Combined effects of Ascophyllum nodosum seaweed extract and biological control agents on Meloidogyne javanica in soybean

References

• Abbasi MW, Ahmed N, Zaki MJ, Shuakat SS, Khan D. 2014. Potential of Bacillus species against Meloidogyne javanica parasitizing eggplant (Solanum melongena L.) and induced biochemical changes. Plant Soil. 375:159–173. doi:10.1007/s11104-013-1931-6.
   Web of Science ®Google Scholar
• Abdel-Azeem A, Nada AA, O’Donovan A, Thakur VK, Elkelish A. 2020. Mycogenic silver nanoparticles from endophytic Trichoderma atroviride with antimicrobial activity. J Renew Mater. 8:171–185. doi:10.32604/jrm.2020.08960.
   Web of Science ®Google Scholar
• Abd El-Rahman SS, Mazen MM, Mohamed HI, Mahmoud NM. 2012. Induction of defence related enzymes and phenolic compounds in lupin (Lupinus albus L.) and their effects on host resistance against Fusarium wilt. Eur J Plant Pathol. 134:105–116. doi:10.1007/s10658-012-0028-z.
   Web of Science ®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):e90402. doi:10.1371/journal.pone.0090402.
   PubMed Web of Science ®Google Scholar
• Almeida AA, Abe VHF, Gonçalves RM, Balbi-Peña MI, Santiago DC. 2017. Seed treatment for management of Meloidogyne javanica in soybean. Sem Cien Agrar. 38(5):2995–3005. doi:10.5433/1679-0359.2017v38n5p2995.
   Web of Science ®Google Scholar
• Alves TS, Campos LL, Elias Neto N, Matsuoka M, Loureiro MF. 2011. Biomassa e atividade microbiana de solo sob vegetação nativa e diferentes sistemas de manejos. Acta Sci Agron. 33(2):341–347. doi:10.4025/actasciagron.v33i2.4841.
   Google Scholar
• Audibert L, Fauchon M, Blanc N, Hauchard D, Ar Gall E. 2010. Phenolic compounds in the brown seaweed Ascophyllum nodosum: distribution and radical-scavenging activities. Phytochem Anal. 21(5):399–405. doi:10.1002/pca.1210.
   PubMed Web of Science ®Google Scholar
• Battacharyya D, Babgohari MZ, Rathor P, Prithiviraj B. 2015. Seaweed extracts as biostimulants in horticulture. Sci Hortic. 196:39–48. doi:10.1016/j.scienta.2015.09.012.
   Web of Science ®Google Scholar
• Boneti JIS, Ferraz S. 1981. Modificações do método de Hussey & Barker para extração de ovos de Meloidogyne exigua em raízes de cafeeiro. Fitopatol Bras. 6:553.
   Google Scholar
• Chen M, Zhao Y, Yu S. 2015. Optimisation of ultrasonic-assisted extraction of phenolic compounds, antioxidants, and anthocyanins from sugar beet molasses. Food Chem. 172:543–550. doi:10.1016/j.foodchem.2014.09.110.
   PubMed Web of Science ®Google Scholar
• Corte GD, Pinto FF, Stefanello MT, Gulart C, Ramos JP, Balardin RS. 2014. Tecnologia de aplicação de agrotóxicos no controle de fitonematoides em soja. Cienc Rural. 44(9):1534–1540. doi:10.1590/0103-8478cr20130738.
   Google Scholar
• Craigie JS. 2011. Seaweed extract stimuli in plant science and agriculture. J Appl Phycol. 23:371–393. doi:10.1007/s10811-010-9560-4.
   Web of Science ®Google Scholar
• Cunha EQ, Stone LF, Ferreira EPB, Didonet AD, Moreira JAA, Leandro WM. 2011. Sistemas de preparo do solo e culturas de cobertura na produção orgânica de feijão e milho: II - atributos biológicos do solo. Rev Bras Cienc Solo. 35(2):603–611. doi:10.1590/S0100-06832011000200029.
   Google Scholar
• Demoling F, Figueroa D, Baath E. 2007. Comparison of factors limiting bacterial growth in different soils. Soil Biol Biochem. 39(10):2485–2495. doi:10.1016/j.soilbio.2007.05.002.
   Web of Science ®Google Scholar
• du Jardin P. 2012. The science of plant biostimulants - A bibliographic analysis. https://orbi.uliege.be/bitstream/2268/169257/1/Plant_Biostimulants_final_report_bio_2012_en.pdf.
