Abstract
Oxygen deprivation (hypoxia and anoxia) is an environmental stress affecting plants worldwide in many natural and man-made ecosystems. Aquaporins exhibit multiple physiological functions in challenging environments. The central role of aquaporins in plant water relations has been widely acknowledged, but the role of aquaporins under O2 deficiency remains elusive. Growing evidence has shown that aquaporins are involved in pore-mediated gas trans-membrane movement. In this thesis, Arabidopsis thaliana, tobacco (Nicotiana tabacum L.) and trembling aspen (Populus tremuloides Michx.) seedlings were studied to shed more light on the responses of aquaporins to root hypoxia. Oxygen transport through aquaporins was also examined in yeast heterologously expressing aquaporins from plant, human and fungal organisms. In tobacco, after one week of root hypoxia treatment, plants produced twice as many adventitious roots as the aerated plants, but their maximum length was reduced. Hypoxia severely reduced net photosynthesis, transpiration rates, and photosynthetic light responses. Relative transcript abundance of the examined aquaporins in lateral roots was reduced by hypoxia, but in adventitious roots it remained unchanged. This apparent lack of an effect of root hypoxia on the aquaporin expression likely contributed to maintenance of high hydraulic conductance in adventitious roots. Lateral roots had lower porosity compared with adventitious roots and the expression of the ACS (1-aminocyclopropane-1-carboxylate synthase) gene was induced in hypoxic lateral roots, but not in adventitious roots, providing additional evidence that lateral roots were more affected by hypoxia compared with adventitious roots. ATP concentrations were markedly lower in both hypoxic lateral and adventitious roots compared with aerated roots, while the expression of fermentation-related genes, ADH1 (alcohol dehydrogenase 1) and PDC1 (pyruvate decarboxylase 1), was higher in lateral roots compared with adventitious roots. Since root porosity was greater in adventitious compared with lateral roots, the results suggest that the improved O2 delivery and stable root aquaporin expression in adventitious roots were likely the key factors helping flooded tobacco plants maintain high rates of root hydraulic conductance and, consequently, shoot gas exchange. Effects of ethylene on hypoxia tolerance in plants are little understood. In this thesis research, I examined the physiology and gene expression of several aquaporins in aspen (Populus tremuloides) seedlings exposed to root hypoxia and treated with exogenous ethylene. Ethylene enhanced net photosynthesis, light saturation level for net photosynthesis, transpiration rates, and root hydraulic conductance in hypoxic plants. Root O2 concentrations increased in the hypoxic plants treated with ethylene compared to the hypoxic plants that were not subjected to ethylene treatment. The effect of ethylene on root O2 content could be either due to the enhanced net photosynthesis or facilitated O2 transport from shoots. Ethylene triggered the expression of PIP2;4 aquaporin in hypoxic aspen which could potentially help facilitate root water transport. The enhanced root water transport by ethylene could be also partly responsible for the increase in net photosynthesis of the hypoxic plants which, in turn, could enhance root O2 supply. Arabidopsis seedlings were subjected to waterlogging and compared with well-aerated plants. Photosynthesis and transpiration were inhibited by waterlogging. Waterlogging increased the relative transcript abundance of ADH, PDC-1, and NIP2;1 in plants. After 24 and 48 hours of waterlogging, relative transcript abundance of most of the PIPs decreased, while PIP1;1 and PIP1;4 in waterlogged roots exhibited significantly higher relative transcript abundance compared with aerated roots suggesting that they may play a role in plant resistance mechanisms under hypoxic conditions. O2 permeability of various human, plant, and fungal aquaporins was examined by co-expressing heterologous aquaporin and myoglobin in yeast. Two of the most promising O2-transporters (Homo sapiens AQP1 and N. tabacum PIP1;3) were confirmed to facilitate O2 transport in further spectrophotometric assay using yeast protoplasts. The over-expression of NtPIP1;3 in yeasts significantly increased their O2 uptake rates in suspension culture. In N. tabacum roots subjected to hypoxic conditions in hydroponic culture, it demonstrated a sharp increase in the relative transcript abundance of the O2-transporting aquaporin NtPIP1;3 after seven-day hypoxia treatment, accompanied by the increase in root ATP levels, particularly in the apical root segments. The results show that the functional significance of aquaporin-mediated O2 transport should be considered in further studies and that the possibility of controlling the rate of transmembrane O2 transport should be further explored.
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Claims 20
Claim · model-written summary
Root hypoxia for one week doubled the number of adventitious roots in tobacco relative to aerated plants.
- Taxon
- tobacco
Nicotiana tabacume0 - Treatment
- root hypoxia treatmente0
- Outcome
- adventitious rootse1
- Direction
- twice as manye1
- Value
- twicee1
- Comparator
- aerated plantse1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e1“plants produced twice as many adventitious roots as the aerated plants”
Claim · model-written summary
Root hypoxia reduced the maximum length of the adventitious roots of tobacco.
