Broad and Complex Roles of NBR1-Mediated Selective Autophagy in Plant Stress Responses

Abstract

Selective autophagy is a highly regulated degradation pathway for the removal of specific damaged or unwanted cellular components and organelles such as protein aggregates. Cargo selectivity in selective autophagy relies on the action of cargo receptors and adaptors. In mammalian cells, two structurally related proteins p62 and NBR1 act as cargo receptors for selective autophagy of ubiquitinated proteins including aggregation-prone proteins in aggrephagy. Plant NBR1 is the structural and functional homolog of mammalian p62 and NBR1. Since its first reports almost ten years ago, plant NBR1 has been well established to function as a cargo receptor for selective autophagy of stress-induced protein aggregates and play an important role in plant responses to a broad spectrum of stress conditions including heat, salt and drought. Over the past several years, important progress has been made in the discovery of specific cargo proteins of plant NBR1 and their roles in the regulation of plant heat stress memory, plant-viral interaction and special protein secretion. There is also new evidence for a possible role of NBR1 in stress-induced pexophagy, sulfur nutrient responses and abscisic acid signaling. In this review, we summarize these progresses and discuss the potential significance of NBR1-mediated selective autophagy in broad plant responses to both biotic and abiotic stresses.

Keywords: NBR1; autophagy; plant heat tolerance; plant stress responses; plant virus interaction; protein aggregates; selective autophagy receptor.

Figure 1

The phylogenetic relationship of NBR1 homologs from plants and metazoans. The tree was inferred using the neighbor-joining method. Phylogenetic analyses were conducted in MEGA5. Bootstrap values from 1000 replicates were used to assess the robustness of the tree. NBR1 homologs in the phylogenetic analysis include those from Homo sapiens (Human NBR1), Mus musculus (Mouse NBR1), Danio rerio (Zebrafish NBR1), Xenopus tropicalis (Xenopus NBR1), Marchantia polymorpha (Mapoly0100s0042 and Mapoly0039s0051), Physcomitrella patens (Pp3c7_8990V3 and Pp3c11_16970V3), Amborella trichopoda (AmTr scaffold00049.238), Ananas comosus(Aco013530), Brachypodium distachyon (Bradi3g47580 and Bradi5g13400), Oryza sativa (LOC_Os02g38050 and LOC_Os04g40090), Sorghum bicolor (Sobic.004G200200 and Sobic.006G119900), Zea mays (GRMZM2G139846_T01 and GRMZM2G092447_T01), Aquilegia coerulea (Aqcoe3G144200), Solanum lycopersicum (Solyc03g112230.2 and Solyc06g071770.2), Solanum tuberosum (PGSC0003DMT400069639 and PGSC0003DMT400046670), Populus trichocarpa (Potri.012G085700), Ricinus communis (30147.m013869), Arabidopsis thaliana (AT4G24690), Cucumis sativus (Cucsa.098760), Glycine max (Glyma.05G041600 and Glyma.17G084700), Medicago truncatula (Medtr4g104880).

Figure 2

NBR1-mediated selective autophagy in plant stress responses. The cargo proteins and biological roles of NBR1 in aggrephagy, heat stress memory, antiviral defense and Exo70E2 are well supported by biochemical, molecular and genetic evidence. Studies through analysis of protein localization, gene expression, protein-protein interactions and transgenic overexpression have also suggested possible roles of NBR1 in stress-induced pexophagy, S nutrient response and ABA signaling.