Abstract
Tropospheric ozone (O3) is one of the most common air pollutants in industrialized countries, and an increasing problem in rapidly industrialising and developing countries in Asia, Africa and South America. Elevated concentrations of tropospheric O3 can lead to decrease in photosynthesis rate and therefore affect the normal metabolism, growth and seed production. Acute and high O3 episodes can lead to extensive damage leading to dead tissue in plants. Thus, O3 derived growth defects can lead to reduction in crop yield thereby leading to economical losses. Despite the extensive research on this area, many questions remain open on how these processes are controlled. In this study, the stress-induced signaling routes and the components involved were elucidated in more detail starting from visual damage to changes in gene expression, signaling routes and plant hormone interactions that are involved in O3-induced cell death. In order to elucidate O3-induced responses in Arabidopsis, mitogen-activated protein kinase (MAPK) signaling was studied using different hormonal signaling mutants. MAPKs were activated at the beginning of the O3 exposure. The activity of MAPKs, which were identified as AtMPK3 and AtMPK6, reached the maximum at 1 and 2 hours after the start of the exposure, respectively. The activity decreased back to clean air levels at 8 hours after the start of the exposure. Both AtMPK3 and AtMPK6 were translocated to nucleus at the beginning of the O3 exposure where they most likely affect gene expression. Differences were seen between different hormonal signaling mutants. Functional SA signaling was shown to be needed for the full protein levels and activation of AtMPK3. In addition, AtMPK3 and AtMPK6 activation was not dependent on ethylene signaling. Finally, jasmonic acid was also shown to have an impact on AtMPK3 protein levels and AtMPK3 activity. To further study O3-induced cell death, an earlier isolated O3 sensitive Arabidopsis mutant rcd1 was mapped, cloned and further characterized. RCD1 was shown to encode a gene with WWE and ADP-ribosylation domains known to be involved in protein-protein interactions and cell signaling. rcd1 was shown to be involved in many processes including hormonal signaling and regulation of stress-responsive genes. rcd1 is sensitive against O3 and apoplastic superoxide, but tolerant against paraquat that produces superoxide in chloroplast. rcd1 is also partially insensitive to glucose and has alterations in hormone responses. These alterations are seen as ABA insensitivity, reduced jasmonic acid sensitivity and reduced ethylene sensitivity. All these features suggest that RCD1 acts as an integrative node in hormonal signaling and it is involved in the hormonal regulation of several specific stress-responsive genes. Further studies with the rcd1 mutant showed that it exhibits the classical features of programmed cell death, PCD, in response to O3. These include nuclear shrinkage, chromatin condensation, nuclear DNA degradation, cytosol vesiculation and accumulation of phenolic compounds and eventually patches of HR-like lesions. rcd1 was found to produce extensive amount of salicylic acid and jasmonic acid in response to O3. Double mutant studies showed that SA independent and dependent processes were involved in the O3-induced PCD in rcd1 and that increased sensitivity against JA led to increased sensitivity against O3. Furthermore, rcd1 had alterations in MAPK signature that resembled changes that were previously seen in mutants defective in SA and JA signaling. Nitric oxide accumulation and its impact on O3-induced cell death were also studied. Transient accumulation of NO was seen at the beginning of the O3 exposure, and during late time points, NO accumulation coincided with the HR-like lesions. NO was shown to modify defense gene expression, such as, SA and ethylene biosynthetic genes. Furthermore, rcd1 was shown to produce more NO in control conditions. In conclusion, NO was shown to be involved in O3-induced signaling leading to attenuation of SA biosynthesis and other defense related genes.
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Claims 20
Claim · model-written summary
MAPKs were activated at the beginning of ozone exposure in Arabidopsis.
