Nutrient starvation-induced autophagy is a conserved process in eukaryotes. Plants defective in autophagy show hypersensitivity to carbon and nitrogen limitation. However, the role of autophagy in plant phosphate (Pi) starvation response is relatively less explored. Among the core autophagy-related (ATG) genes,ATG8encodes a ubiquitin-like protein involved in autophagosome formation and selective cargo recruitment. TheArabidopsis thaliana ATG8genes,AtATG8fandAtATG8h, are notably induced in roots under low Pi. In this study, we show that such upregulation correlates with their promoter activities and can be suppressed in thephosphate response 1(phr1) mutant. Yeast one-hybrid analysis failed to attest the binding of theAtPHR1 transcription factor to the promoter regions ofAtATG8fandAtATG8h. Dual luciferase reporter assays inArabidopsismesophyll protoplasts also indicated thatAtPHR1 could not transactivate the expression of both genes. Loss ofAtATG8f andAtATG8h leads to decreased root microsomal-enriched ATG8 but increased ATG8 lipidation. Moreover, atg8f/atg8hmutants exhibit reduced autophagic flux estimated by the vacuolar degradation of ATG8 in the Pi-limited root but maintain normal cellular Pi homeostasis with reduced number of lateral roots. While the expression patterns ofAtATG8fandAtATG8hoverlap in the root stele,AtATG8fis more strongly expressed in the root apex and root hair and remarkably at sites where lateral root primordia develop. We hypothesize that Pi starvation-induction ofAtATG8f andAtATG8h may not directly contribute to Pi recycling but rely on a second wave of transcriptional activation triggered by PHR1 that fine-tunes cell type-specific autophagic activity.