acid, and pathogen elicitors. J Exp Bot 61(3): 831-841.
Miliute I, Buzaite O, Baniulis D, Stanys V. 2015. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agriculture 102(4): 465-478.
Munif A, Herliyana EN, Pradana AP. 2019. Endophytic bacterial consortium originated from forestry plant roots and their nematicidal activity against Meloidogyne incognita infestation in greenhouse. Acta Univ Agric et Silvic 67(5): 1171-1182.
Mustafa S, Kabir S, Shabbir U, Batool R. 2019. Plant growth promoting rhizobacteria in sustainable agriculture: from theoretical to pragmatic approach. Symbiosis 78(2): 115-123.
Ntalli NG, Caboni P. 2012. Botanical nematicides: a review. J Agric Food Chem. 60(40): 9929-9940.
O’Brien PA. 2017. Biological control of plant diseases. Australas Plant Path 46(4): 293-304.
Pavithra G, Bindal S, Rana M, Srivastava S. 2020. Role of endophytic microbes against plant pathogens: a review. Asian J Plant Sci 19(1): 54-62.
Pieterse CM, Zamioudis C, Berendsen RL, Weller DM, Van Wees SC, Bakker PA. 2014. Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52: 347-375.
Podolich O, Ardanov P, Zaets I, Pirttilä AM, Kozyrovska N. 2015. Reviving of the endophytic bacterial community as a putative mechanism of plant resistance. Plant and Soil 388(1): 367-377.
Príncipe A, Alvarez F, Castro MG, Zachi L, Fischer SE, Mori GB, Jofré E. 2007. Biocontrol and PGPR features in native strains isolated from saline soils of Argentina. Curr Microbiol 55(4): 314-322.
Ralmi NHAA, Khandaker MM, Mat N. 2016. Occurrence and control of root knot nematode in crops: a review. Aust J Crop Sci 11(12): 1649-1654.
Rosenblueth M, Martínez-Romero E. 2006. Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19(8): 827-837.
Santos MLd, Berlitz DL, Wiest SLF, Schünemann R, Knaak N, Fiuza LM. 2018. Benefits associated with the interaction of endophytic bacteria and plants. Braz Arch Biol Technol 61: : e18160431.
Shetty LJ, Sakr FM, Al-Obaidy K, Patel MJ, Shareef H. 2015. A brief review on medicinal plant Tagetes erecta Linn. J Appl Pharm Sci 5(3): 91-95.
Singh T, Prajapati A, Maru A, Chaudhary R, Patel D. 2019. Root-knot nematodes (Meloidogyne spp.) infecting pomegranate: a review. Agric Rev 40(4): 309-313.
Stoltzfus J, So R, Malarvithi P, Ladha J, De Bruijn F. 1997. Isolation of endophytic bacteria from rice and assessment of their potential for supplying rice with biologically fixed nitrogen. Plant and Soil 194(1): 25-36.
Stroze CT, Baida FC, Balbi-Peña MI, Dias-Arieira CR, Santiago DC. 2019. Tagetes minuta propagation and interaction with Nematoide. J Agric Sci 11(1): 139-148.
Sturz AV, Christie BR, Nowak J. 2000. Bacterial endophytes: potential role in developing sustainable systems of crop production. Crit Rev Plant Sci 19(1): 1-30.
Subedi S, Thapa B, Shrestha J. 2020. Root-knot nematode (Meloidogyne incognita) and its management: a review. J Agric Nat Resour 3(2): 21-31.
Taghavi S, Van Der Lelie D, Hoffman A, Zhang Y-B, Walla MD, Vangronsveld J, Newman L, Monchy S. 2010. Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6(5): e1000943.
Vallad GE, Goodman RM. 2004. Systemic acquired resistance and induced systemic resistance in conventional agriculture. Crop Sci 44(6): 1920-1934.
Vallet-Gely I, Novikov A, Augusto L, Liehl P, Bolbach G, Péchy-Tarr M, Cosson P, Keel C, Caroff M, Lemaitre B. 2010. Association of hemolytic activity of Pseudomonas entomophila, a versatile soil bacterium, with cyclic lipopeptide production. Appl Environ Microbiol 76(3): 910-921.
Verma P, Verma A. 2012. Evaluation of antibacterial activity of different parts of Tagetes erecta. Int J Pharm Life Sci 3(6): 1766-1768.
Verma SC, Ladha JK, Tripathi AK. 2001. Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91(2-3): 127-141.
Win KT, Tanaka F, Okazaki K, Ohwaki Y. 2018. The ACC deaminase expressing endophyte Pseudomonas spp. enhances NaCl stress tolerance by reducing stress-related ethylene production, resulting in improved growth, photosynthetic performance, and ionic balance in tomato plants. Plant Physiol Biochem 127: 599-607.
Wiratno W, Syakir M, Sucipto I, Pradana AP. 2019. Isolation and characterization of endophytic bacteria from roots of Piper nigrum and their activities against Fusarium oxysporum and Meloidogyne incognita. Biodiversitas 20(3): 682-687.
XU L-w, Juan C, QI H-y, SHI Y-p. 2012. Phytochemicals and their biological activities of plants in Tagetes L. Chin Herb Med 4(2): 103-117.
Yadav AN, Verma P, Singh B, Chauhan VS, Suman A, Saxena AK. 2017. Plant growth promoting bacteria: biodiversity and multifunctional attributes for sustainable agriculture. Adv Biotechnol Microbiol 5(5): 1-16.
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