Abstract
BackgroundSeed metabolism is dynamically adjusted to oxygen availability. Processes underlying this auto-regulatory mechanism control the metabolic efficiency under changing environmental conditions/stress and thus, are of relevance for biotechnology. Non-symbiotic hemoglobins have been shown to be involved in scavenging of nitric oxide (NO) molecules, which play a key role in oxygen sensing/balancing in plants and animals. Steady state levels of NO are suggested to act as an integrator of energy and carbon metabolism and subsequently, influence energy-demanding growth processes in plants.ResultsWe aimed to manipulate oxygen stress perception in Arabidopsis seeds by overexpression of the non-symbiotic hemoglobin AtHb1 under the control of the seed-specific LeB4 promoter. Seeds of transgenic AtHb1 plants did not accumulate NO under transient hypoxic stress treatment, showed higher respiratory activity and energy status compared to the wild type. Global transcript profiling of seeds/siliques from wild type and transgenic plants under transient hypoxic and standard conditions using Affymetrix ATH1 chips revealed a rearrangement of transcriptional networks by AtHb1 overexpression under non-stress conditions, which included the induction of transcripts related to ABA synthesis and signaling, receptor-like kinase- and MAP kinase-mediated signaling pathways, WRKY transcription factors and ROS metabolism. Overexpression of AtHb1 shifted seed metabolism to an energy-saving mode with the most prominent alterations occurring in cell wall metabolism. In combination with metabolite and physiological measurements, these data demonstrate that AtHb1 overexpression improves oxidative stress tolerance compared to the wild type where a strong transcriptional and metabolic reconfiguration was observed in the hypoxic response.ConclusionsAtHb1 overexpression mediates a pre-adaptation to hypoxic stress. Under transient stress conditions transgenic seeds were able to keep low levels of endogenous NO and to maintain a high energy status, in contrast to wild type. Higher weight of mature transgenic seeds demonstrated the beneficial effects of seed-specific overexpression of AtHb1.
Highlights
Seed metabolism is dynamically adjusted to oxygen availability
To avoid any stress-induced artefacts that might be induced by dissection of seeds from the siliques, whole siliques were used for further studies
Screening our dataset for other differentially expressed transcripts involved in electron transport chain/ATP synthesis, we found five other transcripts, encoding ATP synthase, NADH dehydrogenase, NADH:ubiquinone oxidoreductase, cytochrome C oxidoreductase subunit 5c (COX 5C), with a tendency to higher expression in AtHb1 seeds under hypoxia
Summary
Seed metabolism is dynamically adjusted to oxygen availability. Processes underlying this autoregulatory mechanism control the metabolic efficiency under changing environmental conditions/stress and are of relevance for biotechnology. There are three major groups: (i) symbiotic or leghemoglobins, facilitating oxygen diffusion to nitrogen-fixing bacteria in nodules of plants (ii) non-symbiotic hemoglobins (nsHbs) found in numerous species, and (iii) the processes, like stomatal closure, programmed cell death and pathogen resistance [9]. Seeds of crop species experience a regular oxygen deficiency during both development and germination [12]. This leads to ATP limitation and subsequently, to a restriction of high energy-demanding processes like cell division, growth and storage product synthesis [13]. The molecular mechanisms of the seeds’ response to hypoxia might resemble those of other plant organs [15,16,17] and tissue types [18] of Arabidopsis, but detailed transcriptomic studies are lacking
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