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The role of thioredoxins in acclimation to light
The role of thioredoxins in acclimation to light
The photosynthetic conversion of light energy into chemical energy represents one of the most important processes on our planet. Changing light conditions lead to uneven stress on the photosystems in plants and influence all subsequent processes in the chloroplasts. Sessile land plants are able to adapt to these changes. The protein family of thioredoxins (TRXs) plays an important role in these processes. Thioredoxins are plastid oxidoreductases that mediate energy in the form of electrons between plastidial light and carbon reactions. Oxidized TRXs are reduced on a cascade via photosystem I (PSI), ferredoxin (Fd) and eventually by ferredoxin-thioredoxin reductase (FTR), and therefore grouped together as the FTR system. In addition, there is the ferredoxin-NADPH-dependent system (FNR), whose representative is NAPDH-dependent thioredoxin C (NTRC), which combines an NADPH sensitive domain and a TRX. Studies suggest that these two systems interact to modulate their activity. The activity of these redox modulators is characterized by thiol modification of cysteines. This very fast modulation in the seconds to minutes range is crucial for the stability and function of target proteins. Known roles of TRX include, first and foremost, light-dependent reduction, and thus activation of Calvin-Benson cycle (CBC) enzymes after prolonged darkness, maintenance of redox homeostasis and the antioxidant system, and plastid gene expression. Since little is known about the role of the FTR and FNR systems in regulating longer-term responses to changing light conditions, the present work has now used high-throughput methods and the reverse genetics approach to investigate the influence of the TRXs f1, m1, m2, and NTRC on photosynthesis, central metabolism, the CBC and on the proteome once different light energy and exposure times are available to the plant. Here it was shown that the cell response, at the level of photosynthesis and metabolism, to short-term changes between moderate and higher light in the range of minutes to hours depends rather little on the TRX/NTRC system. For more rapid changes between low and high light on the order of minutes, photosynthetic adaptation in ntrc mutants originating from control conditions is blocked, while wild type plants were increasingly able to acclimatize to this condition over days. This suggests an important role for NTRC in adaptation to rapidly changing, so-called fluctuating light, which is closest to natural conditions. Further, longer-term acclimation to high light, low light, and fluctuating light, in the range of days with higher average light intensity, showed mostly overlap between wild type and the TRX mutants, with most changes visible in high light. In the wild type, central metabolism, CBC, and stress response proteins were boosted here, whereas translational processes were down-regulated. Disruption of NTRC expression impaired the quantum efficiency of photosystem II as seen previously, especially in fluctuating light, but also in high light. By comparison with all other conditions, it was noticeable that the ntrc mutant lacked any dynamic adaptation and stimulation at the level of metabolism and proteome, especially in high light. It seems conclusive that NTRC is important for long-term re-modeling of cellular processes, that are not restricted to the chloroplast and control parts of the translational apparatus. Furthermore, the experiments highlight the known roles of TRX f1 and NTRC in the regulation of the CBC under control conditions and during transitions between darkness and light, and in the process, they have uncovered a possible in vivo role for TRXs m1 and m2 in regulating the CBC and photosynthesis under low light. In summary, the presented findings suggest that, despite the very short-lived mechanism of redox reactions, there is a long-term effect that enables the plant to adapt to changing light intensities, especially with the help of NTRC, to optimize photosynthesis and growth.
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Dziubek, Dejan
2022
Englisch
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Dziubek, Dejan (2022): The role of thioredoxins in acclimation to light. Dissertation, LMU München: Fakultät für Biologie
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Abstract

The photosynthetic conversion of light energy into chemical energy represents one of the most important processes on our planet. Changing light conditions lead to uneven stress on the photosystems in plants and influence all subsequent processes in the chloroplasts. Sessile land plants are able to adapt to these changes. The protein family of thioredoxins (TRXs) plays an important role in these processes. Thioredoxins are plastid oxidoreductases that mediate energy in the form of electrons between plastidial light and carbon reactions. Oxidized TRXs are reduced on a cascade via photosystem I (PSI), ferredoxin (Fd) and eventually by ferredoxin-thioredoxin reductase (FTR), and therefore grouped together as the FTR system. In addition, there is the ferredoxin-NADPH-dependent system (FNR), whose representative is NAPDH-dependent thioredoxin C (NTRC), which combines an NADPH sensitive domain and a TRX. Studies suggest that these two systems interact to modulate their activity. The activity of these redox modulators is characterized by thiol modification of cysteines. This very fast modulation in the seconds to minutes range is crucial for the stability and function of target proteins. Known roles of TRX include, first and foremost, light-dependent reduction, and thus activation of Calvin-Benson cycle (CBC) enzymes after prolonged darkness, maintenance of redox homeostasis and the antioxidant system, and plastid gene expression. Since little is known about the role of the FTR and FNR systems in regulating longer-term responses to changing light conditions, the present work has now used high-throughput methods and the reverse genetics approach to investigate the influence of the TRXs f1, m1, m2, and NTRC on photosynthesis, central metabolism, the CBC and on the proteome once different light energy and exposure times are available to the plant. Here it was shown that the cell response, at the level of photosynthesis and metabolism, to short-term changes between moderate and higher light in the range of minutes to hours depends rather little on the TRX/NTRC system. For more rapid changes between low and high light on the order of minutes, photosynthetic adaptation in ntrc mutants originating from control conditions is blocked, while wild type plants were increasingly able to acclimatize to this condition over days. This suggests an important role for NTRC in adaptation to rapidly changing, so-called fluctuating light, which is closest to natural conditions. Further, longer-term acclimation to high light, low light, and fluctuating light, in the range of days with higher average light intensity, showed mostly overlap between wild type and the TRX mutants, with most changes visible in high light. In the wild type, central metabolism, CBC, and stress response proteins were boosted here, whereas translational processes were down-regulated. Disruption of NTRC expression impaired the quantum efficiency of photosystem II as seen previously, especially in fluctuating light, but also in high light. By comparison with all other conditions, it was noticeable that the ntrc mutant lacked any dynamic adaptation and stimulation at the level of metabolism and proteome, especially in high light. It seems conclusive that NTRC is important for long-term re-modeling of cellular processes, that are not restricted to the chloroplast and control parts of the translational apparatus. Furthermore, the experiments highlight the known roles of TRX f1 and NTRC in the regulation of the CBC under control conditions and during transitions between darkness and light, and in the process, they have uncovered a possible in vivo role for TRXs m1 and m2 in regulating the CBC and photosynthesis under low light. In summary, the presented findings suggest that, despite the very short-lived mechanism of redox reactions, there is a long-term effect that enables the plant to adapt to changing light intensities, especially with the help of NTRC, to optimize photosynthesis and growth.