Abstract
Mitochondria have a non-energy-conserving alternative oxidase (AOX) proposed to support photosynthesis, perhaps by promoting energy balance under varying growth conditions. To investigate this, wild-type (WT) Nicotiana tabacum were compared with AOX knockdown and overexpression lines. In addition, the amount of AOX protein in WT plants was compared with that of chloroplast light-harvesting complex II (LHCB2), whose amount is known to respond to chloroplast energy status. With increased growth irradiance, WT leaves maintained higher rates of respiration in the light (RL), but no differences in RL or photosynthesis were seen between the WT and transgenic lines, suggesting that, under non-stress conditions, AOX was not critical for leaf metabolism, regardless of growth irradiance. However, under drought, the AOX amount became an important determinant of RL, which in turn was an important determinant of chloroplast energy balance (measured as photosystem II excitation pressure, EP), and photosynthetic performance. In the WT, the AOX amount increased and the LHCB2 amount decreased with increased growth irradiance or drought severity. These changes in protein amounts correlated strongly, in opposing ways, with growth EP. This suggests that a signal deriving from the photosynthetic electron transport chain status coordinately controls the amounts of AOX and LHCB2, which then both contribute to maintaining chloroplast energy balance, particularly under stress conditions.
Highlights
Respiration in the mitochondrion and photosynthesis in the chloroplast share important carbon and energy intermediates, and it is thought that these pathways must act in a coordinated manner to optimize energy metabolism in the leaf cell (Hoefnagel et al, 1998; Gardestrӧm et al., 2002; Noctor et al, 2007; Noguchi and Yoshida, 2008; Nunes-Nesi et al, 2008; Tcherkez et al, 2012; Gardestrӧm and Igamberdiev, 2016)
This comparison was done for plants grown at low, medium, and high irradiance since it has been observed in tobacco and other species that plants maintain higher amounts of alternative oxidase (AOX) protein at higher growth irradiance
Under optimal growth conditions, there were no differences in respiration rate (RD or respiration in the light (RL)) or photosynthetic performance across the tobacco lines differing in AOX amount, regardless of whether the plants were grown at low, medium, or high irradiance (Table 1)
Summary
Respiration in the mitochondrion and photosynthesis in the chloroplast share important carbon and energy intermediates, and it is thought that these pathways must act in a coordinated manner to optimize energy metabolism in the leaf cell (Hoefnagel et al, 1998; Gardestrӧm et al., 2002; Noctor et al, 2007; Noguchi and Yoshida, 2008; Nunes-Nesi et al, 2008; Tcherkez et al, 2012; Gardestrӧm and Igamberdiev, 2016). The availability of AOX knockdown/knockout plants, in the model species Arabidopsis thaliana, have greatly aided such work The majority of these more recent studies have used immediate and short-term (usually a few hours) increases in irradiance (high light stress) as a means to rapidly challenge chloroplast energy balance and evaluate the importance of AOX in correcting such imbalances (Zhang et al, 2010; Florez-Sarasa et al, 2011; Yoshida et al, 2011a, b; Vishwakarma et al, 2014; Watanabe et al, 2016). We show that differences in AOX protein amount across a wide range of growth conditions correlate strongly with differences in chloroplast energy balance, suggesting that the AOX respiration capacity of leaves is tightly linked to chloroplast metabolic status
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