A tissue-specific rescue strategy reveals the local roles of autophagy in leaves and seeds for resource allocation

Autophagy is a vesicular mechanism that plays a fundamental role in nitrogen remobilization from senescing leaves to seeds. The Arabidopsis (Arabidopsis thaliana) autophagy (atg) mutants exhibit early senescence, reduced biomass, and low seed yield. The atg seeds also exhibit major changes in N and C concentrations. During plant development, autophagy genes are expressed in the source leaves and in the sink seeds during maturation. We thus addressed the question of whether the seed composition defects in atg mutants are caused by defective N remobilization from source leaves or whether they are due to the absence of autophagy in seeds during maturation. To answer this question, we restored autophagy activity in the atg5 mutant by expressing the wild-type (WT) ATG5 allele specifically in source leaves using the senescence-associated gene 12 (SAG12) promoter or specifically in seeds using the Glycinin-1 promoter, or in both organs using both constructs. In atg5, N remobilization from the rosettes to seeds was almost completely reestablished when transformed with the pSAG12::ATG5 construct. However, transformation with the pSAG12::ATG5 construct only partially restored seed composition. In contrast, seed N and C composition was largely restored by transformation with the pGly::ATG5 construct, even though the early leaf senescence phenotype was maintained in the atg5 background. Cotransformation with pSAG12::ATG5 and pGly::ATG5 completely restored the WT remobilization and seed composition phenotypes. Our results highlight the essential role of autophagy in leaves for nitrogen supply and in seeds for the establishment of carbon and nitrogen reserves.