The Science

Among the photosynthetic eukaryotes, higher plants have the most diverse morphology and physiology. Yet without exception and regardless of photosynthetic pathways, all higher plants share thylakoid architectures characterized by appressed grana stacks and unstacked stroma lamellae. This architecture is lacking in other oxygenic photosynthetic organisms (e.g., cyanobacteria and algae). A new theory suggests that plants swell and shrink grana stacks to control electron transport in tandem with the opening and closing of small holes on leaf surfaces known as stomata to control gas exchange between the leaf’s inside and outside. This process is like how an accordionist plays music by controlling the rhythms of bellows and air buttons.

The Impact

Higher plants have two photosystems (II and I) that must coordinate to pass electrons for photosynthesis. The new theory suggests that grana stacks expand the degree of ultrastructural control on photosynthesis through thylakoid swelling and shrinking in coordination with varying stomatal conductance and turgor of guard cells. This process allows land plants to adapt to dry and high-irradiance environments. This theory not only successfully explains a long-standing mystery but also unifies many well-known phenomena of thylakoid structure and function of higher plants.

Summary

In higher plants, photosystems II and I are found in grana stacks and unstacked stroma lamellae, respectively. To connect them, electron carriers negotiate tortuous multimedia paths and are subject to macromolecular blocking. Why does evolution select an apparently unnecessary, inefficient bipartition? This study proposes that grana stacks, acting like bellows in accordions, increase the degree of ultrastructural control on photosynthesis through thylakoid swelling and 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 and 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 and high irradiance adaptation of photosynthetic machinery to improve fitness in challenging land environments. This theory unifies many well-known but seemingly unconnected phenomena of thylakoid structure and function in higher plants.

Principal Investigator

Lianhong Gu
Oak Ridge National Laboratory
lianhong-gu@ornl.gov

Program Manager

Daniel Stover
U.S. Department of Energy, Biological and Environmental Research (SC-33)
Environmental System Science
daniel.stover@science.doe.gov

Funding

This research is supported by the Biological and Environmental Research (BER) Program within the U.S. Department of Energy’s (DOE) Office of Science. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for DOE under contract DE-AC05-00OR22725. Additional support was received from National Science Foundation Macrosystem Biology (Award 1926488), U.S. Department of Agriculture–National Institute of Food and Agriculture Hatch Fund (1014740), Cornell Initiative for Digital Agriculture Research Innovation Fund, and Ontario Ministry of Agriculture, Food and Rural Affairs for two Alliance Tier 1 Awards (UofG2016-2732 and UG-T1-2021-100932).

References