   Google Scholar
• du Jardin P. 2015. Plant biostimulants: definition, concept, main categories and regulation. Sci Hortic. 196:3–14. doi:10.1016/j.scienta.2015.09.021.
   Web of Science ®Google Scholar
• Escudero N, Lopez-Llorca LV. 2012. Effects on plant growth and root-knot nematode infection of an endophytic GFP transformant of the nematophagous fungus Pochonia chlamydosporia. Symbiosis. 57:33–42. doi:10.1007/s13199-012-0173-3.
   Web of Science ®Google Scholar
• Ferreira DF. 2011. Sisvar: a computer statistical analysis system. Cienc Agrotec. 35:1039–1042. doi:10.1590/S1413-70542011000600001.
   Web of Science ®Google Scholar
• Fischer IH, Bueno CJ, Garcia MJM, Almeida AM. 2010. Reação de maracujazeiro-amarelo ao complexo fusariose-nematoide de galha. Acta Sci Agron. 32(2):223–227. doi:10.4025/actasciagron.v32i2.3445.
   Google Scholar
• Freitas MA, Pedrosa EMR, Mariano RLR, Guimarães LMP. 2012. Seleção de Trichoderma spp. como potenciais agentes de biocontrole para Meloidogyne incognita em cana-de-açúcar. Nematropica. 42(1):115–122.
   Google Scholar
• Gattoni K, Xiang N, Lawaju B, Lawrence KS, Park SW, Kloepper JW. 2019. Potential mechanism of action for Bacillus spp. inducing resistance to Meloidogyne incognita on cotton. Proceedings of the Abstracts of the 58th Annual Meeting of the Society of Nematologists, North Carolina.
   Google Scholar
• Ghahremani Z, Escudero N, Saus E, Gabaldón T, Sorribas FJ. 2019. Pochonia chlamydosporia induces plant-dependent systemic resistance to Meloidogyne incognita. Front Plant Sci. 10:945. doi:10.3389/fpls.2019.00945.
   PubMed Web of Science ®Google Scholar
• Giné A, Bonmatí M, Sarro A, Stchiegel A, Valero J, Ornat C, Fernandez C, Sorribas FJ. 2013. Natural occurrence of fungal egg parasites of root-knot nematodes, Meloidogyne spp. in organic and integrated vegetable production systems in Spain. Bio Control. 58:407–416.
   Web of Science ®Google Scholar
• Holdt SL, Kraan S. 2011. Bioactive compounds in seaweed; funcional food applications and legislation. J Appl Phycol. 23(3):543–597.
   Web of Science ®Google Scholar
• Hussey RS, Barker KR. 1973. A comparison of methods colleting inocula of Meloidogyne spp. including a new technique. Plant Dis. 57(1):1025–1028.
   Google Scholar
• Ishii T, Kitabayashi H, Aikawa J, Matsumoto I, Kadoya K, Kirino S. 2000. Effects of alginate oligosaccharide and polyamines on hyphal growth of vesicular-arbuscular mycorrhizal fungi and their infectivity of citrus roots. 1030–1032. Proc Int Soc Citricult. 2:1030–1032.
   Google Scholar
• Islam KR, Weil RR. 2000. Land use effects on soil quality in a tropical forest ecosystem of Bangladesh. Agric Ecosyst Environ. 79(1):9–16. doi:10.1016/S0167-8809(99)00145-0.
   Web of Science ®Google Scholar
• Jamal Q, Cho JY, Moon JH, Munir S, Anees M, Kim KY. 2017. Identification for the first time of cyclo (d-Pro-l-Leu) produced by Bacillus amyloliquefaciens Y1 as a nematocide for control of Meloidogyne incognita. Molecules. 22:11. 1839. doi:10.3390/molecules22111839.
   Web of Science ®Google Scholar
• Jenkins T, Blunden G, Wu Y, Hankins SD, Gabrielsen BO. 1998. Are the reductions in nematode attack on plants treated with seaweed extracts the result of stimulation of the formaldehyde cycle? Acta Biol Hung. 49(2–4):421–427. doi:10.1007/BF03543065.
   PubMed Web of Science ®Google Scholar
• Jenkinson DS, Powlson DS. 1976. The effects of biocidal treatments on metabolism in soil - V: a method for measuring soil biomass. Soil Biol Biochem. 8:209–213. doi:10.1016/0038-0717(76)90005-5.
   Web of Science ®Google Scholar
• Jensen JP, Beeman AQ, Njus ZL, Kalwa U, Pandey S, Tylka GL. 2018. Movement and motion of soybean cyst nematode Heterodera glycines populations and individuals in response to Abamectin. Phytopathol. 108(7):885–891. doi:10.1094/PHYTO-10-17-0339-R.
