Abstract
The non-energy-conserving alternative oxidase (AOX) respiration of plant mitochondria is known to interact with chloroplast photosynthesis. This may have consequences for growth, particularly under sub-optimal conditions when energy imbalances can impede photosynthesis. This hypothesis was tested by comparing the metabolism and growth of wild-type Nicotiana tabacum with that of AOX knockdown and overexpression lines during a prolonged steady-state mild to moderate water deficit. Under moderate water deficit, the AOX amount was an important determinant of the rate of both mitochondrial respiration in the light and net photosynthetic CO2 assimilation (A) at the growth irradiance. In particular, AOX respiration was necessary to maintain optimal proton and electron fluxes at the chloroplast thylakoid membrane, which in turn prevented a water-deficit-induced biochemical limitation of photosynthesis. As a result of differences in A, AOX overexpressors gained more biomass and knockdowns gained less biomass than wild-type during moderate water deficit. Biomass partitioning also differed, with the overexpressors having a higher percentage, and the knockdowns having a lower percentage, of total above-ground biomass in reproductive tissue than wild-type. The results establish that improving chloroplast energy balance by using a non-energy-conserving respiratory electron sink can increase photosynthesis and growth during prolonged water deficit.
Highlights
Photosynthesis and respiration represent the core of carbon and energy metabolism, and are key determinants of growth (Stitt et al, 2010; Millar et al, 2011)
In response to a rapid onset of water deficit stress, the severity of which increased continually over time, the alternative oxidase (AOX) amount in Nicotiana tabacum leaf was a strong determinant of the rate of respiration in the light (RL) (Dahal et al, 2014; Dahal and Vanlerberghe, 2017)
We show that AOX respiration improves net CO2 assimilation rate (A) by promoting energy balance in the chloroplast, in particular by staving off changes in the thylakoid proton circuit that otherwise culminate in a biochemical limitation of photosynthesis
Summary
Photosynthesis and respiration represent the core of carbon and energy metabolism, and are key determinants of growth (Stitt et al, 2010; Millar et al, 2011). These metabolic systems may experience energy imbalances, such as a mismatch between supply and demand for ATP and/. The absorption of light energy by chloroplast thylakoid pigments drives the generation of ATP and NADPH, which. Reduced availability of CO2 during water deficit, due to stomatal closure, reduces the consumption of ATP and NADPH being generated by the thylakoid reactions (Lawlor, 2002; Flexas et al, 2004)
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