Ascomycetous isolates promote soil biological and nutritional attributes in corn and soybeans in sandy and clayey soils

Rhizosphere - Tập 24 - Trang 100625 - 2022
Bruno Borges Barbosa1, Jayder Pereira Pimentel1, Nathália Silva Rodovalho1, Simone Cristina Braga Bertini1, Ajay Kumar2, Luiz Fernando Romanholo Ferreira3, Lucas Carvalho Basilio Azevedo1
1Instituto de Ciências Agrárias, Federal University of Uberlândia, Campus Glória, 38410-337, Uberlândia, Minas Gerais, Brazil
2Agriculture Research Organization Volcani Center Israel, Brazil
3Waste and Effluent Treatment Laboratory, Institute of Technology and Research (ITP), Graduate Program in Process Engineering, Tiradentes University, Farolândia, Aracaju, SE, 49032-490, Brazil

Tài liệu tham khảo

Ahmad, 2020, Endophytic Metarhizium robertsii promotes maize growth, suppresses insect growth, and alters plant defense gene expression, Biol. Control, 144, 10.1016/j.biocontrol.2019.104167 Alef, 1995, Soil respiration, 214 Alves, 2021, Fungal endophytes inoculation improves soil nutrient availability, arbuscular mycorrhizal colonization and common bean growth, Rhizosphere, 18, 10.1016/j.rhisph.2021.100330 Amsili, 2021, Cropping system and soil texture shape soil health outcomes and scoring functions, Soil Security, 4, 10.1016/j.soisec.2021.100012 Ashrafi, 2014, Co-inoculations of arbuscular mycorrhizal fungi and rhizobia under salinity in alfalfa, Soil Sci. Plant Nutr., 60, 619, 10.1080/00380768.2014.936037 Barelli, 2020, Plant microbiome analysis after Metarhizium amendment reveals increases in abundance of plant growth-promoting organisms and maintenance of disease-suppressive soil, PLoS One, 15, e0231150, 10.1371/journal.pone.0231150 Baron, 2020, Purpureocillium lilacinum and Metarhizium marquandii as plant growth-promoting fungi, PeerJ, 8, 10.7717/peerj.9005 Barra-Bucarei, 2020, Beauveria bassiana multifunction as an endophyte: growth promotion and biologic control of Trialeurodes vaporariorum (Westwood)(Hemiptera: aleyrodidae) in tomato, Insects, 11, 591, 10.3390/insects11090591 Batool, 2022, Myco-synergism boosts herbivory-induced maize defense by triggering antioxidants and phytohormone signaling, Front. Plant Sci., 13, 10.3389/fpls.2022.790504 Blond, 2018, Non-host larvae negatively impact persistence of the entomopathogen Beauveria bassiana in soil, J. Invertebr. Pathol., 156, 19, 10.1016/j.jip.2018.07.001 Canassa, 2019, Effects of bean seed treatment by the entomopathogenic fungi Metarhizium robertsii and Beauveria bassiana on plant growth, spider mite populations and behavior of predatory mites, Biol. Control, 132, 199, 10.1016/j.biocontrol.2019.02.003 Castro, 2016, Persistence of Brazilian isolates of the entomopathogenic fungi Metarhizium anisopliae and M. robertsii in strawberry crop soil after soil drench application, Agric. Ecosyst. Environ., 233, 361, 10.1016/j.agee.2016.09.031 Cavello, 2015, Plant growth promotion activity of keratinolytic fungi growing on a recalcitrant waste known as “hair waste”, Biotechnol. Res. Int., 1, 10.1155/2015/952921 Centeno, 2017, Textura do solo: conceitos e aplicações em solos arenosos, Revista Brasileira de Engenharia e Sustentabilidade, 4, 31, 10.15210/rbes.v4i1.11576 Choi, 2018, Mechanisms underlying establishment of arbuscular mycorrhizal symbioses, Annu. Rev. Phytopathol., 56, 135, 10.1146/annurev-phyto-080516-035521 Corrêa‐Moreira, 2022, Purpureocillium lilacinum an emergent pathogen: antifungal susceptibility of environmental and clinical strains, Lett. Appl. Microbiol., 75, 45, 10.1111/lam.13707 Dexter, 2004, Soil physical quality: Part I. Theory, effects of soil texture, density, and organic matter, and effects on root growth, Geoderma, 120, 201, 10.1016/j.geoderma.2003.09.004 Doni, 2022, Multi-omics approaches for deciphering