Growth at Elevated CO₂ Requires Acclimation of the Respiratory Chain to Support Photosynthesis

Abstract

Plants will experience an elevated atmospheric concentration of CO (ECO) in the future. Growth of tobacco () at ECO more than doubled the leaf protein amount of alternative oxidase (AOX), a non-energy-conserving component of mitochondrial respiration. To test the functional significance of this AOX increase, wild-type tobacco was compared with AOX knockdown and overexpression lines, following growth at ambient CO or ECO The ECO-grown AOX knockdowns had a reduced capacity for triose phosphate use (TPU) during photosynthesis compared with the other plant lines. This TPU limitation of CO assimilation was associated with an increased accumulation of glucose-6-phosphate, sucrose, and starch in the leaves of the knockdowns. Under TPU-limiting conditions, the size of the proton gradient and proton motive force across the thylakoid membrane was enhanced in the knockdowns relative to the other plant lines, suggesting a restriction of chloroplast ATP synthase activity. This restriction was not due to a decline in ATP synthase (AtpB) protein amount. The knockdowns also displayed a photosystem stoichiometry adjustment at ECO, which was absent in the other plant lines. Additional experiments showed that the way in which AOX supports photosynthesis at ECO is distinct from its previously described role in supporting photosynthesis during water deficit. The results are discussed in terms of how AOX contributes to TPU capacity and the maintenance of chloroplast ATP synthase activity at ECO Overall, the evidence suggests that AOX respiration is needed to maintain both the carbon and energy balance in photosynthetic tissues during growth at ECO.

Signaling interactions between mitochondria and chloroplasts in Nicotiana tabacum leaf

“…AA, MYXO and OLIGO are respiratory inhibitors, each with a well‐established site of action in the mitochondrion (Soole and Menz ). However, it is also well established that photosynthetic metabolism in the chloroplast depends upon extensive interactions with respiratory metabolism in the mitochondrion (Hoefnagel et al , Raghavendra and Padmasree , Sweetlove et al , Tcherkez et al , Gandin et al , Gardeström and Igamberdiev , Dahal et al , Dahal and Vanlerberghe , ). In this case, one might expect that a disruption of mitochondrial function might also perturb chloroplast function, at least in the light, and hence potentially engage retrograde signals from both organelles.…”

“…This could confound the identification of mitochondrial retrograde signal(s) and signal transduction proteins. A related complication is that important metabolic interactions must occur between photosynthesis and respiration in the light (Hoefnagel et al , Raghavendra and Padmasree , Sweetlove et al , Tcherkez et al , Gandin et al , Gardeström and Igamberdiev , Dahal et al , Dahal and Vanlerberghe , ). Thus, disruption of mitochondrial function by inhibitors or mutants may indirectly alter energy metabolism in the chloroplast, resulting in the generation of additional chloroplast‐derived retrograde signals.…”

Improving Potato Stress Tolerance and Tuber Yield Under a Climate Change Scenario – A Current Overview

“…In a comprehensive review of several crop species, Ainsworth and Long (2005) reported that the predicted rise in atmospheric CO 2 concentrations will benefit most C 3 plants. Elevated CO 2 is expected to stimulate photosynthesis and enhance light use efficiency into biomass and crop yield as well as improve water use efficiency (WUE) through closing stomata and preventing transpirational water loss (Ainsworth and Rogers, 2007; Dahal et al, 2014b; Dahal and Vanlerberghe, 2018a). Short-term exposure of C 3 plants from ambient to elevated CO 2 immediately stimulate the rates of photosynthesis (Cheng et al, 1998; Long et al, 2004; Ainsworth and Rogers, 2007; Dahal et al, 2012).…”

Roles for Plant Mitochondrial Alternative Oxidase Under Normoxia, Hypoxia, and Reoxygenation Conditions

“…Plants were irrigated every other day and fertilized every 2 weeks with a 20-20-20 fertilizer containing 5.9% of nitrate nitrogen. The transgenic lines used in this study have been characterized earlier (Amirsadeghi et al, 2006;Wang et al, 2011;Wang and Vanlerberghe, 2013;Dahal and Vanlerberghe, 2018a). Amongst these, RI29 is the most effective knockdown (no detectable leaf AOX protein), while faint amounts of leaf AOX protein can still sometimes be detected in RI9.…”