植物细胞选择性自噬研究进展

园艺学报 2017 44 10 2015 2028 Acta Horticulturae Sinica doi 10 16420 j issn 0513 353x 2017 0144 http www ahs ac cn 2015 收稿日期 收稿日期 2017 04 21 修回日期 修回日期 2017 08 04 基金项目 基金项目 国家自然科学基金项目 31301813 国家重点研发计划支持项目 2016YFD0201004 辽宁省农业领域青年科技创新人才 培养计划项目 2015040 国家现代农业产业体系建设专项资金项目 CARS 25 中央财政农业科技推广项目 GCNT LN 17 通信作者 Author for correspondence E mail tianlaili 植物细胞选择性自噬研究进展 杨小龙 李漾漾 刘玉凤 齐明芳 李天来 沈阳农业大学园艺学院 设施园艺省部共建教育部重点试验室 环渤海湾地区设施蔬菜优质高效生产协同创新中 心 沈阳 110866 摘 要 摘 要 植物在生长发育和响应环境胁迫过程中不断产生受损的细胞器和蛋白质等 这些物质必须 被及时且适宜的降解 其中 细胞自噬就是一个在进化上保守的主要降解途径 自噬体通过受体蛋白选 择性地识别并靶向特异的组分和蛋白复合物 然后传递至液泡中降解 使其能够循环再利用 从而调节 细胞内的关键反应过程 近些年的研究揭示了自噬在植物生命活动的多个过程中均发挥重要作用 本文 中主要综述了植物细胞选择性自噬的最新研究进展 包括自噬体形成过程 货物识别 分类以及在生长 发育 植物免疫和响应非生物胁迫中的作用 关键词 关键词 选择性自噬 蛋白降解 货物受体 植物免疫 非生物胁迫 中图分类号 中图分类号 Q 942 5 Q 943 2 文献标志码 文献标志码 A 文章编号 文章编号 0513 353X 2017 10 2015 14 Review of Selective Autophagy in Plant Cell YANG Xiaolong LI Yangyang LIU Yufeng QI Mingfang and LI Tianlai College of Horticulture Shenyang Agriculture University Key Laboratory of Protected Horticulture of Education Ministry and Liaoning Province Collaborative Innovation Center of Protected Vegetable Surrounding Bohai Gulf Region Shenyang 110866 China Abstract Plants continuously produce damaged organelles and proteins in the process of growth and response to environmental stresses which must be timely and appropriately degraded Autophagy is a major cellular degradation pathway conserved during evolution in plants Autophagosomes selectively recognize and target specific compartments and protein complexes through cargo receptor proteins then deliver them to the vacuole for degradation and recycling which regulates the critical reactions within the cell Researches in recent years have revealed the importance of autophagy in many aspects of plant life In this article the latest advances of plant cell selective autophagy are reviewed including autophagosome formation cargo recognition and types of selective autophagy and the role in growth and development immune and response to abiotic stress Keywords selective autophagy protein degradation cargo receptor plant immune abiotic stress 生物体对受损或不再需要的细胞器 蛋白质 脂类和其他细胞成分的重塑有助于物质代谢和养 分管理 这对正常的生长发育和胁迫适应性起着关键作用 在这个过程中存在两个进化上保守的降 Yang Xiaolong Li Yangyang Liu Yufeng Qi Mingfang Li Tianlai Review of selective autophagy in plant cell 2016 Acta Horticulturae Sinica 2017 44 10 2015 2028 解机制 泛素 蛋白酶体系统 Ubiquitin Proteasome system UPS 和细胞自噬 Autophagy Khaminets et al 2016 游全远和何祖华 2016 自噬是真核生物细胞内普遍存在的大分子降解过程 主要存 在微自噬 巨自噬和分子伴侣介导的自噬 既具有持家能力又能响应环境胁迫 在自噬相关基因 Autophagy related genes ATGs 的调控下自噬体可以将一些多余或受损的细胞器 蛋白质等胞质 内含物送入液泡中进行降解 这些物质的循环利用有利于维持细胞内稳态 帮助生物体抵抗外界胁 迫 Bassham 2007 Liu 7 互作并 介导 PIP2 7 由质膜传递到液泡 值得注意的是 在这个过程中细胞表面 PIP2 7 数量的降低似乎能够 调节细胞透水性 而透水性在高温和干旱胁迫下起着重要作用 Hachez et al 2014 TSPO 对植物 生长和发育不是十分重要 但似乎通过结合并解除卟啉类物质的毒性从而保护植物细胞免受氧化胁 迫 Cui et al 2015 Honig 等 2012a 发现 在碳饥饿情况下 拟南芥 ATI1 和 ATI2 被转移到新形成的球形结构 ATI 小体 沿着内质网向液泡移动 这暗示 ATI 小体直接参与内质网 液泡之间的交易过程 在 ABA 处理后 缺乏 ati1 和 ati2 的拟南芥表现出延迟发芽 表明 ATI 小体可能介导 ABA 或 ABA 相关蛋白 的选择性降解 Honig et al 2012a 2012b 此外 在诱导衰老后 ATI1 能选择性结合到特殊的质 体相关小体 ATI PS 并招募 Atg8 蛋白介导 ATI PS 小体通过自噬过程在液泡中完成降解 这与 Rubisco 蛋白酶体 RCBs 不同 RCBs 更大且主要包含基质蛋白质 Rubisco ATI1 与定位于叶绿体 的蛋白质 如 NPQ4 PrxA 和 APE1 等互作 它们需要与 Atg8f 和 Atg5 结合才能被传递到液泡 在 ati1 突变体株系中 PrxA 蛋白含量升高 表明该蛋白无法进入液泡中完成降解过程 这些发现表明 ATI1 是植物细胞特有的自噬货物受体 Michaeli et al 2014b 在番茄中发现的蛋白激酶 ADI3 AvrPto dependent Pto interacting protein 3 也被认为是一种植 物自噬受体 这涉及到细胞程序性死亡过程 PCD 在病菌侵染之后 ADI3 AvrPto 和 Pto 形成 复杂的复合物 其形成能够阻止 ADI3 向细胞核转移 消除依赖 ADI3 的 PCD 抑制能够诱导高度灵 敏的反应 Ek Ramos