Reciprocal modulation of responses to nitrate starvation and hypoxia in roots and leaves of Arabidopsis thaliana

ABSTRACT

The flooding of agricultural land leads to hypoxia and nitrate leaching. While understanding the plant’s response to these conditions is essential for crop improvement, the effect of extended nitrate limitation on subsequent hypoxia has not been studied in an organ-specific manner. We cultivated Arabidopsis thaliana without nitrate for 1 week before inducing hypoxia by bubbling the hydroponic solution with nitrogen gas for 16 h. In the roots, the transcripts of two transcription factor genes (HRA1, HRE2) and three genes involved in fermentation (SUS4, PDC1, ADH1) were ~10- to 100-fold upregulated by simultaneous hypoxia and nitrate starvation compared to the control condition (replete nitrate and oxygen). In contrast, this hypoxic upregulation was ~5 to 10 times stronger when nitrate was available. The phytoglobin genes PGB1 and PGB2, involved in nitric oxide (NO) scavenging, were massively downregulated by nitrate starvation (~1000-fold and 10⁵-fold, respectively), but only under ambient oxygen levels; this was reflected in a 2.5-fold increase in NO concentration. In the leaves, HRA1, SUS4, and RAP2.3 were upregulated ~20-fold by hypoxia under nitrate starvation, whereas this upregulation was virtually absent in the presence of nitrate. Our results highlight that the plant’s responses to nitrate starvation and hypoxia can influence each other.

Keywords:

• Nitrogen deficiency
• hypoxia
• climate change
• combined stress
• Arabidopsis thaliana

Acknowledgments

Dr V. Safavi-Rizi was supported by Leipzig University’s Flexible Fund. We thank Dr W. Brenner for his help with RT-qPCR software and initial evaluations of the primers melting curves, and R. Sacher for her technical assistance with plant cultivation and seed sterilization. We are thankful to the Open Access Publishing Fund of Leipzig University supported by the German Research Foundation within the program Open Access Publication Funding.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/15592324.2023.2300228

Additional information

Funding

The work was supported by the Universität Leipzig [Open Access Publishing Fund]; Universität Leipzig [Flexible Fund].