Abstract
In higher plants, photosystems II and I are found in grana stacks and unstacked stroma lamellae, respectively. To connect them, electron carriers negotiate tortuous multi-media paths and are subject to macromolecular blocking. Why does evolution select an apparently unnecessary, inefficient bipartition? Here we systematically explain this perplexing phenomenon. We propose that grana stacks, acting like bellows in accordions, increase the degree of ultrastructural control on photosynthesis through thylakoid swelling/shrinking induced by osmotic water fluxes. This control coordinates with variations in stomatal conductance and the turgor of guard cells, which act like an accordion's air button. Thylakoid ultrastructural dynamics regulate macromolecular blocking/collision probability, direct diffusional pathlengths, division of function of Cytochrome b6f complex between linear and cyclic electron transport, luminal pH via osmotic water fluxes, and the separation of pH dynamics between granal and lamellar lumens in response to environmental variations. With the two functionally asymmetrical photosystems located distantly from each other, the ultrastructural control, nonphotochemical quenching, and carbon-reaction feedbacks maximally cooperate to balance electron transport with gas exchange, provide homeostasis in fluctuating light environments, and protect photosystems in drought. Grana stacks represent a dry/high irradiance adaptation of photosynthetic machinery to improve fitness in challenging land environments. Our theory unifies many well-known but seemingly unconnected phenomena of thylakoid structure and function in higher plants.
| Original language | English |
|---|---|
| Pages (from-to) | 319-329 |
| Number of pages | 11 |
| Journal | New Phytologist |
| Volume | 236 |
| Issue number | 2 |
| DOIs | |
| State | Published - Oct 2022 |
Funding
The authors benefited from discussions on photosynthetic electron transport with Drs Joe Berry, Albert Porcar-Castell, and Xinyou Yin. Three anonymous referees and Dr Tracy Lawson made insightful comments and suggestions on earlier drafts, which led to considerable improvement of the article. We are grateful to these colleagues. We also thank Dr Jeff Wood and Ms Jena Gu for comments on the manuscript. This research is supported by the US Department of Energy (DOE), Office of Science, Biological and Environmental Research Program. ORNL is managed by UT-Battelle, LLC, for the DOE under contract DE-AC05-00OR22725. YS and JH acknowledge support from NSF Macrosystem Biology (Award 1926488), the USDA-NIFA Hatch Fund (1014740), and the Cornell Initiative for Digital Agriculture Research Innovation Fund. BG and TM acknowledge the support of the Ontario Ministry of Agriculture, Food and Rural Affairs for two OMAFRA-Alliance-T1 Awards (UofG2016-2732 and UG-T1-2021-100932). The authors benefited from discussions on photosynthetic electron transport with Drs Joe Berry, Albert Porcar‐Castell, and Xinyou Yin. Three anonymous referees and Dr Tracy Lawson made insightful comments and suggestions on earlier drafts, which led to considerable improvement of the article. We are grateful to these colleagues. We also thank Dr Jeff Wood and Ms Jena Gu for comments on the manuscript. This research is supported by the US Department of Energy (DOE), Office of Science, Biological and Environmental Research Program. ORNL is managed by UT‐Battelle, LLC, for the DOE under contract DE‐AC05‐00OR22725. YS and JH acknowledge support from NSF Macrosystem Biology (Award 1926488), the USDA‐NIFA Hatch Fund (1014740), and the Cornell Initiative for Digital Agriculture Research Innovation Fund. BG and TM acknowledge the support of the Ontario Ministry of Agriculture, Food and Rural Affairs for two OMAFRA‐Alliance‐T1 Awards (UofG2016‐2732 and UG‐T1‐2021‐100932).
Keywords
- cytochrome bf complex
- electron transport
- grana stacks
- photosystems
- stroma lamellae
- thylakoid