More recently, it has been reported that NTRC is required for efficient light
energy utilization. Under growth light conditions, the ntrc mutant displays high
levels of energy dissipation by non-photochemical quenching (NPQ) with the
concomitant decrease of the photosynthetic performance (Thormählen et al. 2015;
Naranjo et al. 2016b; Carrillo et al. 2016). Plants lacking NTRC accumulate more
protons in the thylakoid lumen at low and moderate light intensities leading to the
synthesis of zeaxanthin and the activation of the rapid inducible and reversible
component of NPQ, namely the energy- or ΔpH-dependent quenching (qE) (Naranjo
et al. 2016b; Carrillo et al. 2016). The higher accumulation of protons in the absence
of NTRC has been attributed to a lower reduction of the ATP synthase (ATPase)
γ-subunit (Naranjo et al. 2016b; Carrillo et al. 2016), though other mechanisms may
be also involved. The lower photosynthetic performance of the ntrc mutant leads to a
state of permanent starvation for light energy, which may explain its retarded growth
phenotype, particularly under conditions of light limitation like short-day photoperiod. Blocking NPQ in the ntrc mutant background by the lack of the PS II subunit
S (PsbS), in the double mutant ntrc psbs, causes the partial recovery of the photosynthetic performance and growth (Naranjo et al. 2016b). Furthermore, since the
induction and recovery of qE are essential to cope with rapid changes in light
intensities, the growth of the ntrc mutant is even more compromised under fluctuating light conditions (Thormählen et al. 2017).
2.3 NADPH-Dependent Thioredoxin Reductase C Acts
Concertedly with Other Chloroplast Thioredoxins
The finding of the participation of NTRC in the redox regulation of biosynthetic
pathways previously known to be regulated by TRX raised the issue of the relationship of NTRC with the different TRX in chloroplasts (see Fig. 3). This issue has been
addressed in recent years by the analysis of Arabidopsis mutants combining the
deficiency of NTRC and TRX. The different mutants analyzed lacking NTRC and
f-type TRX (Thormählen et al. 2015; Ojeda et al. 2017) or NTRC and TRXx (Ojeda
et al. 2017) have in common a very severe growth inhibition phenotype, in agreement with the severe impairment of the efficiency of use of light energy and redox
regulation of CBC enzymes in these mutants. In line with these results, Arabidopsis
mutants combining the lack of NTRC and the deficiency of m-type TRX show as
well a severe growth retard and impairment of the redox regulation of enzymes of the
tetrapyrrole biosynthesis pathway (Da et al. 2017). Altogether, these results support
the notion of a concerted action of NTRC with other plastidial TRX, such as those of
types f, x, and m in chloroplast redox regulation. The finding that the double mutant
combining the deficiency of NTRC and the catalytic subunit of FTR is not viable
(Yoshida and Hisabori 2016b) lends further support to this notion.
An initial possibility to explain the concerted action of NTRC and TRX in
chloroplast redox regulation is that both systems share common targets, so that the
On the Elaborate Network of Thioredoxins in Higher Plants
237
energy utilization. Under growth light conditions, the ntrc mutant displays high
levels of energy dissipation by non-photochemical quenching (NPQ) with the
concomitant decrease of the photosynthetic performance (Thormählen et al. 2015;
Naranjo et al. 2016b; Carrillo et al. 2016). Plants lacking NTRC accumulate more
protons in the thylakoid lumen at low and moderate light intensities leading to the
synthesis of zeaxanthin and the activation of the rapid inducible and reversible
component of NPQ, namely the energy- or ΔpH-dependent quenching (qE) (Naranjo
et al. 2016b; Carrillo et al. 2016). The higher accumulation of protons in the absence
of NTRC has been attributed to a lower reduction of the ATP synthase (ATPase)
γ-subunit (Naranjo et al. 2016b; Carrillo et al. 2016), though other mechanisms may
be also involved. The lower photosynthetic performance of the ntrc mutant leads to a
state of permanent starvation for light energy, which may explain its retarded growth
phenotype, particularly under conditions of light limitation like short-day photoperiod. Blocking NPQ in the ntrc mutant background by the lack of the PS II subunit
S (PsbS), in the double mutant ntrc psbs, causes the partial recovery of the photosynthetic performance and growth (Naranjo et al. 2016b). Furthermore, since the
induction and recovery of qE are essential to cope with rapid changes in light
intensities, the growth of the ntrc mutant is even more compromised under fluctuating light conditions (Thormählen et al. 2017).
2.3 NADPH-Dependent Thioredoxin Reductase C Acts
Concertedly with Other Chloroplast Thioredoxins
The finding of the participation of NTRC in the redox regulation of biosynthetic
pathways previously known to be regulated by TRX raised the issue of the relationship of NTRC with the different TRX in chloroplasts (see Fig. 3). This issue has been
addressed in recent years by the analysis of Arabidopsis mutants combining the
deficiency of NTRC and TRX. The different mutants analyzed lacking NTRC and
f-type TRX (Thormählen et al. 2015; Ojeda et al. 2017) or NTRC and TRXx (Ojeda
et al. 2017) have in common a very severe growth inhibition phenotype, in agreement with the severe impairment of the efficiency of use of light energy and redox
regulation of CBC enzymes in these mutants. In line with these results, Arabidopsis
mutants combining the lack of NTRC and the deficiency of m-type TRX show as
well a severe growth retard and impairment of the redox regulation of enzymes of the
tetrapyrrole biosynthesis pathway (Da et al. 2017). Altogether, these results support
the notion of a concerted action of NTRC with other plastidial TRX, such as those of
types f, x, and m in chloroplast redox regulation. The finding that the double mutant
combining the deficiency of NTRC and the catalytic subunit of FTR is not viable
(Yoshida and Hisabori 2016b) lends further support to this notion.
An initial possibility to explain the concerted action of NTRC and TRX in
chloroplast redox regulation is that both systems share common targets, so that the
On the Elaborate Network of Thioredoxins in Higher Plants
237