Abstract
Autophagy is a major catabolic pathway by which eukaryotic cells deliver unnecessary or damaged cytoplasmic material to the vacuole for its degradation and recycling in order to maintain cellular homeostasis. Mounting evidence suggests the existence of a strong link between autophagy and the production of reactive oxygen species in several systems. Here, we review recent studies in algae and plants describing redox control of autophagy and discuss the conserved regulatory proteins that may transmit redox signals to the autophagic machinery.
Communicated by Francisco M. Cánovas
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References
Alvarez C, Garcia I, Moreno I, Perez-Perez ME, Crespo JL, Romero LC, Gotor C (2012) Cysteine-generated sulfide in the cytosol negatively regulates autophagy and modulates the transcriptional profile in Arabidopsis. Plant Cell 24:4621–4634
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, Yoshimoto K (2006) Autophagy in development and stress responses of plants. Autophagy 2:2–11
Blaby-Haas CE, Merchant SS (2012) The ins and outs of algal metal transport. Biochim Biophys Acta 1823:1531–1552
Blaby-Haas CE, Merchant SS (2013) Iron sparing and recycling in a compartmentalized cell. Curr Opin Microbiol 16:677–685
Chaouch S, Queval G, Noctor G (2012) AtRbohF is a crucial modulator of defence-associated metabolism and a key actor in the interplay between intracellular oxidative stress and pathogenesis responses in Arabidopsis. Plant J 69:613–627
Chen X, Tian D, Kong X, Chen Q, E F AA, Hu X, Jia A (2016) The role of nitric oxide signalling in response to salt stress in Chlamydomonas reinhardtii. Planta 244:651–669
Diaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL (2008) The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 4:851–865
Farmer LM, Rinaldi MA, Young PG, Danan CH, Burkhart SE, Bartel B (2013) Disrupting autophagy restores peroxisome function to an Arabidopsis lon2 mutant and reveals a role for the LON2 protease in peroxisomal matrix protein degradation. Plant Cell 25:4085–4100
Glaesener AG, Merchant SS, Blaby-Haas CE (2013) Iron economy in Chlamydomonas reinhardtii. Front Plant Sci 4:337
Grossman AR, Lohr M, Im CS (2004) Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 38:119–173
Han S, Wang Y, Zheng X, Jia Q, Zhao J, Bai F, Hong Y, Liu Y (2015) Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana. Plant Cell 27:1316–1331
He C, Klionsky DJ (2009) Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43:67–93
Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, Mizushima N, Tanida I, Kominami E, Ohsumi M, Noda T, Ohsumi Y (2000) A ubiquitin-like system mediates protein lipidation. Nature 408:488–492
Inwood W, Yoshihara C, Zalpuri R, Kim KS, Kustu S (2008) The ultrastructure of a Chlamydomonas reinhardtii mutant strain lacking phytoene synthase resembles that of a colorless alga. Mol Plant 1:925–937
Izumi M, Ishida H, Nakamura S, Hidema J (2017) Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell. pii: tpc.00637.2016. doi: 10.1105/tpc.16.00637
Jamers A, Blust R, De Coen W, Griffin JL, Jones OA (2013) An omics based assessment of cadmium toxicity in the green alga Chlamydomonas reinhardtii. Aquat Toxicol 126:355–364
Kim J, Lee H, Lee HN, Kim SH, Shin KD, Chung T (2013) Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell 25:4956–4966
Laureano-Marin AM, Moreno I, Romero LC, Gotor C (2016) Negative regulation of autophagy by sulfide is independent of reactive oxygen species. Plant Physiol 171:1378–1391
Li F, Vierstra RD (2012) Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–537
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260
Liu Y, Bassham DC (2012) Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63:215–237
Liu Y, Xiong Y, Bassham DC (2009) Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5:954–963
Liu Y, Burgos JS, Deng Y, Srivastava R, Howell SH, Bassham DC (2012) Degradation of the endoplasmic reticulum by autophagy during endoplasmic reticulum stress in Arabidopsis. Plant Cell 24:4635–4651
Marshall RS, Li F, Gemperline DC, Book AJ, Vierstra RD (2015) Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol Cell 58:1053–1066
Masclaux-Daubresse C, Clement G, Anne P, Routaboul JM, Guiboileau A, Soulay F, Shirasu K, Yoshimoto K (2014) Stitching together the multiple dimensions of autophagy using metabolomics and transcriptomics reveals impacts on metabolism, development, and plant responses to the environment in Arabidopsis. Plant Cell 26:1857–1877
Mizushima N, Yoshimori T, Ohsumi Y (2011) The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27:107–132
Niyogi KK, Bjorkman O, Grossman AR (1997) The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci U S A 94:14162–14167
Okamoto K, Kondo-Okamoto N, Ohsumi Y (2009) Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17:87–97