the microbial modulation of plants' genetic potentials: what's known and what's next?, Rhizosphere, 10.1016/j.rhisph.2022.100613 Druzhinina, 2011, Trichoderma: the genomics of opportunistic success, Nat. Rev. Microbiol., 9, 749, 10.1038/nrmicro2637 Duan, 2021, Improvement of wheat productivity and soil quality by arbuscular mycorrhizal fungi is density-and moisture-dependent, Agron. Sustain. Dev., 41, 1, 10.1007/s13593-020-00659-8 Ebadi, 2018, Biocontrol potential of Pochonia chlamydosporia var. chlamydosporia isolates against Meloidogyne javanica on pistachio. Egypt, J. Biol. Pest. Control., 28, 1 Escudero, 2016, Chitosan enhances parasitism of Meloidogyne javanica eggs by the nematophagous fungus Pochonia chlamydosporia, Fungal Biol, 120, 572, 10.1016/j.funbio.2015.12.005 Farias, 2018, Consortium of five fungal isolates conditioning root growth and arbuscular mycorrhiza in soybean, corn, and sugarcane, Na. Acad. Bras. Cienc, 90, 3649, 10.1590/0001-3765201820180161 Ferreira, 2011, Sisvar: a computer statistical analysis system, Cienc. E Agrotecnol, 35, 1039, 10.1590/S1413-70542011000600001 Fontana, 2021, Endophytic fungi: biological control and induced resistance to phytopathogens and abiotic stresses, Pathogens, 10, 570, 10.3390/pathogens10050570 Garg, 2018, Salicylic acid improves arbuscular mycorrhizal symbiosis, and chickpea growth and yield by modulating carbohydrate metabolism under salt stress, Mycorrhiza, 28, 727, 10.1007/s00572-018-0856-6 Gatiboni, 2008, Fósforo da biomassa microbiana e atividade de fosfatases ácidas durante a diminuição do fósforo disponível no solo, Pesqui. Agropecu. Bras., 43, 1085, 10.1590/S0100-204X2008000800019 Giovannetti, 1980, An evaluation of techniques for measuring vesicular arbuscular mycorrhizal infection in roots, New Phytol., 84, 489, 10.1111/j.1469-8137.1980.tb04556.x Gouveia, 2022, The nematophagous root endophyte Pochonia chlamydosporia alters tomato metabolome, Rhizosphere Green, 2006, Assay for fluorescein diacetate hydrolytic activity: optimization for soil samples, Soil Biol. Biochem., 38, 693, 10.1016/j.soilbio.2005.06.020 Greenfield, 2016, Beauveria bassiana and Metarhizium anisopliae endophytically colonize cassava roots following soil drench inoculation, Biol. Control, 95, 40, 10.1016/j.biocontrol.2016.01.002 Gupta, 2020, Arbuscular mycorrhizal fungi: the potential soil health indicators, 183, 10.1007/978-3-030-44364-1_11 Halifu, 2019, Effects of two Trichoderma strains on plant growth, rhizosphere soil nutrients, and fungal community of Pinus sylvestris var. mongolica annual seedlings, Forests, 10, 758, 10.3390/f10090758 Hart, 2002, Host plant benefit from association with arbuscular mycorrhizal fungi: variation due to differences in size of mycelium, Biol. Fertil. Soils, 36, 357, 10.1007/s00374-002-0539-4 Hotaka, 2015, Efficacy of Purpureocillium lilacinum CKPL-053 in controlling Thrips palmi (Thysanoptera: thripidae) in orchid farms in Thailand, Appl. Entomol. Zool, 50, 317, 10.1007/s13355-015-0339-6 Hou, 2015, Phosphatase activity in relation to key litter and soil properties in mature subtropical forests in China, Sci. Total Environ., 515–516, 83, 10.1016/j.scitotenv.2015.02.044 Hu, 2019, The better suppression of pepper Phytophthora blight by arbuscular mycorrhizal (AM) fungus than Purpureocillium lilacinum alone or combined with AM fungus, J. Soils Sediments, 20, 792, 10.1007/s11368-019-02438-9 Kakabouki, 2021, Effect of colonization of Trichoderma harzianum on growth development and CBD content of hemp (Cannabis sativa L.), Microorganisms, 9, 518, 10.3390/microorganisms9030518 Kiriachek, 2009, 1 Latz, 2021, Succession of the fungal endophytic microbiome of wheat is dependent on tissue-specific interactions between host genotype and environment, Sci. Total Environ., 