Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana

Abstract

Nitric oxide (NO) and ethylene are signalling molecules that are synthesized in response to oxygen depletion. Non-symbiotic plant haemoglobins (Hbs) have been demonstrated to act in roots under oxygen depletion to scavenge NO. Using Arabidopsis thaliana plants, the online emission of NO or ethylene was directly quantified under normoxia, hypoxia (0.1–1.0% O2), or full anoxia. The production of both gases was increased with reduced expression of either of the Hb genes GLB1 or GLB2, whereas NO emission decreased in plants overexpressing these genes. NO emission in plants with reduced Hb gene expression represented a major loss of nitrogen equivalent to 0.2mM nitrate per 24h under hypoxic conditions. Hb gene expression was greatly enhanced in flooded roots, suggesting induction by reduced oxygen diffusion. The function could be to limit loss of nitrogen under NO emission. NO reacts with thiols to form S-nitrosylated compounds, and it is demonstrated that hypoxia substantially increased the content of S-nitrosylated compounds. A parallel up-regulation of Hb gene expression in the normoxic shoots of the flooded plants may reflect signal transmission from root to shoot via ethylene and a role for Hb in the shoots. Hb gene expression was correlated with ethylene-induced upward leaf movement (hyponastic growth) but not with hypocotyl growth, which was Hb independent. Taken together the data suggest that Hb can influence flood-induced hyponasty via ethylene-dependent and, possibly, ethylene-independent pathways.

Waterproofing Crops: Effective Flooding Survival Strategies

“…This led to the suggestion that MPK6 may participate in maintaining poorly translated mRNAs during the stress so that they may be translated upon reoxygenation. Mitochondrial emission of NO also occurs under severe hypoxia (less than 1% oxygen) and was linked to signal transduction and metabolism (Hebelstrup et al, 2012;Hill, 2012). Hebelstrup et al (2012) showed that NO contributes to ethylene-dependent leaf hyponasty.…”

“…Mitochondrial emission of NO also occurs under severe hypoxia (less than 1% oxygen) and was linked to signal transduction and metabolism (Hebelstrup et al, 2012;Hill, 2012). Hebelstrup et al (2012) showed that NO contributes to ethylene-dependent leaf hyponasty. The levels of NO and the degree of hyponasty were reduced by the overexpression of class 1 nonsymbiotic hemoglobin genes, including HEMOGLOBIN1 (HB1/ GLB1), a core hypoxia-responsive gene of Arabidopsis (Mustroph et al, 2009).…”

Nitrogen metabolism in plants under low oxygen stress

“…NO emission Igamberdiev et al ( , 2010 and Stoimenova et al (2007) was 2.5-fold higher in Hb-silenced plants compared to Hb overexpressors, suggesting that in plants, Hb is involved in the response to hypoxia through the modulation of NO emission and the loss of N to the atmosphere (Dordas et al 2003a). Thus, an additional positive effect of Hb/NO cycle could be to limit N loss under NO emission when oxygen concentration in the medium is close to anoxia (below 0.1 % O 2 ) (Hebelstrup et al 2012).…”

“…1). NO was shown to interact with Hb from different plant species in a Hb/NO cycle, in which the excess NAD(P)H is oxidized for the conversion of NO into nitrate (Hebelstrup et al 2012;Besson-Bard et al 2008b). When alfalfa plants overexpressing Hb were compared to wild type or to Hb-antisense plants, symptoms of hypoxia were improved, leading to a longer survival of the Hb overexpressors (Dordas et al 2003a).…”

AtGGM2014, an Arabidopsis gene co-expression network for functional studies

“…Genes in module #106, such as HB1 and ADH1, mainly function in the hypoxia response. In plants, hypoxia stress induces ethylene production, which in turn promotes upward leaf movement (hyponastic growth) that involves cell growth and expansion [42,43]. ARL & ORS1's connection to both ethylene signaling and hypoxia response genes indicates that these two genes might play an important role in hyponastic growth.…”