Fingers for signaling? A possible role of stromules in intracellular communication

Plastid stromules are frequently observed under stress, yet their function remains enigmatic. In the current study, we tested 2 alternative hypotheses: stromules might channel metabolic flux from plastids to peroxisomes during jasmonate biosynthesis, or they might serve as conduits for plastid–nucleus retrograde signaling. We used Nicotiana tabacum BY-2 cells to investigate stromulation in nonphotosynthetic plastids. Fluorescent markers for stroma, plastid outer membrane, peroxisomes, and the 12-oxo-phytodienoic acid (OPDA) exporter were combined with confocal visualization and AI-based quantification of stromule frequency and length. Exogenous methyl jasmonate (MeJA) and salicylic acid (SA) each triggered a rapid (∼60 min) ∼3-fold increase in stromule frequency. This increase primarily resulted from more initiation events, rather than elongation. Disrupting microtubules with oryzalin stopped MeJA from causing stromule formation, while actin depolymerization had no effect. Inhibition of jasmonate biosynthesis with Phenidone prevented SA-triggered stromule formation. MeJA-induced expression of genes involved in jasmonate biosynthesis (AOC) and jasmonate responses (JAZ1 and JAZ3) was further amplified when stromule formation was suppressed by oryzalin, suggesting that stromules modulate jasmonate-dependent gene expression. ... mehrThe GFP-fusion of the OPDA exporter JASSY showed a significant preference for stromules, and over 80% of them associated with peroxisomes. Stromule frequency was highest during the cell-expansion phase. We discuss our findings in the context of a role for stromules in stress-dependent retrograde signaling from plastids to the nucleus.