Overmyer K, Brosche M, Kangasjarvi J (2003) Reactive oxygen species and hormonal control of cell death. Trends Plant Sci 8:335–342
Ozgur R, Turkan I, Uzilday B, Sekmen AH (2014) Endoplasmic reticulum stress triggers ROS signalling, changes the redox state, and regulates the antioxidant defence of Arabidopsis thaliana. J Exp Bot 65:1377–1390
Perez-Martin M, Perez-Perez ME, Lemaire SD, Crespo JL (2014) Oxidative stress contributes to autophagy induction in response to endoplasmic reticulum stress in Chlamydomonas reinhardtii. Plant Physiol 166:997–1008
Perez-Martin M, Blaby-Haas CE, Perez-Perez ME, Andres-Garrido A, Blaby IK, Merchant SS, Crespo JL (2015) Activation of autophagy by metals in Chlamydomonas reinhardtii. Eukaryot Cell 14:964–973
Perez-Perez ME, Crespo JL (2010) Autophagy in the model alga Chlamydomonas reinhardtii. Autophagy 6:562–563
Perez-Perez ME, Florencio FJ, Crespo JL (2010) Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii. Plant Physiol 152:1874–1888
Perez-Perez ME, Lemaire SD, Crespo JL (2012a) Reactive oxygen species and autophagy in plants and algae. Plant Physiol 160:156–164
Perez-Perez ME, Couso I, Crespo JL (2012b) Carotenoid deficiency triggers autophagy in the model green alga Chlamydomonas reinhardtii. Autophagy 8:376–388
Perez-Perez ME, Zaffagnini M, Marchand CH, Crespo JL, Lemaire SD (2014) The yeast autophagy protease Atg4 is regulated by thioredoxin. Autophagy 10:1953–1964
Perez-Perez ME, Lemaire SD, Crespo JL (2016) Control of autophagy in Chlamydomonas is mediated through redox-dependent inactivation of the ATG4 protease. Plant Physiol 172:2219–2234
Reumann S, Bartel B (2016) Plant peroxisomes: recent discoveries in functional complexity, organelle homeostasis, and morphological dynamics. Curr Opin Plant Biol 34:17–26
Sandmann G, Albrecht M (1990) Accumulation of colorless carotenes and derivatives during interaction of bleaching herbicides with phytoene desaturation. Z Naturforsch C 45:487–491
Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z (2007) Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 26:1749–1760
Sharma SS, Dietz KJ (2009) The relationship between metal toxicity and cellular redox imbalance. Trends Plant Sci 14:43–50
Shemi A, Ben-Dor S, Vardi A (2015) Elucidating the composition and conservation of the autophagy pathway in photosynthetic eukaryotes. Autophagy 11:701–715
Shibata M, Oikawa K, Yoshimoto K, Kondo M, Mano S, Yamada K, Hayashi M, Sakamoto W, Ohsumi Y, Nishimura M (2013) Highly oxidized peroxisomes are selectively degraded via autophagy in Arabidopsis. Plant Cell 25:4967–4983
Stoiber TL, Shafer MM, Armstrong DE (2013) Induction of reactive oxygen species in chlamydomonas reinhardtii in response to contrasting trace metal exposures. Environ Toxicol 28:516–523
Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R (2011) Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 14:691–699
Thompson AR, Vierstra RD (2005) Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8:165–173
Torres MA, Jones JD, Dangl JL (2005) Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nat Genet 37:1130–1134
Torres MA, Jones JD, Dangl JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiol 141:373–378
Tsukada M, Ohsumi Y (1993) Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae. FEBS Lett 333:169–174
Tu BP, Weissman JS (2004) Oxidative protein folding in eukaryotes: mechanisms and consequences. J Cell Biol 164:341–346
Walter P, Ron D (2011) The unfolded protein response: from stress pathway to homeostatic regulation. Science 334:1081–1086
Woo J, Park E, Dinesh-Kumar SP (2014) Differential processing of Arabidopsis ubiquitin-like Atg8 autophagy proteins by Atg4 cysteine proteases. Proc Natl Acad Sci U S A 111:863–868
Xiong Y, Contento AL, Nguyen PQ, Bassham DC (2007) Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143:291–299
Yorimitsu T, Nair U, Yang Z, Klionsky DJ (2006) Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281:30299–30304
Yoshimoto K, Jikumaru Y, Kamiya Y, Kusano M, Consonni C, Panstruga R, Ohsumi Y, Shirasu K (2009) Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 21:2914–2927
Acknowledgments
This work was supported in part by Ministerio de Economía y Competitividad grants BFU2015-68216-P and BIO2015-74432-JIN to JLC and MEPP, respectively.
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Pérez-Pérez, M.E., Couso, I., Domínguez-González, M., Lemaire, S.D., Crespo, J.L. (2017). Redox Control of Autophagy in Photosynthetic Organisms. In: Cánovas, F., Lüttge, U., Matyssek, R. (eds) Progress in Botany Vol. 79. Progress in Botany, vol 79. Springer, Cham. https://doi.org/10.1007/124_2017_6
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DOI: https://doi.org/10.1007/124_2017_6
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