Pexophagy suppresses ROS-induced damage in leaf cells under high-intensity light.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
05 12 2022
05 12 2022
Historique:
received:
06
12
2020
accepted:
18
11
2022
entrez:
5
12
2022
pubmed:
6
12
2022
medline:
11
12
2022
Statut:
epublish
Résumé
Although light is essential for photosynthesis, it has the potential to elevate intracellular levels of reactive oxygen species (ROS). Since high ROS levels are cytotoxic, plants must alleviate such damage. However, the cellular mechanism underlying ROS-induced leaf damage alleviation in peroxisomes was not fully explored. Here, we show that autophagy plays a pivotal role in the selective removal of ROS-generating peroxisomes, which protects plants from oxidative damage during photosynthesis. We present evidence that autophagy-deficient mutants show light intensity-dependent leaf damage and excess aggregation of ROS-accumulating peroxisomes. The peroxisome aggregates are specifically engulfed by pre-autophagosomal structures and vacuolar membranes in both leaf cells and isolated vacuoles, but they are not degraded in mutants. ATG18a-GFP and GFP-2×FYVE, which bind to phosphatidylinositol 3-phosphate, preferentially target the peroxisomal membranes and pre-autophagosomal structures near peroxisomes in ROS-accumulating cells under high-intensity light. Our findings provide deeper insights into the plant stress response caused by light irradiation.
Identifiants
pubmed: 36470866
doi: 10.1038/s41467-022-35138-z
pii: 10.1038/s41467-022-35138-z
pmc: PMC9722907
doi:
Substances chimiques
Reactive Oxygen Species
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7493Informations de copyright
© 2022. The Author(s).
Références
Oikawa, K., Hayashi, M., Hayashi, Y. & Nishimura, M. Re‐evaluation of physical interaction between plant peroxisomes and other organelles using live‐cell imaging techniques. J. Integr. Plant Biol. 61, 836–852 (2019).
Kozaki, A. & Takeba, G. Photorespiration protects C3 plants from photooxidation. Nature 384, 557–560 (1996).
doi: 10.1038/384557a0
Takahashi, S., Bauwe, H. & Badger, M. Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair but not acceleration of damage processes in Arabidopsis. Plant Physiol. 144, 487–494 (2007).
doi: 10.1104/pp.107.097253
Apel, K. & Hirt, H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu. Rev. Plant Biol. 55, 373–399 (2004).
doi: 10.1146/annurev.arplant.55.031903.141701
Corpas, F. J., Barroso, J. B. & del Rı́o, L. A. Peroxisomes as a source of reactive oxygen species and nitric oxide signal molecules in plant cells. Trends Plant Sci. 6, 145–150 (2001).
doi: 10.1016/S1360-1385(01)01898-2
del Río, L. A. & López-Huertas, E. ROS generation in peroxisomes and its role in cell signaling. Plant Cell Physiol. 57, 1364–1376 (2016).
Foyer, C. H., Bloom, A. J., Queval, G. & Noctor, G. Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu. Rev. Plant Biol. 60, 455–484 (2009).
doi: 10.1146/annurev.arplant.043008.091948
Noctor, G. & Foyer, C. H. Intracellular redox compartmentation and ROS-related communication in regulation and signaling. Plant Physiol. 171, 1581–1592 (2016).
doi: 10.1104/pp.16.00346
Sandalio, L. M. & Romero-Puertas, M. C. Peroxisomes sense and respond to environmental cues by regulating ROS and RNS signalling networks. Ann. Bot. 116, 475–485 (2015).
doi: 10.1093/aob/mcv074
Willekens, H. Catalase is a sink for H2O2 and is indispensable for stress defence in C3 plants. EMBO J. 16, 4806–4816 (1997).
doi: 10.1093/emboj/16.16.4806
Shibata, M. et al. Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 25, 4967–4983 (2013).
doi: 10.1105/tpc.113.116947
Zhang, J. et al. A tuberous sclerosis complex signalling node at the peroxisome regulates mTORC1 and autophagy in response to ROS. Nat. Cell Biol. 15, 1186–1196 (2013).
doi: 10.1038/ncb2822
Pérez-Pérez, M. E., Lemaire, S. D. & Crespo, J. L. Reactive oxygen species and autophagy in plants and algae. Plant Physiol. 160, 156–164 (2012).
doi: 10.1104/pp.112.199992
Yoshimoto, K. et al. Organ-specific quality control of plant peroxisomes is mediated by autophagy. J. Cell Sci. https://doi.org/10.1242/jcs.139709 (2014).
doi: 10.1242/jcs.139709
Xie, Z. & Klionsky, D. J. Autophagosome formation: core machinery and adaptations. Nat. Cell Biol. 9, 1102–1109 (2007).
