活性氧调控植物细胞自噬的研究进展
收稿日期: 2018-01-12
录用日期: 2018-03-13
网络出版日期: 2019-07-31
基金资助
国家科技支撑计划(2015BAD16B01-3);国家自然科学基金(31530057, No.31672210, No.31670183)
Advances in the Regulation on Autophagy by Reactive Oxygen Species in Plant Cells
Received date: 2018-01-12
Accepted date: 2018-03-13
Online published: 2019-07-31
马丹颖,季东超,徐勇,陈彤,田世平 . 活性氧调控植物细胞自噬的研究进展[J]. 植物学报, 2019 , 54(1) : 81 -92 . DOI: 10.11983/CBB18012
Damaged proteins, organelles or exogenous substances are engulfed in double membrane vesicles and delivered to the lysosome (vacuoles) for degradation and recycled in eukaryotes. This highly conserved biological process is called autophagy. Reactive oxygen species (ROS) are byproducts of cellular aerobic metabolism, which are widely involved in the regulating different biological processes as signaling molecules. Recent evidence suggests a strong link between autophagy and ROS in plants. Here, we summarize the types and roles of ROS and describe the molecular mechanism of autophagy according to the latest research in plants. The effect of ROS on regulation of autophagy is mainly discussed.
Key words： autophagy; reactive oxygen species; regulation
| 1 | 蔡霞, 方晓艾, 田兰婷, 赵雪艳 ( 2016). 显微镜技术在植物细胞自噬研究中的应用. 电子显微学报 35, 180-185. |
| 2 | 黄晓, 李发强 ( 2016). 细胞自噬在植物细胞程序性死亡中的作用. 植物学报 51, 859-862. |
| 3 | 景红娟, 周广舟, 谭晓荣, 平康康, 任雪建 ( 2012). 活性氧对植物自噬调控的研究进展. 植物学报 47, 534-542. |
| 4 | 林植芳, 刘楠 ( 2012). 活性氧调控植物生长发育的研究进展. 植物学报 47, 74-86. |
| 5 | 刘洋, 张静, 王秋玲, 侯岁稳 ( 2018). 植物细胞自噬研究进展. 植物学报 53, 5-16. |
| 6 | 任晨霞, 龚清秋 ( 2014). 细胞自噬在植物碳氮营养中作用的研究进展. 中国细胞生物学学报 36, 407-414. |
| 7 | 王燕, 刘玉乐 ( 2010). 植物细胞自噬研究进展. 中国细胞生物学学报 32, 677-689. |
| 8 | 杨小龙, 李漾漾, 刘玉凤, 齐明芳, 李天来 ( 2017). 植物细胞选择性自噬研究进展. 园艺学报 44, 2015-2028. |
| 9 | Ahmad P, Jaleel CA, Salem MA, Nabi G, Sharma S ( 2010). Roles of enzymatic and nonenzymatic antioxidants in plants during abiotic stress. Crit Rev Biotechnol 30, 161-175. |
| 10 | Alers S, L?f?er AS, Wesselborg S, Stork B ( 2012). Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol 32, 2-11. |
| 11 | Alexander A, Cai SL, Kim J, Nanez A, Sahin M, MacLean KH, Inoki K, Guan KL, Shen JJ, Person MD, Kusewitt D, Mills GB, Kastan MB, Walker CL ( 2010). ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA 107, 4153-4158. |
| 12 | Apel K, Hirt H ( 2004). Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55, 373-399. |
| 13 | Asada K ( 2006). Production and scavenging of reactive oxy- gen species in chloroplasts and their functions. Plant Phy- siol 141, 391-396. |
| 14 | Ashford TP, Porter KR ( 1962). Cytoplasmic components in hepatic cell lysosomes. Cell Biol 12, 198-202. |
| 15 | Bassham DC ( 2007). Plant autophagy—more than a starvation response. Curr Opin Plant Biol 10, 587-593. |
| 16 | Bernales S, McDonald KL, Walter P ( 2006). Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4, e423. |
| 17 | Bienert GP, Chaumont F ( 2014). Aquaporin-facilitated transmembrane diffusion of hydrogen peroxide. Biochim Biophys Acta 1840, 1596-1604. |
| 18 | Blagosklonny MV ( 2008). Aging: ROS or TOR. Cell Cycle 7, 3344-3354. |
| 19 | Buchanan BB, Balmer Y ( 2005). Redox regulation: a broadening horizon. Annu Rev Plant Biol 56, 187-220. |
