The flexibility of metabolic interactions between chloroplasts and mitochondria in Nicotiana tabacum leaf

Abstract

To examine the effect of mitochondrial function on photosynthesis, wild-type and transgenic Nicotiana tabacum with varying amounts of alternative oxidase (AOX) were treated with different respiratory inhibitors. Initially, each inhibitor increased the reduction state of the chloroplast electron transport chain, most severely in AOX knockdowns and least severely in AOX overexpressors. This indicated that the mitochondrion was a necessary sink for photo-generated reductant, contributing to the 'P700 oxidation capacity' of photosystem I. Initially, the Complex III inhibitor myxothiazol and the mitochondrial ATP synthase inhibitor oligomycin caused an increase in photosystem II regulated non-photochemical quenching not evident with the Complex III inhibitor antimycin A (AA). This indicated that the increased quenching depended upon AAsensitive cyclic electron transport (CET). Following 12 h with oligomycin, the reduction state of the chloroplast electron transport chain recovered in all plant lines. Recovery was associated with large increases in the protein amount of chloroplast ATP synthase and mitochondrial uncoupling protein. This increased the capacity for photophosphorylation in the absence of oxidative phosphorylation and enabled the mitochondrion to act again as a sink for photo-generated reductant. Comparing the AA and myxothiazol treatments at 12 h showed that CET optimized photosystem I quantum yield, depending upon the P700 oxidation capacity. When this capacity was too high, CET drew electrons away from other sinks, moderating the P700 + amount. When P700 oxidation capacity was too low, CET acted as an electron overflow, moderating the amount of reduced P700. This study reveals flexible chloroplast-mitochondrion interactions able to overcome lesions in energy metabolism.

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

“…A key role of respiratory flexibility as mediated by UCP1 has been attributed to photorespiratory metabolism, but also drought and salt stress responses ( Sweetlove et al, 2006 ; Begcy et al, 2011 ; recently reviewed by Barreto et al, 2020 ). Loss of AOX1a has been reported to increase susceptibility of leaves to combined drought and light stress and other conditions challenging the energy and/or carbon balance in the photosynthetic cell, in agreement with a role in providing an electron sink to avoid photoinhibition ( Giraud et al, 2008 ; Smith et al, 2009 ; Kühn et al, 2015 ; Shapiguzov et al, 2019 ; Alber and Vanlerberghe, 2021 ) . 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 ).…”

“…The similarity of the root growth phenotype between aox1a and ucp1 seedlings in response to DTT ( Figure 3 ) provides correlative evidence for a degree of physiological redundancy between AOX1a and UCP1, even though their biochemical mechanisms are not related, and their regulation differs. Both AOX and UCP proteins can enhance the capacity of mitochondrial respiration to maintain cellular redox homeostasis and avoid metabolic over-reduction ( Barreto et al, 2020 ; Vanlerberghe et al, 2020 ; Alber and Vanlerberghe, 2021 ). Indications for in planta uncoupling function of UCP1 have been provided by impaired photorespiration in an Arabidopsis ucp1 mutant and enhanced drought and salt stress tolerance in Nicotiana tabacum UCP1 over-expressors ( Sweetlove et al, 2006 ; Begcy et al, 2011 ; Barreto et al, 2014 , 2017 ).…”

The Complementary Roles of Chloroplast Cyclic Electron Transport and Mitochondrial Alternative Oxidase to Ensure Photosynthetic Performance

“…Both modeling and experimental studies suggest that the mETC is a net sink for electrons derived from chloroplast metabolism in the light ( Krömer, 1995 ; Buckley and Adams, 2011 ; Cheung et al, 2015 ; Shameer et al, 2019 ; Yamada et al, 2020 ; Alber and Vanlerberghe, 2021 ). One abundant source of electrons is a carbon reaction in the photorespiration pathway.…”

“…Another interesting observation was that UCP1 overexpression in tobacco resulted in an increased abundance of transcripts encoding several major cETC components, but not mETC components ( Laitz et al, 2015 ). In another study, inhibition of mitochondrial oxidative phosphorylation in the light with oligomycin resulted in a strong induction of both UCP and cATP synthase that was then able to maintain cETC activity and cell viability ( Alber and Vanlerberghe, 2021 ). These studies suggest a connection between mitochondrial UCP’s and photosynthesis that deserves further study.…”

Alternative oxidase1a and 1d limit proline-dependent oxidative stress and aid salinity recovery in Arabidopsis

“…The benefit of increased AOX capacity towards photosynthesis therefore coincides with this period of rapid Pro metabolism. In actively photosynthesizing cells, AOX is thought to optimize photosynthetic rates by better allowing the mETC to safely oxidize excess reductant exported by the plastid (Dahal et al, 2015, Del-Saz et al, 2018, Alber and Vanlerberghe, 2021. Vishwakarma et al (2014) first observed higher NADH/NAD + and NADPH/NADP + ratios in high light treated aox1a Arabidopsis plants.…”