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Enhanced Photosynthesis and Carbon Metabolism Favor Arsenic Tolerance in Artemisia annua, a Medicinal Plant as Revealed by Homology-Based Proteomics.

Rai R, Pandey S, Shrivastava AK, Pandey Rai S - Int J Proteomics (2014)

Bottom Line: However, a decrease in the above variables was recorded under 150  μ M treatments.While an increased accumulation of ATP synthase, ferredoxin-NADP(H) oxidoreductase, and FeS-rieske proteins supported the operation of cyclic electron transport, mdr ABC transporter protein and pcs gene might be involved in As detoxification.This study not only affirmed the role of energy metabolism proteins but also identified potential candidates responsible for As tolerance in plants.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Morphogenesis, Center of Advanced Study in Botany, Banaras Hindu University, Varanasi 221005, India.

ABSTRACT
This paper provides the first proteomic evidence of arsenic (As) tolerance and interactive regulatory network between primary and secondary metabolism in the medicinal plant, Artemisia annua. While chlorophyll fluorescence and photosynthetic rate depicted mild inhibition, there was a significant enhancement in PSI activity, whole chain, ATP, and NADPH contents in 100  μ M As treatments compared to the control plants. However, a decrease in the above variables was recorded under 150  μ M treatments. Proteomic decoding of the survival strategy of A. annua under As stress using 2-DE followed by MALDI-MS/MS revealed a total of 46 differentially expressed protein spots. In contrast to other plants where As inhibits photosynthesis, A. annua showed appreciable photosynthetic CO2 assimilation and allocation of carbon resources at 100  μ M As concentration. While an increased accumulation of ATP synthase, ferredoxin-NADP(H) oxidoreductase, and FeS-rieske proteins supported the operation of cyclic electron transport, mdr ABC transporter protein and pcs gene might be involved in As detoxification. The most interesting observation was an increased accumulation of LEAFY like novel protein conceivably responsible for an early onset of flowering in A. annua under As stress. This study not only affirmed the role of energy metabolism proteins but also identified potential candidates responsible for As tolerance in plants.

No MeSH data available.


Related in: MedlinePlus

Hypothetical model depicting As tolerance and interactive protein network between primary and secondary metabolism in Artemisia annua.
© Copyright Policy - open-access
Related In: Results  -  Collection


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fig7: Hypothetical model depicting As tolerance and interactive protein network between primary and secondary metabolism in Artemisia annua.