| 20 | Budanov AV ( 2011). Stress-responsive sestrins link p53 with redox regulation and mammalian target of rapamycin signaling. Antioxid Redox Signal 15, 1679-1690. |
| 21 | 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. |
| 22 | Chung T, Phillips AR, Vierstra RD ( 2010). ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG- 12A and ATG12B loci.Plant J 62, 483-493. |
| 23 | Chung T, Suttangkakul A, Vierstra RD ( 2009). 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 149, 220-234. |
| 24 | Coll NS, Smidler A, Puigvert M, Popa C, Valls M, Dangl JL ( 2014). The plant metacaspase AtMC1 in pathogen-trig- gered programmed cell death and aging: functional linkage with autophagy. Cell Death Differ 21, 1399-1408. |
| 25 | Dames SA, Mulet JM, Rathgeb-Szabo K, Hall MN, Grzesiek S ( 2005). The solution structure of the FATC domain of the protein kinase target of rapamycin suggests a role for redox-dependent structural and cellular stability. J Biol Chem 280, 20558-20564. |
| 26 | del Río LA ( 2011). Peroxisomes as a cellular source of reactive nitrogen species signal molecules. Arch Biochem Bio- phys 506, 1-11. |
| 27 | del Río LA, Corpas FJ, Sandalio LM, Palma JM, Gómez M, Barroso JB ( 2002). Reactive oxygen species, antioxidant systems and nitric oxide in peroxisomes. J Exp Bot 53, 1255-1272. |
| 28 | Dewaele M, Maes H, Agostinis P ( 2010). ROS-mediated mechanisms of autophagy stimulation and their relevance in cancer therapy. Autophagy 6, 838-854. |
| 29 | Díaz-Troya S, Pérez-Pérez ME, Pérez-Martín M, Moes S, Jeno P, Florencio FJ, Crespo JL ( 2011). Inhibition of protein synthesis by TOR inactivation revealed a conserved regulatory mechanism of the BiP chaperone in Chlamydomonas.Plant Physiol 157, 730-741. |
| 30 | Finkel T ( 2011). Signal transduction by reactive oxygen species. J Cell Biol 194, 7-15. |
| 31 | Foyer CH, Bloom AJ, Queval G, Noctor G ( 2009). Photorespiratory metabolism: genes, mutants, energetics, and redox signaling. Annu Rev Plant Biol 60, 455-484. |
| 32 | Foyer CH, Noctor G ( 2003). Redox sensing and signaling associated with reactive oxygen in chloroplasts, peroxi- somes and mitochondria. Physiol Plant 119, 355-364. |
| 33 | Gechev TS, Van Breusegem F, Stone JM, Denev I, Laloi C ( 2006). Reactive oxygen species as signals that modulate plant stress responses and programmed cell death. BioEssays 28, 1091-1101. |
| 34 | Han SJ, Wang Y, Zheng XJ, Jia Q, Zhao JP, Bai F, Hong YG, Liu YL ( 2015). Cytoplastic glyceraldehyde-3-phosph- ate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamia- na.Plant Cell 27, 1316-1331. |
| 35 | Han SJ, Yu BJ, Wang Y, Liu YL ( 2011). Role of plant autophagy in stress response. Protein & Cell 2, 784-791. |
| 36 | Hayward AP, Dinesh-Kumar SP ( 2011). What can plant autophagy do for an innate immune response? Annu Rev Phytopathol 49, 557-576. |
| 37 | He CC, Klionsky DJ ( 2009). Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43, 67-93. |
| 38 | Henry E, Fung N, Liu J, Drakakaki G, Coaker G ( 2015). Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLoS Genet 11, e1005199. |
| 39 | Hofius D, Li L, Hafrén A, Coll NS ( 2017). Autophagy as an emerging arena for plant-pathogen interactions. Curr Opin Plant Biol 38, 117-123. |
