Is autophagy always a death sentence? A case study of highly selective cytoplasmic degradation during phloemogenesis.

Abstract

The transformation of sieve elements (SEs) from meristematic cells, equipped with a full complement of organelles, to specialized transport tubes devoid of a nucleus, has long been enigmatic. We hypothesized a strong involvement of various degradation pathways, particularly macroautophagy in this context, emphasizing the importance of autophagic selectivity in the remaining viability of these cells. Experiments were performed on pioneer roots of Populus trichocarpa cultivated in rhizotrons under field conditions. Through anatomical, ultrastructural and molecular analyses, we delineate the stages of phloemogenesis and the concurrent alterations in the cytoplasmic composition of SEs. Notably, we observed not only macroautophagic structures, but also the formation of autophagic plastids, the selective degradation of specific organelles, vacuole disruption and the release of vacuolar contents. These events initially lead to localized reductions in cytoplasm density, but organelle-rich cytoplasmic phase is safeguarded from the extensive damage by a membrane system derived from the endoplasmic reticulum. SE ultimately develops into a conduit containing electron-translucent cytoplasm. Eventually, mature SE is a tube filled only by the translucent cytoplasm, with sparse organelles tethered to the cell wall. Although the activation of programmed cell death pathways was postulated, the persistence of SEs indicates that protoplast depletion is meticulously regulated by hitherto unidentified mechanisms. This research elucidates the sequential processes occurring in these cells during phloemogenesis and unveils novel insights into the mechanisms of selective autophagy.