   PubMed Web of Science ®Google Scholar
• Kauffman GL, Kneivel DP, Watschke TL. 2007. Effects of a biostimulant on the heat tolerance associated with photosynthetic capacity, membrane thermostability, and polyphenol production of perennial ryegrass. Crop Sci. 47:261–267.
   Web of Science ®Google Scholar
• Khan SA, Abid M, Hussain F. 2015. Nematicidal activity of seaweeds against Meloidogyne javanica. Pak J Nematol. 33:195–203.
   Google Scholar
• Kuwada K, Ishii T, Matsushita I, Matsumoto I, Kadoya K. 1999. Effect of seaweed extracts on hyphal growth of vesicular arbuscular mycorrhizal fungi and their infectivity on trifoliate Orange roots. J Jpn Soc Hortic Sci. 68:321–326. doi:10.2503/jjshs.68.321.
   Google Scholar
• Kuwada K, Utamura M, Matsushita I, Ishii T. 2000. Effect of tangle stock ground extracts on in vitro hyphal growth of vesicular-arbuscular mycorrhizal fungi and their in vivo infections of citrus roots. Proc Int Citrus Cong. 9:1034–1037.
   Google Scholar
• Lopes CVA, Albuquerque GSC. 2018. Agrotóxicos e seus impactos na saúde humana e ambiental: uma revisão sistemática. Saúde debate. 42:117. doi:10.1590/0103-1104201811714.
   Google Scholar
• López-Búcio J, Pelagio-Flores R, Herrera-Estrella A. 2015. Trichoderma as biostimulant: exploiting the multilevel properties of a plant beneficial fungus. Sci Hortic. 196:109–123. doi:10.1016/j.scienta.2015.08.043.
   Web of Science ®Google Scholar
• Machado DFM, Tavares AP, Lopes SJ, Silva ACF. 2015. Trichoderma spp. na emergência e crescimento de mudas de cambará (Gochnatia polymorpha (Less.) Cabrera). Rev Arvore. 39(1):167–176. doi:10.1590/0100-67622015000100016.
   Google Scholar
• Makunde PT, Dimbi S, Mahere TS. 2018. Leguminous crops as an alternative rotation with tobacco to control Meloidogyne javanica. J Entomol Nematol. 10(1):1–5. doi:10.5897/JEN2017.0192.
   Google Scholar
• Martínez‐Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM. 2017. Shifting from priming of salicylic acid‐to jasmonic acid‐regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol. 213(3):1363–1377. doi:10.1111/nph.14251.
   PubMed Web of Science ®Google Scholar
• Medeiros HA, Resende RS, Ferreira FC, Freitas LG, Rodrigues FA. 2015. Induction of resistance in tomato against Meloidogyne javanica by Pochonia chlamydosporia. Nematoda. 2:e10015.
   Google Scholar
• Metwally WE, Khalil AE, Mostafa FAM. 2019. Biopesticides as eco-friendly alternatives for the management of root-knot nematode, Meloidogyne incognita on cowpea (Vigna unguiculata L.). Egypt J Agronematol. 18(2):129–145. doi:10.21608/ejaj.2019.51846.
   Google Scholar
• Montero L, Sánchez-Camargo AP, García-Cañas V, Tanniou A, Stiger-Pouvreau V, Russo M, Rastrelli L, Cifuentesa A, Herrero M, Ibáñez E. 2016. Anti-proliferative activity and chemical characterization by comprehensive two-dimensional liquid chromatography coupled to mass spectrometry of phlorotannins from the brown macroalga Sargassum muticum collected on North-Atlantic coasts. J Chromatogr A. 1428:115–125. doi:10.1016/j.chroma.2015.07.053.
   PubMed Web of Science ®Google Scholar
• Moreira R, Sineiro J, Chenlo F, Arufe S, Díaz-Varela D. 2017. Aqueous extracts of Ascophyllum nodosum obtained by ultrasound-assisted extraction: effects of drying temperature of seaweed on the properties of extracts. J Appl Phycol. 29:3191–3200. doi:10.1007/s10811-017-1159-6.
   Web of Science ®Google Scholar
• Mukhtar T. 2018. Management of root-knot nematode, Meloidogyne incognita, in tomato with two Trichoderma species. Pak J Zool. 50(4):1589–1592. doi:10.17582/journal.pjz/2018.50.4.sc15.