- Taxon
- tobaccoNicotiana tabacume0
- Treatment
- root hypoxia treatmente0
- Outcome
- maximum lengthe2
- Direction
- reducede2
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e2“but their maximum length was reduced”
Claim · model-written summary
Hypoxia severely reduced net photosynthesis, transpiration rates and photosynthetic light responses in tobacco.
- Taxon
- tobaccoNicotiana tabacume0
- Treatment
- Hypoxiae3
- Outcome
- net photosynthesis, transpiration rates, and photosynthetic light responsese3
- Direction
- severely reducede3
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e3“Hypoxia severely reduced net photosynthesis, transpiration rates, and photosynthetic light responses”
Claim · model-written summary
Hypoxia reduced the relative transcript abundance of the examined aquaporins in lateral roots of tobacco.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- lateral rootse4
- Treatment
- hypoxiae4
- Gene
- aquaporinse4
- Outcome
- Relative transcript abundancee4
- Direction
- reducede4
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e4“Relative transcript abundance of the examined aquaporins in lateral roots was reduced by hypoxia, but in adventitious roots it remained unchanged”
Claim · model-written summary
Hypoxia left the relative transcript abundance of the examined aquaporins unchanged in adventitious roots of tobacco.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- adventitious rootse4
- Treatment
- hypoxiae4
- Gene
- aquaporinse4
- Outcome
- Relative transcript abundancee4
- Direction
- remained unchangede4
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e4“Relative transcript abundance of the examined aquaporins in lateral roots was reduced by hypoxia, but in adventitious roots it remained unchanged”
Claim · model-written summary
Lateral roots of tobacco had lower porosity than adventitious roots.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- Lateral rootse5
- Outcome
- porositye5
- Direction
- lowere5
- Comparator
- adventitious rootse5
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e5“Lateral roots had lower porosity compared with adventitious roots”
Claim · model-written summary
Hypoxia induced expression of the ACS (1-aminocyclopropane-1-carboxylate synthase) gene in lateral roots of tobacco but not in adventitious roots.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- lateral rootse6
- Treatment
- hypoxice6
- Gene
- ACS (1-aminocyclopropane-1-carboxylate synthase)e6
- Outcome
- expressione6
- Direction
- inducede6
- Qualifier
- but not in adventitious rootse6
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e6“the expression of the ACS (1-aminocyclopropane-1-carboxylate synthase) gene was induced in hypoxic lateral roots, but not in adventitious roots”
Claim · model-written summary
ATP concentrations were markedly lower in both hypoxic lateral and adventitious roots of tobacco than in aerated roots.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- lateral and adventitious rootse7
- Treatment
- hypoxice7
- Outcome
- ATP concentrationse7
- Direction
- lowere7
- Comparator
- aerated rootse7
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e7“ATP concentrations were markedly lower in both hypoxic lateral and adventitious roots compared with aerated roots”
Claim · model-written summary
Expression of ADH1 and PDC1 was higher in lateral roots than in adventitious roots of tobacco.
- Taxon
- tobaccoNicotiana tabacume0
- Organ / stage
- lateral rootse1
- Gene
- ADH1 (alcohol dehydrogenase 1) and PDC1 (pyruvate decarboxylase 1)e1
- Outcome
- expressione1
- Direction
- highere1
- Comparator
- adventitious rootse1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In tobacco, after one week of root hypoxia treatment”
e1“the expression of fermentation-related genes, ADH1 (alcohol dehydrogenase 1) and PDC1 (pyruvate decarboxylase 1), was higher in lateral roots compared with adventitious roots”
Claim · model-written summary
Ethylene enhanced net photosynthesis, light saturation level for net photosynthesis and transpiration rates in hypoxic aspen seedlings.
Verbatim
e0“aspen (Populus tremuloides) seedlings”
e1“Ethylene enhanced net photosynthesis, light saturation level for net photosynthesis, transpiration rates, and root hydraulic conductance in hypoxic plants”
e2“the hypoxic plants that were not subjected to ethylene treatment”
Claim · model-written summary
Ethylene enhanced root hydraulic conductance in hypoxic aspen seedlings.
Verbatim
e0“aspen (Populus tremuloides) seedlings”
e1“Ethylene enhanced net photosynthesis, light saturation level for net photosynthesis, transpiration rates, and root hydraulic conductance in hypoxic plants”
e2“the hypoxic plants that were not subjected to ethylene treatment”
Claim · model-written summary
Ethylene increased root O2 concentrations in hypoxic aspen seedlings.
