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Roles of Autophagy in Chloroplast Recycling☆

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Roles of Autophagy in Chloroplast Recycling☆ View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Biochimica et Biophysica Acta 1837 (2014) 512–521 Contents lists available at ScienceDirect Biochimica et Biophysica Acta journal homepage: www.elsevier.com/locate/bbabio Review Roles of autophagy in chloroplast recycling☆ Hiroyuki Ishida a,⁎, Masanori Izumi b,ShinyaWadaa, Amane Makino a,c a Graduate School of Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan b Department of Environmental Life Sciences, Graduate School of Life Sciences, Tohoku University, Katahira, Aoba-ku, Sendai 980-8577, Japan c Core Research for Evolutional Science and Technology (CREST), Japan Science and Technology Agency, Chiyoda-ku, Tokyo 102-0076, Japan article info abstract Article history: Chloroplasts are the primary energy suppliers for plants, and much of the total leaf nitrogen is distributed to these Received 29 July 2013 organelles. During growth and reproduction, chloroplasts in turn represent a major source of nitrogen to be re- Received in revised form 1 November 2013 covered from senescing leaves and used in newly-forming and storage organs. Chloroplast proteins also can be Accepted 7 November 2013 an alternative substrate for respiration under suboptimal conditions. Autophagy is a process of bulk degradation Available online 19 November 2013 and nutrient sequestration that is conserved in all eukaryotes. Autophagy can selectively target chloroplasts as whole organelles and or as Rubisco-containing bodies that are enclosed by the envelope and specifically contain Keywords: Autophagy the stromal portion of the chloroplast. Although information is still limited, recent work indicates that chloroplast Chloroplast recycling via autophagy plays important roles not only in developmental processes but also in organelle quality Leaf senescence control and adaptation to changing environments. This article is part of a Special Issue entitled: Dynamic and Nutrient recycling ultrastructure of bioenergetic membranes and their components. Rubisco © 2013 Elsevier B.V. All rights reserved. 1. Introduction are remobilized. During leaf senescence, Rubisco and other chloroplast proteins are gradually degraded as a major source of nitrogen for Chloroplasts are the characteristic organelles of plants and photoauto- recycling, and this degradation correlates with a decline in photosynthetic trophs. In addition to performing photosynthesis, chloroplasts are central activity [6–8]. Additionally, these proteins can be degraded under star- to plant metabolism. For example, assimilation of nutrients and biosyn- vation conditions caused by darkness, with their carbon skeletons thesis of various metabolites such as amino acids, fatty acids, pigments serving as substrates for respiration [6,9]. As the levels of the inner and hormones, occur in chloroplasts. During the vegetative growth components decline, chloroplasts gradually shrink and transform into stage, the majority of plant nitrogen and other nutrients are distributed gerontoplasts, in which thylakoid membranes are disintegrated and to leaves [1,2]. Further, approximately 80% of the total leaf nitrogen is plastoglobules accumulate, and the cellular population of chloroplasts found within chloroplasts, mainly as photosynthetic proteins, in C3 plants concomitantly declines. [3]. Around 70% of chloroplast nitrogen is present in the stroma and the The vacuole in leaf mesophyll cells occupies as much as 80% to over remaining portion is in the thylakoid membrane. The chloroplast 90% of the total cell volume and is rich in a wide range of lytic hydrolases carbon-fixing enzyme Rubisco (ribulose-1,5-bisphosphate carboxylase/ [10]. In fact, most or all of the proteolytic activity against Rubisco has oxygenase) is exceptionally abundant, accounting for 10 to 30% of the been found in the vacuolar fraction [11], and several vacuolar cysteine leaf nitrogen [4,5]. In addition, around 7% of leaf nitrogen is found in proteases are induced in a senescence-associated manner [12].Studies the light-harvesting chlorophyll a/b protein of photosystem II (LHCII) in in the early 1980s led to the proposal that sequential degradation of the thylakoid membrane [5]. chloroplasts within the vacuole serves as the major pathway for chloro- Because plants are sessile, efficient use and recycling of assimilated plast protein degradation in senescing leaves [11,13]. Under electron nutrients are particularly important for their survival and fitness under microscopy, chloroplasts appear to be either within the vacuole or with- ever-changing environments. Senescence represents the final develop- in invaginations of the tonoplast