| 40 | Hofius D, Munch D, Bressendorff S, Mundy J, Petersen M ( 2011). Role of autophagy in disease resistance and hypersensitive response-associated cell death. Cell Death Differ 18, 1257-1262. |
| 41 | Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura SI, Natsume T, Takehana K, Yamada N, Guan JL, Oshiro N, Mizushima N ( 2009). Nutrient-dependent mTORC1 association with the ULK1-Atg13- FIP200 complex required for autophagy. Mol Biol Cell 20, 1981-1991. |
| 42 | Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y, Makino A, Ohsumi Y, Hanson MR, Mae T ( 2008). Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process.Plant Physiol 148, 142-155. |
| 43 | Izumi M, Ishida H, Nakamura S, Hidema J ( 2017). Entire photodamaged chloroplasts are transported to the central vacuole by autophagy. Plant Cell 29, 377-394. |
| 44 | Izumi M, Wada S, Makino A, Ishida H ( 2010). The autophagic degradation of chloroplasts via Rubisco-containing bodies is specifically linked to leaf carbon status but not nitrogen status in Arabidopsis. Plant Physiol 154, 1196-1209. |
| 45 | Kamada Y, Funakoshi T, Shintani T, Nagano K, Ohsumi M, Ohsumi Y ( 2000). Tor-mediated induction of autophagy via an Apg1 protein kinase complex. J Cell Biol 150, 1507-1513. |
| 46 | Kihara A, Noda T, Ishihara N, Ohsumi Y ( 2001). Two distinct Vps34 phosphatidylinositol 3-kinase complexes function in autophagy and carboxypeptidase Y sorting in Saccharomyces cerevisiae.J Cell Biol 152, 519-530. |
| 47 | Kirisako T, Ichimura Y, Okada H, Kabeya Y, Mizushima N, Yoshimori T, Ohsumi M, Takao T, Noda T, Ohsumi Y ( 2000). The reversible modi?cation regulates the membrane-binding state of Apg8/Aut7 essential for autophagy and the cytoplasm to vacuole targeting pathway. J Cell Biol 151, 263-276. |
| 48 | Kissová I, Deffieu M, Manon S, Camougrand N ( 2004). Uth1p is involved in the autophagic degradation of mitochondria. J Biol Chem 279, 39068-39074. |
| 49 | Kwon SI, Cho HJ, Jung JH, Yoshimoto K, Shirasu K, Park OK ( 2010 a). The Rab GTPase RabG3b functions in auto- phagy and contributes to tracheary element differentiation in Arabidopsis. Plant J 64, 151-164. |
| 50 | Kwon SI, Cho HJ, Park OK ( 2010 b). Role of Arabidopsis RabG3b and autophagy in tracheary element differentiation. Autophagy 6, 1187-1189. |
| 51 | Ledford HK, Chin BL, Niyogi KK ( 2007). Acclimation to singlet oxygen stress in Chlamydomonas reinhardtii.Eukaryot Cell 6, 919-930. |
| 52 | Lenz HD, Haller E, Melzer E, Kober K, Wurster K, Stahl M, Bassham DC, Vierstra RD, Parker JE, Bautor J, Molina A, Escudero V, Shindo T, van der Hoorn RA, Gust AA, Nürnberger T ( 2011). Autophagy differentially controls plant basal immunity to biotrophic and necrotrophic patho- gens. Plant J 66, 818-830. |
| 53 | Levine B, Klionsky DJ ( 2017). Autophagy wins the 2016 Nobel Prize in Physiology or Medicine: breakthroughs in baker’s yeast fuel advances in biomedical research. Proc Natl Acad Sci USA 114, 201-205. |
| 54 | Liu YL, Schiff M, Czymmek K, Tallóczy Z, Levine B, Dinesh-Kumar SP ( 2005). Autophagy regulates programmed cell death during the plant innate immune response. Cell 121, 567-577. |
| 55 | Liu YM, Bassham DC ( 2012). Autophagy: pathways for self-eating in plant cells. Annu Rev Plant Biol 63, 215-237. |
