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)