Mentions: The physiological traits monitored revealed contrastingly differences under 100 and 150 μM As treatments. While PSI activity, transpiration rate, ATP, and NADPH contents of 100 μM As treated A. annua plants showed an increase over the control values, a decrease for these parameters was recorded at 150 μM As treatments. On the other hand, PSII activity registered decline under both the treatments, this being more pronounced at 150 μM As treatments. The Fv/Fm ratio, considered as indicator of the photochemical processes in photosystem 2 (PSII), depicted only a minor inhibition at 100 μM but severe reduction under 150 μM As treatments. Above findings were supported by the protein data having increased abundance of ATP synthase α subunit, rieske protein, and ferredoxin-NADP reductase (FNR) under 100 μM As treatments, suggesting their likely role in As tolerance. Moreover, this enhancement unswervingly indicates operation of Fd-dependent cyclic electron transport (CET) in the test organism. In general, plants exposed to abiotic stresses show downregulation of linear electron flow (LEF) and activation of cyclic electron transport (CET) when linear electron flow becomes saturated [56, 57]. It could be anticipated that under 100 μM As treatment the LEF is partially replaced by CET around PSI and the upregulated CET in turn provides energy to the Calvin cycle [58] thereby meeting the energy demand. Appreciable increase in NADPH content seems justified in view of its requirement as reducing equivalents during CO2 fixation on one hand and maintaining a ratio of reduced glutathione for scavenging ROS. By contrast, under 150 μM As treatments, the down regulated FNR disrupts CET. The electrons so accumulated suppress the charge separation of PSII reaction centre leading to damage of PSII as attested by the results of decreased Fv/Fm ratios and decreased ATP content (Table 2, Figure 7). Four proteins of chlorophyll a/b binding category (CP26 in PS II) displayed a mixed expression under 100 and 150 μM As treatments. Altered levels of multiple forms of this protein have been reported in rice seedling under high temperature [59] and H2O2 stress [60]. Another protein (spot 11) identified as chloroplast PS I type III chlorophyll a/b binding protein was increased in 100 μM As treatment. This may confer enhanced resistance of PSI as known for Hordeum vulgare against boron stress [61]. While (OECP2) protein spot 4 (intact) depicted increased relative abundance, the protein (spot 5) BLAST identified as oxygen-evolving complex protein (OEC1) was decreased under both treatments. OECP2 are manganese stabilizing proteins playing crucial roles in photosystem II stability [41], their decreased accumulation supports the damaged PSII under As treatments. A marked increase in P protein subunit of glycine associated with photorespiration was found in 150 mM As-stressed plants. Its overexpression stimulated photorespiration in Anabaena sp. under As stress [41]. These results clearly demonstrated that inhibition of photosynthetic rate in 150 μM As treated A. annua was not the consequence of stomatal closure (reflected by high intercellular CO2 value) hence CO2 limitation may not be the real cause for reduced carbon assimilation rates. The decrease in assimilation rates could be due to low ATP and NADPH contents (Table 2) and consequent impairment of the photosynthesis [47, 62]. Furthermore, the photosynthetic rate is known to weaken in the presence of heavy metals due to alterations in the active site of rubisco subunits [63, 64]. By contrast, PSI complex machinery might be envisioned to support the damaged PSII and maintain NADPH pool in 100 μM As treated plants as observed in As-tolerant cordgrass Spartina densiflora [65] and Ricinus communis [66].


Enhanced Photosynthesis and Carbon Metabolism Favor Arsenic Tolerance in Artemisia annua, a Medicinal Plant as Revealed by Homology-Based Proteomics.

Rai R, Pandey S, Shrivastava AK, Pandey Rai S - Int J Proteomics (2014)

Hypothetical model depicting As tolerance and interactive protein network between primary and secondary metabolism in Artemisia annua.
© Copyright Policy - open-access
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC4020366&req=5

