Carotenoid deficiency triggers autophagy in the model green alga Chlamydomonas reinhardtii

References

• Murchie EH, Niyogi KK. Manipulation of photoprotection to improve plant photosynthesis. Plant Physiol 2011; 155:86 - 92; http://dx.doi.org/10.1104/pp.110.168831; PMID: 21084435
   PubMed Web of Science ®Google Scholar
• Rochaix JD. Assembly of the photosynthetic apparatus. Plant Physiol 2011; 155:1493 - 500; http://dx.doi.org/10.1104/pp.110.169839; PMID: 21239619
   PubMed Web of Science ®Google Scholar
• Rochaix JD. Regulation of photosynthetic electron transport. Biochim Biophys Acta 2011; 1807:375 - 83; http://dx.doi.org/10.1016/j.bbabio.2010.11.010; PMID: 21118674
   PubMed Web of Science ®Google Scholar
• Grossman AR, Lohr M, Im CS. Chlamydomonas reinhardtii in the landscape of pigments. Annu Rev Genet 2004; 38:119 - 73; http://dx.doi.org/10.1146/annurev.genet.38.072902.092328; PMID: 15568974
   PubMed Web of Science ®Google Scholar
• Lohr M. Carotenoids. In: Stern DB, ed. The Chlamydomonas Sourcebook Organellar and Metabolic Processes. Amsterdam: Academic Press, 2009:799-817.
   Google Scholar
• Boussiba S. Carotenogenesisin the green alga Haematococcus pluvialis: cellular physiology and stress response. Physiol Plant 2000; 108:111 - 7; http://dx.doi.org/10.1034/j.1399-3054.2000.108002111.x
   Web of Science ®Google Scholar
• Del Campo JA, Garcia-Gonzalez M, Guerrero MG. Outdoor cultivation of microalgae for carotenoid production: current state and perspectives. Appl Microbiol Biotechnol 2007; 74:1163 - 74; http://dx.doi.org/10.1007/s00253-007-0844-9; PMID: 17277962
   PubMed Web of Science ®Google Scholar
• Havaux M, Niyogi KK. The violaxanthin cycle protects plants from photooxidative damage by more than one mechanism. Proc Natl Acad Sci USA 1999; 96:8762 - 7; http://dx.doi.org/10.1073/pnas.96.15.8762; PMID: 10411949
   PubMed Web of Science ®Google Scholar
• Niyogi KK, Bjorkman O, Grossman AR. The roles of specific xanthophylls in photoprotection. Proc Natl Acad Sci USA 1997; 94:14162 - 7; http://dx.doi.org/10.1073/pnas.94.25.14162; PMID: 9391170
   PubMed Web of Science ®Google Scholar
• Peterman EJ, Gradinaru CC, Calkoen F, Borst JC, van Grondelle R, van Amerongen H. Xanthophylls in light-harvesting complex II of higher plants: light harvesting and triplet quenching. Biochemistry 1997; 36:12208 - 15; http://dx.doi.org/10.1021/bi9711689; PMID: 9315858
   PubMed Web of Science ®Google Scholar
• Sarry JE, Montillet JL, Sauvaire Y, Havaux M. The protective function of the xanthophyll cycle in photosynthesis. FEBS Lett 1994; 353:147 - 50; http://dx.doi.org/10.1016/0014-5793(94)01028-5; PMID: 7926040
   PubMed Web of Science ®Google Scholar
• Armstrong GA, Hearst JE. Carotenoids 2: Genetics and molecular biology of carotenoid pigment biosynthesis. FASEB J 1996; 10:228 - 37; PMID: 8641556
   PubMed Web of Science ®Google Scholar
• Cazzonelli CI, Pogson BJ. Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 2010; 15:266 - 74; http://dx.doi.org/10.1016/j.tplants.2010.02.003; PMID: 20303820
   PubMed Web of Science ®Google Scholar
• Cunningham FX, Gantt E. Genes and Enzymes of Carotenoid Biosynthesis in Plants. Annu Rev Plant Physiol Plant Mol Biol 1998; 49:557 - 83; http://dx.doi.org/10.1146/annurev.arplant.49.1.557; PMID: 15012246
   PubMed Web of Science ®Google Scholar
