Milburn Grace, Morris Cheyenne M, Kosola Eileen, Patel-Tupper Dhruv, Liu Jian, Pham Dominique H, Acosta-Gamboa Lucia, Stone William D, Pardi Sarah, Hillman Kylee, McHargue William E, Becker Eric, Kang Xiaojun, Sumner Josh, Bailey Catherine, Thielen Peter M, Jander Georg, Kane Cade N, McAdam Scott A M, Lawton Thomas J, Nusinow Dmitri A, Zhang Feng, Gore Michael A, Cheng Jianlin, Niyogi Krishna K, Zhang Ru
Donald Danforth Plant Science Center, St. Louis, MO, USA.
Current address: Washington University in Saint Louis, Plant and Microbial Biosciences Program, St. Louis, MO, USA.
bioRxiv. 2025 Jan 15:2025.01.12.632622. doi: 10.1101/2025.01.12.632622.
Light is essential for photosynthesis; however, excess light can increase the accumulation of photoinhibitory reactive oxygen species that reduce photosynthetic efficiency. Plants have evolved photoprotective non-photochemical quenching (NPQ) pathways to dissipate excess light energy. In tobacco and soybean (C plants), overexpression of three NPQ genes, e (VDE), (PsbS), and (ZEP), hereafter VPZ, resulted in faster NPQ induction and relaxation kinetics, and increased crop yields in field conditions. NPQ is well-studied in C plants; however, NPQ and the translatability of the VPZ approach in C plants is poorly understood. The green foxtail is an excellent model to study photosynthesis and photoprotection in C plants. To understand the regulation of NPQ and photosynthesis in C plants, we performed transient overexpression in Setaria protoplasts and generated (and employed) stable transgenic Setaria plants overexpressing one of the three Arabidopsis NPQ genes or all three NPQ genes (AtVPZ lines). Overexpressing (OE) and in Setaria produced similar results as in C plants, with increased or reduced zeaxanthin (thus NPQ), respectively. However, overexpressing appeared to be challenging in Setaria, with largely reduced NPQ in protoplasts and under-represented homozygous AtPsbS-OE lines, potentially due to competitive and tight heterodimerization of AtPsbS and SvPsbS proteins. Furthermore, Setaria AtVPZ lines had increased zeaxanthin, faster NPQ induction, higher NPQ level, but slower NPQ relaxation. Despite this, AtVPZ lines had improved growth as compared to wildtype under several conditions, especially high temperatures, which is not related to the faster relaxation of NPQ but may be attributable to increased zeaxanthin and NPQ in C plants. Our results identified shared and unique characteristics of the NPQ pathway in C model Setaria as compared to C plants and provide insights to improve C crop yields under fluctuating environmental conditions.
光对于光合作用至关重要；然而，过量的光会增加光抑制性活性氧的积累，从而降低光合效率。植物进化出了光保护非光化学猝灭（NPQ）途径来耗散多余的光能。在烟草和大豆（C4植物）中，三个NPQ基因，即VDE（e）、PsbS（ ）和ZEP（ ）（以下简称VPZ）的过表达导致NPQ诱导和弛豫动力学加快，并提高了田间条件下的作物产量。NPQ在C4植物中已有深入研究；然而，C3植物中NPQ以及VPZ方法的可转化性却知之甚少。绿色狗尾草是研究C3植物光合作用和光保护的优良模型。为了了解C3植物中NPQ和光合作用的调控机制，我们在狗尾草原生质体中进行了瞬时过表达，并生成（并使用）了稳定的转基因狗尾草植株，这些植株过表达了三个拟南芥NPQ基因之一或全部三个NPQ基因（AtVPZ系）。在狗尾草中过表达VDE（e）和ZEP（ ）产生了与C4植物中相似的结果，分别使玉米黄质增加或减少（从而使NPQ增加或减少）。然而，在狗尾草中过表达PsbS（ ）似乎具有挑战性，原生质体中的NPQ大幅降低，纯合AtPsbS-OE系的代表性不足，这可能是由于AtPsbS和SvPsbS蛋白的竞争性紧密异源二聚化所致。此外，狗尾草AtVPZ系的玉米黄质增加、NPQ诱导更快、NPQ水平更高，但NPQ弛豫较慢。尽管如此，在几种条件下，尤其是高温条件下，AtVPZ系与野生型相比生长有所改善，这与NPQ更快的弛豫无关，而可能归因于C3植物中玉米黄质和NPQ的增加。我们的结果确定了C3模式植物狗尾草中NPQ途径与C4植物相比的共同和独特特征，并为在波动环境条件下提高C3作物产量提供了见解。