fig7: Hypothetical model depicting As tolerance and interactive protein network between primary and secondary metabolism in Artemisia annua.
Mentions: The physiological traits monitored revealed contrastingly differences under 100 and 150 μM As treatments. While PSI activity, transpiration rate, ATP, and NADPH contents of 100 μM As treated A. annua plants showed an increase over the control values, a decrease for these parameters was recorded at 150 μM As treatments. On the other hand, PSII activity registered decline under both the treatments, this being more pronounced at 150 μM As treatments. The Fv/Fm ratio, considered as indicator of the photochemical processes in photosystem 2 (PSII), depicted only a minor inhibition at 100 μM but severe reduction under 150 μM As treatments. Above findings were supported by the protein data having increased abundance of ATP synthase α subunit, rieske protein, and ferredoxin-NADP reductase (FNR) under 100 μM As treatments, suggesting their likely role in As tolerance. Moreover, this enhancement unswervingly indicates operation of Fd-dependent cyclic electron transport (CET) in the test organism. In general, plants exposed to abiotic stresses show downregulation of linear electron flow (LEF) and activation of cyclic electron transport (CET) when linear electron flow becomes saturated [56, 57]. It could be anticipated that under 100 μM As treatment the LEF is partially replaced by CET around PSI and the upregulated CET in turn provides energy to the Calvin cycle [58] thereby meeting the energy demand. Appreciable increase in NADPH content seems justified in view of its requirement as reducing equivalents during CO2 fixation on one hand and maintaining a ratio of reduced glutathione for scavenging ROS. By contrast, under 150 μM As treatments, the down regulated FNR disrupts CET. The electrons so accumulated suppress the charge separation of PSII reaction centre leading to damage of PSII as attested by the results of decreased Fv/Fm ratios and decreased ATP content (Table 2, Figure 7). Four proteins of chlorophyll a/b binding category (CP26 in PS II) displayed a mixed expression under 100 and 150 μM As treatments. Altered levels of multiple forms of this protein have been reported in rice seedling under high temperature [59] and H2O2 stress [60]. Another protein (spot 11) identified as chloroplast PS I type III chlorophyll a/b binding protein was increased in 100 μM As treatment. This may confer enhanced resistance of PSI as known for Hordeum vulgare against boron stress [61]. While (OECP2) protein spot 4 (intact) depicted increased relative abundance, the protein (spot 5) BLAST identified as oxygen-evolving complex protein (OEC1) was decreased under both treatments. OECP2 are manganese stabilizing proteins playing crucial roles in photosystem II stability [41], their decreased accumulation supports the damaged PSII under As treatments. A marked increase in P protein subunit of glycine associated with photorespiration was found in 150 mM As-stressed plants. Its overexpression stimulated photorespiration in Anabaena sp. under As stress [41]. These results clearly demonstrated that inhibition of photosynthetic rate in 150 μM As treated A. annua was not the consequence of stomatal closure (reflected by high intercellular CO2 value) hence CO2 limitation may not be the real cause for reduced carbon assimilation rates. The decrease in assimilation rates could be due to low ATP and NADPH contents (Table 2) and consequent impairment of the photosynthesis [47, 62]. Furthermore, the photosynthetic rate is known to weaken in the presence of heavy metals due to alterations in the active site of rubisco subunits [63, 64]. By contrast, PSI complex machinery might be envisioned to support the damaged PSII and maintain NADPH pool in 100 μM As treated plants as observed in As-tolerant cordgrass Spartina densiflora [65] and Ricinus communis [66].

Bottom Line: However, a decrease in the above variables was recorded under 150  μ M treatments.While an increased accumulation of ATP synthase, ferredoxin-NADP(H) oxidoreductase, and FeS-rieske proteins supported the operation of cyclic electron transport, mdr ABC transporter protein and pcs gene might be involved in As detoxification.This study not only affirmed the role of energy metabolism proteins but also identified potential candidates responsible for As tolerance in plants.

View Article: PubMed Central - PubMed

Affiliation: Laboratory of Morphogenesis, Center of Advanced Study in Botany, Banaras Hindu University, Varanasi 221005, India.

ABSTRACT
This paper provides the first proteomic evidence of arsenic (As) tolerance and interactive regulatory network between primary and secondary metabolism in the medicinal plant, Artemisia annua. While chlorophyll fluorescence and photosynthetic rate depicted mild inhibition, there was a significant enhancement in PSI activity, whole chain, ATP, and NADPH contents in 100  μ M As treatments compared to the control plants. However, a decrease in the above variables was recorded under 150  μ M treatments. Proteomic decoding of the survival strategy of A. annua under As stress using 2-DE followed by MALDI-MS/MS revealed a total of 46 differentially expressed protein spots. In contrast to other plants where As inhibits photosynthesis, A. annua showed appreciable photosynthetic CO2 assimilation and allocation of carbon resources at 100  μ M As concentration. While an increased accumulation of ATP synthase, ferredoxin-NADP(H) oxidoreductase, and FeS-rieske proteins supported the operation of cyclic electron transport, mdr ABC transporter protein and pcs gene might be involved in As detoxification. The most interesting observation was an increased accumulation of LEAFY like novel protein conceivably responsible for an early onset of flowering in A. annua under As stress. This study not only affirmed the role of energy metabolism proteins but also identified potential candidates responsible for As tolerance in plants.

No MeSH data available.


Related in: MedlinePlus