Autophagy Plays a Role in Chloroplast Degradation during Senescence in Individually Darkened Leaves

Wada, Shin‐Ichiro; Ishida, Hideyuki; Izumi, Masanori; Yoshimoto, Kohki; Ohsumi, Yoshinori; Mae, Tadahiko; Makino, Amane

doi:10.1104/pp.108.130013

Cited by 318 publications

(353 citation statements)

References 39 publications

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“…ATG5 and other core ATG genes are involved in the degradation of chloroplasts (Ishida et al, 2008;Wada et al, 2009), amyloplasts (Nakayama et al, 2012), and endoplasmic reticulum (ER) (Liu et al, 2012). However, whether the core ATG genes are also required for the degradation of other types of organelles, such as peroxisomes, mitochondria, and oil bodies, has not been clear.…”

Section: Discussionmentioning

confidence: 99%

“…CA inhibits degradation in the vacuole by blocking the acidification of the vacuole and has been used to stabilize autophagic cargoes in the vacuole (Yoshimoto et al, 2004;Wada et al, 2009;Liu et al, 2012). If peroxisomes are autophagic cargoes targeted into the vacuole for degradation, CA may stabilize peroxisomes that would be degraded otherwise.…”

Section: Peroxisomal Proteins Are Targeted To the Central Vacuole Formentioning

confidence: 99%

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Autophagy-Related Proteins Are Required for Degradation of Peroxisomes inArabidopsisHypocotyls during Seedling Growth

et al. 2013

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Plant peroxisomes play a pivotal role during postgerminative growth by breaking down fatty acids to provide fixed carbons for seedlings before the onset of photosynthesis. The enzyme composition of peroxisomes changes during the transition of the seedling from a heterotrophic to an autotrophic state; however, the mechanisms for the degradation of obsolete peroxisomal proteins remain elusive. One candidate mechanism is autophagy, a bulk degradation pathway targeting cytoplasmic constituents to the lytic vacuole. We present evidence supporting the autophagy of peroxisomes in Arabidopsis thaliana hypocotyls during seedling growth. Mutants defective in autophagy appeared to accumulate excess peroxisomes in hypocotyl cells. When degradation in the vacuole was pharmacologically compromised, both autophagic bodies and peroxisomal markers were detected in the wild-type vacuole but not in that of the autophagy-incompetent mutants. On the basis of the genetic and cell biological data we obtained, we propose that autophagy is important for the maintenance of peroxisome number and cell remodeling in Arabidopsis hypocotyls.

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Section: Discussionmentioning

confidence: 99%

Section: Peroxisomal Proteins Are Targeted To the Central Vacuole Formentioning

confidence: 99%

Autophagy-Related Proteins Are Required for Degradation of Peroxisomes inArabidopsisHypocotyls during Seedling Growth

et al. 2013

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“…During senescence of Arabidopsis leaves kept in darkness (a form of carbon starvation for photosynthetic autotrophs), autophagy seems to be responsible for degradation of the chloroplasts, 24 and root development also becomes impaired in different atg mutants during nitrogen starvation. 18,20 Perhaps not surprisingly, autophagy functions in the removal of oxidized proteins during oxidative stress in Arabidopsis, 25 and downregulation of ATG18a using interference RNA (RNAi) renders plants more sensitive to salt and drought stress.…”

Section: Autophagy In Plantsmentioning

confidence: 99%

“…24,25 Such accumulated cellular debris may well disrupt homeostasis, leading to pleiotropic effects including accumulation of danger-associated molecular patterns (DAMPs) 68 triggering SA accumulation, and subsequent production of secreted pathogenesis-related (PR) proteins accompanied by ER stress. Autophagy is required to dampen the deleterious effects caused by ER stress and it is well described in other models that atg mutants die upon increased ER stress.…”

Section: Autophagy In Plant Immunity and Hypersensitive Cell Deathmentioning

confidence: 99%

Role of autophagy in disease resistance and hypersensitive response-associated cell death

