James Maxence, Trouverie Jacques, Bernay Benoit, Marmagne Anne, Chardon Fabien, Gemin Marin-Pierre, Etienne Philippe, Masclaux-Daubresse Céline
Normandie Université, UNICAEN, INRAE, UMR 950 EVA, SFR Normandie Végétal (FED4277), Caen, F-14000, France.
Université de Caen Normandie, US EMerode, Plateforme Proteogen, Caen, F-14000, France.
Plant J. 2025 Jul;123(2):e70359. doi: 10.1111/tpj.70359.
Autophagy is essential for homeostasis and nutrient recycling. Its activity increases with aging and in response to deficiencies. The effects of defective autophagy on root metabolism have not yet been described. Addressing this question through root proteome analyses, we found that most V-ATPases were less abundant in the roots of autophagy mutants than in wild type. V-ATPases deficit, associated with lower root water contents and lower nitrate, magnesium, and potassium concentrations, indicated that the disturbance of cellular ion and water management in autophagy mutants was likely related to vacuole function. Isotopic δC analyses and leaf temperature measurements using thermography showed that water deficit in autophagy mutants was not due to excess transpiration, as the conductance of stomata was reduced in mutants compared to wild type. Many proteins related to the catabolism of amino acids and lipids and the tricarboxylic acid (TCA) cycle were over-abundant in atg mutants. The increase in several proteases that paralleled amino acid catabolism suggested that in the absence of autophagic flux, compensatory processes could be established to degrade proteins, recycle amino acids, and fuel TCA. Whether the V-ATPases defect affects energy metabolism and promotes lipid and amino acid catabolism to compensate and fuel TCA remains to be explored. In conclusion, this report establishes for the first time a correlation between autophagy and vacuole function through V-ATPases, particularly with regard to water and ion management. Additionally, this report shows the exacerbation of amino acid catabolism in relation to the stimulation of the TCA cycle in autophagy mutants.
自噬对于体内平衡和营养物质循环至关重要。其活性会随着衰老以及对营养缺乏的反应而增加。自噬缺陷对根系代谢的影响尚未见报道。通过根系蛋白质组分析来解决这个问题，我们发现与野生型相比，大多数V-ATP酶在自噬突变体的根系中丰度较低。V-ATP酶缺乏与较低的根系含水量以及较低的硝酸盐、镁和钾浓度相关，这表明自噬突变体细胞内离子和水分管理的紊乱可能与液泡功能有关。使用热成像进行的同位素δC分析和叶片温度测量表明，自噬突变体中的水分亏缺并非由于过度蒸腾，因为与野生型相比，突变体的气孔导度降低了。许多与氨基酸和脂质分解代谢以及三羧酸（TCA）循环相关的蛋白质在atg突变体中过量表达。与氨基酸分解代谢平行增加的几种蛋白酶表明，在缺乏自噬通量的情况下，可以建立补偿过程来降解蛋白质、回收氨基酸并为TCA提供燃料。V-ATP酶缺陷是否会影响能量代谢并促进脂质和氨基酸分解代谢以进行补偿并为TCA提供燃料仍有待探索。总之，本报告首次通过V-ATP酶建立了自噬与液泡功能之间的关联，特别是在水分和离子管理方面。此外，本报告显示了自噬突变体中氨基酸分解代谢相对于TCA循环刺激加剧的情况。