Verbatim
e0“aspen (Populus tremuloides) seedlings”
e1“Root O2 concentrations increased in the hypoxic plants treated with ethylene”
e2“the hypoxic plants that were not subjected to ethylene treatment”
Claim · model-written summary
Ethylene triggered expression of the PIP2;4 aquaporin in hypoxic aspen.
Not reportedComparator
Verbatim
e0“Ethylene triggered the expression of PIP2;4 aquaporin in hypoxic aspen”
Claim · model-written summary
Waterlogging inhibited photosynthesis and transpiration in Arabidopsis seedlings relative to well-aerated plants.
- Taxon
- Arabidopsis
Arabidopsise0 - Treatment
- waterlogginge0
- Outcome
- Photosynthesis and transpiratione1
- Direction
- inhibitede1
- Comparator
- well-aerated plantse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Arabidopsis seedlings were subjected to waterlogging and compared with well-aerated plants”
e1“Photosynthesis and transpiration were inhibited by waterlogging”
Claim · model-written summary
Waterlogging increased relative transcript abundance of ADH, PDC-1 and NIP2;1 in Arabidopsis plants relative to well-aerated plants.
- Taxon
- ArabidopsisArabidopsise0
- Treatment
- Waterlogginge1
- Gene
- ADH, PDC-1, and NIP2;1e1
- Outcome
- relative transcript abundancee1
- Direction
- increasede1
- Comparator
- well-aerated plantse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Arabidopsis seedlings were subjected to waterlogging and compared with well-aerated plants”
e1“Waterlogging increased the relative transcript abundance of ADH, PDC-1, and NIP2;1 in plants”
Claim · model-written summary
After 24 and 48 hours of waterlogging, relative transcript abundance of most PIPs in Arabidopsis decreased.
- Taxon
- ArabidopsisArabidopsise0
- Treatment
- 24 and 48 hours of waterlogginge1
- Gene
- PIPse1
- Outcome
- relative transcript abundancee1
- Direction
- decreasede1
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Arabidopsis seedlings were subjected to waterlogging and compared with well-aerated plants”
e1“After 24 and 48 hours of waterlogging, relative transcript abundance of most of the PIPs decreased”
Claim · model-written summary
In waterlogged Arabidopsis roots, PIP1;1 and PIP1;4 transcript abundance was significantly higher than in aerated roots, which may indicate a role in resistance under hypoxia.
- Taxon
- ArabidopsisArabidopsise0
- Organ / stage
- waterlogged rootse1
- Treatment
- waterloggede1
- Gene
- PIP1;1 and PIP1;4e1
- Outcome
- relative transcript abundancee1
- Direction
- highere1
- Qualifier
- may play a role in plant resistance mechanisms under hypoxic conditionse2
- Comparator
- aerated rootse1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“Arabidopsis seedlings were subjected to waterlogging and compared with well-aerated plants”
e1“while PIP1;1 and PIP1;4 in waterlogged roots exhibited significantly higher relative transcript abundance compared with aerated roots”
e2“may play a role in plant resistance mechanisms under hypoxic conditions”
Claim · model-written summary
Over-expression of NtPIP1;3 in yeast significantly increased O2 uptake rates in suspension culture.
- Taxon
- N. tabacumNicotiana tabacume0
- Treatment
- over-expression of NtPIP1;3 in yeastse1
- Gene
- NtPIP1;3e1
- Outcome
- O2 uptake ratese1
- Direction
- increasede1
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“N. tabacum PIP1;3”
e1“The over-expression of NtPIP1;3 in yeasts significantly increased their O2 uptake rates in suspension culture”
Claim · model-written summary
Seven-day root hypoxia sharply increased relative transcript abundance of NtPIP1;3 in tobacco roots in hydroponic culture.
- Taxon
- N. tabacumNicotiana tabacume0
- Organ / stage
- rootse0
- Treatment
- seven-day hypoxia treatmente0
- Gene
- NtPIP1;3e0
- Outcome
- relative transcript abundancee0
- Direction
- increasee0
- Setting
- hydroponic culturee0
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In N. tabacum roots subjected to hypoxic conditions in hydroponic culture, it demonstrated a sharp increase in the relative transcript abundance of the O2-transporting aquaporin NtPIP1;3 after seven-day hypoxia treatment”
Claim · model-written summary
Seven-day root hypoxia increased root ATP levels in tobacco, particularly in apical root segments.
- Taxon
- N. tabacumNicotiana tabacume0
- Organ / stage
- apical root segmentse1
- Treatment
- seven-day hypoxia treatmente0
- Outcome
- root ATP levelse1
- Direction
- increasee1
Not reportedComparator
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
e0“In N. tabacum roots subjected to hypoxic conditions in hydroponic culture, it demonstrated a sharp increase in the relative transcript abundance of the O2-transporting aquaporin NtPIP1;3 after seven-day hypoxia treatment”
e1“accompanied by the increase in root ATP levels, particularly in the apical root segments”
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