Calderan-Rodrigues Maria Juliana, Luzarowski Marcin, Monte-Bello Carolina Cassano, Minen Romina I, Zühlke Boris M, Nikoloski Zoran, Skirycz Aleksandra, Caldana Camila
Max Planck Institute of Molecular Plant Physiology, Potsdam, Germany.
Boyce Thompson Institute, Ithaca, NY, United States.
Front Plant Sci. 2021 Dec 22;12:758933. doi: 10.3389/fpls.2021.758933. eCollection 2021.
As autotrophic organisms, plants capture light energy to convert carbon dioxide into ATP, nicotinamide adenine dinucleotide phosphate (NADPH), and sugars, which are essential for the biosynthesis of building blocks, storage, and growth. At night, metabolism and growth can be sustained by mobilizing carbon (C) reserves. In response to changing environmental conditions, such as light-dark cycles, the small-molecule regulation of enzymatic activities is critical for reprogramming cellular metabolism. We have recently demonstrated that proteogenic dipeptides, protein degradation products, act as metabolic switches at the interface of proteostasis and central metabolism in both plants and yeast. Dipeptides accumulate in response to the environmental changes and act direct binding and regulation of critical enzymatic activities, enabling C flux distribution. Here, we provide evidence pointing to the involvement of dipeptides in the metabolic rewiring characteristics for the day-night cycle in plants. Specifically, we measured the abundance of 13 amino acids and 179 dipeptides over short- (SD) and long-day (LD) diel cycles, each with different light intensities. Of the measured dipeptides, 38 and eight were characterized by day-night oscillation in SD and LD, respectively, reaching maximum accumulation at the end of the day and then gradually falling in the night. Not only the number of dipeptides, but also the amplitude of the oscillation was higher in SD compared with LD conditions. Notably, rhythmic dipeptides were enriched in the glucogenic amino acids that can be converted into glucose. Considering the known role of Target of Rapamycin (TOR) signaling in regulating both autophagy and metabolism, we subsequently investigated whether diurnal fluctuations of dipeptides levels are dependent on the TOR Complex (TORC). The mutant (), known for the substantial reduction of TOR kinase activity, was characterized by the augmented accumulation of dipeptides, which is especially pronounced under LD conditions. We were particularly intrigued by the group of 16 dipeptides, which, based on their oscillation under SD conditions and accumulation in , can be associated with limited C availability or photoperiod. By mining existing protein-metabolite interaction data, we delineated putative protein interactors for a representative dipeptide Pro-Gln. The obtained list included enzymes of C and amino acid metabolism, which are also linked to the TORC-mediated metabolic network. Based on the obtained results, we speculate that the diurnal accumulation of dipeptides contributes to its metabolic adaptation in response to changes in C availability. We hypothesize that dipeptides would act as alternative respiratory substrates and by directly modulating the activity of the focal enzymes.
作为自养生物，植物捕获光能以将二氧化碳转化为ATP、烟酰胺腺嘌呤二核苷酸磷酸（NADPH）和糖类，这些对于生物合成的构件、储存和生长至关重要。在夜间，通过调动碳（C）储备可以维持新陈代谢和生长。响应不断变化的环境条件，如光暗循环，酶活性的小分子调节对于重新编程细胞代谢至关重要。我们最近证明，蛋白ogenic二肽，即蛋白质降解产物，在植物和酵母中作为蛋白质稳态和中心代谢界面处的代谢开关。二肽响应环境变化而积累，并通过直接结合和调节关键酶活性来实现碳通量分布。在这里，我们提供证据表明二肽参与植物昼夜循环的代谢重布线特征。具体而言，我们在短日（SD）和长日（LD）昼夜循环中测量了13种氨基酸和179种二肽的丰度，每个循环具有不同的光照强度。在所测量的二肽中，分别有38种和8种在SD和LD中表现出昼夜振荡，在一天结束时达到最大积累，然后在夜间逐渐下降。与LD条件相比，不仅二肽的数量，而且振荡幅度在SD中更高。值得注意的是，有节奏的二肽富含可转化为葡萄糖的生糖氨基酸。考虑到雷帕霉素靶蛋白（TOR）信号在调节自噬和代谢中的已知作用，我们随后研究了二肽水平的昼夜波动是否依赖于TOR复合物（TORC）。以TOR激酶活性大幅降低而闻名的突变体（），其特征是二肽积累增加，在LD条件下尤为明显。我们特别感兴趣的是一组16种二肽，基于它们在SD条件下的振荡和在中的积累，可能与有限的碳可用性或光周期有关。通过挖掘现有的蛋白质-代谢物相互作用数据，我们描绘了代表性二肽Pro-Gln的推定蛋白质相互作用者。获得的列表包括碳和氨基酸代谢的酶，它们也与TORC介导的代谢网络相关。基于获得的结果，我们推测二肽的昼夜积累有助于其响应碳可用性变化的代谢适应。我们假设二肽将作为替代呼吸底物并通过直接调节关键酶的活性来发挥作用。
