Towards elucidation of dynamic structural changes of plant thylakoid architecture

Philosophical Transactions of the Royal Society B: Biological Sciences, Dec 2012

Long-term acclimation of shade versus sun plants modulates the composition, function and structural organization of the architecture of the thylakoid membrane network. Significantly, these changes in the macroscopic structural organization of shade and sun plant chloroplasts during long-term acclimation are also mimicked following rapid transitions in irradiance: reversible ultrastructural changes in the entire thylakoid membrane network increase the number of grana per chloroplast, but decrease the number of stacked thylakoids per granum in seconds to minutes in leaves. It is proposed that these dynamic changes depend on reversible macro-reorganization of some light-harvesting complex IIb and photosystem II supracomplexes within the plant thylakoid network owing to differential phosphorylation cycles and other biochemical changes known to ensure flexibility in photosynthetic function in vivo. Some lingering grana enigmas remain: elucidation of the mechanisms involved in the dynamic architecture of the thylakoid membrane network under fluctuating irradiance and its implications for function merit extensive further studies.

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Towards elucidation of dynamic structural changes of plant thylakoid architecture

Jan M. Anderson () 2 Peter Horton 1 Eun-Ha Kim 0 2 Wah Soon Chow 2 0 Department of Agricultural Biotechnology , 126 Suin-ro, Gwonsoon-gu Suwon, 441-707 Gyeonggido , South Korea 1 Department of Molecular Biology and Biotechnology, University of Sheffield , Sheffield S10 2TN , UK 2 Division of Plant Science, Research School of Biology, The Australian National University , Canberra, Australian Capital Territory 0200 , Australia Long-term acclimation of shade versus sun plants modulates the composition, function and structural organization of the architecture of the thylakoid membrane network. Significantly, these changes in the macroscopic structural organization of shade and sun plant chloroplasts during long-term acclimation are also mimicked following rapid transitions in irradiance: reversible ultrastructural changes in the entire thylakoid membrane network increase the number of grana per chloroplast, but decrease the number of stacked thylakoids per granum in seconds to minutes in leaves. It is proposed that these dynamic changes depend on reversible macro-reorganization of some light-harvesting complex IIb and photosystem II supracomplexes within the plant thylakoid network owing to differential phosphorylation cycles and other biochemical changes known to ensure flexibility in photosynthetic function in vivo. Some lingering grana enigmas remain: elucidation of the mechanisms involved in the dynamic architecture of the thylakoid membrane network under fluctuating irradiance and its implications for function merit extensive further studies. 1. INTRODUCTION The static view of the structural organization of the unique plant thylakoid membrane network inferred from transmission electron micrographs, being but snapshots in time, cannot capture their highly organized and dynamically regulated ultrastructure. To survive and thrive under ever-fluctuating light, plants have evolved long-term acclimation strategies to optimize photosynthetic efficiency and resource utilization [1 3] that are intertwined with vital shortterm structural and functional flexibility under fluctuating irradiance [4 7]. Granal stacks in higher plants have been selected during evolution for the integrated, multifaceted advantages and optimization of photosynthesis they confer in diverse and ever-fluctuating light environments [8 11]. In this article, we emphasize that the elaborate dynamic structural changes of more but shorter grana versus fewer but taller grana and vice versa observed in hours, days to seasons in chloroplasts of shade and sun plants are mimicked in seconds to minutes in leaves in response to increasing fluctuating light. Although there have been few examples of snapshots that capture dynamics from experiments with leaves under controlled fluctuating conditions, we suggest that they are caused by the reversible phosphorylation of thylakoid proteins and the various changes associated with non-photochemical quenching (NPQ), the D1 protein repair cycle and the photoprotection of non-functional photosystem II (PSII) under very high irradiance. This highly dynamic regulation of ultrastructure and function of plant thylakoids is intriguing yet still puzzling, especially in the remarkably dynamic three-dimensional architecture of plant thylakoids in vivo. Hence, some lingering grana enigmas concerning the dynamic structural changes in the architecture of the thylakoid network in vivo are also discussed. 2. SUPRAMOLECULAR ORGANIZATION AND THYLAKOID ARCHITECTURE UNDER ACCLIMATION AND FLUCTUATING IRRADIANCE The highly dynamic structural organization of the continuous thylakoid membrane network of higher plant chloroplasts is intriguing, especially in its elaborate three-dimensional architecture. The continuous thylakoid network that encloses one internal aqueous lumenal space is structurally differentiated into two distinct morphological regions: cylindrical, tightly appressed granal thylakoids (grana stacks) are interconnected by single stromal thylakoids whose outer surfaces face the stroma. This elaborate structural membrane architecture is accompanied by compositional and functional differentiation with respect to the location of the thylakoid pigment protein complexes termed lateral heterogeneity. PSII/light-harvesting complex II (LHCII) supercomplexes and extra LHCII are mainly segregated in dynamically regulated grana, whereas photosystem I (PSI) and ATP synthase are confined to stromal thylakoids and end granal membranes, while cytochrome (cyt) b6f complexes are reversibly located between stacked and unstacked thylakoid regions ([12 15] and references therein). Long-term acclimation of plants grown in nature or controlled conditions related to light quantity and quality is well understood [1,2]. With long-term acclimation, the ratio of granal to stromal membrane domains in higher plant chloroplasts is highly variable: the chloroplasts of sun and high-light grown plants have more grana with fewer (5 16) stacked (...truncated)


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Jan M. Anderson, Peter Horton, Eun-Ha Kim, Wah Soon Chow. Towards elucidation of dynamic structural changes of plant thylakoid architecture, Philosophical Transactions of the Royal Society B: Biological Sciences, 2012, pp. 3515-3524, 367/1608, DOI: 10.1098/rstb.2012.0373