et al 2010 2014 ADI3 基因的沉默与自噬的抑制有相似的结果 侵染后高 度灵敏的细胞死亡反应将不受控制地进行传播 此外 ADI3 直接并特异地与番茄 Atg8h 结合 但 他们之间特异互作的意义仍然未知 研究者认为 ADI3 可能与自噬一起控制 PCD 的发生 并且在番 茄中共沉默 ADI3 和编码关键自噬相关蛋白 ATG7 ATG5 ATG6 PI3K ATG8H 的基因可以导 致其他的表型效应 Devarenne 2011 泛素 26S 蛋白酶体对于维持细胞稳态十分重要 26S 蛋白酶体的形成与降解过程受到精确的 调控 Marshall 7 through protein protein interactions and autophagic degradation The Plant Cell 26 12 4974 4990 Hackenberg T Juul T AuzinaA Gwi d S Ma olepszy A van der Kelen K Dam S Bressendorff S Lorentzen A Roepstorff P Nielsen K L Jorgensen J E Hofius D BreusegemF V Petersen M Andersen S U 2013 Catalase and NO CATALASE ACTIVITY1 promote autophagy dependent cell death in Arabidopsis The Plant Cell 25 11 4616 4626 Han S J Wang Y Zheng X Y Jia Q Zhao J P Bai F Hong Y G Liu Y L 2015 Cytoplastic glyceraldehyde 3 phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in Nicotiana benthamiana Plant Cell 27 4 1316 1331 Harrison Lowe N J Olsen L J 2008 Autophagy protein 6 ATG6 is required for pollen germination in Arabidopsis thaliana Autophagy 4 3 339 348 Hav M Marmagne A Chardon F Masclaux Daubresse C 2016 Nitrogen remobilisation during leaf senescence lessons from Arabidopsis to crops Journal of Experimental Botany erw365 Hillwig M S Contento A L Meyer A Ebany D Bassham D C MacIntosh G C 2011 RNS2 a conserved member of the RNase T2 family is necessary for ribosomal RNA decay in plants Proceedings of the National Academy of Science of the United States of America 108 3 杨小龙 李漾漾 刘玉凤 齐明芳 李天来 植物细胞选择性自噬研究进展 园艺学报 2017 44 10 2015 2028 2025 1093 1098 Honig A Avin Wittenberg T Galili G 2012b Selective autophagy in the aid of plant germination and response to nutrient starvation Autophagy 8 5 838 839 Honig A Avin Wittenberg T Ufaz S Galili G 2012a A new type of compartment defined by plant specific Atg8 interacting proteins is induced upon exposure of Arabidopsis plants to carbon starvation Plant Cell 24 1 288 303 Huang H Kawamata T Horie T Tsugawa H Nakayama Y Ohsumi Y Fukusaki E 2015 Bulk RNA degradation by nitrogen starvation induced autophagy in yeast The EMBO Journal 34 2 154 168 Ishida H Yoshimoto K Izumi M Reisen D Yano Y Makino A Ohsumi Y Hanson M R Mae T 2008 Mobilization of rubisco and stroma localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene dependent autophagic process Plant Physiology 148 1 142 155 Ishida H Yoshimoto K 2008 Chloroplasts are partially mobilized to the vacuole by autophagy Autophagy 4 7 961 962 Izumi M Hidema J Ishida H 2015a From Arabidopsis to cereal crops conservation of chloroplast protein degradation by autophagy indicates its fundamental role in plant productivity Plant Signaling and Behavior 10 11 e1101199 Izumi M Hidema J Makino A Ishida H 2013 Autophagy contributes to nighttime energy availability for growth in Arabidopsis Plant Physiology 161 4 1682 1693 Izumi M Hidema J Wada S Kondo E Kurusu T Kuchitsu K Makino A Ishida H 2015b Establishment of monitoring methods for autophagy in rice reveals autophagic recycling of chloroplasts and root plastids during energy limitation Plant Physiology 167 4 1307 1320 Jing Hongjuan Zhou Guangzhou Tan Xiaorong Ping Kangkang Ren Xuejian 2012 Research progress in regulation of reactive oxygen species in plant autophagy Bulletin of Botany 47 5 534 542 in Chinese 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 5 534 542 Khaminets A Behl C Dikic I 2016 Ubiquitin dependent and independent signals in selective autophagy Trends in Cell Biology 26 1 6 16 Khan M S Hemalatha S 2015 Autophagy molecular insight and