   Web of Science ®Google Scholar
• Muñoz-Leoz B, Garbisu C, Charcosset JY, Sánchez-Pérez JM, Antigüedad I, Ruiz-Romera E. 2013. Non-target effects of three formulated pesticides on microbially-mediated processes in a clay-loam soil. Sci Total Environ. 449:345–354. doi:10.1016/j.scitotenv.2013.01.079.
   PubMed Web of Science ®Google Scholar
• Ngala BM, Valdes Y, Dos Santos G, Perry RN, Wesemael WML. 2016. Seaweed-based products from Ecklonia maxima and Ascophyllum nodosum as control agents for the root-knot nematodes Meloidogyne chitwoodi and Meloidogyne hapla on tomato plants. J Appl Phycol. 28:2073–2082. doi:10.1007/s10811-015-0684-4.
   Web of Science ®Google Scholar
• Nianlai C, Min H, Chunyan D, Shaimei Y. 2010. The effects of inducing treatments on phenolic metabolism of melon leaves. Acta Hortic. 379:1759–1766.
   Google Scholar
• Peres JCF, Carvalho LR, Gonçalez E, Berian LOS, Felicio JD. 2012. Evaluation of antifungal activity of seaweed extracts. Ciênc Agrotec. 36(3):294–299. doi:10.1590/S1413-70542012000300004.
   Web of Science ®Google Scholar
• Radwan MA, Abu-Elamayem MM, Farrag SAA, Ahmed NS. 2011. Integrated management of Meloidogyne incognita infecting tomato using bio-agents mixed with either oxamyl or organic amendments. Nematol Medit. 39:151–156.
   Google Scholar
• Radwan MA, Farrag SAA, Abu-Elamayem MM, Ahmed NS. 2012. Biological control of the root-knot nematode, Meloidogyne incognita on tomato using bioproducts of microbial origin. Appl Soil Ecol. 56:58–62. doi:10.1016/j.apsoil.2012.02.008.
   Web of Science ®Google Scholar
• Rinaldi LK, Miamoto A, Calandrelli A, Silva MTR, Chidichima LPS, Pereira CB, Dias-Arieira CR. 2021. Control of Meloidogyne javanica and induction of resistance-associated enzymes in soybean by extracts of Ascophyllum nodosum. J Appl Psychol. 33:2655–2666.
   Google Scholar
• Ritzinger CHP, Fancelli M, Ritzinger R. 2010. Nematoides: bioindicadores de sustentabilidade e mudanças edafoclimáticas. Rev Bras Frutic. 32(4):1289–1296. doi:10.1590/S0100-29452010000400045.
   Google Scholar
• Rocha AG, Pitombo LM, Bresolin JD, da Silva WTL, Espindola ELG, Oliveira VBM. 2020. Single and combined toxicity of the pesticides abamectin and difenoconazole on soil microbial activity and Enchytraeus crypticus population. SN Appl Sci. 2:1390. doi:10.1007/s42452-020-3175-4.
   Web of Science ®Google Scholar
• Sahebani N, Hadavi N. 2008. Biological control of the root-knot nematode Meloidogyne javanica by Trichoderma harzianum. Soil Biol Biochem. 40:2016–2020. doi:10.1016/j.soilbio.2008.03.011.
   Web of Science ®Google Scholar
• Sharma IP, Sharma AK. 2017. Physiological and biochemical changes in tomato cultivar PT-3 with dual inoculation of mycorrhiza and PGPR against root-knot nematode. Symbiosis. 71:175–183. doi:10.1007/s13199-016-0423-x.
   Web of Science ®Google Scholar
• Shukla PS, Grace ME, Mohd A, Sruti B, Critchley AT, Balakrishnan P. 2019. Ascophyllum nodosum-based biostimulants: sustainable applications in agriculture for the stimulation of plant growth, stress tolerance, and disease management. Front Plant Sci. 10:655. doi:10.3389/fpls.2019.00655.
   PubMed Web of Science ®Google Scholar
• Sikora RA, Schafer K, Dababat AA. 2007. Modes of action associated with microbially induced in planta suppression of plant-parasitic nematodes. Australas Plant Pathol. 36:124–134. doi:10.1071/AP07008.
   Web of Science ®Google Scholar
• Silva EE, Azevedo PHS, De-Polli H. 2007. Determinação da respiração basal (RBS) e quociente metabólico do solo (qCO2). Embrapa: Seropédica; p. 4. (Comunicado técnico, 99).