| 56 | Liu YM, 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. |
| 57 | Liu YM, Xiong Y, Bassham DC ( 2009). Autophagy is required for tolerance of drought and salt stress in plants. Autophagy 5, 954-963. |
| 58 | Malhotra JD, Kaufman RJ ( 2007). Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal 9, 2277-2293. |
| 59 | Meijer WH, van der Klei IJ, Veenhuis M, Kiel JAKW ( 2007). ATG genes involved in non-selective autophagy are conserved from yeast to man, but the selective Cvt and pexo- phagy pathways also require organism-speci?c genes. Autophagy 3, 106-116. |
| 60 | Minina EA, Moschou PN, Vetukuri RR, Sanchez-Vera V, Cardoso C, Liu QS, Elander PH, Dalman K, Beganovic M, Yilmaz JL, Marmon S, Shabala L, Suarez MF, Ljung K, Novák O, Shabala S, Stymne S, Hofius D, Bozhkov PV ( 2018). Transcriptional stimulation of rate-limiting components of the autophagic pathway improves plant fitness. J Exp Bot 69, 1415-1432. |
| 61 | Mizushima N ( 2010). The role of the Atg1/ULK1 complex in autophagy regulation. Curr Opin Cell Biol 22, 132-139. |
| 62 | Mizushima N, Yoshimori T, Ohsumi Y ( 2011). The role of Atg proteins in autophagosome formation. Annu Rev Cell Dev Biol 27, 107-132. |
| 63 | M?ller IM ( 2001). Plant mitochondria and oxidative stress: electron transport, NADPH turnover and metabolism of reactive oxygen species. Annu Rev Plant Physiol Plant Mol Biol 52, 561-591. |
| 64 | Moreau M, Azzopardi M, Clément G, Dobrenel T, Marchive C, Renne C, Martin-Magniette ML, Taconnat L, Renou JP, Robaglia C, Meyer C ( 2012). Mutations in the Arabidopsis homolog of LST8/GβL, a partner of the target of rapamycin kinase, impair plant growth, flowering, and metabolic adaptation to long days. Plant Cell 24, 463-481. |
| 65 | Nakatogawa H, Suzuki K, Kamada Y, Ohsumi Y ( 2009). Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol 10, 458-467. |
| 66 | Okamoto K, Kondo-Okamoto N, Ohsumi Y ( 2009). Mitochondria-anchored receptor Atg32 mediates degradation of mitochondria via selective autophagy. Dev Cell 17, 87-97. |
| 67 | Pérez-Pérez ME, Couso I, Crespo JL ( 2012 a). Carotenoid de?ciency triggers autophagy in the model green alga Chlamydomonas reinhardtii.Autophagy 8, 376-388. |
| 68 | Pérez-Pérez ME, Florencio FJ, Crespo JL ( 2010). Inhibition of target of rapamycin signaling and stress activate autophagy in Chlamydomonas reinhardtii.Plant Physiol 152, 1874-1888. |
| 69 | Pérez-Pérez ME, Lemaire SD, Crespo JL ( 2012 b). Reactive oxygen species and autophagy in plants and algae. Plant Physiol 160, 156-164. |
| 70 | Pu YT, Luo XJ, Bassham DC ( 2017). TOR-dependent and - independent pathways regulate autophagy in Arabidopsis thaliana.Front Plant Sci 8, 1204. |
| 71 | Qi H, Xia FN, Xie LJ, Yu LJ, Chen QF, Zhuang XH, Wang Q, Li FQ, Jiang LW, Xie Q, Xiao S ( 2017). TRAF family proteins regulate autophagy dynamics by modulating AU- TOPHAGY PROTEIN6 stability in Arabidopsis. Plant Cell 29, 890-911. |
| 72 | Rahal A, Kumar A, Singh V, Yadav B, Tiwari R, Chakraborty S, Dhama K ( 2014). Oxidative stress, prooxidants, and antioxidants: the interplay. Biomed Res Int 2014, 761264. |