in mesophyll protoplasts isolated from mental stage and a form of programmed cell death in each organ of plants. wheat (Triticum aestivum) leaves undergoing darkness-induced senes- Leaf senescence can be viewed as primarily a process through which cence [13]. Based on those findings, the authors proposed that chloro- cellular macromolecules are actively degraded and their components plasts were taken up in the vacuole by ‘a phagocytic-type mechanism’. The process of delivery of cytoplasmic components such as proteins and organelles to the vacuole for degradation is now widely recognized ☆ This article is part of a Special Issue entitled: Dynamic and ultrastructure of bioenergetic as autophagy. membranes and their components. The decline in Rubisco protein levels is much faster than that of chlo- ⁎ Corresponding author at: Department of Applied Plant Science, Graduate School of roplast population size during senescence [8,14,15]. Similarly, the de- Agricultural Sciences, Tohoku University, Tsutsumidori-Amamiyamachi, Aoba-ku, Sendai 981-8555, Japan. Tel.: +81 22 717 8767; fax: +81 22 717 8765. creases in major chloroplast proteins do not proceed in parallel; Rubisco E-mail address: [email protected] (H. Ishida). decreasesfasterthandoesLHCII,forexample[16,17]. These two proteins 0005-2728/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.bbabio.2013.11.009 H. Ishida et al. / Biochimica et Biophysica Acta 1837 (2014) 512–521 513 are synthesized mainly during leaf expansion and turn over less after that Cvt complex to the pre-autophagosomal structure (PAS), where the [18,19]. These results indicate that alternative pathways or mechanisms Cvt vesicle is formed [29,37,38]. Atg11 is also important for pexophagy other than autophagy of entire chloroplasts must function in Rubisco and mitophagy [37,39]. During starvation-induced autophagy, Atg17, degradation. Accordingly, much effort in the study of Rubisco degrada- Atg29, and Atg31 are essential as regulators to form the Atg1 kinase tion has been focused on chloroplast proteases rather than autophagy complex, which is required for the induction of autophagosome forma- [20–23]. It is now evident that a number of proteases inside chloroplasts tion. Here, the target of rapamycin (TOR) kinase is known to be an up- play crucial and diverse roles in chloroplast development and mainte- stream negative regulator of the Atg 1 complex [40,41]. Under nutrient- nance. Recent genome-wide studies have revealed the existence of pro- rich conditions, the TOR complex 1 (TORC1) hyperphosphorylates teases of prokaryotic origin in chloroplasts. Of these, ATP-dependent Atg13, promoting the dissociation of the Atg1 kinase complex. Under proteases such as Clp, FtsH, and Lon are considered to be the major en- starvation conditions, TORC1 is inactivated, Atg13 is rapidly dephos- zymes involved in the gradual degradation of proteins into oligopeptides phorylated, the Atg1 complex is formed, and autophagy is induced. and amino acids [24]. Some of these proteases could play important roles in the senescence-associated bulk degradation of chloroplast proteins, 2.2. Autophagy in plants but whether this is the case remains controversial [25,26]. Plant autophagy has long been studied by morphological observa- 2. Autophagy tion using microscopy [33]. More recently, initial genome-wide studies opened the door to molecular analysis of plant autophagy by identifying 2.1. Lessons from yeast a number of genes homologous to yeast ATGs and some of their knock- out mutants in Arabidopsis (Arabidopsis thaliana) [42,43].Although Autophagy is an evolutionarily conserved system for bulk degra- Arabidopsis does not have homologs of the subtype-specific ATGs [44], dation of intracellular components in eukaryotes. The mechanism of the Arabidopsis genome contains homologs of almost all core ATGs autophagy has been particularly well studied in yeast species, in identified in yeast [33,45].TheonlyexceptionisATG14,whichisalso which cytosol, sometimes including entire organelles, is engulfed missing in rice (Ozyza sativa)andChlamydomonas (Chlamydomonas in membrane-bound vesicles [27]. These vesicles are delivered to reinhardtii) [45]. Several Arabidopsis ATG homologs are present in mul- lytic compartments, namely vacuoles or lysosomes, where the vesicles tiple copies, and some of those are functionally redundant [46,47].The and their contents are degraded by a variety of resident hydrolases. roles of Arabidopsis ATGs have been studied using T-DNA insertional Two morphologically distinct forms of autophagy, called microautophagy knock-out mutants and RNA interference knockdown mutants. In addi- and macroautophagy, have been observed in wide range of organisms tion, a live-cell system for monitoring autophagy in plants
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