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Autophagy Plays Prominent Roles in Amino Acid, Nucleotide, and Carbohydrate Metabolism during Fixed-Carbon Starvation in Maize.
The Plant Cell ( IF 10.0 ) Pub Date : 2020-09-01 , DOI: 10.1105/tpc.20.00226
Fionn McLoughlin 1 , Richard S Marshall 1 , Xinxin Ding 2, 3 , Elizabeth C Chatt 1 , Liam D Kirkpatrick 1 , Robert C Augustine 1 , Faqiang Li 4 , Marisa S Otegui 2, 3 , Richard D Vierstra 4, 5
Affiliation  

Autophagic recycling of proteins, lipids, nucleic acids, carbohydrates, and organelles is essential for cellular homeostasis and optimal health, especially under nutrient-limiting conditions. To better understand how this turnover affects plant growth, development, and survival upon nutrient stress, we applied an integrated multiomics approach to study maize (Zea mays) autophagy mutants subjected to fixed-carbon starvation induced by darkness. Broad metabolic alterations were evident in leaves missing the core autophagy component ATG12 under normal growth conditions (e.g., lipids and secondary metabolism), while changes in amino acid-, carbohydrate-, and nucleotide-related metabolites selectively emerged during fixed-carbon starvation. Through combined proteomic and transcriptomic analyses, we identified numerous autophagy-responsive proteins, which revealed processes underpinning the various metabolic changes seen during carbon stress as well as potential autophagic cargo. Strikingly, a strong upregulation of various catabolic processes was observed in the absence of autophagy, including increases in simple carbohydrate levels with a commensurate drop in starch levels, elevated free amino acid levels with a corresponding reduction in intact protein levels, and a strong increase in the abundance of several nitrogen-rich nucleotide catabolites. Altogether, this analysis showed that fixed-carbon starvation in the absence of autophagy adjusts the choice of respiratory substrates, promotes the transition of peroxisomes to glyoxysomes, and enhances the retention of assimilated nitrogen.



中文翻译:


在玉米固定碳饥饿期间,自噬在氨基酸、核苷酸和碳水化合物代谢中发挥着重要作用。



蛋白质、脂质、核酸、碳水化合物和细胞器的自噬回收对于细胞稳态和最佳健康至关重要,特别是在营养限制条件下。为了更好地了解这种周转如何影响植物在营养胁迫下的生长、发育和存活,我们应用综合多组学方法来研究遭受黑暗诱导的固定碳饥饿的玉米( Zea mays )自噬突变体。在正常生长条件下(例如脂质和次生代谢),缺失核心自噬成分 ATG12 的叶子中存在明显的广泛代谢变化,而在固定碳饥饿期间选择性地出现氨基酸、碳水化合物和核苷酸相关代谢物的变化。通过蛋白质组学和转录组学的结合分析,我们鉴定了许多自噬响应蛋白,这些蛋白质揭示了碳胁迫期间各种代谢变化的基础过程以及潜在的自噬货物。引人注目的是,在没有自噬的情况下,观察到各种分解代谢过程的强烈上调,包括简单碳水化合物水平增加,淀粉水平相应下降,游离氨基酸水平升高,完整蛋白质水平相应降低,以及几种富氮核苷酸分解代谢物的丰度。总而言之,该分析表明,在没有自噬的情况下,固定碳饥饿会调整呼吸底物的选择,促进过氧化物酶体向乙醛酸酶体的转变,并增强同化氮的保留。

更新日期:2020-09-05
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