| 73 | Ren MZ, Qiu SQ, Venglat P, Xiang DQ, Feng L, Selvaraj G, Datla R ( 2011). Target of rapamycin regulates development and ribosomal RNA expression through kinase domain in Arabidopsis. Plant Physiol 155, 1367-1382. |
| 74 | Reumann S, Voitsekhovskaja O, Lillo C ( 2010). From signal transduction to autophagy of plant cell organelles: lessons from yeast and mammals and plant-specific features. Protoplasma 247, 233-256. |
| 75 | Robaglia C, Thomas M, Meyer C ( 2012). Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 15, 301-307. |
| 76 | Rutkowski DT, Kaufman RJ ( 2007). That which does not kill me makes me stronger: adapting to chronic ER stress. Trends Biochem Sci 32, 469-476. |
| 77 | Santos CX, Tanaka LY, Wosniak J Jr, Laurindo FRM ( 2009). Mechanisms and implications of reactive oxygen species generation during the unfolded protein response: roles of endoplasmic reticulum oxidoreductases, mitochondrial electron transport, and NADPH oxidase. Antioxid Redox Signal 11, 2409-2427. |
| 78 | Schafer FQ, Wang HP, Kelley EE, Cueno KL, Martin SM, Buettner GR ( 2002). Comparing beta-carotene, vitamin E and nitric oxide as membrane antioxidants. Biol Chem 383, 671-681. |
| 79 | Scheler C, Durner J, Astier J ( 2013). Nitric oxide and reactive oxygen species in plant biotic interactions. Curr Opin Plant Biol 16, 534-539. |
| 80 | Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, Elazar Z ( 2007). Reactive oxygen species are essential for autophagy and speci?cally regulate the activity of Atg4. EMBO J 26, 1749-1760. |
| 81 | Schieke SM, Finkel T ( 2006). Mitochondrial signaling, TOR, and life span. Biol Chem 387, 1357-1361. |
| 82 | 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. |
| 83 | Shin JH, Yoshimoto K, Ohsumi Y, Jeon JS, An G ( 2009). OsATG10b, an autophagosome component, is needed for cell survival against oxidative stresses in rice. Mol Cells 27, 67-74. |
| 84 | Soto-Burgos J, Bassham DC ( 2017) SnRK1 activates autophagy via the TOR signaling pathway in Arabidopsis thaliana.PLoS One 12, e0182591. |
| 85 | Sun X, Wang P, Jia X, Huo LQ, Che RM, Ma FW ( 2018). Improvement of drought tolerance by overexpressing Md- ATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple.Plant Biotechnol J 16, 545-557. |
| 86 | Suttangkakul A, Li FQ, Chung T, Vierstra RD ( 2011). The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23, 3761-3779. |
| 87 | 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. |
| 88 | Swanson S, Gilroy S ( 2010). ROS in plant development. Physiol Plant 138, 384-392. |
| 89 | Tal R, Winter G, Ecker N, Klionsky DJ, Abeliovich H ( 2007). Aup1p, a yeast mitochondrial protein phosphatase homolog, is required for efficient stationary phase mitophagy and cell survival. J Biol Chem 282, 5617-5624. |
| 90 | Thompson AR, Vierstra RD ( 2005). Autophagic recycling: lessons from yeast help define the process in plants. Curr Opin Plant Biol 8, 165-173. |
| 91 | Tolkovsky AM ( 2009). Mitophagy. Biochim Biophys Acta 1793, 1508-1515. |
| 92 | Tsugane K, Kobayashi K, Niwa Y, Ohba Y, Wada K, Kobayashi H ( 1999). A recessive Arabidopsis mutant that grows photoautotrophically under salt stress shows enhanced active oxygen detoxification. Plant Cell 11, 1195-1206. |
| 93 | Ungermann C, Langosch D ( 2005). Functions of SNAREs in intracellular membrane fusion and lipid bilayer mixing. J Cell Sci 118, 3819-3828. |
