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Endophytic colonization of Arabidopsis thaliana by Gluconacetobacter diazotrophicus and its effect on plant growth promotion, plant physiology, and activation of plant defense

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Abstract

Background and aims

Gluconacetobacter diazotrophicus is a plant growth-promoting bacteria (PGPB) that colonizes several plant species. Here, we studied the internal colonization of Arabidopsis thaliana tissues by G. diazotrophicus and analyzed its effects on physiology, growth, and activation of plant immune system during such association.

Methods

A. thaliana seedlings were inoculated with G. diazotrophicus and grown in substrate for 50 days. Effects on plant growth were estimated by quantifying number of leaves, leaf area, and fresh and dry weight. Endophytic bacterial population was determined by colony-forming unit (CFU), and its location in plant tissues was assayed by epifluorescence microscopy of red fluorescent protein-labeled bacterium. Whole canopy gas exchange (photosynthesis and transpiration) was determined using a portable photosynthesis system.

Results

G. diazotrophicus efficiently promoted A. thaliana plant growth at 50 days after inoculation. Inoculated plants showed higher whole canopy photosynthesis, lower whole plant transpiration, and increased water-use efficiency. The bacterium colonized preferentially root xylem. The inoculation of plants defective in systemic acquired resistance (SAR)-associated defense revealed that plant immune system plays an important role during the early association stages.

Conclusions

G. diazotrophicus endophytically colonizes A. thaliana roots, promotes plant growth, and increases whole canopy photosynthesis. Our results indicate that A. thaliana is useful for molecular studies of the mechanisms involved in the interaction between plants and PGPB, especially those involving G. diazotrophicus.

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Acknowledgments

This research was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Financiadora de Estudos e Projetos (FINEP), Fundação de Amparo a Pesquisa do Estado do Rio de Janeiro (FAPERJ), and Instituto Nacional de Ciências e Tecnologia em Fixação Biológica de Nitrogênio (INCT-FBN). First author received fellowship from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES.

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    1. Laboratório de Biotecnologia, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Av. Alberto Lamego, 2000, Campos dos Goytacazes, Rio de Janeiro, Brazil

      A. L. S. Rangel de Souza, S. A. De Souza, M. V. V. De Oliveira, N. D. Da Silva, P. L. Rangel, C. R. S. Panisset & G. A. De Souza Filho

    2. Laboratório de Melhoramento Genético Vegetal, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Av. Alberto Lamego, 2000, Campos dos Goytacazes, Rio de Janeiro, Brazil

      T. M. Ferraz, F. A. M. M. A. Figueiredo & E. Campostrini

    3. Laboratório de Biologia Celular e Tecidual, Universidade Estadual do Norte Fluminense Darcy Ribeiro (UENF), Av. Alberto Lamego, 2000, Campos dos Goytacazes, Rio de Janeiro, Brazil

      F. L. Olivares

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    1. A. L. S. Rangel de Souza
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    Correspondence to G. A. De Souza Filho.

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    Responsible Editor: Euan K. James.

    A. L. S. Rangel de Souza and S. A. De Souza contributed equally to this work.

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    Fig. S1

    Comparison of growth promotion by G. diazotrophicus PAL5 strains in A. thaliana plants. Seven-day-old wild-type (Col-0) plants were inoculated with G. diazotrophicus PAL5 wild-type, kanamycin-resistant strain (GD-Kan) and DsRed-expressing strain (GD-F) at a concentration of 106 CFU mL−1. The number of leaves (a), fresh weight of aerial (b), and root parts (c) and the number of bacteria in inoculated roots (d) were determined 50 days post-inoculation (dpi). Twenty plants from each treatment were used for this analysis. These experiments were repeated three times with similar results. Error bars represent the standard deviation. Significant differences between treatments are represented by * (ANOVA, p < 0.05). (GIF 370 kb)

    High resolution image (TIFF 324 kb)

    Fig. S2

    Effect on plant growth, at 28 dpi, of A. thaliana inoculated with GD-Kan (106 CFU mL−1). The number of leaves (a), total leaf area (b), dry weight of aerial (c) and root (d) parts were determined 28 days post inoculation (dpi). Twenty plants from each treatment were used for these analyses. These experiments were repeated three times with similar results. Error bars represent the standard deviation. Significant differences between treatments are represented by * (ANOVA, p < 0.05). (GIF 17 kb)

    High resolution image (TIFF 7938 kb)

    Fig. S3

    Plant growth promotion by G. diazotrophicus GD-Kan strains in A. thaliana wild-type (Col-0) and NahG lines. Seven-day-old seedlings were inoculated with 106 CFU mL−1 of GD-Kan. At 28 and 50 dpi, dry weight of roots and shoots was the quantified. Twenty plants from each treatment were used for these analyses. Experiments were repeated three times with similar results. Error bars represent the standard deviation. Significant differences between treatments are represented by * (ANOVA, p < 0.05). (GIF 25 kb)

    High resolution image (TIFF 8196 kb)

    Table S1

    Bacterial concentration in root tissue inoculated with G. diazotrophicus PAL5 kanamycin-resistant strain (GD-Kan) and DsRed expressing strain (GD-F) at 50 days post-inoculation (dpi.) (GIF 27 kb) (GIF 34 kb)

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    Table S2

    Bacterial concentration in the shoots and roots of Col-0 and NahG plants inoculated with G. diazotrophicus PAL5 kanamycin-resistant strain (GD-Kan) at 28 days post-inoculation (dpi.) (GIF 34 kb)

    High resolution image (TIFF 442 kb)

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    Rangel de Souza, A.L.S., De Souza, S.A., De Oliveira, M.V.V. et al. Endophytic colonization of Arabidopsis thaliana by Gluconacetobacter diazotrophicus and its effect on plant growth promotion, plant physiology, and activation of plant defense. Plant Soil 399, 257–270 (2016). https://doi.org/10.1007/s11104-015-2672-5

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