Josiane Fukami

Universidade Estadual de Londrina

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Mariangela Hungría

Universidade Estadual de Londrina

Francisco Javier Ollero

Universidad de Sevilla

Marco Antônio Nogueira

Brazilian Agricultural Research Corporation

Manuel Megı́as

Universidad de Sevilla

Paula Cerezini

Universidade Estadual de Londrina

Maria Helena Machado

Fundação Oswaldo Cruz

Lúcia Sadayo Assari Takahashi

Universidade Estadual de Londrina

Suzana Heiko Nakatani

Sheila Ariana Xavier

Universidade Estadual de Londrina

Renata Pinheiro Sobottka

Pedra Agroindustrial (Brazil)

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Universidade Estadual de Londrina

National Council for Scientific and Technological Development

Brazilian Agricultural Research Corporation

Universidad de Sevilla

Universidade Federal do Rio de Janeiro

Coordenação de Aperfeicoamento de Pessoal de Nível Superior

United States Nuclear Regulatory Commission

Universidade de São Paulo

ORCID

Universidade Estadual Paulista (Unesp)

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Revealing strategies of quorum sensing in Azospirillum brasilense strains Ab-V5 and Ab-V6

Archives of Microbiology (2017)

Josiane Fukami Julia Laura Fernandes Abrantes Pablo del Cerro Marco Antônio Nogueira Francisco Javier Ollero

Azospirillum brasilense

10.1007/s00203-017-1422-x

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Citations (56)

Phytohormones and induction of plant-stress tolerance and defense genes by seed and foliar inoculation with Azospirillum brasilense cells and metabolites promote maize growth

AMB Express (2017)

Josiane Fukami Francisco Javier Ollero Manuel Megı́as Mariangela Hungría

Azospirillum spp. are plant-growth-promoting bacteria used worldwide as inoculants for a variety of crops. Among the beneficial mechanisms associated with Azospirillum inoculation, emphasis has been given to the biological nitrogen fixation process and to the synthesis of phytohormones. In Brazil, the application of inoculants containing A. brasilense strains Ab-V5 and Ab-V6 to cereals is exponentially growing and in this study we investigated the effects of maize inoculation with these two strains applied on seeds or by leaf spray at the V2.5 stage growth—a strategy to relieve incompatibility with pesticides used for seed treatment. We also investigate the effects of spraying the metabolites of these two strains at V2.5. Maize growth was promoted by the inoculation of bacteria and their metabolites. When applied via foliar spray, although A. brasilense survival on leaves was confirmed by confocal microscopy and cell recovery, few cells were detected after 24 h, indicating that the effects of bacterial leaf spray might also be related to their metabolites. The major molecules detected in the supernatants of both strains were indole-3-acetic acid, indole-3-ethanol, indole-3-lactic acid and salicylic acid. RT-PCR of genes related to oxidative stress (APX1, APX2, CAT1, SOD2, SOD4) and plant defense (pathogenesis-related PR1, prp2 and prp4) was evaluated on maize leaves and roots. Differences were observed according to the gene, plant tissue, strain and method of application, but, in general, inoculation with Azospirillum resulted in up-regulation of oxidative stress genes in leaves and down-regulation in roots; contrarily, in general, PR genes were down-regulated in leaves and up-regulated in roots. Emphasis should be given to the application of metabolites, especially of Ab-V5 + Ab-V6 that in general resulted in the highest up-regulation of oxidative-stress and PR genes both in leaves and in roots. We hypothesize that the benefits of inoculation of Azospirillum on seeds or by leaf spray, as well as of leaf spraying of Azospirillum metabolites, are strongly correlated with the synthesis of phytohormones and by eliciting genes related to plant-stress tolerance and defense against pathogens.