• Hirschberg J. Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 2001; 4:210 - 8; http://dx.doi.org/10.1016/S1369-5266(00)00163-1; PMID: 11312131
   PubMed Web of Science ®Google Scholar
• Sager R, Zalokar M. Pigments and photosynthesis in a carotenoid-deficient mutant of Chlamydomonas. Nature 1958; 182:98 - 100; http://dx.doi.org/10.1038/182098a0; PMID: 13566193
   PubMed Web of Science ®Google Scholar
• Harris EH. Chlamydomonas as a Model Organism. Annu Rev Plant Physiol Plant Mol Biol 2001; 52:363 - 406; http://dx.doi.org/10.1146/annurev.arplant.52.1.363; PMID: 11337403
   PubMed Web of Science ®Google Scholar
• Waters MT, Langdale JA. The making of a chloroplast. EMBO J 2009; 28:2861 - 73; http://dx.doi.org/10.1038/emboj.2009.264; PMID: 19745808
   PubMed Web of Science ®Google Scholar
• McCarthy SS, Kobayashi MC, Niyogi KK. White mutants of Chlamydomonas reinhardtii are defective in phytoene synthase. Genetics 2004; 168:1249 - 57; http://dx.doi.org/10.1534/genetics.104.030635; PMID: 15579683
   PubMed Web of Science ®Google Scholar
• Xiong Y, Contento AL, Nguyen PQ, Bassham DC. Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 2007; 143:291 - 9; http://dx.doi.org/10.1104/pp.106.092106; PMID: 17098847
   PubMed Web of Science ®Google Scholar
• Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 2009; 10:458 - 67; http://dx.doi.org/10.1038/nrm2708; PMID: 19491929
   PubMed Web of Science ®Google Scholar
• Xie Z, Klionsky DJ. Autophagosome formation: core machinery and adaptations. Nat Cell Biol 2007; 9:1102 - 9; http://dx.doi.org/10.1038/ncb1007-1102; PMID: 17909521
   PubMed Web of Science ®Google Scholar
• Tsukada M, Ohsumi Y. Isolation and characterization of autophagy-defective mutants of Saccharomyces cerevisiae.. FEBS Lett 1993; 333:169 - 74; http://dx.doi.org/10.1016/0014-5793(93)80398-E; PMID: 8224160
   PubMed Web of Science ®Google Scholar
• Bassham DC. Plant autophagy–more than a starvation response. Curr Opin Plant Biol 2007; 10:587 - 93; http://dx.doi.org/10.1016/j.pbi.2007.06.006; PMID: 17702643
   PubMed Web of Science ®Google Scholar
• Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y, Olsen LJ, et al. Autophagy in development and stress responses of plants. Autophagy 2006; 2:2 - 11; PMID: 16874030
   PubMed Web of Science ®Google Scholar
• Díaz-Troya S, Perez-Perez ME, Florencio FJ, Crespo JL. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 2008; 4:851 - 65; PMID: 18670193
   PubMed Web of Science ®Google Scholar
• Bassham DC. Function and regulation of macroautophagy in plants. Biochim Biophys Acta 2009; 1793:1397 - 403; http://dx.doi.org/10.1016/j.bbamcr.2009.01.001; PMID: 19272302
   PubMed Web of Science ®Google Scholar
• Ichimura Y, Kirisako T, Takao T, Satomi Y, Shimonishi Y, Ishihara N, et al. A ubiquitin-like system mediates protein lipidation. Nature 2000; 408:488 - 92; http://dx.doi.org/10.1038/35044114; PMID: 11100732
   PubMed Web of Science ®Google Scholar
• Contento AL, Xiong Y, Bassham DC. Visualization of autophagy in Arabidopsis using the fluorescent dye monodansylcadaverine and a GFP-AtATG8e fusion protein. Plant J 2005; 42:598 - 608; http://dx.doi.org/10.1111/j.1365-313X.2005.02396.x; PMID: 15860017
   PubMed Web of Science ®Google Scholar
• Thompson AR, Doelling JH, Suttangkakul A, Vierstra RD. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol 2005; 138:2097 - 110; http://dx.doi.org/10.1104/pp.105.060673; PMID: 16040659
   PubMed Web of Science ®Google Scholar
• Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, et al. Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 2004; 16:2967 - 83; http://dx.doi.org/10.1105/tpc.104.025395; PMID: 15494556
   PubMed Web of Science ®Google Scholar
• Pérez-Pérez ME, Crespo JL. Autophagy in the model alga Chlamydomonas reinhardtii.. Autophagy 2010; 6:562 - 3; http://dx.doi.org/10.4161/auto.6.4.11822; PMID: 20404489
   PubMed Web of Science ®Google Scholar
• Pérez-Pérez ME, Florencio FJ, Crespo JL. Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii.. Plant Physiol 2010; 152:1874 - 88; http://dx.doi.org/10.1104/pp.109.152520; PMID: 20107021
   PubMed Web of Science ®Google Scholar
• Inwood W, Yoshihara C, Zalpuri R, Kim KS, Kustu S. The ultrastructure of a Chlamydomonas reinhardtii mutant strain lacking phytoene synthase resembles that of a colorless alga. Mol Plant 2008; 1:925 - 37; http://dx.doi.org/10.1093/mp/ssn046; PMID: 19825593
   PubMed Web of Science ®Google Scholar
• Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, et al. Mobilization of rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 2008; 148:142 - 55; http://dx.doi.org/10.1104/pp.108.122770; PMID: 18614709
   PubMed Web of Science ®Google Scholar
• Izumi M, Wada S, Makino A, Ishida H. The autophagic degradation of chloroplasts via rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 2010; 154:1196 - 209; http://dx.doi.org/10.1104/pp.110.158519; PMID: 20807997
   PubMed Web of Science ®Google Scholar
• Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, et al. Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 2009; 149:885 - 93; http://dx.doi.org/10.1104/pp.108.130013; PMID: 19074627
   PubMed Web of Science ®Google Scholar
• Sandmann G, Albrecht M. Accumulation of colorless carotenes and derivatives during interaction of bleaching herbicides with phytoene desaturation. Z Naturforsch C 1990; 45:487 - 91
   Web of Science ®Google Scholar
• Li Z, Wakao S, Fischer BB, Niyogi KK. Sensing and responding to excess light. Annu Rev Plant Biol 2009; 60:239 - 60; http://dx.doi.org/10.1146/annurev.arplant.58.032806.103844; PMID: 19575582
   PubMed Web of Science ®Google Scholar
• Finazzi G, Furia A, Barbagallo RP, Forti G. State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii.. Biochim Biophys Acta 1999; 1413:117 - 29; http://dx.doi.org/10.1016/S0005-2728(99)00089-4; PMID: 10556624
   PubMed Web of Science ®Google Scholar
• Babbs CF, Pham JA, Coolbaugh RC. Lethal hydroxyl radical production in paraquat-treated plants. Plant Physiol 1989; 90:1267 - 70; http://dx.doi.org/10.1104/pp.90.4.1267; PMID: 16666920
   PubMed Web of Science ®Google Scholar
• Suzuki N, Miller G, Morales J, Shulaev V, Torres MA, Mittler R. Respiratory burst oxidases: the engines of ROS signaling. Curr Opin Plant Biol 2011; http://dx.doi.org/10.1016/j.pbi.2011.07.014; PMID: 21862390
   PubMed Web of Science ®Google Scholar
• Liu Y, Xiong Y, Bassham DC. Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 2009; 5:954 - 63; http://dx.doi.org/10.4161/auto.5.7.9290; PMID: 19587533
   PubMed Web of Science ®Google Scholar
• Anderson A, Bothwell JH, Laohavisit A, Smith AG, Davies JM. NOX or not? Evidence for algal NADPH oxidases. Trends Plant Sci 2011; 16:579 - 81; http://dx.doi.org/10.1016/j.tplants.2011.09.003; PMID: 22000495
   PubMed Web of Science ®Google Scholar
