High Light Acclimation in the Secondary Plastids Containing Diatom Phaeodactylum tricornutum is Triggered by the Redox State of the Plastoquinone Pool    

Abstract

In diatoms, the process of energy-dependent chlorophyll fluorescence quenching (qE) has an important role in photoprotection. Three components are essential for qE: (1) the light-dependent generation of a transthylakoidal proton gradient; (2) the deepoxidation of the xanthophyll diadinoxanthin (Dd) into diatoxanthin (Dt); and (3) specific nucleus-encoded antenna proteins, called Light Harvesting Complex Protein X (LHCX). We used the model diatom Phaeodactylum tricornutum to investigate the concerted light acclimation response of the qE key components LHCX, proton gradient, and xanthophyll cycle pigments (Dd+Dt) and to identify the intracellular light-responsive trigger. At high-light exposure, the up-regulation of three of the LHCX genes and the de novo synthesis of Dd+Dt led to a pronounced rise of qE. By inhibiting either the conversion of Dd to Dt or the translation of LHCX genes, qE amplification was abolished and the diatom cells suffered from stronger photoinhibition. Artificial modification of the redox state of the plastoquinone (PQ) pool via 3-(3,4-dichlorophenyl)-1,1-dimethylurea and 5-dibromo-6-isopropyl-3-methyl-1,4-benzoquinone resulted in a disturbance of Dd+Dt synthesis in an opposite way. Moreover, we could increase the transcription of two of the four LHCX genes under low-light conditions by reducing the PQ pool using 5-dibromo-6-isopropyl-3-methyl-1,4-benzoquinone. Altogether, our results underline the central role of the redox state of the PQ pool in the light acclimation of diatoms. Additionally, they emphasize strong evidence for the existence of a plastid-to-nucleus retrograde signaling mechanism in an organism with plastids that derived from secondary endosymbiosis.

Light harvesting proteins regulate non-photochemical fluorescence quenching in the marine diatom Thalassiosira pseudonana

“…1A). This is consistent with the results obtained in P. tricornutum [21]. Moreover, the addition of DCMU significantly reduced the amount and percentage of Dt in HL (Table 1).…”

“…It is noteworthy that the NPQ value with DTT treatment was higher than that without DTT during the LL recovery period. These observations are different from the results obtained in the diatom P. tricornutum, where DTT treatment strongly inhibited the induction of NPQ during HL treatment and did not prevent relaxation of NPQ during the LL recovery period [21]. T. pseudonana possesses one DDE and two violaxanthin deepoxidase-like enzymes (VDL) [11].…”

Energy dissipation pathways in Photosystem 2 of the diatom, Phaeodactylum tricornutum, under high-light conditions

“…Most eukaryotic algae have an active xanthophyll cycle (the VAZ cycle or its alternative that involves de-epoxidation of diadinoxanthin (Dd) to diatoxanthin (Dt) (Falkowski and Raven 2007)) as well as proteins homologous to Lhcsr (Niyogi and Truong 2013). In diatoms, antenna-related NPQ is thought to be similar to that in green algae and be driven by structural rearrangements in one of the antenna proteins, Lhcx (Lhcsr homologous) (Bailleul et al 2010;Lavaud et al 2012;Lepetit et al 2013;Goss and Lepetit 2015). Upon DpHdriven de-epoxidation of Dd and protonation of some antenna proteins (presumably Lhcx), PS2 antenna efficiently quenches excited states of chlorophyll a (Lepetit et al 2013;Goss and Lepetit 2015).…”

“…In diatoms, antenna-related NPQ is thought to be similar to that in green algae and be driven by structural rearrangements in one of the antenna proteins, Lhcx (Lhcsr homologous) (Bailleul et al 2010;Lavaud et al 2012;Lepetit et al 2013;Goss and Lepetit 2015). Upon DpHdriven de-epoxidation of Dd and protonation of some antenna proteins (presumably Lhcx), PS2 antenna efficiently quenches excited states of chlorophyll a (Lepetit et al 2013;Goss and Lepetit 2015). Additionally NPQ might be accompanied by partial antenna detachment, which may also contribute to overall NPQ through quenching in the detached FCP oligomers (Miloslavina et al 2009;Gundermann and Büchel 2012).…”

Fucoxanthin-Chlorophyll-Proteins and Non-Photochemical Fluorescence Quenching of Diatoms

“…11.1 ; note that in T. pseudonana, Lhcx1 and Lhcx2 encode identical proteins). Transcript levels depend on growth light intensity, whereby, in P. tricornutum, up-regulation under HL is most pronounced for Lhcx2 , followed by Lhcx3 and Lhcx1 (Nymark et al 2009(Nymark et al , 2013Lepetit et al 2013 ). In Chaetoceros neogracile , a centric diatom the genome of which has not been sequenced, Park et al ( 2010 ) found up-regulation of Lhcx genes under HL, which also correlated with Dt accumulation and formation of NPQ.…”