Azospirillum brasilense

10.1186/s13568-017-0453-7

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Accessing inoculation methods of maize and wheat with Azospirillum brasilense

AMB Express (2016)

Josiane Fukami Marco Antônio Nogueira Ricardo Silva Araújo Mariangela Hungría

The utilization of inoculants containing Azospirillum is becoming more popular due to increasing reports of expressive gains in grain yields. However, incompatibility with pesticides used in seed treatments represents a main limitation for a successful inoculation. Therefore, in this study we searched for alternatives methods for seed inoculation of maize and wheat, aiming to avoid the direct contact of bacteria with pesticides. Different doses of inoculants containing Azospirillum brasilense were employed to perform inoculation in-furrow, via soil spray at sowing and via leaf spray after seedlings had emerged, in comparison to seed inoculation. Experiments were conducted first under greenhouse controlled conditions and then confirmed in the field at different locations in Brazil. In the greenhouse, most parameters measured responded positively to the largest inoculant dose used in foliar sprays, but benefits could also be observed from both in-furrow and soil spray inoculation. However, our results present evidence that field inoculation with plant-growth promoting bacteria must consider inoculant doses, and point to the need of fine adjustments to avoid crossing the threshold of growth stimulation and inhibition. All inoculation techniques increased the abundance of diazotrophic bacteria in plant tissues, and foliar spray improved colonization of leaves, while soil inoculations favored root and rhizosphere colonization. In field experiments, inoculation with A. brasilense allowed for a 25 % reduction in the need for N fertilizers. Our results have identified alternative methods of inoculation that were as effective as the standard seed inoculation that may represent an important strategy to avoid the incompatibility between inoculant bacteria and pesticides employed for seed treatment.

Azospirillum brasilense

Seed treatment

10.1186/s13568-015-0171-y

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Diversity and plant growth-promoting traits of endophytic bacteria isolated from maize cropped in organic and low-input agricultural systems in southern Brazil

D. S. L. Fagotti Josiane Fukami Paula Cerezini André Luíz Martinez de Oliveira Galdino Andrade

Plant growth-promoting bacteria (PGPB) may enhance plant growth and health through several mechanisms, contributing for sustainable agriculture. We isolated and characterized endophytic bacteria from stems of landrace maize (Zea mays L.) grown under low-input and organic systems in southern Brazil. The 16S rRNA analysis revealed 83 isolates within 14 genera, including α-Proteobacteria, β-Proteobacteria, γ-Proteobacteria, Actinomycetia, and Bacilli classes. The synthesis of indolic compounds was widespread among the strains, as well as the enhancement of N concentration in N-free media, a putative capacity for biological nitrogen fixation. Phosphate solubilization prevailed in Burkholderia and Paraburkholderia strains, while siderophores production was observed in all genera, except Microbacterium. Inoculation with selected strains confirmed growth-promotion on maize plantlets, particularly Sphingomonas sp. CNPSo 2378 and Bacillus velezensis CNPSo 2384, whose genomes were sequenced and revealed PGPB features and evolutionary relationships, shedding light on the diversity, functional traits, and occurrence in low-input and organic agricultural systems. Data summary The 16S rRNA gene sequences have been deposited in the NCBI GenBank database, with accession numbers provided in supplementary material (Table S1). The genomic sequences have also been deposited in the GenBank database, with the following accession numbers: JAXCMJ000000000 for CNPSo 2378 and JAXCMK000000000 for CNPSo 2384. Raw data on the effects of bacterial isolates on the plant growth-promoting of maize plantlets are available at figshare database, with the following DOI: 10.6084/m9.figshare.27610290.

Plant Diversity

10.1099/acmi.0.000948.v1

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Superação da dormência de sementes de Cupressuslusitanica Mill Dormancybreak in seeds of Cupressuslusitanica Mill

Sheila Ariana Xavier Josiane Fukami Lidiane Carla Vilanova Miotto Renata Pinheiro Sobottka

Cupressus lusitanica Mill. is a multipurpose tree species with a high potential for wood production in Brazil. The main objective was to evaluate methods to dormancy break to promote seed germinationin C. lusitanica. The following treatments were used: T1 (intact seeds); T2 (soaking in water for 24 hours); T3 (soaking in water for 36 hours); T4 (stratification on 4 °C for 30 days); T5 (immersion in water for 8 hours + stratification on 4 °C for 30 days); T6 (immersion in water for 8 hours + stratification on 4 °C for 20 days); T7 (immersion for 12 hours + stratification on 4 °C for 20 days); T8 (soaking in hot water at 80oC for 5 minutes); T9 (sulfuric acid soaking for 5 minutes). It was evaluated the percentage and germination speed (IVG). The resultsweresubmitted to ANOVA andmeanswere comparedusingthe Skott-Knott. The treatments T5, T2 and T7 showedhighergermination, and T7 higherspeedofgermination, thesecanberecommended for overcomingseeddormancyof C. lusitanica.

