Autophagy contributes to auxin-driven developmental plasticity in response to changes in carbon and nitrogen...

Plants, as sessile living systems, have the capacity to respond to both internal and external signals by modulating their growth and developmental programs. Autophagy is a recycling process which is known to respond to these signals, yet its role as an integrative regulatory node coordinating environmental inputs and developmental outputs remains underexplored, particularly outside model angiosperms like Arabidopsis thaliana. Here, we investigate how manipulating the supply of carbon and nitrogen affects the modulation of autophagy in relation to the auxin-driven chloronema-to-caulonema transition in the bryophyte Physcomitrium patens. We show that autophagy-deficient mutants display a loss of coordinated plasticity in response to changes in C and N availability, and that they exhibit an initially enhanced yet ultimately unsustainable response to nitrogen deficiency alongside attenuated responses to external sucrose. We propose that these altered responses reflect a modified basal state in the mutants, evidenced by higher intrinsic caulonemal growth, sucrose accumulation, altered auxin homeostasis, and differential auxin-related gene expression. Consistent with this, exogenous auxin elicits a diminished developmental response but accelerates senescence in the mutants. Finally, we show how alterations to the supply of C/N correlate with changes in the modulation of autophagic flux, rising when this ratio is most unbalanced. We propose a working model in which high autophagic activity is associated with chloroplast-rich chloronemal cells, whereas caulonemata-inducing conditions decrease autophagic flux. Thus, we describe a cell-type-specific modulation of autophagy, where it is negatively correlated with caulonemal development. Together, our findings identify autophagy as a key regulator within the system that modulates ordered and adaptive responses to both external nutrient availability and internal hormonal signaling.