The chloroplast NADPH thioredoxin reductase C, NTRC, controls non‐photochemical quenching of light energy and photosynthetic electron transport in <i>Arabidopsis</i>

Naranjo, Belén; Mignée, Clara; Krieger‐Liszkay, Anja; Hornero‐Méndez, Dámaso; Gallardo‐Guerrero, Lourdes; Cejudo, Francisco Javier; Lindahl, Marika

doi:10.1111/pce.12652

Cited by 100 publications

(137 citation statements)

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“…1, B and C). As reported previously Naranjo et al, 2016aNaranjo et al, , 2016b, the deficiency of NTRC causes more severe impairment on photosynthesis performance than the deficiency of type-f Trxs, as shown by the extensive NPQ at low light intensity, the lower photosynthetic ETR, and the rate of carbon fixation (Fig. 4) in the ntrc mutant.…”

Section: Discussion Ntrc Acts In Concert With Different Types Of Trxsmentioning

confidence: 56%

“…2, B and C) of FBPase suggest that the impairment of these redox regulatory systems affects photosynthesis performance. Previous reports have shown that the deficiency of NTRC, but not of Trxs f or Trx x, provokes enhanced nonphotochemical quenching (NPQ) at low light intensity (Naranjo et al, 2016a(Naranjo et al, , 2016b, hence causing a poor efficiency in the utilization of light energy by the ntrc mutant. Thus, as a first step to determine the effect of the combined deficiencies of NTRC and Trxs f or x on photosynthetic performance, we analyzed NPQ in the different lines under study.…”

Section: Resultsmentioning

confidence: 99%

“…4C). Previous reports have shown that the deficiency of NTRC causes the impairment of light utilization and slightly affects the redox state of the g-subunit of ATPase, hence affecting the qE component of NPQ (Carrillo et al, 2016;Naranjo et al, 2016b). Therefore, the combined deficiency of NTRC and f-or x-type Trxs affects the redox regulation of chloroplast metabolic pathways such as the CalvinBenson cycle but also the efficiency of light utilization, which ultimately might be the reason for the severe growth-retarded phenotype shown by the ntrc-trxx and ntrc-trxf1f2 mutants.…”

Section: Discussion Ntrc Acts In Concert With Different Types Of Trxsmentioning

confidence: 99%

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NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

et al. 2017

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ORCID IDs: 0000-0001-8141-9679 (M.G.); 0000-0002-9570-9746 (A.J.S.); 0000-0001-9512-349X (P.G.); 0000-0002-3936-5491 (F.J.C.).Thiol-dependent redox regulation of enzyme activity plays a central role in the rapid acclimation of chloroplast metabolism to ever-fluctuating light availability. This regulatory mechanism relies on ferredoxin reduced by the photosynthetic electron transport chain, which fuels reducing power to thioredoxins (Trxs) via a ferredoxin-dependent Trx reductase. In addition, chloroplasts harbor an NADPH-dependent Trx reductase, which has a joint Trx domain at the carboxyl terminus, termed NTRC. Thus, a relevant issue concerning chloroplast function is to establish the relationship between these two redox systems and its impact on plant development. To address this issue, we generated Arabidopsis (Arabidopsis thaliana) mutants combining the deficiency of NTRC with those of Trxs f, which participate in metabolic redox regulation, and that of Trx x, which has antioxidant function. The ntrc-trxf1f2 and, to a lower extent, ntrc-trxx mutants showed severe growth-retarded phenotypes, decreased photosynthesis performance, and almost abolished light-dependent reduction of fructose-1,6-bisphosphatase. Moreover, the combined deficiency of both redox systems provokes aberrant chloroplast ultrastructure. Remarkably, both the ntrc-trxf1f2 and ntrc-trxx mutants showed high mortality at the seedling stage, which was overcome by the addition of an exogenous carbon source. Based on these results, we propose that NTRC plays a pivotal role in chloroplast redox regulation, being necessary for the activity of diverse Trxs with unrelated functions. The interaction between the two thiol redox systems is indispensable to sustain photosynthesis performed by cotyledons chloroplasts, which is essential for early plant development.

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Section: Discussion Ntrc Acts In Concert With Different Types Of Trxsmentioning

confidence: 56%

Section: Resultsmentioning

confidence: 99%

Section: Discussion Ntrc Acts In Concert With Different Types Of Trxsmentioning

confidence: 99%

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NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

et al. 2017

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“…Even though ASA and DTT have diverse physiological roles in plant tissues, they have respectively been used as NPQ promoters and NPQ inhibitors to investigate the role of NPQ in plants, as they obviously contribute to changes in NPQ (Bilger and Björkman, 1990; Neubauer, 1993; Mohanty and Yamamoto, 1996; Xu et al, 1999; Ivanov and Edwards, 2000; Yin et al, 2010; Roháček et al, 2014; Naranjo et al, 2015; Quaas et al, 2015). The leaves of the rice plants grown under 600 μmol m −2 s −1 were sprayed with 10 mM DTT in 0.005% (v/v) Tween-80 (DTT treatment), 15 mM ASA in 0.005% (v/v) Tween-80 (ASA treatment), and 0.005% (v/v) Tween-80 in water (control treatment).…”

