Biochemical and molecular properties of LHCX1, the essential regulator of dynamic photoprotection in diatoms

Biochemical and molecular properties of LHCX1, the essential regulator of dynamic photoprotection in diatoms
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DOI:
10.1093/plphys/kiab425
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发表时间:
2021-09-07
期刊:
影响因子:
7.4
通讯作者:
Ruban, Alexander, V
Ruban, Alexander, V
中科院分区:
生物学1区
文献类型:
--
作者:
Giovagnetti, Vasco;Jaubert, Marianne;Ruban, Alexander, V

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光捕获受类囊体腔酸化触发的过程调节,称为非光化学“能量依赖性淬灭”(qE)。在硅藻中,qE由捕光复合体(LHC)蛋白LHCX 1控制,而LHC胁迫相关(LHCSR)和光系统II亚基S蛋白分别是绿色藻类和植物所必需的。在这里,我们报告了LHCX1的生化和分子特征,以研究其在qE中的作用。我们发现,当生长在间歇性光照下,三角褐指藻形成非常大的qE,由于LHCX1组成上调。这种“超级qE”在LHCX1敲除突变体中被废除。LHCX1的生化和光谱分析表明,这种蛋白质可能不同的结合色素相对于光捕获天线蛋白的主要池的字符。瞬时颜料结合或不结合颜料的可能性进行了讨论。转基因三角褐指藻品系中推定的可质子化残基(D95和E205)的靶向诱变不改变qE能力,表明它们不参与感测管腔pH,这与LHCSR 3中保守的残基不同。我们的研究结果表明LHCX1和LHCSR3在qE调节中的功能差异。我们认为LHCX1是独立进化的,以便于动态跟踪湍流沃茨中的光波动。LHCX(类)蛋白在具有次生红色质体的生物体(如硅藻)中的进化可能赋予了动态光保护控制的选择性优势,最终导致其生态成功。
Light harvesting is regulated by a process triggered by the acidification of the thylakoid lumen, known as nonphotochemical "energy-dependent quenching" (qE). In diatoms, qE is controlled by the light-harvesting complex (LHC) protein LHCX1, while the LHC stress-related (LHCSR) and photosystem II subunit S proteins are essential for green algae and plants, respectively. Here, we report a biochemical and molecular characterization of LHCX1 to investigate its role in qE. We found that, when grown under intermittent light, Phaeodactylum tricornutum forms very large qE, due to LHCX1 constitutive upregulation. This "super qE" is abolished in LHCX1 knockout mutants. Biochemical and spectroscopic analyses of LHCX1 reveal that this protein might differ in the character of binding pigments relative to the major pool of light-harvesting antenna proteins. The possibility of transient pigment binding or not binding pigments at all is discussed. Targeted mutagenesis of putative protonatable residues (D95 and E205) in transgenic P. tricornutum lines does not alter qE capacity, showing that they are not involved in sensing lumen pH, differently from residues conserved in LHCSR3. Our results suggest functional divergence between LHCX1 and LHCSR3 in qE modulation. We propose that LHCX1 evolved independently to facilitate dynamic tracking of light fluctuations in turbulent waters. The evolution of LHCX(-like) proteins in organisms with secondary red plastids, such as diatoms, might have conferred a selective advantage in the control of dynamic photoprotection, ultimately resulting in their ecological success.