Dual RNA-seq of maize and H. seropedicae ZAE94 association, in different doses of nitrate, reveals novel insights into Plant-PGPB-environment relationship

Front Plant Sci. 2024 Mar 13:15:1346523. doi: 10.3389/fpls.2024.1346523. eCollection 2024.

Abstract

The interactions between plants, beneficial bacteria and their environment are profoundly shaped by various environmental factors, including light, temperature, water availability, and soil quality. Despite efforts to elucidate the molecular mechanisms involved in the association between plants and beneficial bacteria, like Plant Growth-Promoting Bacteria (PGPB), with many studies focusing on the transcriptional reprogramming in the plant, there is no report on the modulation of genetic controls from both plant and associated bacteria standpoints, in response to environment. The main goal of this study was to investigate the relationship between plant-bacteria-environment signaling, using as a model maize plants inoculated with H. seropedicae ZAE94 and cultivated with different doses of N (0.3 and 3 mM). For this purpose, we performed rRNA-depleted RNA-seq to determine the global gene expression of both maize roots and associated H. seropedicae ZAE94. Our results revealed a differential modulation of maize nitrogen metabolism, phytohormone and cell wall responses when associated with H. seropedicae ZAE94 at different N concentrations. In parallel, a modulation of the bacterial metabolism could be observed, by regulating genes involved in transport, secretion system, cell mobility, oxidoreductases, and chemotaxis, when bacteria were associated with maize roots and cultivated at different doses of N. The molecular and phenotypic data of maize plantlets suggested that different doses of N fertilization differentially regulated the beneficial effects of bacterial inoculation, as higher doses (3 mM) favored shoot elongation and lower doses (0.3 mM) favored increase in plant biomass. Our results provide a valuable integrated overview of differentially expressed genes in both maize and associated H. seropedicae ZAE94 in response to different N availability, revealing new insights into pathways involved in grass-PGPB associations.

Keywords: Zea mays sp.; beneficial association; beneficial bacteria; cell wall metabolism; differentially expressed genes; hormone metabolism; nitrogen metabolism; transcriptome.

Grants and funding

The author(s) declare that financial support was received for the research, authorship, and/or publication of this article. 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). AR and MU were supported by CNPq PhD fellowships. FT supported by CAPES posdoctoral fellowships. HF and EO were supported by FAPERJ posdoctoral fellowships. AH received support from a CNPq research grant.