role in plant programmed cell death and defense mechanism International Research Journal of Biological Sciences 4 78 83 Kim H P Wang X Lee S J Huang M H Wan Y Ryter S W Choi A M 2008 Autophagic proteins regulate cigarette smoke induced apoptosis protective role of heme oxygenase 1 Autophagy 4 7 887 895 Kurusu T Hanamata S Kuchitsu K 2016 Quantitative live cell imaging of autophagic flux and roles of autophagy in reproductive development in plants Bioimages 24 1 11 Kwon S I Park O K 2008 Autophagy in plants Journal of Plant Biology 51 5 313 320 Lamb C A Yoshimori T Tooze S A 2013 The autophagosome origins unknown biogenesis complex Nature Review Molecular Cell Biology 14 12 759 774 Le Bars R Marion J Le Borgne R Satiat Jeunemaitre B Bianchi M W 2014 ATG5 defines a phagophore domain connected to the endoplasmic reticulum during autophagosome formation in plants Nature Communications 5 4121 Lee T A Wetering S W V Brusslan J A 2013 Stromal protein degradation is incomplete in Arabidopsis thaliana autophagy mutants undergoing natural senescence BMC Research Notes 6 1 17 Li F Chung T Vierstra R D 2014 AUTOPHAGY RELATED11 plays a critical role in general autophagy and senescence induced mitophagy in Arabidopsis Plant Cell 26 2 788 807 Li F Vierstra R D 2014 Arabidopsis ATG11 a scaffold that links the ATG1 ATG13 kinase complex to general autophagy and selective mitophagy Autophagy 10 8 1466 1467 Li Y Kabbage M Liu W Dickman M B 2016 Aspartyl protease mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants Plant Cell 28 1 233 247 Lingard M J Monroe Augustus M Bartel B 2009 Peroxisome associated matrix protein degradation in Arabidopsis Proceedings of the National Academy of Science of the United States of America 106 11 4561 4566 Liu Y Bassham D C 2012 Autophagy pathways for self eating in plant cells Annual Review of Plant Biology 63 215 237 Liu Y Burgos J S Deng Y Srivastava R Howell S H Bassham D C 2012 Degradation of the endoplasmic reticulum by autophagy during Yang Xiaolong Li Yangyang Liu Yufeng Qi Mingfang Li Tianlai Review of selective autophagy in plant cell 2026 Acta Horticulturae Sinica 2017 44 10 2015 2028 endoplasmic reticulum stress in Arabidopsis Plant Cell 24 11 4635 4651 Maqbool A Hughes R K Dagdas Y F Tregidgo N Zess E Belhaj K Round A Bozkurt T O Kamoun S Banfield M J 2011 Structural basis of host Autophagy related Protein 8 ATG8 binding by the irish potato famine pathogen effector protein PexRD54 Journal of Biological Chemistry 291 38 20270 20282 Marshall R S Li F Gemperline D C Book A J Vierstra R D 2015 Autophagic degradation of the 26S proteasome is mediated by the dual ATG8 ubiquitin receptor RPN10 in Arabidopsis Molecular Cell 58 6 1053 1066 Marshall R S Vierstra R D 2015 Eat or be eaten the autophagic plight of inactive 26S proteasomes Autophagy 11 10 1927 1928 Michaeli S Avin Wittenberg T Galili G 2014a Involvement of autophagy in the direct ER to vacuole protein trafficking route in plants Frontiers in Plant Science 5 134 Michaeli S Galili G Genschik P Fernie A R Avin Wittenberg T 2016 Autophagy in plants what s new on the menu Trends in Plant Science 21 2 134 144 Michaeli S Honig A Levanony H Peled Zehavi H Galili G 2014b Arabidopsis ATG8 INTERACTING PROTEIN1 is involved in autophagy dependent vesicular trafficking of plastid proteins to the vacuole Plant Cell 26 10 4084 4101 Moreau M Azzopardi M Cl ment G Dobrenel T Marchive C Renne C Martin Magniette M M Taconnat L Renou J P Robaglia C Meyer C 2012 Mutations in the