Genome-wide transcriptome profiling provides insights into the responses of maize (Zea mays L.) to diazotrophic bacteria

  • Pablo R. Hardoim
  • Thais L. G. de Carvalho
  • Helkin G. F. Ballesteros
  • Daniel Bellieny-RabeloEmail author
  • Cristian A. Rojas
  • Thiago M. Venancio
  • Paulo C. G. Ferreira
  • Adriana S. Hemerly
Regular Article



We applied for the first time a high-throughput transcriptome approach to elucidate biochemical and physiological mechanisms controlling early events in the interaction between maize seedlings and different beneficial diazotrophic bacteria.


mRNA transcriptomes from maize (Zea mays L.) seedlings were characterized seven days after inoculation with Azospirillum brasilense sp245 and Herbaspirillum seropedicae HRC54. The expression profiles of selected genes were validated by quantitative reverse transcription–polymerase chain reaction analysis.


Transcriptome profiling revealed a total of 764 and 3595 differentially expressed genes (DEGs) in maize when exclusively associated with A. brasilense and H. seropedicae, respectively, whereas 455 DEGs were shared by both treatments. Our results support the modulation of the host nitrogen metabolism and phytohormone responses by both diazotrophic bacteria as well as distinct activation of host immune responses.


Diazotrophic bacteria modulate maize metabolism, with some common responses to both beneficial bacteria, while others are specific to each bacterial species. This study provides a valuable contribution on how these beneficial bacteria might amend host metabolism to improve growth and fitness.


Plant-microbe interactions RNA-seq Phytohormones Nitrogen metabolism Cell wall membrane receptors Cytoplasmic receptors 



abscisic acid


auxin response factor




bri1-ems-suppressor 1


coiled-coil receptor, nucleotide-binding sites, and leucine-rich repeated domains


counts per million


damage-associated molecular patterns


days after inoculation


differentially expressed genes




gene ontology


gibberellic acids


basic helix-loop-helix


homeobox domain


indole acetic acid


membrane-based interactome network database


multidimensional scaling


nitrate reductase


nitrite reductase


nitrogen use efficiency


pattern recognition receptors


pattern trigger immunity


quantitative reverse transcription–polymerase chain reaction


receptor-like cytoplasmic kinases


cysteine receptor-like kinase


receptor-like kinase


recognition peronospora parasítica




salicylic acid


toll and interleukin receptor, nucleotide-binding sites, and leucine-rich repeated domains


transcription factors



The research was supported by Instituto Nacional de Ciência de Tecnologia (INCT) in Biological Nitrogen Fixation, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro (FAPERJ), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Newton Fund grant (BB/N013476/1). PRH and HGFB were supported by CNPq posdoctoral and PhD fellowships, respectively. TLGC and CAR were supported by FAPERJ posdoctoral fellowships. ASH and PCGF receive support from a CNPq research grant.

Supplementary material

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Fig. S1 Non-metric multidimensional scaling (MDS) ordination on RNA-seq library transcript abundance profiling of maize samples inoculated with Azospirillum brasilense (azos_in), Herbaspirillum seropedicae (herb_in) and mock-inoculated (uninoculated). (PDF 39 kb)
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Fig. S2 Functional multidimesional scatterplots of GO enriched terms for biological process (a and b) and molecular function (c and d). Functional enriched GO terms identified in maize DEGs repressed (a and c) and induced (b after inoculation with Herbaspirillum seropedicae were independently analyzed with AgriGO and summarized using REVIGO semantic similarity-based scatterplots. For each category, enriched GO terms are plotted after the redundancy removal of semantic similarities. Semantically similar GO terms remain close together in the plot. Bubble color indicates adjusted p value for the false discovery rates, whereas large bubble size indicates more frequency count of the GO term in the underlying GO database. (PDF 603 kb)
11104_2019_4193_MOESM11_ESM.pdf (374 kb)
Fig. S3 Mapman visualization of maize differentially expressed genes (DEGs) involved in biotic stress response when inoculated by both diazotrophic bacteria Azospirillum brasilense and Herbaspirillum seropedicae (a) or solely inoculated with A. brasilense (b) and H. seropedicae (c). Inoculated plants were compared to mock-inoculated plants and each block represents rescaled log2 ratios (red, induced; blue, repressed) of a specific DEG. (PDF 373 kb)
11104_2019_4193_MOESM12_ESM.pdf (61 kb)
Fig. S4 Schematic representation of maize differentially expressed genes (DEGs) involved in auxin and brassinosteroids (BRs) metabolism when induced (red colors) or repressed (blue colors) after inoculation with Herbaspirillum seropedicae (square) or common to Azospirillum brasilense and H. seropedicae (circle) datasets. The genes arf1 and arf7 encode auxin response factor enzymes, while gene br6ox1 encodes a protein involved in the biosynthesis of BRs and the bzr1 gene is a positive regulator of the BR signaling pathway. (PDF 60 kb)
11104_2019_4193_MOESM13_ESM.pdf (116 kb)
Fig. S5 Heatmap of transcription factor (TF) families from maize differentially expressed genes (DEGs) inoculated with diazotrophic bacteria Herbaspirillum seropedicae (Herb) and Azospirillum brasilense (Azos). Values are shown as log2 fold change related to mock-inoculated plants when induced (A) and repressed (B) by both diazotrophic bacteria, as well as induced (C) and repressed (D) in plants solely inoculated with H. seropedicae. The transcriptional regulatory families of AP2-EREBP, ethylene responsive factor; BES1, Brassinosteroids-related transcription factor; bHLH, basic Helix-Loop-Helix; C2C2, CONSTANS LIKE genes; MYB, Myb DNA-binding domain; ARF, Auxin Response Factor; HB, Homeobox KNOX1 KNOX2 domains; SBP, Squamosa promoter Binding Proteins domain; trihelix, helix-loop-helix-loop-helix; AUX_IAA, AUX_IAA domain; bZIP, basic region/leucine zipper motif; C2H2, zinc-finger domain; CCAAT, CBFB_NFYA CBFD_NFYB_HMF CCAAT-Dr1 NF-YB NF-YC domains; GNAT, Gcn5-related N-acetyltransferases; WRKY, WRKY domain; C3H, zf-CCCH domain; CAMTA, calmodulin binding transcription activators; orphans; PHD, plant homeodomain; SET, SET domain; SNF2, SNF2_N domain are shown. (PDF 115 kb)


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Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Pablo R. Hardoim
    • 1
  • Thais L. G. de Carvalho
    • 1
    • 2
  • Helkin G. F. Ballesteros
    • 1
  • Daniel Bellieny-Rabelo
    • 3
    • 4
    Email author
  • Cristian A. Rojas
    • 5
  • Thiago M. Venancio
    • 3
  • Paulo C. G. Ferreira
    • 1
  • Adriana S. Hemerly
    • 1
  1. 1.Instituto de Bioquímica Médica Leopoldo de Meis, Laboratório de Biologia Molecular de PlantasUniversidade Federal do Rio de JaneiroRio de JaneiroBrazil
  2. 2.Departamento de BiologiaPontifícia Universidade Católica do Rio de JaneiroRio de JaneiroBrazil
  3. 3.Centro de Biociências e Biotecnologia, Laboratório de Química e Função de Proteínas e PeptídeosUniversidade Estadual do Norte Fluminense Darcy RibeiroCampos dos GoytacazesBrazil
  4. 4.Department of Biochemistry, Genetics and MicrobiologyUniversity of PretoriaPretoriaSouth Africa
  5. 5.Universidade Federal da Integração Latino-AmericanaFoz do IguaçuBrazil

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