Section: Methodsmentioning

confidence: 99%

Non-photochemical Quenching Plays a Key Role in Light Acclimation of Rice Plants Differing in Leaf Color

et al. 2017

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Non-photochemical quenching (NPQ) is an important photoprotective mechanism in rice; however, little is known regarding its role in the photosynthetic response of rice plants with differing in leaf color to different irradiances. In this study, two rice genotypes containing different chlorophyll contents, namely Zhefu802 (high chlorophyll) and Chl-8 (low chlorophyll), were subjected to moderate or high levels of light intensity at the 6-leaf stage. Chl-8 possessed a lower chlorophyll content and higher chlorophyll a:b ratio compared with Zhefu802, while Pn, Fv/Fm, and ΦPSII contents were higher in Chl-8. Further results indicated that no significant differences were observed in the activities of Rubisco, Mg2+-ATPase, and Ca2+-ATPase between these genotypes. This suggested that no significant difference in the capacity for CO2 assimilation exists between Zhe802 and Chl-8. Additionally, no significant differences in stomatal limitation were observed between the genotypes. Interestingly, higher NPQ and energy quenching (qE), as well as lower photoinhibitory quenching (qI) and production of reactive oxygen species (ROS) was observed in Chl-8 compared with Zhefu802 under both moderate and high light treatments. This indicated that NPQ could improve photosynthesis in rice under both moderate and high light intensities, particularly the latter, whereby NPQ alleviates photodamage by reducing ROS production. Both zeaxanthin content and the expression of PsbS1 were associated with the induction of NPQ under moderate light, while only zeaxanthin was associated with NPQ induction under high light. In summary, NPQ could improve photosynthesis in rice under moderate light and alleviate photodamage under high light via a decrease in ROS generation.

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“…Only a few targets were shown to be controlled by NTRC. NTRC functions in the abiotic oxidative stress response (Serrato et al, 2004), starch synthesis (Michalska et al, 2009), Chl synthesis Pérez-Ruiz et al, 2014), the Calvin-Benson cycle (Thormählen et al, 2015), lateral root formation in Arabidopsis (Kirchsteiger et al, 2012), nonphotochemical quenching (Naranjo et al, 2016), as a holdase chaperone function enhancing thermotolerance to Arabidopsis (Chae et al, 2013), and as an electron donor of 2-Cys-peroxiredoxin, thus playing a key role in the detoxification of reactive oxygen species (ROS; Pérez-Ruiz et al, 2006;Spínola et al, 2008;Kirchsteiger et al, 2009). Recent research suggested that cooperative control of chloroplast functions via the ferredoxin-thioredoxin reductase (FTR)/TRX and NTRC pathways is essential for plant viability.…”

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confidence: 99%

Thioredoxin and NADPH-Dependent Thioredoxin Reductase C Regulation of Tetrapyrrole Biosynthesis

Wang

et al. 2017

Plant Physiol.

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In chloroplasts, thioredoxin (TRX) isoforms and NADPH-dependent thioredoxin reductase C (NTRC) act as redox regulatory factors involved in multiple plastid biogenesis and metabolic processes. To date, less is known about the functional coordination between TRXs and NTRC in chlorophyll biosynthesis. In this study, we aimed to explore the potential functions of TRX m and NTRC in the regulation of the tetrapyrrole biosynthesis (TBS) pathway. Silencing of three genes, TRX m1, TRX m2, and TRX m4 (TRX ms), led to pale-green leaves, a significantly reduced 5-aminolevulinic acid (ALA)-synthesizing capacity, and reduced accumulation of chlorophyll and its metabolic intermediates in Arabidopsis (Arabidopsis thaliana). The contents of ALA dehydratase, protoporphyrinogen IX oxidase, the I subunit of Mg-chelatase, Mg-protoporphyrin IX methyltransferase (CHLM), and NADPH-protochlorophyllide oxidoreductase were decreased in triple TRX m-silenced seedlings compared with the wild type, although the transcript levels of the corresponding genes were not altered significantly. Protein-protein interaction analyses revealed a physical interaction between the TRX m isoforms and CHLM. 4-Acetoamido-4-maleimidylstilbene-2,2-disulfonate labeling showed the regulatory impact of TRX ms on the CHLM redox status. Since CHLM also is regulated by NTRC , we assessed the concurrent functions of TRX m and NTRC in the control of CHLM. Combined deficiencies of three TRX m isoforms and NTRC led to a cumulative decrease in leaf pigmentation, TBS intermediate contents, ALA synthesis rate, and CHLM activity. We discuss the coordinated roles of TRX m and NTRC in the redox control of CHLM stability with its corollary activity in the TBS pathway.

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The chloroplast NADPH thioredoxin reductase C, NTRC, controls non‐photochemical quenching of light energy and photosynthetic electron transport in Arabidopsis

Cited by 100 publications

References 82 publications

NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

NADPH Thioredoxin Reductase C and Thioredoxins Act Concertedly in Seedling Development

Non-photochemical Quenching Plays a Key Role in Light Acclimation of Rice Plants Differing in Leaf Color

Thioredoxin and NADPH-Dependent Thioredoxin Reductase C Regulation of Tetrapyrrole Biosynthesis

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