Arabidopsis homolog of LST8 G L a partner of the target of rapamycin kinase impair plant growth flowering and metabolic adaptation to long days Plant Cell 24 2 463 481 Nakatogawa H Ohbayashi S Sakoh Nakatogawa M Kakuta S Suzuki S W Kirisako H Kondo Kakuta C Noda N N Yamamoto H Ohsumi Y 2012 The autophagy related protein kinase Atg1 interacts with the ubiquitin like protein Atg8 via the Atg8 family interacting motif to facilitate autophagosome formation Journal of Biological Chemistry 287 34 28503 28507 Niki T Saito S Gladish D K 2014 Granular bodies in root primary meristem cells of Zea mays L var cuscoensis K Poaceae that enter young vacuoles by invagination a novel ribophagy mechanism Protoplasma 251 5 1141 1149 Noda N N Ohsumi Y Inagaki F 2010 Atg8 family interacting motif crucial for selective autophagy The FEBS Journal 584 7 1379 1385 Pourcel L Irani N G Lu Y Riedl K Schwartz S Grotewold E 2010 The formation of anthocyanic vacuolar inclusions in Arabidopsis thaliana and implications for the sequestration of anthocyanin pigments Molecular Plant 3 1 78 90 Qin G Ma Z Zhang L Xing S Hou X Deng J Liu J Chen Z Qu L J Gu H 2007 Arabidopsis AtBECLIN 1 AtAtg6 AtVps30 is essential for pollen germination and plant development Cell Research 17 3 249 263 Ren C Liu J Gong Q 2014 Functions of autophagy in plant carbon and nitrogen metabolism Frontiers in Plant Science 5 301 Ren H Li Y N Zhao F F Pu X J Wei L J Lv X Zhu F Lin H H 2016 The role of autophagy in alleviating damage of aluminum stress in Arabidopsis thaliana Plant Growth Regulation 79 2 167 175 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 12 4967 4983 Spitzer C Li F Buono R Roschzttardtz H Chung T Zhang M Osteryoung K W Vierstra R D Otegui M S 2015 The endosomal protein CHARGED MULTIVESICULAR BODY PROTEIN1 regulates the autophagic turnover of plastids in Arabidopsis Plant Cell 27 2 391 402 Sun Y Li H Huang J R 2012 Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts Molecular Plant 5 2 387 400 Suzuki H Osawa T Fujioka Y Noda N N 2017 Structural biology of the core autophagy machinery Current Opinion in Structural Biology 43 10 17 van Wijk K J 2015 Protein maturation and proteolysis in plant plastids mitochondria and peroxisomes Annual Review of Plant Biology 66 75 111 Vanhee C Zapotoczny G MasquelierD Ghislain M Batoko H 2011 The Arabidopsis multistress regulator TSPO is a heme binding membrane protein and a potential scavenger of porphyrins via an autophagy dependent degradation mechanism The Plant Cell 23 2 785 805 Veljanovski V Batoko H 2014 Selective autophagy of non ubiquitylated targets in plants looking for cognate receptor adaptor proteins Frontiers in Plant Science 5 308 杨小龙 李漾漾 刘玉凤 齐明芳 李天来 植物细胞选择性自噬研究进展 园艺学报 2017 44 10 2015 2028 2027 Voitsekhovskaja O V Schiermeyer A Reumann S 2014 Plant peroxisomes are degraded by starvation induced and constitutive autophagy in tobacco BY 2 suspension cultured cells Frontiers in Plant Science 5 629 Wada S Hayashida Y Izumi M Kurusu T Hanamata S Kanno K Kojima S Yamaya T Kuchitsu K Makino A Ishida H 2015 Autophagy supports biomass production and nitrogen use efficiency at the vegetative stage in rice Plant Physiology 168 1 60 73 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 Physiology 149 2 885 893 Wang P Sun X Chang C Feng F Liang D Cheng L Ma F W 2013 Delay in leaf senescence of Malus hupehensis by long term melatonin application is associated with its regulation of metabolic status and protein degradation Journal of Pineal