Tomato Fruit Chromoplasts Behave as Respiratory Bioenergetic Organelles during Ripening

Abstract

During tomato (Solanum lycopersicum) fruit ripening, chloroplasts differentiate into photosynthetically inactive chromoplasts. It was recently reported that tomato chromoplasts can synthesize ATP through a respiratory process called chromorespiration. Here we show that chromoplast oxygen consumption is stimulated by the electron donors NADH and NADPH and is sensitive to octyl gallate (Ogal), a plastidial terminal oxidase inhibitor. The ATP synthesis rate of isolated chromoplasts was dependent on the supply of NAD(P)H and was fully inhibited by Ogal. It was also inhibited by the proton uncoupler carbonylcyanide m-chlorophenylhydrazone, suggesting the involvement of a chemiosmotic gradient. In addition, ATP synthesis was sensitive to 2,5-dibromo-3-methyl-6-isopropyl-p-benzoquinone, a cytochrome b 6 f complex inhibitor. The possible participation of this complex in chromorespiration was supported by the detection of one of its components (cytochrome f) in chromoplasts using immunoblot and immunocytochemical techniques. The observed increased expression of cytochrome c 6 during ripening suggests that it could act as electron acceptor of the cytochrome b 6 f complex in chromorespiration. The effects of Ogal on respiration and ATP levels were also studied in tissue samples. Oxygen uptake of mature green fruit and leaf tissues was not affected by Ogal, but was inhibited increasingly in fruit pericarp throughout ripening (up to 26% in red fruit). Similarly, Ogal caused a significant decrease in ATP content of red fruit pericarp. The number of energized mitochondria, as determined by confocal microscopy, strongly decreased in fruit tissue during ripening. Therefore, the contribution of chromoplasts to total fruit respiration appears to increase in late ripening stages.

The impact of photosynthesis on initiation of leaf senescence

“…In chromoplasts isolated from tomato ( Solanum lycopersicum cv. Micro‐Tom; Renato et al ), generation of a proton motif force by electron transport involving the NDH complex, PQ and PTOX has been shown to take place. The same is the case in etioplasts (Kambakam et al ).…”

High‐level expression of a novel chromoplast phosphate transporter ClPHT4;2 is required for flesh color development in watermelon

“…Tomato chromoplasts were recently observed to synthesize ATP through chromorespiration activites of respiratory bioenergetic organelles during fruit ripening (Pateraki et al, 2013;Renato et al, 2014). Wang et al (2013) also observed high metabolic activities and an abundance of transport-related proteins in watermelon chromoplasts.…”

Electron transport pathways in isolated chromoplasts from Narcissus pseudonarcissus L.

“…Chromoplasts from different species use either NADPH or NADH as the preferred electron donor. Addition of NADH resulted in higher respiratory activity in tomato chromoplasts than NADPH (Renato et al ., ), while the opposite was found with daffodil chromoplasts (Nievelstein et al ., ). Chromorespiration may be related to a similar process in chloroplasts, chlororespiration, first been described by Bennoun () as a light‐independent electron transport pathway from NAD(P)H to O 2 .…”

“…The tomato chromoplast proteome revealed the presence of NDH complex subunits and of the cytochrome b 6 f complex (Barsan et al ., ; Wang et al ., ), rendering these two likely components of the respiratory electron transport chain. Furthermore, it has been suggested that a type II NDH contributes to the reduction in the PQ pool (Renato et al ., ). The participation of the cyt b 6 f complex in chromorespiration is corroborated by the partial sensitivity of ATP synthesis to DBMIB, an inhibitor of the cyt b 6 f complex (Renato et al ., ).…”