Metacaspases are distant relatives of animal caspases present in fungi, protozoa and plants. Our previous studies established the plant metacaspase AtMC1 as a major positive regulator of pathogen-triggered programmed cell death (PCD). We have now unveiled an additional, pro-survival homeostatic function of AtMC1 during aging in plants. This function acts in parallel to a similar pro-survival function of autophagy. Autophagy acts also as a positive regulator of pathogen-triggered PCD in parallel to AtMC1, indicating a common developmental switch for both pathways. The novel pro-survival role of AtMC1 is functionally related to its prodomain-mediated aggregate localization and clearance, in agreement with recent findings using the single budding yeast metacaspase YCA1. The fact that type I metacaspases can have both pro-survival and pro-death roles depending on their spatio-temporal context is of major evolutionary significance. Based on our data we propose a unifying model whereby autophagy and AtMC1 are part of parallel pathways, both positively regulating pathogen-triggered cell death in young plants –when these functions are not masked by the cumulative stresses of aging- and negatively regulating aging in older plants –revealed by the increasing damaged proteins and organelles that require clearing.