Nitric Oxide Turnover Under Hypoxia Results in the Rapid Increased Expression of the Plastid-Localized Phosphorylated Pathway of Serine Biosynthesis.

Somaieh Zafari,Greg C Vanlerberghe,Abir U Igamberdiev

doi:10.3389/fpls.2021.780842

Abstract

The plant mitochondrial electron transport chain influences carbon and nitrogen metabolism under near anoxic conditions through its involvement in the phytoglobin-nitric oxide cycle, where the respiratory chain reduces nitrite to nitric oxide (NO), followed by NO conversion to nitrate by class 1 phytoglobin. Wild type (WT) and transgenic tobacco (Nicotiana tabacum L.) with differing amounts of alternative oxidase (AOX) were used to manipulate NO generation under hypoxia, and to examine whether this in turn influenced the gene expression of two stress-related amino acid biosynthetic pathways, the plastid-localized phosphorylated pathway of serine biosynthesis (PPSB), and the γ-aminobutyric acid (GABA) shunt. Under hypoxia, leaf NO emission rate was highest in AOX overexpressors and lowest in AOX knockdowns, with WT showing an intermediate rate. In turn, the rate of NO emission correlated with the degree to which amino acids accumulated. This amino acid accumulation was associated with the increased expression of the enzymes of the stress-related amino acid biosynthetic pathways. However, induction of the PPSB occurred much earlier than the GABA shunt. This work shows that high rates of NO turnover associate with rapid gene induction of the PPSB, establishing a clear link between this pathway and the maintenance of carbon, nitrogen and energy metabolism under hypoxia.

Highlights

Plant acclimation to oxygen deficiency involves increased glycolytic fermentation (Kennedy et al, 1992) and upregulation of nitrate reductase (NR) (Botrel and Kaiser, 1997)
To gain a comprehensive insight into how alternative oxidase (AOX) interconnects to the phosphorylated pathway of serine biosynthesis (PPSB) and GABA shunt under low oxygen, plants were subjected to nitrogen atmosphere for an extensive time course, and the samples were taken at 0 h, 3, 6, 12, 24, and 48 h of the anoxic condition
The leaf ATP/ADP ratio was higher by 1.5 times in the overexpressor B8 and lower by more than 50% in the knockdown RI29 as compared to wild type (WT) (Figure 1C)

Summary

Introduction

Plant acclimation to oxygen deficiency involves increased glycolytic fermentation (Kennedy et al, 1992) and upregulation of nitrate reductase (NR) (Botrel and Kaiser, 1997). The latter relates to nitrogen turnover by the class 1 phytoglobin-nitric oxide (Pgb1-NO) cycle, an alternative to the classical fermentation pathways (Igamberdiev and Hill, 2004, 2018; Gupta and Igamberdiev, 2011; Hebelstrup and Møller, 2015). Under hypoxic (near anoxic) conditions, AOX activity accelerates NO generation. It is possible that the effect of AOX on NO metabolism under hypoxia is by some indirect mechanism, as discussed elsewhere (Jayawardhane et al, 2020)

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Results

Conclusion