| 94 | üstün S, Hafrén A, Hofius D ( 2017). Autophagy as a mediator of life and death in plants. Curr Opin Plant Biol 40, 122-130. |
| 95 | van Dongen JT, Licausi F ( 2015). Oxygen sensing and signaling. Annu Rev Plant Biol 66, 345-367. |
| 96 | Wada S, Ishida H, Izumi M, Yoshimoto K, Ohsumi Y, Mae T, Makino A ( 2009). Autophagy plays a role in chloroplast degradation during senescence in individually darkened leaves. Plant Physiol 149, 885-893. |
| 97 | Wang CW, Klionsky DJ ( 2003). The molecular mechanism of autophagy. Mol Med 9, 65-76. |
| 98 | Wang Y, Liu YL ( 2013). Autophagic degradation of leaf starch in plants. Autophagy 9, 1247-1248. |
| 99 | Wang Y, Yu BJ, Zhao JP, Guo JB, Li Y, Han SJ, Huang L, Du YM, Hong YG, Tang DZ, Liu YL ( 2013). Autophagy contributes to leaf starch degradation. Plant Cell 25, 1383-1399. |
| 100 | Wang Y, Zheng XY, Yu BJ, Han SJ, Guo JB, Tang HP, Yu AYL, Deng HT, Hong YG, Liu YL ( 2015). Disruption of microtubules in plants suppresses macroautophagy and triggers starch excess-associated chloroplast autophagy. Autophagy 11, 2259-2274. |
| 101 | Xia KF, Liu T, Ouyang J, Wang R, Fan T, Zhang MY ( 2011). Genome-wide identification, classification, and expression analysis of autophagy-associated gene homologues in rice ( Oryza sativa L.).DNA Res 18, 363-377. |
| 102 | Xiong Y, Contento AL, Bassham DC ( 2007 a). Disruption of autophagy results in constitutive oxidative stress in Ara- bidopsis. Autophagy 3, 257-258. |
| 103 | Xiong Y, Contento AL, Nguyen PQ, Bassham DC ( 2007 b). Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis. Plant Physiol 143, 291-299. |
| 104 | Xiong Y, McCormack M, Li L, Hall Q, Xiang CB, Sheen J ( 2013). Glucose-TOR signaling reprograms the transcriptome and activates meristems. Nature 496, 181-186. |
| 105 | Xiong Y, Sheen J ( 2014). The role of target of rapamycin signaling networks in plant growth and metabolism. Plant Physiol 164, 499-512. |
| 106 | Xu GY, Wang SS, Han SJ, Xie K, Wang Y, Li JL, Liu YL ( 2017). Plant Bax Inhibitor-1 interacts with ATG6 to regulate autophagy and programmed cell death. Autophagy 13, 1161-1175. |
| 107 | Yorimitsu T, Nair U, Yang ZF, Klionsky DJ ( 2006). Endoplasmic reticulum stress triggers autophagy. J Biol Chem 281, 30299-30304. |
| 108 | Yoshimoto K, Hanaoka H, Sato S, Kato T, Tabata S, Noda T, Ohsumi Y ( 2004). Processing of ATG8s, ubiquitin-like proteins, and their deconjugation by ATG4s are essential for plant autophagy. Plant Cell 16, 2967-2983. |
| 109 | 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. |
| 110 | Yoshimoto K, Takano Y, Sakai Y ( 2010). Autophagy in plants and phytopathogens. FEBS Lett 584, 1350-1358. |
| 111 | Zhang DY, Wang W, Sun XJ, Xu DQ, Wang CY, Zhang Q, Wang HF, Luo WW, Chen Y, Chen HY, Liu ZX ( 2016). AMPK regulates autophagy by phosphorylating BECN1 at threonine 388. Autophagy 12, 1447-1459. |
| 112 | Zhou XM, Zhao P, Wang W, Zou J, Cheng TH, Peng XB, Sun MX ( 2015). A comprehensive, genome-wide analysis of autophagy-related genes identified in tobacco suggests a central role of autophagy in plant response to various environmental cues. DNA Res 22, 245-257. |
/
| 〈 |
|
〉 |
首页