Abstract
BACKGROUND: With the increasing interest in metabolic engineering of plants using genetic manipulation and gene editing technologies to enhance growth, nutritional value and environmental adaptation, a major concern is the potential of undesirable broad and distant effects of manipulating the target gene or metabolic step in the resulting plant. A comprehensive transcriptomic and metabolomic analysis of the product may shed some useful light in this regard. The present study used these two techniques with plant cell cultures to analyze the effects of genetic manipulation of a single step in the biosynthesis of polyamines because of their well-known roles in plant growth, development and stress responses. RESULTS: The transcriptomes and metabolomes of a control and a high putrescine (HP) producing cell line of poplar (Populus nigra x maximowiczii) were compared using microarrays and GC/MS. The HP cells expressed an ornithine decarboxylase transgene and accumulated several-fold higher concentrations of putrescine, with only small changes in spermidine and spermine. The results show that up-regulation of a single step in the polyamine biosynthetic pathway (i.e. ornithine → putrescine) altered the expression of a broad spectrum of genes; many of which were involved in transcription, translation, membrane transport, osmoregulation, shock/stress/wounding, and cell wall metabolism. More than half of the 200 detected metabolites were significantly altered (p ≤ 0.05) in the HP cells irrespective of sampling date. The most noteworthy differences were in organic acids, carbohydrates and nitrogen-containing metabolites. CONCLUSIONS: The results provide valuable information about the role of polyamines in regulating nitrogen and carbon use pathways in cell cultures of high putrescine producing transgenic cells of poplar vs. their low putrescine counterparts. The results underscore the complexity of cellular responses to genetic perturbation of a single metabolic step related to nitrogen metabolism in plants. Combined with recent studies from our lab, where we showed that higher putrescine production caused an increased flux of glutamate into ornithine concurrent with enhancement in glutamate production via additional nitrogen and carbon assimilation, the results from this study provide guidance in designing transgenic plants with increased nitrogen use efficiency, especially in plants intended for non-food/feed applications (e.g. increased biomass production for biofuels).
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Claims 5
Claim · model-written summary
The high-putrescine poplar line accumulated several-fold more putrescine, with only small changes in spermidine and spermine.
- Treatment
- ornithine decarboxylase transgenee0
- Gene
- ornithine decarboxylasee0
- Outcome
- concentrations of putrescinee0
- Direction
- highere0
- Value
- several-folde0
PopulusNot reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“The HP cells expressed an ornithine decarboxylase transgene and accumulated several-fold higher concentrations of putrescine, with only small changes in spermidine and spermine.”
e1“cell line of poplar (Populus nigra x maximowiczii)”
Claim · model-written summary
Up-regulating ornithine to putrescine biosynthesis altered expression of a broad range of genes.
- Treatment
- up-regulation of a single step in the polyamine biosynthetic pathwaye0
- Outcome
- expression of a broad spectrum of genese0
- Qualifier
- transcription, translation, membrane transport, osmoregulation, shock/stress/wounding, and cell wall metabolisme0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“up-regulation of a single step in the polyamine biosynthetic pathway (i.e. ornithine → putrescine) altered the expression of a broad spectrum of genes; many of which were involved in transcription, translation, membrane transport, osmoregulation, shock/stress/wounding, and cell wall metabolism.”
e1“cell line of poplar (Populus nigra x maximowiczii)”
Claim · model-written summary
More than half of 200 detected metabolites differed significantly in high-putrescine cells regardless of sampling date.
- Treatment
- HP cellse0
- Outcome
- detected metabolitese0
- Value
- More than half of the 200e0
- Qualifier
- irrespective of sampling datee0
Not reportedComparatorDirection
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“More than half of the 200 detected metabolites were significantly altered (p ≤ 0.05) in the HP cells irrespective of sampling date.”
e1“cell line of poplar (Populus nigra x maximowiczii)”
Claim · model-written summary
The most notable metabolite differences involved organic acids, carbohydrates and nitrogen-containing metabolites.
- Outcome
- differences were in organic acids, carbohydrates and nitrogen-containing metabolitese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“The most noteworthy differences were in organic acids, carbohydrates and nitrogen-containing metabolites.”
e1“cell line of poplar (Populus nigra x maximowiczii)”
Claim · model-written summary
The authors suggest these results can guide engineering plants for increased nitrogen use efficiency.
- Outcome
- designing transgenic plants with increased nitrogen use efficiencye0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“the results from this study provide guidance in designing transgenic plants with increased nitrogen use efficiency, especially in plants intended for non-food/feed applications (e.g. increased biomass production for biofuels).”
e1“cell line of poplar (Populus nigra x maximowiczii)”