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Chinese scientists explain energy transfer mechanism in chloroplasts and its evolution

Chinese scientists explain energy transfer mechanism in chloroplasts and its evolution
2025-03-12
(Press-News.org) A recent study by Chinese scientists has revealed the intricate molecular machinery driving energy exchange within chloroplasts, shedding light on a key event in the evolution of plant life. Led by FAN Minrui from the Center for Excellence in Molecular Plant Sciences of the Chinese Academy of Sciences, the research elucidates the structure and function of the ATP/ADP translocator—a crucial member of the nucleotide transporter (NTT) family of proteins—which facilitates the transfer of energy across chloroplast membranes.

Their findings were published online in Nature in an article entitled “Structure and mechanism of the plastid/parasite ATP/ADP translocator” on March 13.

The findings not only deepen our understanding of chloroplast endosymbiosis—the process by which ancient bacteria became integrated into plant cells as chloroplasts—but also offer potential avenues for improving crop yields and developing new drugs to combat intracellular pathogens.

Chloroplasts are essential for energy production in plants—playing a similar role as mitochondria (the powerhouses of animal cells) do in animals. However, mitochondria use the ATP/ADP translocator AAC to export ATP (the “energy currency” of cells) to the cytoplasm and import ADP for ATP synthesis. In contrast, chloroplasts employ an NTT protein to import ATP from the cytoplasm to fuel photosynthesis, starch synthesis, and fatty acid synthesis, while exporting ADP and inorganic phosphate (Pi). Notably, the chloroplast NTT protein is highly specific for ATP/ADP, unlike some related proteins in diatoms that can transport a broader range of nucleotides.

A long-standing question has been the origin of the NTT protein in chloroplasts. The endosymbiotic theory posits that chloroplasts evolved from cyanobacteria. However, free-living cyanobacteria lack NTT proteins. One hypothesis suggests that an ancestral eukaryotic cell engulfed both a cyanobacterium and a Chlamydia-like bacterium. The cyanobacterium may have acquired an NTT protein from Chlamydia through horizontal gene transfer (gene exchange between organisms), since Chlamydia uses a similar protein to steal ATP from host cells. This protein was then retained during chloroplast evolution. The “energy parasitism” exhibited by Chlamydia and the unique function of this NTT protein have intrigued scientists for years.

To verify this hypothesis, the research group determined the three-dimensional structures of NTT proteins from both Arabidopsis chloroplasts and Chlamydia pneumoniae at near-atomic resolution (2.72–2.90 Å). They found that the NTT proteins consist of 12 transmembrane helices, adopting a fold typical of major facilitator superfamily (MFS) transporters. The structures revealed that both proteins share a similar overall architecture despite significant species-specific differences. This supports the hypothesis that the chloroplast NTT protein originated from a Chlamydia-like ancestor.

The study also identified the ATP (or ADP and Pi) binding site within the NTT protein. The binding of ATP involves extensive interactions between its three moieties (adenine, ribose, and phosphate) and the NTT protein. The adenine portion of ATP is sandwiched between aromatic and hydrophobic amino acid residues, with its negatively charged phosphate groups interacting with surrounding positively charged amino acid residues.

The binding site for ADP is similar to that of ATP, but with some conformational differences: The phosphate groups of ATP adopt an extended conformation, whereas the phosphate groups of ADP are folded, resulting in slight variations in the surrounding interacting residues.

Interestingly, the binding position for Pi corresponds exactly to the position of ATP’s γ-phosphate group. To validate these structural findings, the researchers conducted ATP/ADP exchange experiments based on chemiluminescence as well as ATP-32P uptake experiments using radioactive isotopes.

The researchers also analyzed the thermal stability of the NTT protein and found that Pi significantly enhanced ADP binding, suggesting a cooperative effect between the two. This finding aligns with the co-transport properties of ADP and Pi in the NTT protein.

Additionally, the study revealed that when an evolutionarily conserved asparagine residue (N282 in Arabidopsis AtNTT1) in the NTT protein mutates to alanine, the transport activity towards other nucleotides (such as GTP, CTP, and UTP) significantly increases. This suggests that this residue may play a crucial role in the specific recognition of ATP by the NTT protein.

By comparing the structures of the NTT protein in different conformations, along with conducting mutational and functional experiments, the study reveals that the N-terminal and C-terminal domains of the NTT protein are relatively rigid. These domains move relative to each other, and by altering their interactions, the protein facilitates the binding, transmembrane transport, and release of ATP or ADP plus Pi.

This transport mechanism aligns with the “rocker-switch” alternating pathway model of the MFS. In this model, the conformational changes between the N-terminal and C-terminal domains allow the protein to alternately open and close its transport pathway, ensuring the efficient binding and release of the substrate and facilitating its translocation across the membrane. This mechanism is critical to the NTT protein’s ability to carry out its role in ATP/ADP exchange and the co-transport of Pi.

This study not only unveils the molecular mechanism of substrate recognition and transmembrane transport by the chloroplast and Chlamydia ATP/ADP translocator NTT protein but also deepens our understanding of the transmembrane energy transfer mechanism in chloroplast endosymbiosis. It also provides valuable insights on engineering NTT proteins to improve crop yields and designing NTT protein inhibitors to treat diseases caused by obligate intracellular pathogens.

This research was funded by the Center for Excellence in Molecular Plant Sciences of the Chinese Academy of Sciences, the Strategic Priority Research Program of the Chinese Academy of Sciences, the Shanghai Branch of the Chinese Academy of Sciences, and the Science and Technology Innovation Action Plan of Shanghai.

END

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[Press-News.org] Chinese scientists explain energy transfer mechanism in chloroplasts and its evolution