Improved photosynthetic performance during severe drought in Nicotiana tabacum overexpressing a nonenergy conserving respiratory electron sink

Abstract

SummaryChloroplasts have means to manage excess reducing power but these mechanisms may become restricted by rates of ATP turnover. Alternative oxidase (AOX) is a mitochondrial terminal oxidase that uncouples the consumption of reducing power from ATP synthesis.Physiological and biochemical analyses were used to compare respiration and photosynthesis of Nicotiana tabacum wild-type (WT) plants with that of transgenic lines overexpressing AOX, under both well-watered and drought stress conditions.With increasing drought severity, AOX overexpression acted to increase respiration in the light (R L ) relative to WT. CO 2 and light response curves indicated that overexpression also improved photosynthetic performance relative to WT, as drought severity increased. This was not due to an effect of AOX amount on leaf water status or the development of the diffusive limitations that occur due to drought. Rather, AOX overexpression dampened photosystem stoichiometry adjustments and losses of key photosynthetic components that occurred in WT.The results indicate that AOX amount influences R L , particularly during severe drought, when cytochrome pathway respiration may become increasingly restricted. This impacts the chloroplast redox state, influencing how the photosynthetic apparatus responds to increasing drought severity. In particular, the development of biochemical limitations to photosynthesis are dampened in plants with increased nonenergy conserving R L .

Coordinated regulation of photosynthetic and respiratory components is necessary to maintain chloroplast energy balance in varied growth conditions

“…S2A–D). This corresponds with our previous work at 150 PPFD (Dahal et al , 2014, 2015). A similar pattern across plant lines was also evident in the 400 PPFD- and 700 PPFD-grown plants experiencing low RWC’s and measured at saturating irradiance (Supplementary Fig.…”

“…However, in AOX knockdown plants a lower stress severity threshold (RWC of about 75–80%) already induced this limitation, while in AOX overexpression plants a much higher stress threshold (RWC below about 55%) was necessary to induce this limitation. These results are consistent with a model whereby the non-energy-conserving nature of AOX respiration can act to alleviate chloroplast energy imbalances, hence increasing the threshold level of drought stress necessary to induce the biochemical limitations of photosynthesis (Dahal et al , 2014, 2015; Dahal and Vanlerberghe, 2017). …”

“…We previously established that tobacco AOX is critical to maintain respiration and photosynthesis during drought (Dahal et al , 2014, 2015). These previous studies were done at a low growth irradiance of 150 PPFD.…”

Triose phosphate use limitation of photosynthesis: short-term and long-term effects

“…Lines with reduced AOX also showed obvious TPU and at a lower capacity than WT. The AOX appeared to help tobacco tolerate water stress (Dahal et al 2015). Without the AOX, presumably to help dissipate energy when photosynthetic electron transport was in excess, TPU limitation was induced.…”

Analysis of Posttranslational Activation of Alternative Oxidase Isoforms

“…Studies in Arabidopsis and tobacco (Nicotiana tabacum) clearly revealed a role for AOX in the dissipation of excessive reducing power while maintaining photosynthesis under high-light stress (Florez-Sarasa et al, 2011Dahal et al, 2014Dahal et al, , 2015Vanlerberghe et al, 2016). In Arabidopsis, aox1a knockout plants cannot be complemented by the expression of other isogenes (Strodtkötter et al, 2009;Kühn et al, 2015).…”