Modulating the activities of chloroplasts and mitochondria promotes ATP production and plant growth

Abstract

Efficient photosynthesis requires a balance of ATP and NADPH production/consumption in chloroplasts as the linear electron flow generates a higher NADPH/ATP ratio than that is consumed by the Calvin-Benson-Bassham cycle. Recent works suggested that ATP importation into mature chloroplasts of Arabidopsis thaliana is negligible, and therefore the exportation of reducing equivalents from chloroplasts is important for balancing stromal ATP/NADPH ratio. Here we showed that the overexpression of purple acid phosphatase 2 on the outer membranes of chloroplasts and mitochondria can streamline the production and consumption of reducing equivalents in these two organelles, respectively. A higher capacity of consumption of reducing equivalents in mitochondria can indirectly help chloroplasts to balance the ATP/NADPH ratio in stroma and recycle NADP+, the electron acceptors of the linear electron flow. A higher rate of ATP and NADPH production from the linear electron flow, a higher capacity of carbon fixation by the Calvin-Benson-Bassham cycle and a greater consumption of NADH in mitochondria, enhance photosynthesis in the chloroplasts, ATP production in the mitochondria, sucrose synthesis in the cytosol, and eventually boosting plant growth and seed yields in the overexpression lines.One-Sentence SummaryThis study demonstrates the importance of chloroplast-mitochondria cooperation in redox balance and illustrates that an optimized function of mitochondria can enhance the efficiency of photosynthesis.

Overlapping Functions of the Paralogous Proteins AtPAP2 and AtPAP9 in Arabidopsis thaliana

“…Under long-day (16 h light at 22 °C/8 h dark at 18 °C) growth conditions, the OE lines of AtPAP9 did not display any growth promotion effect compared with wild-type Arabidopsis thaliana ecotype Columbia-0 (WT) and T-DNA lines ( Figure 2 A). Overall, the typical early-bolting and high-seed-yield phenotypes of the AtPAP2 OE line (OE7) were not observed in the OE lines of AtPAP9 ( Table 1 ) [ 8 , 19 ]. The electron transport rate (ETR) and non-photochemical quenching (NPQ) of the AtPAP9 OE and T-DNA lines were similar to the WT line, which correlated with their growth phenotypes ( Figure 2 C).…”

“…AtPAP2 interacts with the mature protein portion of a small subunit of rubisco (mSSU) and a number of chloroplast proteins, and plays a role in the import of pSSU into chloroplasts [ 11 , 19 ]. To compare the binding specificities of AtPAP2 and AtPAP9, yeast two-hybrid (Y2H) assay ( Figure 3 A) and bimolecular fluorescence complementation assay (BiFC) ( Figure 3 B) were carried out.…”

“…The overexpression of AtPAP2 on both organelles promotes the plant growth and seed yield of Arabidopsis thaliana by coordinating the physiology of chloroplasts and mitochondria simultaneously [ 8 , 18 ]. The chloroplasts of the AtPAP2 OE line exhibit a higher PSI/PSII ratio and ETR and fix more CO 2 , whereas the mitochondria of the AtPAP2 OE line can consume more reducing equivalents and generate more ATP compared with the WT line [ 19 ]. The higher consumption of reducing equivalents in the mitochondria can indirectly enhance the regeneration of stromal NADP + , electron acceptors of the linear electron flow [ 19 ], and thus the leaves of the AtPAP2 overexpression line contain higher ATP/NADPH and NADP + /NADPH ratios during photosynthesis compared with the WT line [ 18 ].…”

“…The chloroplasts of the AtPAP2 OE line exhibit a higher PSI/PSII ratio and ETR and fix more CO 2 , whereas the mitochondria of the AtPAP2 OE line can consume more reducing equivalents and generate more ATP compared with the WT line [ 19 ]. The higher consumption of reducing equivalents in the mitochondria can indirectly enhance the regeneration of stromal NADP + , electron acceptors of the linear electron flow [ 19 ], and thus the leaves of the AtPAP2 overexpression line contain higher ATP/NADPH and NADP + /NADPH ratios during photosynthesis compared with the WT line [ 18 ]. Surprisingly, when AtPAP2 is solely overexpressed in mitochondria, the transgenic lines exhibit high leaf-ATP, low sucrose, low seed-yield, and early-senescence phenotypes, possibly due to overreactive mitochondria [ 20 ].…”

“…Here, we show that AtPAP9 and AtPAP2 serve partially redundant biological functions in chloroplast protein import. However, unlike AtPAP2, overexpression of AtPAP9 in Arabidopsis thaliana does not promote plant growth, possibly due to its inability to be targeted to mitochondria and modulate mitochondrial activity [ 19 ].…”