A Theoretical Investigation of Xanthophyll–Protein Hydrogen Bonding in the Photosystem II Antenna

Photoprotective nonphotochemical quenching (NPQ) in higher
plants
is the result of the formation of energy-quenching traps in the light-harvesting
antenna of photosystem II (PSII). The primary driving forces behind
NPQ are the protonation of the thylakoid lumen and the de-epoxidation
of the xanthophyll violaxanthin to zeaxanthin in the antenna. There
is currently some disagreement over whether de-epoxidation occurs
only at the peripheral, V1, binding site of the major LHCII or also
at the internal, L2, site of the minor antenna CP29 complex of PSII.
We have used density functional theory (DFT) to study of hydrogen
bonding between xanthophylls and the protein scaffold of LHCII and
CP29. We argue that a lack of hydrogen bonding for violaxanthin in
LHCII is consistent with it being weakly bound and accessible for
de-epoxidation. Conversely, the strong violaxanthin–protein
hydrogen bonding at the L2 site of CP29 is consistent with evidence
that it is not readily accessible for de-epoxidation and therefore
quenching by zeaxanthin at the L2 of CP29 is an unlikely candidate
for in vivo NPQ.

高等植物中的光保护性非光化学淬灭（nonphotochemical quenching, NPQ），是光系统II（photosystem II, PSII）捕光天线内能量淬灭陷阱形成的直接结果。NPQ的核心驱动因素为类囊体腔的质子化作用，以及天线复合物中紫黄质（violaxanthin）向玉米黄质（zeaxanthin）的脱环氧化反应。目前学界对于脱环氧化作用是否仅发生在主要捕光复合物II（LHCII）的外周V1结合位点，还是同时也可发生在PSII次要捕光天线CP29复合物的内部L2结合位点，仍存在一定学术争议。本研究借助密度泛函理论（DFT），针对LHCII与CP29中的叶黄素与蛋白质骨架之间的氢键相互作用展开了探究。我们提出，紫黄质在LHCII中缺乏氢键结合的现象，与其结合力较弱、易于发生脱环氧化反应的特性相符。与之相反，紫黄质在CP29的L2位点与蛋白质骨架之间存在强氢键作用，这一特征与"该位点的紫黄质不易发生脱环氧化"的实验证据相吻合，因此通过CP29的L2位点上的玉米黄质实现淬灭，并非体内NPQ的潜在可行机制。