doi: 10.1038/ncb1007-1102
Mizushima, N., Yoshimori, T. & Ohsumi, Y. The role of Atg proteins in autophagosome formation. Annu. Rev. Cell Dev. Biol. 27, 107–132 (2011).
doi: 10.1146/annurev-cellbio-092910-154005
Liu, Y. & Bassham, D. C. Autophagy: pathways for self-eating in plant cells. Annu. Rev. Plant Biol. 63, 215–237 (2012).
doi: 10.1146/annurev-arplant-042811-105441
Ohsumi, Y. Historical landmarks of autophagy research. Cell Res. 24, 9–23 (2014).
doi: 10.1038/cr.2013.169
Farré, J.-C. & Subramani, S. Mechanistic insights into selective autophagy pathways: lessons from yeast. Nat. Rev. Mol. Cell Biol. 17, 537–552 (2016).
doi: 10.1038/nrm.2016.74
Nair, U., Cao, Y., Xie, Z. & Klionsky, D. J. Roles of the lipid-binding motifs of Atg18 and Atg21 in the cytoplasm to vacuole targeting pathway and autophagy. J. Biol. Chem. 285, 11476–11488 (2010).
doi: 10.1074/jbc.M109.080374
Obara, K. & Ohsumi, Y. PtdIns 3-kinase orchestrates autophagosome formation in yeast. J. Lipids 2011, 1–9 (2011).
doi: 10.1155/2011/498768
Oku, M. & Sakai, Y. Pexophagy in yeasts. Biochim. Biophys. Acta - Mol. Cell Res. 1863, 992–998 (2016).
doi: 10.1016/j.bbamcr.2015.09.023
Anding, A. L. & Baehrecke, E. H. Cleaning house: selective autophagy of organelles. Dev. Cell 41, 10–22 (2017).
doi: 10.1016/j.devcel.2017.02.016
Filomeni, G., De Zio, D. & Cecconi, F. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death Differ. 22, 377–388 (2015).
doi: 10.1038/cdd.2014.150
Sinclair, A. M., Trobacher, C. P., Mathur, N., Greenwood, J. S. & Mathur, J. Peroxule extension over ER-defined paths constitutes a rapid subcellular response to hydroxyl stress. Plant J. 59, 231–242 (2009).
doi: 10.1111/j.1365-313X.2009.03863.x
Brunkard, J. O., Runkel, A. M. & Zambryski, P. C. Chloroplasts extend stromules independently and in response to internal redox signals. Proc. Natl Acad. Sci. USA 112, 10044–10049 (2015).
doi: 10.1073/pnas.1511570112
Xiong, Y., Contento, A. L., Nguyen, P. Q. & Bassham, D. C. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol. 143, 291–299 (2007).
doi: 10.1104/pp.106.092106
Kimori, Y., Hikino, K., Nishimura, M. & Mano, S. Quantifying morphological features of actin cytoskeletal filaments in plant cells based on mathematical morphology. J. Theor. Biol. 389, 123–131 (2016).
doi: 10.1016/j.jtbi.2015.10.031
Xiong, Y., Contento, A. L. & Bassham, D. C. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J. 42, 535–546 (2005).
doi: 10.1111/j.1365-313X.2005.02397.x
Krick, R., Tolstrup, J., Appelles, A., Henke, S. & Thumm, M. The relevance of the phosphatidylinositolphosphat-binding motif FRRGT of Atg18 and Atg21 for the Cvt pathway and autophagy. FEBS Lett. 580, 4632–4638 (2006).
doi: 10.1016/j.febslet.2006.07.041
Tamura, N. et al. Atg18 phosphoregulation controls organellar dynamics by modulating its phosphoinositide-binding activity. J. Cell Biol. 202, 685–698 (2013).
doi: 10.1083/jcb.201302067
Vermeer, J. E. M. et al. Visualization of PtdIns3 P dynamics in living plant cells. Plant J. 47, 687–700 (2006).
doi: 10.1111/j.1365-313X.2006.02830.x
de Torres Zabala, M. et al. Chloroplasts play a central role in plant defence and are targeted by pathogen effectors. Nat. Plants 1, 15074 (2015).
doi: 10.1038/nplants.2015.74
Yamauchi, S. et al. Autophagy controls reactive oxygen species homeostasis in guard cells that is essential for stomatal opening. Proc. Natl Acad. Sci. USA 116, 19187–19192 (2019).
doi: 10.1073/pnas.1910886116
Liu, Y., Xiong, Y. & Bassham, D. C. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5, 954–963 (2009).
doi: 10.4161/auto.5.7.9290
Luo, L. et al. Autophagy is rapidly induced by salt stress and is required for salt tolerance in Arabidopsis. Front. Plant Sci. 8, 1459 (2017).
