A discrete role for alternative oxidase under hypoxia to increase nitric oxide and drive energy production

• Published in: Free radical biology & medicine 2018-07, Vol.122, p.40-51
• Main Authors: Vishwakarma, Abhaypratap, Kumari, Aprajita, Mur, Luis A.J., Gupta, Kapuganti Jagadis
• Format: Article
• Language: English
• Subjects: Adenosine Triphosphate - biosynthesis; Alternative oxidase; Arabidopsis - genetics; Arabidopsis - growth & development; Arabidopsis - metabolism; Arabidopsis Proteins - genetics; Energy efficiency; Energy Metabolism - genetics; Flagellin - genetics; Gene Expression Regulation, Plant; Hemoglobins - genetics; Hypoxia - genetics; Hypoxia - metabolism; Mitochondria - genetics; Mitochondria - metabolism; Mitochondrial Proteins - genetics; Mitochondrial Proteins - metabolism; Nitrate Reductase - genetics; Nitric oxide; Nitric Oxide - biosynthesis; Nitric Oxide - metabolism; Oxidoreductases - genetics; Oxidoreductases - metabolism; Oxygen - metabolism; Peroxynitrite; Peroxynitrous Acid - metabolism; Plant Proteins - genetics; Plant Proteins - metabolism; Plant Roots - genetics; Plant Roots - metabolism; Plants, Genetically Modified - genetics; Plants, Genetically Modified - metabolism; Reactive Oxygen Species - metabolism; Seedlings - genetics; Seedlings - metabolism; Superoxide
• ISSN: 0891-5849; 1873-4596
• DOI: 10.1016/j.freeradbiomed.2018.03.045

Alternative oxidase (AOX) is an integral part of the mitochondrial electron transport and can prevent reactive oxygen species (ROS) and nitric oxide (NO) production under non-stressed, normoxic conditions. Here we assessed the roles of AOX by imposing stress under normoxia in comparison to hypoxic conditions using AOX over expressing (AOX OE) and anti-sense (AOX AS) transgenic Arabidopsis seedlings and roots. Under normoxic conditions stress was induced with the defence elicitor flagellin (flg22). AOX OE reduced NO production whilst this was increased in AOX AS. Moreover AOX AS also exhibited an increase in superoxide and therefore peroxynitrite, tyrosine nitration suggesting that scavenging of NO by AOX can prevent toxic peroxynitrite formation under normoxia. In contrast, during hypoxia interestingly we found that AOX is a generator of NO. Thus, the NO produced during hypoxia, was enhanced in AOX OE and suppressed in AOX AS. Additionally, treatment of WT or AOX OE with the AOX inhibitor SHAM inhibited hypoxic NO production. The enhanced levels of NO correlated with expression of non-symbiotic haemoglobin, increased NR activity and ATP production. The ATP generation was suppressed in nia1,2 mutant and non symbiotic haemoglobin antisense line treated with SHAM. Taken together these results suggest that hypoxic NO generation mediated by AOX has a discrete role by feeding into the haemoglobin-NO cycle to drive energy efficiency under conditions of low oxygen tension. [Display omitted] •Under normoxic conditions AOX acts as scavenger of NO when treated with flg22.•AOX over expressing line displayed less NO under normoxia in response to flg22.•Scavenging of NO by AOX can prevent peroxynitrite formation under normoxia.•In contrast to normoxia, during hypoxia AOX is a generator of NO.•The enhanced levels of NO under hypoxia correlated with ATP production.•Hypoxic NO generation, mediated by AOX, drives the Hb-NO cycle under hypoxia.