759, 10.1016/j.scitotenv.2020.143804 Lee, 2017, Entomopathogenic Beauveria bassiana granules to control soil-dwelling stage of western flower thrips, Frankliniella occidentalis (Thysanoptera: thripidae), Biocontrol, 62, 639, 10.1007/s10526-017-9818-8 Lin, 2018, Genome and secretome analysis of Pochonia chlamydosporia provide new insight into egg-parasitic mechanisms, Sci. Rep., 8, 1123, 10.1038/s41598-018-19169-5 Lopez, 2014, The entomopathogenic fungal endophytes Purpureocillium lilacinum (formerly paecilomyces lilacinus) and Beauveria bassiana negatively affect cotton aphid reproduction under both greenhouse and field conditions, PLoS One, 9 Lopez, 2015, The endophytic fungal entomopathogens Beauveria bassiana and Purpureocillium lilacinum enhance the growth of cultivated cotton (Gossypium hirsutum) and negatively affect survival of the cotton bollworm (Helicoverpa zea), Biol. Control, 89, 53, 10.1016/j.biocontrol.2015.03.010 Mahmoudi, 2021, Arbuscular mycorrhizal traits are good indicators of soil multifunctionality in drylands, Geoderma, 397, 10.1016/j.geoderma.2021.115099 Martínez-Medina, 2010, Trichoderma harzianum and Glomus intraradices modify the hormone disruption induced by Fusarium oxysporum infection in melon plants, Phytopathology, 100, 682, 10.1094/PHYTO-100-7-0682 Meddad-Hamza, 2017, Spatiotemporal variation of arbuscular mycorrhizal fungal colonization in olive (Olea europaea L.) roots across a broad mesic-xeric climatic gradient in North Africa, Sci. Total Environ., 583, 176, 10.1016/j.scitotenv.2017.01.049 Medeiros, 2018, Occurrence of Purpureocillium lilacinum in citrus black fly nymphs, Rev. Bras. Frutic., 40, e327, 10.1590/0100-29452018237 Metwally, 2021, The individual and interactive role of arbuscular mycorrhizal fungi and Trichoderma viride on growth, protein content, amino acids fractionation, and phosphatases enzyme activities of onion plants amended with fish waste, Ecotoxicol. Environ. Saf., 214, 10.1016/j.ecoenv.2021.112072 Moreira, 2021, Biochemical activity and microbial biomass in wetlands (Vereda) and well-drained soils under native vegetation types in Brazilian Cerrado, Appl. Soil Ecol., 160, 10.1016/j.apsoil.2020.103840 Moreno-Salazar, 2020, Plant growth, foliar nutritional content and fruit yield of Capsicum chinense biofertilized with Purpureocillium lilacinum under greenhouse conditions, Sci. Hortic., 261, 10.1016/j.scienta.2019.108950 Morris, 2019, vol. 13, 1639 Mwaura, 2017, Application of an entomopathogenic fungus (Beauveria bassiana) increases potato nematodes reproduction and potato tubers damage caused by Ditylenchus destructor and D. dipsaci, Biol. Control, 115, 23, 10.1016/j.biocontrol.2017.08.012 Naik, 2019, Plant growth promoting microbes: potential link to sustainable agriculture and environment, Biocatal. Agric. Biotechnol., 21, 10.1016/j.bcab.2019.101326 Nasu, 2018, Pochonia chlamydosporia applied via seed treatment for nematode control in two soil types, J. Crop. Prot, 114, 106, 10.1016/j.cropro.2018.08.010 Obayomi, 2021, Soil texture and properties rather than irrigation water type shape the diversity and composition of soil microbial communities, Appl. Soil Ecol., 161, 10.1016/j.apsoil.2020.103834 Ortiz-Urquiza, 2021, The split personality of Beauveria bassiana: understanding the molecular basis of fungal parasitism and mutualism, mSystems, 6, 10.1128/mSystems.00766-21 Poveda, 2019, Trichoderma harzianum favours the access of arbuscular mycorrhizal fungi to non-host Brassicaceae roots and increases plant productivity, Sci. Rep., 9, 10.1038/s41598-019-48269-z Raad, 2019, Transcriptional reprogramming of Arabidopsis thaliana defence pathways by the entomopathogen Beauveria bassiana correlates with resistance against a fungal pathogen but not against insects, Front. Microbiol., 