Foyer, C. H. & Noctor, G. Redox sensing and signalling associated with reactive oxygen in chloroplasts, peroxisomes and mitochondria. Physiol. Plant 119, 355–364 (2003).
doi: 10.1034/j.1399-3054.2003.00223.x
Feierabend, J. & Engel, S. Photoinactivation of catalase in vitro and in leaves. Arch. Biochem. Biophys. 251, 567–576 (1986).
doi: 10.1016/0003-9861(86)90365-6
Shang, W. & Feierabend, J. Dependence of catalase photoinactivation in rye leaves on light intensity and quality and characterization of a chloroplast-mediated inactivation in red light. Photosynth. Res. 59, 201–213 (1999).
doi: 10.1023/A:1006139316546
Oikawa, K. et al. Physical interaction between peroxisomes and chloroplasts elucidated by in situ laser analysis. Nat. Plants 1, 15035 (2015).
doi: 10.1038/nplants.2015.35
Polson, H. E. J. et al. Mammalian Atg18 (WIPI2) localizes to omegasome-anchored phagophores and positively regulates LC3 lipidation. Autophagy 6, 506–522 (2010).
doi: 10.4161/auto.6.4.11863
Proikas-Cezanne, T., Takacs, Z., Dönnes, P. & Kohlbacher, O. WIPI proteins: essential PtdIns3 P effectors at the nascent autophagosome. J. Cell Sci. https://doi.org/10.1242/jcs.146258 (2015).
doi: 10.1242/jcs.146258
Izumi, M., Ishida, H., Nakamura, S. & Hidema, J. Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29, 377–394 (2017).
doi: 10.1105/tpc.16.00637
Tekirdag, K. & Cuervo, A. M. Chaperone-mediated autophagy and endosomal microautophagy: joint by a chaperone. J. Biol. Chem. 293, 5414–5424 (2018).
doi: 10.1074/jbc.R117.818237
Mizushima, N. & Komatsu, M. Autophagy: Renovation of cells and tissues. Cell 147, 728–741 (2011).
doi: 10.1016/j.cell.2011.10.026
Cheng, J. et al. Yeast and mammalian autophagosomes exhibit distinct phosphatidylinositol 3-phosphate asymmetries. Nat. Commun. 5, 3207 (2014).
doi: 10.1038/ncomms4207
Roberts, R. & Ktistakis, N. T. Omegasomes: PI3P platforms that manufacture autophagosomes. Essays Biochem. 55, 17–27 (2013).
doi: 10.1042/bse0550017
Nascimbeni, A. C., Codogno, P. & Morel, E. Phosphatidylinositol‐3‐phosphate in the regulation of autophagy membrane dynamics. FEBS J. 284, 1267–1278 (2017).
doi: 10.1111/febs.13987
Stolz, A., Ernst, A. & Dikic, I. Cargo recognition and trafficking in selective autophagy. Nat. Cell Biol. 16, 495–501 (2014).
doi: 10.1038/ncb2979
Carlsson, S. R. & Simonsen, A. Membrane dynamics in autophagosome biogenesis. J. Cell Sci. https://doi.org/10.1242/jcs.141036 (2015).
doi: 10.1242/jcs.141036
Young, P. G. & Bartel, B. Pexophagy and peroxisomal protein turnover in plants. Biochim. Biophys. Acta - Mol. Cell Res. 1863, 999–1005 (2016).
doi: 10.1016/j.bbamcr.2015.09.005
Hamasaki, M. et al. Autophagosomes form at ER–mitochondria contact sites. Nature 495, 389–393 (2013).
doi: 10.1038/nature11910
Le Bars, R., Marion, J., Le Borgne, R., Satiat-Jeunemaitre, B. & Bianchi, M. W. ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants. Nat. Commun. 5, 4121 (2014).
doi: 10.1038/ncomms5121
Zhuang, X. et al. ATG9 regulates autophagosome progression from the endoplasmic reticulum in Arabidopsis. Proc. Natl Acad. Sci. USA 114, E426–E435 (2017).
Kotani, T., Kirisako, H., Koizumi, M., Ohsumi, Y. & Nakatogawa, H. The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. Proc. Natl Acad. Sci. USA 115, 10363–10368 (2018).
doi: 10.1073/pnas.1806727115
Mizushima, N. et al. A protein conjugation system essential for autophagy. Nature 395, 395–398 (1998).
doi: 10.1038/26506
Komatsu, M. et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J. Cell Biol. 169, 425–434 (2005).
doi: 10.1083/jcb.200412022
Goto-Yamada, S. et al. Sucrose starvation induces microautophagy in plant root cells. Front. Plant Sci. 10, 1604 (2019).