- Taxon
- Arabidopsis thaliana
Arabidopsis thalianat0 - Treatment
- O3 exposuree0
- Gene
- MAPKse0
- Outcome
- activated at the beginning of the O3 exposuree0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“MAPKs were activated at the beginning of the O3 exposure”
Claim · model-written summary
The activities of AtMPK3 and AtMPK6 reached their maximum at 1 and 2 hours after the start of ozone exposure, respectively.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- AtMPK3 and AtMPK6e0
- Outcome
- activity of MAPKse0
- Direction
- maximume0
- Value
- 1 and 2 hourse0
- Qualifier
- after the start of the exposuree0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“The activity of MAPKs, which were identified as AtMPK3 and AtMPK6, reached the maximum at 1 and 2 hours after the start of the exposure, respectively”
Claim · model-written summary
MAPK activity decreased back to clean air levels 8 hours after the start of ozone exposure.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Outcome
- activitye0
- Direction
- decreasede0
- Value
- 8 hourse0
- Comparator
- clean air levelse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“The activity decreased back to clean air levels at 8 hours after the start of the exposure”
Claim · model-written summary
AtMPK3 and AtMPK6 were translocated to the nucleus at the beginning of ozone exposure.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Treatment
- O3 exposuree0
- Gene
- AtMPK3 and AtMPK6e0
- Outcome
- translocated to nucleuse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“Both AtMPK3 and AtMPK6 were translocated to nucleus at the beginning of the O3 exposure”
Claim · model-written summary
Functional SA signaling was needed for full protein levels and activation of AtMPK3.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- AtMPK3e0
- Compound
- SAe0
- Outcome
- full protein levels and activation of AtMPK3e0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“Functional SA signaling was shown to be needed for the full protein levels and activation of AtMPK3”
Claim · model-written summary
AtMPK3 and AtMPK6 activation was not dependent on ethylene signaling.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- AtMPK3 and AtMPK6e0
- Compound
- ethylenee0
- Outcome
- activatione0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“AtMPK3 and AtMPK6 activation was not dependent on ethylene signaling”
Claim · model-written summary
Jasmonic acid had an impact on AtMPK3 protein levels and AtMPK3 activity.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- AtMPK3e0
- Compound
- jasmonic acide0
- Outcome
- AtMPK3 protein levels and AtMPK3 activitye0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“jasmonic acid was also shown to have an impact on AtMPK3 protein levels and AtMPK3 activity”
Claim · model-written summary
RCD1 was shown to encode a gene with WWE and ADP-ribosylation domains.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- RCD1e0
- Outcome
- encode a gene with WWE and ADP-ribosylation domainse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“RCD1 was shown to encode a gene with WWE and ADP-ribosylation domains”
Claim · model-written summary
The rcd1 mutant is sensitive to ozone and apoplastic superoxide.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Treatment
- O3 and apoplastic superoxidee0
- Outcome
- sensitivee0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 is sensitive against O3 and apoplastic superoxide”
Claim · model-written summary
The rcd1 mutant is tolerant to paraquat, which produces superoxide in the chloroplast.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Treatment
- paraquate0
- Outcome
- tolerante0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 is sensitive against O3 and apoplastic superoxide, but tolerant against paraquat”
Claim · model-written summary
The rcd1 mutant is partially insensitive to glucose and has altered hormone responses (ABA insensitivity, reduced jasmonic acid and ethylene sensitivity).
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Outcome
- partially insensitive to glucose and has alterations in hormone responsese0
- Qualifier
- ABA insensitivity, reduced jasmonic acid sensitivity and reduced ethylene sensitivitye1
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 is also partially insensitive to glucose and has alterations in hormone responses”
e1“ABA insensitivity, reduced jasmonic acid sensitivity and reduced ethylene sensitivity”
Claim · model-written summary
The rcd1 mutant exhibits the classical features of programmed cell death in response to ozone.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Treatment
- O3e0
- Outcome
- classical features of programmed cell deathe0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“Further studies with the rcd1 mutant showed that it exhibits the classical features of programmed cell death, PCD, in response to O3”
Claim · model-written summary
The rcd1 mutant produced extensive amounts of salicylic acid and jasmonic acid in response to ozone.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Treatment
- O3e0
- Outcome
- produce extensive amount of salicylic acid and jasmonic acide0
- Direction
- extensive amounte0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 was found to produce extensive amount of salicylic acid and jasmonic acid in response to O3”
Claim · model-written summary
SA-independent and SA-dependent processes were involved in ozone-induced PCD in rcd1.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Compound
- SAe0
- Outcome
- O3-induced PCDe0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“SA independent and dependent processes were involved in the O3-induced PCD in rcd1”
Claim · model-written summary
Increased sensitivity to jasmonic acid led to increased sensitivity to ozone in the double mutant studies.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Compound
- JAe0
- Outcome
- sensitivity against O3e0
- Direction
- increasede0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“increased sensitivity against JA led to increased sensitivity against O3”
Claim · model-written summary
The rcd1 mutant had alterations in MAPK signature resembling those of mutants defective in SA and JA signaling.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Outcome
- alterations in MAPK signaturee0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 had alterations in MAPK signature that resembled changes that were previously seen in mutants defective in SA and JA signaling”
Claim · model-written summary
NO accumulated transiently at the beginning of ozone exposure, and at late time points NO accumulation coincided with HR-like lesions.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Treatment
- O3 exposuree0
- Outcome
- Transient accumulation of NOe0
- Qualifier
- NO accumulation coincided with the HR-like lesionse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“Transient accumulation of NO was seen at the beginning of the O3 exposure, and during late time points, NO accumulation coincided with the HR-like lesions”
Claim · model-written summary
NO modified defense gene expression, such as SA and ethylene biosynthetic genes.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Gene
- SA and ethylene biosynthetic genese0
- Compound
- NOe0
- Outcome
- defense gene expressione0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“NO was shown to modify defense gene expression, such as, SA and ethylene biosynthetic genes”
Claim · model-written summary
The rcd1 mutant produced more NO in control conditions.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Material
- rcd1e0
- Outcome
- produce more NOe0
- Direction
- moree0
- Qualifier
- control conditionse0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“rcd1 was shown to produce more NO in control conditions”
Claim · model-written summary
NO was involved in ozone-induced signaling leading to attenuation of SA biosynthesis and other defense-related genes.
- Taxon
- Arabidopsis thalianaArabidopsis thalianat0
- Compound
- NOe0
- Outcome
- attenuation of SA biosynthesis and other defense related genese0
Organisms pictured · Representative pictures of the matched species, not figures from the paper.
Verbatim
t0“Arabidopsis thaliana”
e0“NO was shown to be involved in O3-induced signaling leading to attenuation of SA biosynthesis and other defense related genes”