Research 55 4 424 434 Wang P Sun X Jia X Wang N Gong X Ma F W 2016a Characterization of an autophagy related gene MdATG8i from apple Frontiers in Plant Science 7 1 16 Wang P Sun X Wang N Jia X Ma F W 2016b Ectopic expression of an autophagy associated MdATG7b gene from apple alters growth and tolerance to nutrient stress in Arabidopsis thaliana Plant Cell Tissue and Organ Culture 128 1 9 23 Wang P Sun X Wang N Tan D X Ma F W 2015a Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings Journal of Pineal Research 58 4 479 489 Wang Y Cai S Y Yin L L Shi K Xia X J Zhou Y H Yu J Q Zhou J 2015b Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy Autophagy 11 11 2033 2047 Wang Yan Liu Yule 2010 Progress in plant autophagy Chinese Journal of Cell Biology 5 677 689 in Chinese 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 5 677 689 Wen X Klionsky D J 2016 The proteasome subunit RPN10 functions as a specific receptor for degradation of the 26S proteasome by macroautophagy in Arabidopsis Autophagy 12 6 905 Wurzer B Zaffagnini G Fracchiolla D Turco E Abert C Romanov J Martens S 2015 Oligomerization of p62 allows for selection of ubiquitinated cargo and isolation membrane during selective autophagy eLife 4 e08941 Xia K Liu T Ouyang J Wang R Fan T Zhang M 2011 Genome wide identification classification and expression analysis of autophagy associated gene homologues in rice Oryza sativa L DNA Research 18 5 363 377 Xiong Y Contento A L Nguyen P Q Bassham D C 2007 Degradation of oxidized proteins by autophagy during oxidative stress in Arabidopsis Plant Physiology 143 1 291 299 Xiong Y Sheen J 2014 The role of target of rapamycin signaling networks in plant growth and metabolism Plant Physiology 164 2 499 512 Xu W Cai S Y Zhang Y Wang Y Ahammed G J Xia X J Shi K Zhou Y H Yu J Q Reiter R J Zhou J 2016 Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants Journal of Pineal Research 61 4 457 469 Yang X Srivastava R Howell S H Bassham D C 2016 Activation of autophagy by unfolded proteins during endoplasmic reticulum stress The Plant Journal 85 1 83 95 Yoshimoto K Shibata M Kondo M Oikawa K Sato M Toyooka K Shirasu K Nishimura M Ohsumi Y 2014 Organ specific quality control of plant peroxisomes is mediated by autophagy Journal of Cell Science 127 6 1161 1168 Yoshimoto K 2012 Beginning to understand autophagy an intracellular self degradation system in plants Plant and Cell Physiology 53 8 1355 1365 You Quanyuan He Zuhua 2016 Research advances on ubiquitin 26S proteasome mediated plant immunity Plant Physiology Communications 52 6 771 781 in Chinese 游全远 何祖华 2016 泛素 26S 蛋白酶体系统参与调控植物免疫研究进展 植物生理学报 52 6 771 781 Yue J Sun H Zhang W Pei D He Y Wang H 2015 Wheat homologs of yeast ATG6 function in autophagy and are implicated in powdery mildew immunity BMC Plant Biology 15 1 1 15 Zeng Xiaowei Liu Cuicui Han Ning BianHongwu Zhu Muyuan 2016 Progress on the autophagic regulators and receptors in plants Hereditas Beijing 38 7 644 650 in Chinese 曾笑威 刘翠翠 韩 凝 边红武 朱睦元 2016 植物自噬的调控因子和受体蛋白研究进展 遗传 38 7 644 650 Yang Xiaolong Li Yangyang Liu Yufeng Qi Mingfang Li Tianlai Review of selective autophagy in plant cell 2028 Acta Horticulturae Sinica 2017 44 10 2015 2028 Zhai Y Guo M Wang H Lu J Liu J Zhang C Gong Z H Lu M H 2016 Autophagy a conserved mechanism for protein degradation responds to heat and other abiotic stresses in Capsicum annuum L Frontiers in Plant Science 7 131 Zheng W Zhou J He Y Xie Q Chen A Zheng H Shi L Zhao X Zhang C Huang Q Fang K Lu G Ebbole D J Li G N