Changes in Respiratory Mitochondrial Machinery and Cytochrome and Alternative Pathway Activities in Response to Energy Demand Underlie the Acclimation of Respiration to Elevated CO₂ in the Invasive Opuntia ficus-indica

Abstract

Studies on long-term effects of plants grown at elevated CO 2 are scarce and mechanisms of such responses are largely unknown. To gain mechanistic understanding on respiratory acclimation to elevated CO 2 , the Crassulacean acid metabolism Mediterranean invasive Opuntia ficus-indica Miller was grown at various CO 2 concentrations. Respiration rates, maximum activity of cytochrome c oxidase, and active mitochondrial number consistently decreased in plants grown at elevated CO 2 during the 9 months of the study when compared to ambient plants. Plant growth at elevated CO 2 also reduced cytochrome pathway activity, but increased the activity of the alternative pathway. Despite all these effects seen in plants grown at high CO 2 , the specific oxygen uptake rate per unit of active mitochondria was the same for plants grown at ambient and elevated CO 2 . Although decreases in photorespiration activity have been pointed out as a factor contributing to the long-term acclimation of plant respiration to growth at elevated CO 2 , the homeostatic maintenance of specific respiratory rate per unit of mitochondria in response to high CO 2 suggests that photorespiratory activity may play a small role on the long-term acclimation of respiration to elevated CO 2 . However, despite growth enhancement and as a result of the inhibition in cytochrome pathway activity by elevated CO 2 , total mitochondrial ATP production was decreased by plant growth at elevated CO 2 when compared to ambient-grown plants. Because plant growth at elevated CO 2 increased biomass but reduced respiratory machinery, activity, and ATP yields while maintaining O 2 consumption rates per unit of mitochondria, we suggest that acclimation to elevated CO 2 results from physiological adjustment of respiration to tissue ATP demand, which may not be entirely driven by nitrogen metabolism as previously suggested.

Leaf‐ and cell‐level carbon cycling responses to a nitrogen and phosphorus gradient in two Arctic tundra species

“…The fi ne-structure organization of these cells appears to be dynamic and adaptable in both species. Instead of simply increasing the number of mitochondria and chloroplasts as reported in other species grown under elevated CO 2 Griffi n et al, 2001 ;Wang et al, 2004 ;Gomez-Casanovas et al, 2007 ), both the size and number of these organelles appear to shift to adapt to the new energy demand. In B. nana , this resulted in decoupled increases in organelle total volume that favored chloroplast growth over mitochondrial growth under the highest N and P availability (500% and 27%, respectively), whereas the opposite was the case in E. vaginatum (35% and 267%).…”

“…Mitochondria and chloroplasts mediate autotrophic carbon fl uxes, and changes in their respective densities (based on direct counts using transmission electron microscopy) can indicate underlying adaptations, as evidenced in responses to elevated CO 2 Griffi n et al, 2001 ;Tissue et al, 2002 ;Wang et al, 2004 ;Gomez-Casanovas et al, 2007 ), canopy position ( Tissue et al, 2002 ), and temperature ( Armstrong et al, 2006a , b ). Direct count measurements of mitochondria are rare and rarer still for fi eldgrown species.…”

Conditional modulation of NAD levels and metabolite profiles in Nicotiana sylvestris by mitochondrial electron transport and carbon/nitrogen supply

“…High CO 2 could also promote mitochondrial ATP production in the WT, for example by favoring increased respiration or partitioning to the COX pathway when photorespiration is inhibited (Igamberdiev et al 1997). It should be noted, however, that elevated CO 2 does not necessarily increase respiration rates and can even inhibit them, as well as cause increased partitioning to the AOX pathway (Bruhn et al 2007;Gomez-Casanovas et al 2007 and work cited therein).…”

Alternative oxidase and plant stress tolerance

“…12 In wheat, for instance, drought stress was associated with an increased conversion of AOX protein from its inactive (oxidized) to active (reduced) form 13 Once in reduced active form second regulatory mechanism comes into action wherein the a-keto acids especially pyruvate come into play. 14,15 The exact mechanism on how pyruvate control AOX has not been elucidated yet. Two conserved cysteine (Cys I and Cys II ) are present in AOX and interactions with these residues have been found to modulate the enzyme activity.…”