• Luykx P, Hoppenrath M, Robinson D. Structure and behaviour of contractile vacuoles in Chlamydomonas reinhardtii.. Protoplasma 1997; 198:73 - 84; http://dx.doi.org/10.1007/BF01282133
   Web of Science ®Google Scholar
• Park H, Eggink L, Roberson R, Hoober J. Transfer of proteins from the chloroplast to vacuoles in Chlamydomonas reinhardtii (Chlorophyta): a pathway for degradation. J Phycol 1999; 35:528 - 38; http://dx.doi.org/10.1046/j.1529-8817.1999.3530528.x
   Web of Science ®Google Scholar
• Sager R, Palade GE. Structure and development of the chloroplast in Chlamydomonas. I. The normal green cell. J Biophys Biochem Cytol 1957; 3:463 - 88; http://dx.doi.org/10.1083/jcb.3.3.463; PMID: 13438931
   PubMedGoogle Scholar
• Komine Y, Eggink LL, Park H, Hoober JK. Vacuolar granules in Chlamydomonas reinhardtii: polyphosphate and a 70-kDa polypeptide as major components. Planta 2000; 210:897 - 905; http://dx.doi.org/10.1007/s004250050695; PMID: 10872220
   PubMed Web of Science ®Google Scholar
• Fischer BB, Krieger-Liszkay A, Hideg E, Snyrychova I, Wiesendanger M, Eggen RI. Role of singlet oxygen in chloroplast to nucleus retrograde signaling in Chlamydomonas reinhardtii.. FEBS Lett 2007; 581:5555 - 60; http://dx.doi.org/10.1016/j.febslet.2007.11.003; PMID: 17997989
   PubMed Web of Science ®Google Scholar
• Fischer BB, Rufenacht K, Dannenhauer K, Wiesendanger M, Eggen RI. Multiple stressor effects of high light irradiance and photosynthetic herbicides on growth and survival of the green alga Chlamydomonas reinhardtii.. Environ Toxicol Chem 2010; 29:2211 - 9; http://dx.doi.org/10.1002/etc.264; PMID: 20872684
   PubMed Web of Science ®Google Scholar
• Niyogi KK, Grossman AR, Bjorkman O. Arabidopsis mutants define a central role for the xanthophyll cycle in the regulation of photosynthetic energy conversion. Plant Cell 1998; 10:1121 - 34; PMID: 9668132
   PubMed Web of Science ®Google Scholar
• Baroli I, Gutman BL, Ledford HK, Shin JW, Chin BL, Havaux M, et al. Photo-oxidative stress in a xanthophyll-deficient mutant of Chlamydomonas. J Biol Chem 2004; 279:6337 - 44; http://dx.doi.org/10.1074/jbc.M312919200; PMID: 14665619
   PubMed Web of Science ®Google Scholar
• Chung T, Suttangkakul A, Vierstra RD. The ATG autophagic conjugation system in maize: ATG transcripts and abundance of the ATG8-lipid adduct are regulated by development and nutrient availability. Plant Physiol 2009; 149:220 - 34; http://dx.doi.org/10.1104/pp.108.126714; PMID: 18790996
   PubMed Web of Science ®Google Scholar
• Bowler C, Slooten L, Vandenbranden S, De Rycke R, Botterman J, Sybesma C, et al. Manganese superoxide dismutase can reduce cellular damage mediated by oxygen radicals in transgenic plants. EMBO J 1991; 10:1723 - 32; PMID: 2050109
   PubMed Web of Science ®Google Scholar
• Herrin DL, Battey JF, Greer K, Schmidt GW. Regulation of chlorophyll apoprotein expression and accumulation. Requirements for carotenoids and chlorophyll. J Biol Chem 1992; 267:8260 - 9; PMID: 1373722
   PubMed Web of Science ®Google Scholar
• Miura E, Kato Y, Sakamoto W. Reactive oxygen species derived from impaired quality control of photosystem II are irrelevant to plasma-membrane NADPH oxidases. Plant Signal Behav 2010; 5:264 - 6; http://dx.doi.org/10.4161/psb.5.3.10604; PMID: 20023407
   PubMedGoogle Scholar
• Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, et al. ROS signaling: the new wave?. Trends Plant Sci 2011; 16:300 - 9; http://dx.doi.org/10.1016/j.tplants.2011.03.007; PMID: 21482172
