Plant autophagy—more than a starvation response

Autophagy is a conserved mechanism for the degradation of cellular contents in order to recycle nutrients or break down damaged or toxic material. This occurs by the uptake of cytoplasmic constituents into the vacuole, where they are degraded by vacuolar hydrolases. In plants, autophagy has been known for some time to be important for nutrient remobilization during sugar and nitrogen starvation and leaf senescence, but recent research has uncovered additional crucial roles for plant autophagy. These roles include the degradation of oxidized proteins during oxidative stress, disposal of protein aggregates, and possibly even removal of damaged proteins and organelles during normal growth conditions as a housekeeping function. A surprising regulatory function for autophagy in programmed cell death during the hypersensitive response to pathogen infection has also been identified.

Introduction

Autophagy (‘self-eating’) is a universal mechanism in eukaryotic cells for digestion of cell contents to recycle needed nutrients, degrade damaged or toxic components, or to reclaim cellular materials as a precursor to cell death. In plants, two major autophagic pathways have been described, microautophagy and macroautophagy [1]. In microautophagy, material is engulfed directly by the vacuole via invagination of the tonoplast, followed by pinching off of the membrane to release a vesicle containing the cytoplasmic constituents inside the vacuole lumen. Microautophagy-like processes have been observed during the deposition of storage proteins in developing wheat seeds [2, 3] and release of rubber particles into the vacuole [4], though these processes do not result in immediate degradation of the material deposited into the vacuole. Microautophagy also occurs in some species during seed germination for degradation of starch granules and storage protein in vacuoles [5, 6]. Macroautophagy, by contrast, is initiated in the cytoplasm with the formation of cup-shaped membranes of unknown source that enclose the material to be degraded. The membranes elongate and eventually fuse together to produce a double-membrane autophagosome containing cytoplasmic material. The outer autophagosomal membrane fuses with the tonoplast, releasing an autophagic body consisting of the inner membrane and contents into the vacuole. Vacuolar acid hydrolases then degrade the autophagic body, and the degradation products are presumably transported back to the cytosol [1]. The functions of macroautophagy in suspension cultures and whole plants in response to sucrose and nitrogen starvation and during senescence have been well described for a number of plant species (for example, see references [7, 8, 9, 10]). The recent development of markers to rapidly and easily detect the occurrence of autophagy in plant cells by the specific labeling of autophagosomes has facilitated the study of autophagy. These markers include a fusion of green fluorescent protein (GFP) with the autophagosome-localized protein ATG8 [11, 12, 13] and the acidotrophic fluorescent dyes monodansylcadaverine (MDC [11]) and LysoTracker Red [14]. In this review, I will summarize advances over the past two years in our understanding of macroautophagy, hereafter simply termed autophagy, and in particular focus on additional physiological roles for autophagy in plants that are now coming to light.