Involvement of Arabidopsis glutaredoxin S14 in the maintenance of chlorophyll content

Abstract

Plant class-II glutaredoxins (GRXs) are oxidoreductases carrying a CGFS active site signature and are able to bind iron-sulfur clusters in vitro. In order to explore the physiological functions of the 2 plastidial class-II isoforms, GRXS14 and GRXS16, we generated knockdown and overexpression Arabidopsis thaliana lines and characterized their phenotypes using physiological and biochemical approaches. Plants deficient in one GRX did not display any growth defect, whereas the growth of plants lacking both was slowed. Plants overexpressing GRXS14 exhibited reduced chlorophyll content in control, high-light, and high-salt conditions. However, when exposed to prolonged darkness, plants lacking GRXS14 showed accelerated chlorophyll loss compared to wild-type and overexpression lines. We observed that the GRXS14 abundance and the proportion of reduced form were modified in wild type upon darkness and high salt. The dark treatment also resulted in decreased abundance of proteins involved in the maturation of iron-sulfur proteins. We propose that the phenotype of GRXS14-modified lines results from its participation in the control of chlorophyll content in relation with light and osmotic conditions, possibly through a dual action in regulating the redox status of biosynthetic enzymes and contributing to the biogenesis of iron-sulfur clusters, which are essential cofactors in chlorophyll metabolism.

Assembly and Transfer of Iron–Sulfur Clusters in the Plastid

“…In Arabidopsis, GRXS14 and GRXS16 have a similar expression profile: both are expressed in green photosynthetic tissues and flowers (Rey et al, 2017 ). Consistent with the expression profile, GRXS14 knockout lines and GRXS16 knockdown lines did not exhibit any phenotypic defects under standard growth conditions (Rey et al, 2017 ). However, the combination of GRXS14 knockout and GRXS16 knockdown resulted in retarded growth, suggesting that GRXS14 and GRXS16 have an overlapping role in the plastid.…”

“…Environmental constraints, such as oxidative stress, prolonged darkness, high irradiance, and high salt, change cellular redox status (Rey et al, 2017 ). Under oxidative stress, GRXS14 knockout lines displayed growth defects in early seedlings (Cheng et al, 2006 ).…”

“…Under oxidative stress, GRXS14 knockout lines displayed growth defects in early seedlings (Cheng et al, 2006 ). Prolonged darkness causes GRXS14 oxidation and reduced contents of proteins involved in maturation of Fe-S proteins (Rey et al, 2017 ). Under prolonged darkness, GRXS14 knockout lines exhibited accelerated chlorophyll loss.…”

Chloroplasts Require Glutathione Reductase to Balance Reactive Oxygen Species and Maintain Efficient Photosynthesis

“…This includes glutaredoxins (Grx) and dehydroascorbate reductase (DHAR). While the involvement of plastid Grxs in iron-sulfur cluster coordination and protein (de)glutathionylation has been shown (Zaffagnini et al, 2012;Moseler et al, 2015;Rey et al, 2017;Zannini et al, 2019), only very few target proteins are currently known. Thus, the future challenge is to identify specific target cysteines affected by a shifting E GSH in order to appraise its potential physiological role in redox regulation and signalling.…”

Branched-chain amino acid catabolism depends on GRXS15 through mitochondrial lipoyl cofactor homeostasis

“…While autonomous pathways for the multistep Fe-S protein maturation process are present in plastids and mitochondria, the cytosolic machinery relies on the export of bound sulfide as a precursor from mitochondria (Schaedler et al, 2014). While plants deficient in plastidic GRXS14 did not display any growth phenotype under non-stress conditions, genetic stacking of a grxs14 null mutant and knockdown of GRXS16 caused pronounced growth retardation (Rey et al, 2017). Exposure of grxs14 and the double mutant to prolonged darkness led to accelerated chlorophyll loss compared to wild type (WT) and decreased abundance of proteins involved in the maturation of Fe-S proteins.…”