Chanoca, A. et al. Anthocyanin vacuolar inclusions form by a microautophagy mechanism. Plant Cell 27, 2545–2559 (2015).
doi: 10.1105/tpc.15.00589
Nakamura, S. & Izumi, M. Regulation of chlorophagy during photoinhibition and senescence: lessons from mitophagy. Plant Cell Physiol. 59, 1135–1143 (2018).
doi: 10.1093/pcp/pcy096
Sieńko, K., Poormassalehgoo, A., Yamada, K. & Goto-Yamada, S. Microautophagy in plants: consideration of its molecular mechanism. Cells 9, 887 (2020).
doi: 10.3390/cells9040887
Subramani, S. A mammalian pexophagy target. Nat. Cell Biol. 17, 1371–1373 (2015).
doi: 10.1038/ncb3253
Motley, A. M., Nuttall, J. M. & Hettema, E. H. Pex3-anchored Atg36 tags peroxisomes for degradation in Saccharomyces cerevisiae. EMBO J. 31, 2852–2868 (2012).
doi: 10.1038/emboj.2012.151
Maehama, T., Taylor, G. S. & Dixon, J. E. PTEN and myotubularin: Novel phosphoinositide phosphatases. Annu. Rev. Biochem. 70, 247–279 (2001).
doi: 10.1146/annurev.biochem.70.1.247
Nguyen, T. N., Padman, B. S. & Lazarou, M. Deciphering the molecular signals of PINK1/Parkin mitophagy. Trends Cell Biol. 26, 733–744 (2016).
doi: 10.1016/j.tcb.2016.05.008
Harper, J. W., Ordureau, A. & Heo, J.-M. Building and decoding ubiquitin chains for mitophagy. Nat. Rev. Mol. Cell Biol. 19, 93–108 (2018).
doi: 10.1038/nrm.2017.129
Mano, S. et al. Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: Dynamic morphology and actin-dependent movement. Plant Cell Physiol. 43, 331–341 (2002).
doi: 10.1093/pcp/pcf037
Zhang, X., Henriques, R., Lin, S.-S., Niu, Q.-W. & Chua, N.-H. Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1, 641–646 (2006).
doi: 10.1038/nprot.2006.97
Ebine, K. et al. A SNARE complex unique to seed plants is required for protein storage vacuole biogenesis and seed development of Arabidopsis thaliana. Plant Cell 20, 3006–3021 (2008).
doi: 10.1105/tpc.107.057711
Arimura, S., Yamamoto, J., Aida, G. P., Nakazono, M. & Tsutsumi, N. Frequent fusion and fission of plant mitochondria with unequal nucleoid distribution. Proc. Natl Acad. Sci. USA 101, 7805–7808 (2004).
doi: 10.1073/pnas.0401077101
Nakagawa, T. et al. Improved gateway binary vectors: High-performance vectors for creation of fusion constructs in transgenic analysis of plants. Biosci. Biotechnol. Biochem. 71, 2095–2100 (2007).
doi: 10.1271/bbb.70216
Sankaran, V. G., Klein, D. E., Sachdeva, M. M. & Lemmon, M. A. High-affinity binding of a FYVE domain to phosphatidylinositol 3-phosphate requires intact phospholipid but not FYVE domain oligomerization. Biochemistry 40, 8581–8587 (2001).
doi: 10.1021/bi010425d
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
doi: 10.1038/nmeth.2019
Asakura, Y. et al. Maize mutants lacking chloroplast FtsY exhibit pleiotropic defects in the biogenesis of thylakoid membranes. Plant Cell 16, 201–214 (2004).
doi: 10.1105/tpc.014787
Yamaguchi, K. & Nishimura, M. Reduction to below threshold levels of glycolate oxidase activities in transgenic tobacco enhances photoinhibition during irradiation. Plant Cell Physiol. 41, 1397–1406 (2000).
doi: 10.1093/pcp/pcd074
Hayashi, Y., Hayashi, M., Hayashi, H., Hara-Nishimura, I. & Nishimura, M. Direct interaction between glyoxysomes and lipid bodies in cotyledons of the Arabidopsis thaliana ped1 mutant. Protoplasma 218, 83–94 (2001).
doi: 10.1007/BF01288364
Tamura, K., Fukao, Y., Iwamoto, M., Haraguchi, T. & Hara-Nishimura, I. Identification and characterization of nuclear pore complex components in Arabidopsis thaliana. Plant Cell 22, 4084–4097 (2011).
doi: 10.1105/tpc.110.079947
Takahashi, D., Li, B., Nakayama, T., Kawamura, Y. & Uemura, M. Shotgun proteomics of plant plasma membrane and microdomain proteins using nano-LC–MS/MS. Methods Mol. Biol. 1072, 481–498 (2014).
doi: 10.1007/978-1-62703-631-3_33
Takahashi, D., Kawamura, Y. & Uemura, M. Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. J. Exp. Bot. 67, 5203–5215 (2016).
doi: 10.1093/jxb/erw279