Role of ATG8 specialization in plant selective autophagy

Phenotypic plasticity is the ability of an organism to adapt to changing environmental conditions. It involves modulating cellular programs, such as metabolism and endomembrane transport, in response to specific environmental cues. These subcellular adjustments underlie variations in plant growth and architecture across different ecological niches. It is a key adaptive mechanism that enables plants to cope with environmental unpredictability. Therefore, understanding the molecular basis of the homeostatic processes that underlie phenotypic plasticity is critical for developing crop varieties that can cope with irregular environmental conditions. Autophagy is an essential quality control mechanism that ensures the timely removal of unwanted or excess macromolecules that could otherwise harm the cell. Autophagy is a very potent recycling/membrane transport process. In contrast to the ubiquitin/proteasome system, where cargo proteins are tagged, unfolded, and degraded one by one at the proteasome, autophagic cargoes are rapidly quarantined from the rest of the cytoplasm. Hence, autophagy facilitates dynamic cell-state switches that are critical for remodeling the cell to adapt to the current environment. Initial studies suggested autophagy is a starvation-induced bulk degradation process. However, it is now well established that autophagy is highly selective. So far, most of the studies on autophagy in plants have focused on the functional characterization of the core ATG machinery. The degree to which selective autophagy contributes to environmental adaptation is poorly understood in plants. The ubiquitin like protein ATG8 is a key player in selective autophagy. The ATG8 gene family is expanded in plants. Functional specialization of the ATG8 gene family, which could contribute to selective autophagy, is currently being overlooked in the plant autophagy field. The central hypothesis of the proposed research is that unique structural elements underpin ATG8 specificity, and ATG8 specialization contributes to selective autophagy. At the completion of this project, we will have generated a thorough understanding of the biophysical properties of ATG8 specialization and expanded the selective autophagy toolbox in plants. This multidisciplinary project will pave the way for future studies that will further dissect selective autophagy in plants and reveal its contribution to phenotypic plasticity in plants.

Autophagy is a cell's recycling system that carries damaged or unwanted parts of the cell to the lytic compartments for remodeling and renovating the cell. This helps eukaryotic organisms to respond to changing environmental conditions and intrinsic demands. Defects in autophagy have been linked to several diseases, including cancer, neurodegeneration, aging in humans and sensitivity to stress, and reduced lifespan in plants. Despite recent advances in mammalian cells, the molecular details of the plant autophagy pathway remain incomplete. In this project, we studied how autophagy processes are compartmentalized within the cell. We showed that small proteins called ATG8 enable multiple autophagy responses simultaneously in the cell. Using ATG8 as bait, we then identified and characterized an adaptor protein that connects the autophagy pathway with the other major vacuolar trafficking pathway called multivesicular bodies. This suggested that vacuolar cargoes are sorted at hubs to coordinate different trafficking routes. In addition, again using ATG8 proteins as baits, we have identified molecular players that mediate the degradation of damaged mitochondria or endoplasmic reticulum. These molecular players led us to characterize new quality control mechanisms that ensure the maintenance of a healthy organelle content in plant cells. Altogether, the proposal led to the discovery of three exciting quality control systems that are essential for stress tolerance in plants. Future studies will reveal how these quality control pathways contribute to plant performance in changing climate conditions.