Dissecting the interaction of photosynthetic electron transfer with mitochondrial signalling and hypoxic response in the Arabidopsis rcd1 mutant

Abstract

The Arabidopsis mutant rcd1 is tolerant to methyl viologen (MV). MV enhances the Mehler reaction, i.e. electron transfer from Photosystem I (PSI) to O 2 , generating reactive oxygen species (ROS) in the chloroplast. To study the MV tolerance of rcd1 , we first addressed chloroplast thiol redox enzymes potentially implicated in ROS scavenging. NADPH-thioredoxin oxidoreductase type C (NTRC) was more reduced in rcd1 . NTRC contributed to the photosynthetic and metabolic phenotypes of rcd1 , but did not determine its MV tolerance. We next tested rcd1 for alterations in the Mehler reaction. In rcd1 , but not in the wild type, the PSI-to-MV electron transfer was abolished by hypoxic atmosphere. A characteristic feature of rcd1 is constitutive expression of mitochondrial dysfunction stimulon (MDS) genes that affect mitochondrial respiration. Similarly to rcd1 , in other MDS-overexpressing plants hypoxia also inhibited the PSI-to-MV electron transfer. One possible explanation is that the MDS gene products may affect the Mehler reaction by altering the availability of O 2 . In green tissues, this putative effect is masked by photosynthetic O 2 evolution. However, O 2 evolution was rapidly suppressed in MV-treated plants. Transcriptomic meta-analysis indicated that MDS gene expression is linked to hypoxic response not only under MV, but also in standard growth conditions. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

Recording true oxygen reduction capacity during photosynthetic electron transfer in Arabidopsis thylakoids and intact leaves

“…The accumulation of ATP that would otherwise be used in the CBB cycle limits the supply of phosphate for further ATP production. The subsequent impairment of ATP-synthase results in the accumulation of a strong proton gradient across the thylakoid membrane, which impairs O 2 production and likely results in a counterintuitively reduced PQ pool as previously described (Shapiguzov, Nikkanen et al 2020). The illuminated rate of O 2 consumption in MV treated leaf discs was approximately twofold the rate of O 2 production, suggesting the accumulation of H 2 O 2 (Fig.…”

Reductive stress triggers ANAC017-mediated retrograde signaling to safeguard the endoplasmic reticulum by boosting mitochondrial respiratory capacity

“…AOX1a has been extensively studied as a core stress response gene in Arabidopsis, emphasizing the general need for avoiding metabolic over-reduction under a variety of stress conditions ( Escobar et al, 2006 ; Giraud et al, 2008 ; Smith et al, 2009 ). AOX1a expression responds strongly to mETC inhibition and is a core component of the mitochondrial dysfunction stimulon (MDS; also named mitochondrial dysfunction regulon ; Vanderauwera et al, 2012 ; De Clercq et al, 2013 ; Shapiguzov et al, 2020 ), based on which it has been used as a model to study mitochondrial retrograde regulation (MRR). Several other MDS members have been identified through a genetic screen based on the response of AOX1a to the complex III inhibitor antimycin A (AA) ( Giraud et al, 2009 ; Van Aken et al, 2013 ; Ng et al, 2013a , 2013b ).…”

Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

“…It can, therefore, be assumed that such interaction developed also in the context of retrograde signalling. Recent results have provided the first evidence that retrograde signals from chloroplasts and mitochondria indeed act in a coordinated or mutual manner for reciprocal regulation of status or gene expression [101][102][103]. In the light of these new results, it should be remembered that mitochondrial and plastid gene expression systems are both under initial control of nuclear-encoded phage-type RNA polymerases that trigger all primary gene expression events in both organelles [104].…”

“…Recently, the Arabidopsis radical-induced cell death 1 (RCD1) protein was shown to bind ANAC017 and ANAC013 transcription factors and is thought to keep them in an inactive state, thereby repressing MRR responses [154]. In this issue, Shapiguzov et al [103] further explore how plants respond to methyl viologen, and show that hypoxia can reduce electron transfer from PSI to oxygen (the Mehler reaction) specifically in rcd1 mutants, but not in WT plants. As rcd1 plants show a constitutively high level of ANAC017 target genes, the authors could confirm that the effect of hypoxia on the Mehler reaction could be mimicked by the preincubation of WT plants with antimycin A (AA) or by overexpression of ANAC013, which both switch on the MRR pathway.…”