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Modulating autophagic activity makes it possible to control the onset of leaf senescence and to stimulate nitrogen recycling

Two publications from the SATURNE team in the Journal of Experimental Botany (February 2025) and in the Annals of Botany (June 2025)
In eukaryotes, autophagy is a longevity factor that cleans cells by contributing to the elimination of macromolecules that have become useless or undesirable. In plants, autophagy plays an essential role in controlling nitrogen fluxes, drawing nitrogen from the degradation of macromolecules in leaf tissues to recycle it and direct it towards seeds to ensure their filling. What is the role of autophagic activity in these processes, and can it be controlled?

To better understand the role of autophagy in the whole plant Arabidopsis thaliana, the impact on various phenotypes such as leaf yellowing, plant biomass, and nitrogen distribution in different organs was evaluated by considering three levels of autophagic activity. These three autophagy levels were obtained by using three types of plants: those in which autophagy was genetically completely abolished (inhibited plants), those in which autophagy was artificially enhanced (stimulated plants), and those in which autophagy remained unmodified and maintained at the original physiological level (wild-type plants).

The study confirmed the beneficial effect of autophagy in the remobilization of nitrogen from leaves to seeds. Inhibited plants showed very low remobilization, whereas plants with stimulated autophagic activity were more efficient at allocating nitrogen to seeds than wild-type plants. Surprisingly, however, both inhibition and stimulation of autophagy induced early leaf senescence. In the first case, this precocity is attributed to the overaccumulation of undesirable macromolecules that were not sufficiently eliminated; in the second case, early senescence is due to excessive depletion of leaf macromolecules used for nitrogen recycling. These results demonstrate the existence of modulation in the onset of senescence symptoms depending on the levels of autophagic activity expressed in leaf tissues over time.

The role of the transcription factors PIF4 and PIF5 in the positive transcriptional control of autophagy genes (ATG) was highlighted. In the absence of PIF4 and PIF5, autophagy genes are less expressed, and the induction of autophagic activity by aging is reduced, resulting in delayed senescence. By overexpressing autophagy genes in plants mutated in PIF4 and PIF5, it is possible to restore autophagic activity and achieve a level of senescence identical to that of the wild-type plant.

Overall, these findings show that both overactivation and inhibition of autophagy trigger early leaf senescence. This explains why a wild-type plant finely regulates its autophagic activity to ensure its longevity. This fine regulation is mediated by numerous actors, including the transcription factors PIF4/PIF5, which constitute a new lever for controlling nitrogen use efficiency.


Research developed at the Institute Jean-Pierre Bourgin for Plant Sciences in collaboration.

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Modulating autophagic activity makes it possible to control the onset of leaf senescence and to stimulate nitrogen recycling
Legend:(a) Autophagic activity is a major factor that stimulates the flow of remobilized nitrogen towards the grain; (b) inhibition (autophagy mutants atg5 and atg7) or stimulation (ATG8 overexpressors) exhibit exacerbated leaf senescence compared to the wild-type plant; (c) PIF4 and PIF5 induce the expression of autophagy genes, and the stay-green phenotype of pif4/5 mutants is due to the suppression of autophagy induction during aging.

IJPB Highlight

References:
James M, Trouverie J, Marmagne A, Chardon F, Frémont J, Etienne P, Masclaux-Daubresse C. Lack or excess of autophagy leads to premature leaf senescence probably owing to unbalanced nutrient management. Ann Bot. 2025
doi: https://doi.org/10.1093/aob/mcaf050

Lee J, Kang MH, Choi D-M, Marmagne A, Park J, Lee H, Gwak E, Lee J-C, Kim J-I, Masclaux-Daubresse C, Lim PO. Phytochrome-interacting factors PIF4 and PIF5 directly regulate autophagy during leaf senescence in Arabidopsis. Journal of experimental botany 2025.
doi: https://doi.org/10.1093/jxb/erae469

Contact:
Céline Masclaux-Daubresse

IJPB team:
"Senescence, Autophagy, Nutrient Recycling and Nitrogen Use Efficiency" SATURNE team

Collaborating teams:
> "Laboratoire d'Ecophysiologie Végétale, Agronomie & nutritions N.C.S." INRAE-UNICAEN 950 EVA, Caen, France
> "Daegu Gyeongbuk Institute of Science and Technology" DGIST, Daegu, Republic of Korea
> "Chonnam National University" Bioscience and Biotechnology, Gwangju, Republic of Korea