Stratification (seeds)

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Dormancybreak in seeds of Cupressuslusitanica Mill
Superação da dormência de sementes de Cupressuslusitanica Mill

DOAJ (DOAJ: Directory of Open Access Journals) (2012)

Sheila Ariana Xavier Josiane Fukami Lidiane Carla Vilanova Miotto Renata Pinheiro Sobottka Suzana Heiko Nakatani

Cupressuslusitanica Mill.is a multipurpose tree species with a high potential for wood production in Brazil. The main objective was to evaluate methods to dormancy break to promote seed germinationin C. lusitanica. The following treatments were used: T1 (intact seeds); T2 (soaking in water for 24 hours); T3 (soaking in water for 36 hours); T4 (stratification on 4 C for 30 days); T5 (immersion in water for 8 hours + stratification on 4 C for 30 days); T6 (immersion in water for 8 hours + stratification on 4 C for 20 days); T7 (immersion for 12 hours + stratification on 4 C for 20 days); T8 (soaking in hot water at 80oC for 5 minutes); T9 (sulfuric acid soaking for 5 minutes). It was evaluated the percentage and germination speed (IVG). The resultsweresubmitted to ANOVA andmeanswere comparedusingthe Skott-Knott. The treatments T5, T2 and T7 showedhighergermination, and T7 higherspeedofgermination, thesecanberecommended for overcomingseeddormancyof C. lusitanica.

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Quorum sensing communication: Bradyrhizobium‐Azospirillum interaction via N‐acyl‐homoserine lactones in the promotion of soybean symbiosis

Journal of Basic Microbiology (2018)

Dáfila dos Santos Lima Fagotti Julia Laura Fernandes Abrantes Paula Cerezini Josiane Fukami Marco Antônio Nogueira

Quorum-sensing (QS) mechanisms are important in intra- and inter-specific communication among bacteria. We investigated QS mechanisms in Bradyrhizobium japonicum strain CPAC 15 and Azospirillum brasilense strains Ab-V5 and Ab-V6, used in commercial co-inoculants for the soybean crop in Brazil. A transconjugant of CPAC 15-QS with partial inactivation of N-acyl-homoserine lactones (AHLs) was obtained and several parameters were evaluated; in vitro, CPAC 15 and the transconjugant differed in growth, but not in biofilm formation, and no differences were observed in the symbiotic performance in vivo. The genome of CPAC 15 carries functional luxI and luxR genes and low amounts of three AHL molecules were detected: 3-OH-C12-AHL, 3-OH-C14-AHL, and 3-oxo-C14-AHL. Multiple copies of luxR-like genes, but not of luxI are present in the genomes of Ab-V5 and Ab-V6, and differences in gene expression were observed when the strains were co-cultured with B. japonicum; we may infer that the luxR-genes of A. brasilense may perceive the AHL molecules of B. japonicum. Soybean symbiotic performance was improved especially by co-inoculation with Ab-V6, which, contrarily to Ab-V5, did not respond to the AHLs of CPAC 15. We concluded that A. brasilense Ab-V5, but not Ab-V6, responded to the QS signals of CPAC 15, and that the synergistic interaction may be credited, at least partially, to the QS interaction. In addition, we confirmed inter- and intra-species QS communication between B. japonicum and A. brasilense and, for Azospirillum, at the strain level, impacting several steps of the symbiosis, from cell growth to plant nodulation and growth.