Hofius

Munch²,

Bressendorff³

et al. 2011

Cell Death Differ

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Ancient autophagy pathways are emerging as key defense modules in host eukaryotic cells against microbial pathogens. Apart from actively eliminating intracellular intruders, autophagy is also responsible for cell survival, for example by reducing the deleterious effects of endoplasmic reticulum stress. At the same time, autophagy can contribute to cellular suicide. The concurrent engagement of autophagy in these processes during infection may sometimes mask its contribution to differing pro-survival and pro-death decisions. The importance of autophagy in innate immunity in mammals is well documented, but how autophagy contributes to plant innate immunity and cell death is not that clear. A few research reports have appeared recently to shed light on the roles of autophagy in plant-pathogen interactions and in disease-associated host cell death. We present a first attempt to reconcile the results of this research. Cell Death and Differentiation (2011) 18, 1257-1262 doi:10.1038/cdd.2011 published online 29 April 2011 Autophagy mediates the degradation of bulk proteins and is also involved in the clearance of damaged organelles, insoluble protein aggregates and lipids. 1-3 Autophagic digestion and recycling can occur as a survival mechanism to maintain cellular homeostasis and to respond to environmental stresses, such as nutrient depletion or pathogen attack, but may also function as a mediator and/or mechanism of programmed cell death. [4][5][6][7][8] Several subtypes of autophagy are described, but macroautophagy (hereafter termed autophagy) is the most extensively studied 9 and will be the only form described here. The process is characterized by the formation of large, double-membrane vesicles called autophagosomes. These structures arise from expanding single membranes (termed phagophores), which enclose cytoplasmic material and organelles for degradation. Completed autophagosomes fuse with the vacuole/lysosome to release the inner singlemembrane vesicle, called the autophagic body, into the lumen for hydrolytic degradation and recycling. 2,10 The mechanism of autophagy is conserved in yeast, plants and metazoans, and involves the action of canonical autophagy related genes (ATG) that synthesize and coordinate membrane rearrangements to allow cellular catabolism. 1,2 The core sets of ATG genes seem to be present in all eukaryotes and to be essential for the autophagy pathway (Figure 1). For instance, induction of autophagy requires the negative regulator target of rapamycin (TOR) kinase and the ATG1 kinase complex, which control the activity of the phosphatidylinositol 3-kinase complex containing, for example, ATG6/Beclin1. 11 Initiation and completion of autophagosome formation involves two ubiquitin-like conjugation systems to produce ATG12-ATG5 and ATG8-phosphatidylethanolamine (ATG8-PE) conjugates. ATG8-PE conjugation involves the cysteine proteinase ATG4 and the E1-like protein ATG7, and lipidated ATG8 is linked to and translocated with autophagosomes to the vacuole. 12 Therefore, conversion from solu...

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“…It is likely that damaged proteins in chloroplasts are mobilized quickly in F plants while CMS plants accumulate oxidized proteins in absence of reproductive sinks. Chloroplastic proteins are major source of nitrogen in leaves for mobilization towards the developing seeds/plant parts (Wada et al 2009) and reproductive sinks drive N mobilization from leaves to grains Khanna-Chopra 2004, 2009;del Molino et al 1995;Mǿller et al 2007). It is tempting to speculate that the better antioxidant defense in chloroplasts of the CMS plants may help in maintaining chloroplasts integrity for a longer period of time than F plants during senescence.…”

Section: Discussionmentioning

confidence: 99%

Delayed expression of SAGs correlates with longevity in CMS wheat plants compared to its fertile plants

Semwal

Singh

Khanna‐Chopra

2014

Physiol Mol Biol Plants

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Reproductive sinks regulate monocarpic senescence in crop plants. Monocarpic senescence was studied in wheat fertile (cv. HW 2041) and its isonuclear cytoplasmic male sterile (CMS) line. CMS plants exhibited slower rate of senescence accompanied by longer green leaf area duration and slower deceleration in chlorophyll, protein content, P N and rubisco content coupled with lower protease activities than fertile (F) plants. CMS plants also exhibited lower ROS levels and less membrane damage than F plants. CMS plants maintained better antioxidant defense, less oxidative damage in chloroplast and higher transcript levels of both rbcL and rbcS genes during senescence than F plants. F plants exhibited early induction and higher expression of SAGs like serine and cysteine proteases, glutamine synthetases GS1 and GS2, WRKY53 transcription factor and decline in transcript levels of CAT1 and CAT2 genes than CMS plants. Hence, using genetically fertile and its CMS line of wheat it is confirmed that delayed senescence in the absence of reproductive sinks is linked with slower protein oxidation, rubisco degradation and delayed activation of SAGs. Better antioxidant defense in chloroplasts at later stages of senescence was able to mitigate the deleterious effects of ROS in CMS plants. We propose that delayed increase in ROS in cytoplasmic male sterile wheat plants resulted in delayed activation of WRKY53, SAGs and the associated biochemical changes than fertile plants.

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Autophagy Plays a Role in Chloroplast Degradation during Senescence in Individually Darkened Leaves

Cited by 318 publications

References 39 publications

Autophagy-Related Proteins Are Required for Degradation of Peroxisomes inArabidopsisHypocotyls during Seedling Growth

Autophagy-Related Proteins Are Required for Degradation of Peroxisomes inArabidopsisHypocotyls during Seedling Growth

Role of autophagy in disease resistance and hypersensitive response-associated cell death

Delayed expression of SAGs correlates with longevity in CMS wheat plants compared to its fertile plants

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