10, 615, 10.3389/fmicb.2019.00615 Raghothama, 2005, Phosphate acquisition, Plant Soil, 274, 37, 10.1007/s11104-004-2005-6 Ribeiro, 2017, Infection of silkworm larvae by the entomopathogenic fungus, Metarhizium anisopliae, 47 Säle, 2021, Ancient lineages of arbuscular mycorrhizal fungi provide little plant benefit, Mycorrhiza, 1 Sato, 2019, Secretion of acid phosphatase from extraradical hyphae of the arbuscular mycorrhizal fungus Rhizophagus clarus is regulated in response to phosphate availability, Mycorrhiza, 29, 599, 10.1007/s00572-019-00923-0 Schnürer, 1982, Fluorescein diacetate hydrolysis as a measure of total microbial activity in soil and litter, Appl. Environ. Microbiol., 43, 1256, 10.1128/aem.43.6.1256-1261.1982 Schumacher, 2014, Rapid cost-effective analysis of microbial activity in soils using modified fluorescein diacetate method, Environ. Sci. Pollut. Res., 22, 4759, 10.1007/s11356-014-3922-4 Sheng, 2022, Metarhizium: an opportunistic middleman for multitrophic lifestyles, Curr. Opin. Microbiol., 69, 10.1016/j.mib.2022.102176 Singh, 2016, Trichoderma asperellum spore dose depended modulation of plant growth in vegetable crops, Microbiol. Res., 193, 74, 10.1016/j.micres.2016.09.002 Smith, 2008, 787 Su, 2017, Inoculating chlamydospores of Trichoderma asperellum SM-12F1 changes arsenic availability and enzyme activity in soils and improves water spinach growth, Chemosphere, 175, 497, 10.1016/j.chemosphere.2017.02.048 Tabatabai, 1994, Soil enzymes, 775 Teixeira, 2017 Thonar, 2011, Traits related to differences in function among three arbuscular mycorrhizal fungi, Plant Soil, 339, 231, 10.1007/s11104-010-0571-3 Treseder, 2013, The extent of mycorrhizal colonization of roots and its influence on plant growth and phosphorus content, Plant Soil, 371, 10.1007/s11104-013-1681-5 Triana, 2017, Evaluation of antifungal activity of Trichoderma asperellum Samuels against fungal pathogens that affect soybean (Glycine max L.) crop, Cultiv. Trop., 38, 15 Van Der Heijden, 2016, A widespread plant-fungal-bacterial symbiosis promotes plant biodiversity, plant nutrition and seedling recruitment, ISME J., 10, 389, 10.1038/ismej.2015.120 Vance, 1987, An extraction method for measuring soil microbial biomass C, Soil Biol. Biochem., 19, 703, 10.1016/0038-0717(87)90052-6 Vierheilig, 1998, Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi, Appl. Environ. Microbiol., 64, 5004, 10.1128/AEM.64.12.5004-5007.1998 Vinhal-Freitas, 2017, Soil textural class plays a major role in evaluating the effects of land use on soil quality indicators, Ecol. Indicat., 74, 182, 10.1016/j.ecolind.2016.11.020 Wang, 2016, Biosynthesis of antibiotic leucinostatins in bio-control fungus Purpureocillium lilacinum and their inhibition on phytophthora revealed by genome mining, PLoS Pathog., 12, 10.1371/journal.ppat.1005685 White, 2017, The state of rhizospheric science in the era of multi-omics: a practical guide to omics technologies, Rhizosphere, 3, 212, 10.1016/j.rhisph.2017.05.003 Wilson, 2009, Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: results from long‐term field experiments, Ecol. Lett., 12, 452, 10.1111/j.1461-0248.2009.01303.x Wu, 2018, The aboveground vegetation type and underground soil property mediate the divergence of soil microbiomes and the biological interactions, Microb. Ecol., 75, 434, 10.1007/s00248-017-1050-7 Xie, 2016, Genome and transcriptome sequences reveal the specific parasitism of the nematophagous Purpureocillium lilacinum 36-1, Front. Microbiol., 7, 1084, 10.3389/fmicb.2016.01084 Zavala‐Gonzalez, 2015, Arabidopsis thaliana root colonization by the nematophagous fungus Pochonia chlamydosporia is modulated by jasmonate signaling and leads to accelerated flowering and improved yield, New Phytol., 213, 351, 10.1111/nph.14106