Homoserine

Bradyrhizobium

10.1002/jobm.201800324

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Azospirillum: benefits that go far beyond biological nitrogen fixation

AMB Express (2018)

Josiane Fukami Paula Cerezini Mariangela Hungría

The genus Azospirillum comprises plant-growth-promoting bacteria (PGPB), which have been broadly studied. The benefits to plants by inoculation with Azospirillum have been primarily attributed to its capacity to fix atmospheric nitrogen, but also to its capacity to synthesize phytohormones, in particular indole-3-acetic acid. Recently, an increasing number of studies has attributed an important role of Azospirillum in conferring to plants tolerance of abiotic and biotic stresses, which may be mediated by phytohormones acting as signaling molecules. Tolerance of biotic stresses is controlled by mechanisms of induced systemic resistance, mediated by increased levels of phytohormones in the jasmonic acid/ethylene pathway, independent of salicylic acid (SA), whereas in the systemic acquired resistance—a mechanism previously studied with phytopathogens—it is controlled by intermediate levels of SA. Both mechanisms are related to the NPR1 protein, acting as a co-activator in the induction of defense genes. Azospirillum can also promote plant growth by mechanisms of tolerance of abiotic stresses, named as induced systemic tolerance, mediated by antioxidants, osmotic adjustment, production of phytohormones, and defense strategies such as the expression of pathogenesis-related genes. The study of the mechanisms triggered by Azospirillum in plants can help in the search for more-sustainable agricultural practices and possibly reveal the use of PGPB as a major strategy to mitigate the effects of biotic and abiotic stresses on agricultural productivity.

Jasmonic acid

Systemic Acquired Resistance

10.1186/s13568-018-0608-1

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Co-inoculation of maize with Azospirillum brasilense and Rhizobium tropici as a strategy to mitigate salinity stress

Functional Plant Biology (2017)

Josiane Fukami Clara de la Osa Francisco Javier Ollero Manuel Megı́as Mariangela Hungría

Plants are highly affected by salinity, but some plant growth-promoting bacteria (PGPB) may trigger induced systemic tolerance (IST), conferring protection against abiotic stresses. We investigated plant mechanisms under saline stress (170mM NaCl) when maize was singly or co-inoculated with Azospirillum brasilense strains Ab-V5 and Ab-V6 and Rhizobium tropici strain CIAT 899. Under greenhouse conditions, plants responded positively to inoculation and co-inoculation, but with differences between strains. Inoculation affected antioxidant enzymes that detoxify reactive oxygen species (ROS) - ascorbate peroxidase (APX), catalase (CAT) and superoxide dismutase (SOD) - mainly in leaves. Proline contents in leaves and roots and malondialdehyde (MDA) in leaves - plant-stress-marker molecules - were significantly reduced due to the inoculation, indicating reduced need for the synthesis of these molecules. Significant differences were attributed to inoculation in the expression of genes related to antioxidant activity, in general with upregulation of APX1, CAT1, SOD2 and SOD4 in leaves, and APX2 in roots. Pathogenesis-related genes PR1, prp2, prp4 and heat-shock protein hsp70 were downregulated in leaves and roots, indicating that inoculation with PGPB might reduce the need for this protection. Together the results indicate that inoculation with PGPB might provide protection from the negative effects of saline stress. However, differences were observed between strains, as A. brasilense Ab-V5 did not show salt tolerance, while the best inoculation treatments to mitigate saline stress were with Ab-V6 and co-inoculation with Ab-V6+CIAT 899. Inoculation with these strains may represent an effective strategy to mitigate salinity stress.

Azospirillum brasilense

APX

Malondialdehyde

10.1071/fp17167

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Citations (132)

Antioxidant activity and induction of mechanisms of resistance to stresses related to the inoculation with Azospirillum brasilense

Archives of Microbiology (2018)

Josiane Fukami Francisco Javier Ollero Clara de la Osa Rocío Valderrama-Fernández Marco Antônio Nogueira

Azospirillum brasilense

APX

Jasmonic acid

Systemic Acquired Resistance

10.1007/s00203-018-1535-x

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Citations (52)