   PubMed Web of Science ®Google Scholar
• Filomeni G, Desideri E, Cardaci S, Rotilio G, Ciriolo MR. Under the ROS...thiol network is the principal suspect for autophagy commitment. Autophagy 2010; 6:999 - 1005; http://dx.doi.org/10.4161/auto.6.7.12754; PMID: 20639698
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Elazar Z. Regulation of autophagy by ROS: physiology and pathology. Trends Biochem Sci 2011; 36:30 - 8; http://dx.doi.org/10.1016/j.tibs.2010.07.007; PMID: 20728362
   PubMed Web of Science ®Google Scholar
• Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy 2011; 7:297 - 300; http://dx.doi.org/10.4161/auto.7.3.14502; PMID: 21252623
   PubMed Web of Science ®Google Scholar
• Kim J, Huang WP, Klionsky DJ. Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J Cell Biol 2001; 152:51 - 64; http://dx.doi.org/10.1083/jcb.152.1.51; PMID: 11149920
   PubMed Web of Science ®Google Scholar
• Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, et al. The reversible modification regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 2000; 151:263 - 76; http://dx.doi.org/10.1083/jcb.151.2.263; PMID: 11038174
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007; 26:1749 - 60; http://dx.doi.org/10.1038/sj.emboj.7601623; PMID: 17347651
   PubMed Web of Science ®Google Scholar
• Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA 2010; 107:4153 - 8; http://dx.doi.org/10.1073/pnas.0913860107; PMID: 20160076
   PubMed Web of Science ®Google Scholar
• Liu Y, Bassham DC. TOR is a negative regulator of autophagy in Arabidopsis thaliana.. PLoS ONE 2010; 5:e11883; http://dx.doi.org/10.1371/journal.pone.0011883; PMID: 20686696
   PubMed Web of Science ®Google Scholar
• Harris EH. The Chlamydomonas Sourcebook. San Diego: Academic Press, 1989.
   Google Scholar
• Crespo JL, Diaz-Troya S, Florencio FJ. Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga Chlamydomonas reinhardtii.. Plant Physiol 2005; 139:1736 - 49; http://dx.doi.org/10.1104/pp.105.070847; PMID: 16299168
   PubMed Web of Science ®Google Scholar
• Cole DG, Diener DR, Himelblau AL, Beech PL, Fuster JC, Rosenbaum JL. Chlamydomonas kinesin-II-dependent intraflagellar transport (IFT): IFT particles contain proteins required for ciliary assembly in Caenorhabditis elegans sensory neurons. J Cell Biol 1998; 141:993 - 1008; http://dx.doi.org/10.1083/jcb.141.4.993; PMID: 9585417
   PubMed Web of Science ®Google Scholar
• Díaz-Troya S, Florencio FJ, Crespo JL. Target of rapamycin and LST8 proteins associate with membranes from the endoplasmic reticulum in the unicellular green alga Chlamydomonas reinhardtii.. Eukaryot Cell 2008; 7:212 - 22; http://dx.doi.org/10.1128/EC.00361-07; PMID: 18039939
   PubMed Web of Science ®Google Scholar
• Baroli I, Do AD, Yamane T, Niyogi KK. Zeaxanthin accumulation in the absence of a functional xanthophyll cycle protects Chlamydomonas reinhardtii from photooxidative stress. Plant Cell 2003; 15:992 - 1008; http://dx.doi.org/10.1105/tpc.010405; PMID: 12671093
   PubMed Web of Science ®Google Scholar
• Joo JH, Wang S, Chen JG, Jones AM, Fedoroff NV. Different signaling and cell death roles of heterotrimeric G protein alpha and beta subunits in the Arabidopsis oxidative stress response to ozone. Plant Cell 2005; 17:957 - 70; http://dx.doi.org/10.1105/tpc.104.029603; PMID: 15705948
   PubMed Web of Science ®Google Scholar