Mitochondrial Alternative Oxidase Maintains Respiration and Preserves Photosynthetic Capacity during Moderate Drought in Nicotiana tabacum    

Abstract

The mitochondrial electron transport chain includes an alternative oxidase (AOX) that is hypothesized to aid photosynthetic metabolism, perhaps by acting as an additional electron sink for photogenerated reductant or by dampening the generation of reactive oxygen species. Gas exchange, chlorophyll fluorescence, photosystem I (PSI) absorbance, and biochemical and protein analyses were used to compare respiration and photosynthesis of Nicotiana tabacum 'Petit Havana SR1' wild-type plants with that of transgenic AOX knockdown (RNA interference) and overexpression lines, under both well-watered and moderate droughtstressed conditions. During drought, AOX knockdown lines displayed a lower rate of respiration in the light than the wild type, as confirmed by two independent methods. Furthermore, CO 2 and light response curves indicated a nonstomatal limitation of photosynthesis in the knockdowns during drought, relative to the wild type. Also relative to the wild type, the knockdowns under drought maintained PSI and PSII in a more reduced redox state, showed greater regulated nonphotochemical energy quenching by PSII, and displayed a higher relative rate of cyclic electron transport around PSI. The origin of these differences may lie in the chloroplast ATP synthase amount, which declined dramatically in the knockdowns in response to drought. None of these effects were seen in plants overexpressing AOX. The results show that AOX is necessary to maintain mitochondrial respiration during moderate drought. In its absence, respiration rate slows and the lack of this electron sink feeds back on the photosynthetic apparatus, resulting in a loss of chloroplast ATP synthase that then limits photosynthetic capacity.

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

“…The amount of ATP synthase will have an effect on the propensity for TPU. Water stress has been shown to reduce ATP synthase protein amount and to induce TPU (Tezara et al 1999;Kohzuma et al 2009;Dahal et al 2014). Thus, it appears when leaves experience low CO 2 , for example as a result of water stress, the capacity for TPU is rapidly reduced both by reducing starch and sucrose synthesis and reducing ATP synthase, leaving TPU capacity only slightly greater than likely to be needed.…”

“…TPU is at the interface between growth and physiology of the plant and the production of resources needed for growth. Dahal et al (2014) found that tobacco plants lacking alternative oxidase showed no propensity for TPU until water-stressed. Unstressed plants had identical responses of A to C i but after water stress a line overexpressing alternative oxidase showed no TPU limitation while WT exhibited a clear TPU limitation.…”

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).…”

Mitochondrial and Chloroplast Stress Responses Are Modulated in Distinct Touch and Chemical Inhibition Phases

“…For example, the glycosyltransferase UGT74E2 targets auxins and upon overexpression triggers profuse shoot branching and drought tolerance (Tognetti et al, 2010). Also, the classical mitochondrial stress marker gene alternative oxidase AOX1a was found to be important during osmotic stress (Dojcinovic et al, 2005;Dahal et al, 2014), and recently it was shown that the mitochondrial outer membrane ATPase AtOM66 (AtBCS1) is a regulator of cell death that controls pathogen resistance, senescence, and drought tolerance . Therefore, it is evident that energy organelle signaling is an important part of general stress responses, and understanding the way it is controlled could provide a means to enhance stress tolerance and, thus, productivity in crop species.…”