   Google Scholar
• Singh UP, Sarma BK, Singh DP. 2003. Effect of plant growth promoting rhizobacteria and culture filtrate of Sclerotium rolfesii on phenolic and salicylic acid contents in chickpea (Cicer arietinum). Curr Microbiol. 46:131–140. doi:10.1007/s00284-002-3834-2.
   PubMed Web of Science ®Google Scholar
• Singh HB, Singh BN, Singh SP, Nautiyal CS. 2010. Solid-state cultivation of Trichoderma harzianum NBRI-1055 for modulating natural antioxidants in soybean seed matrix. Bioresour Technol. 101(16):6444–6453. doi:10.1016/j.biortech.2010.03.057.
   PubMed Web of Science ®Google Scholar
• Sohrabi F, Sheikholeslami M, Heydari R, Rezaee S, Sharifi R. 2020. Investigating the effect of Glomus mosseae, Bacillus subtilis and Trichoderma harzianum on plant growth and controlling Meloidogyne javanica in tomato. Indian Phytopathol. 73:293–300. doi:10.1007/s42360-020-00227-w.
   Google Scholar
• Strack D. 1997. Phenolic Metabolism. In: Dey JB, Harbone JB, editors. Plant Biochemistry. London: Academic Press; p. 554.
   Google Scholar
• Taylor A, Sasser JN. 1978. Biology, identification and control of root-knot nematodes. International Meloidogyne Project 111. North Carolina (NC): Raleigh.
   Google Scholar
• Vos C, Schouteden N, van Tuinen D, Chatagnier O, Elsen A, De Waele D, Panisa B, Gianinazzi-Pearson V. 2013. Mycorrhiza-induced resistance against the root–knot nematode Meloidogyne incognita involves priming of defense gene responses in tomato. Soil Biol Biochem. 60:45–54. doi:10.1016/j.soilbio.2013.01.013.
   Web of Science ®Google Scholar
• Whapham CA, Jenkins T, Blunden G, Hankins SD. 1994. The role of seaweed extracts, Ascophyllum nodosum, in the reduction in fecundity of Meloidogyne javanica. Fundam Appl Nematol. 17:181–183.
   Google Scholar
• Wijesinghe WAJP, Jeon Y. 2012. Exploiting biological activities of brown seaweed Ecklonia cava for potential industrial applications: a review. Int J Food Sci Nutr. 63:225–235. doi:10.3109/09637486.2011.619965.
   PubMed Web of Science ®Google Scholar
• Witt C, Gaunt JL, Galicia CC, Ottow JCG, Neue HU 2000. A rapid chloroform-fumigation extraction method for measuring soil microbial biomass carbon and nitrogen in flooded rice soils. Biol Fert Soils. 30:510–519. doi:10.1007/s003740050030.
   Web of Science ®Google Scholar
• Wu Y, Jenkins T, Blunden G, von Mende N, Hankins SD. 1998. Suppression of fecundity of the root-knot nematode, Meloidogyne javanica, in monoxenic cultures of Arabidopsis thaliana treated with an alkaline extract of Ascophyllum nodosum. J Appl Phycol. 10(1):91. doi:10.1023/A:1008067420092.
   Web of Science ®Google Scholar
• Wu Y, Jenkins T, Blunden G, Whapham C, Hankins DS. 1997. The role of betaines in alkaline extracts of Ascophyllum nodosum in the reduction of Meloidogyne javanica and M. incognita infestations of tomato plants. Fundam Appl Nematol. 20(2):99–102.
   Google Scholar
• Xiang N, Lawrence KS, Donald PA. 2018. Biological control potential of plant growth-promoting rhizobacteria suppression of Meloidogyne incognita on cotton and Heterodera glycines on soybean: a review. J Phytopathol. 166:449–458. doi:10.1111/jph.12712.
   Web of Science ®Google Scholar
• Xiang N, Lawrence KS, Kloepper JW, Donald PA, Mcinroy JA, Lawrence GW. 2017. Biological control of Meloidogyne incognita by spore-forming plant growth-promoting rhizobacteria on cotton. Plant Dis. 101:774–784. doi:10.1094/PDIS-09-16-1369-RE.
   PubMed Web of Science ®Google Scholar
• Yuan Y, Zhang J, Fan J, Clark J, Shen P, Li Y, Zhang C. 2018. Microwave assisted extraction of phenolic compounds from four economic brown macroalgae species and evaluation of their antioxidant activities and inhibitory effects on α-amylase, α-glucosidase, pancreatic lipase and tyrosinase. Food Res Int. 113:288–297.
   PubMed Web of Science ®Google Scholar