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Molecular Mechanism and Role of Autophagy in Plants
- 1. Molecular mechanism of autophagy and its role in plants 1 SHRIKANT YANKANCHI INDIRA GANDHI AGRICULTURAL UNIVERSITY (IGKV) RAIPUR, CG
- 2. 2 Introduction Landmarks of autophagy Classes of Autophagy Genes/Proteins involved in the mechanism autophagy Molecular Mechanism of autophagy Physiological Roles of Autophagy in plants Case studies Conclusion Flow of Seminar
- 3. Introduction 3 Damaged organelles? Aggregated Proteins? Long lived or Abnormal proteins? Part of invading virus Cells turnover http://pdb101.rcsb.org/motm/166 One of the basic rules of the universe is that nothing is perfect. “Perfection simply Doesn’t exist” – Stephen
- 4. Effects of aggregation? 4 continual aggregation of proteins Recycling is essential for life -critical selection factor in evolution -important ability for survival against starvation neurodegenerative diseases Alzheimer’s, Huntington, Parkinson’s, and the prion maladies. Cellular Toxicity
- 5. 5 Yoshinori Ohsumi, 201 degradation Life is in an equilibrium state between synthesis and degradation of proteins Eg: replacement of most proteins every 3 months“difference between organisms and machine”
- 6. How Proteins are degraded? 6 In eukaryotic cells, two major pathways i) The ubiquitin-proteasome pathway and ii) Lysosomal proteolysis mediate protein degradation Cooper, 2000
- 7. 7 E1s-Ubiquitin activating Enzymes E2s-ubiquitin-conjugating enzymes E3s-ubiquitin ligases The process consists three main steps i) The ubiquitin-proteasome pathway The major pathway of selective protein degradation in eukaryotic cells uses ubiquitin as a marker that targets cytosolic and nuclear proteins for rapid proteolysis Activation Conjugation Ligation Three enzymes
- 8. 8 Ubiquitin polyubiquitination Proteosome Peptides E 1 E 1 E 2 E 3 Specific target recognition Short lived proteins
- 9. ii) Lysosomal proteolysis mediate protein degradation 9 Uptake of proteins by lysosome's Yeast and Plants – Vacuole Bulk and Non selective Long lived proteins One of the pathway to uptake cellular proteins -Autophagy Protei ns Vacuole
- 10. Greek words - Auto (Self) phagein (to eat) “ Autophagy is a Highly regulated cellular degradation and recycling process, conserved from yeast to more complex eukaryotes” - Wen and Klionsky, 2016 “ Autophagy is an evolutionarily conserved intracellular process for the vacuolar/lysosomal degradation and recycle of cytoplasmic components” -Yoshimoto, 2012
- 11. Timelines of autophagy 11 1955 Discovery of the Lysosome 1962 Auto (Self) - Phagy (Eating) “Autophagy” Christian de Duve Rockefeller University Nobel Prize (1974)
- 12. Landmarks of autophagy Xin et al., 2014 12 v
- 14. Tokyo Institute of Technology, Tokyo, Japan “Discoveries of mechanisms for autophagy in Yeast – Saccharomyces cerevisiae https://www.nobelprize.org/ 14
- 15. How autophagy activated ? 15 Extracellular and Intracellular factors Growth factors Nutrient deprivation/under starvation Stress- oxidative, salt, ER stress During pathogen invasion Protein aggregation/ organelle aggregation
- 16. Which are the classes of autophagy? 16 Based on mechanisms of transport to lysosome/vacuole Macro-autophagy (Autophagy) Micro-autophagy Chaperone-mediated autophagy (CMA) Xin et al., 2014
- 17. Micro-autophagy 17 The lysosome/vacuole itself engulfs small components of the cytoplasm by inward invagination of the lysosomal membrane
- 18. Class of Microautophagy 18 Non-selective Cytoplasmic material is trapped in the lysosome/vacuole by the random process of membrane invagination Observed in all types of eucaryotic cells Selective Micropexophagy - Cluster of damaged and/or superfluous peroxisomes Micromitophagy - Mitochondria Li et al., 2011
- 19. Role 19 microautophagy functions in a coordinated way with macroautophagy and CMA Helps cells to withstand prolonged starvation by endless recycle of nutrients and energy
- 20. Chaperone-mediated autophagy (CMA)20 Selective pathway Pentapeptide KFERQ heat shock protein of 73kDa (hsc73) hsp70 family of chaperones lamp2a - lysosome-associated membrane protein type 2a (l) Bejarano and Ana Cuervo 201
- 21. Chaperone-mediated autophagy (CMA)Pathway? 21 Substrates identified for this pathway Bejarano and Ana Cuervo 201
- 22. substrates identified for CMA pathway 22 Ribonuclease A Glycolytic enzymes Eg: glyceraldehye-3-phosphate, dehydrogenase, aldolase B, pyruvate kinase, aspartate transcriptions factors or its inhibitors lipogenic enzymes structural proteins calcium-binding proteins
- 23. Activity of CMA pathway 23 CMA is upregulated after periods of nutrient deprivation of 10 hours or longer CMA activation persists past 3 days of starvation becoming a source of recycled amino acids for protein synthesis Part of these amino acids may also be used as cellular Tekirdag and Cuervo, 201
- 24. Role of CMA 24 Tekirdag and Cuervo, 2017
- 25. 25 universal catabolic process of intracellular degradation that delivers cytoplasmic constituents (macromolecules and organelles) to the vacuole/lysosome Major source of amino acid and other essential basic elements (lipids, sugars, nucleotides) - Starvation Highly conserved Formation of “autophagosome” Macro-autophagy (Autophagy) Ryabovol and Minibayeva, 2015
- 26. Terminologies 26 Autophagosome - double membrane vesicle or structure through which cargo delivers to lysosome/vacuole Phagophore - Autophagosome formation is initiated in the cytoplasm with the formation of a cuplike membrane structure, called phagophore or isolation membrane Pre-autophagomal-structure/site (PAS)- the putative site for autophagosome formation
- 27. 27 Which are the Steps of autophagic pathway? 1. Induction 2. Expansion 3. Maturation 4. Fusion 5. Recycling Steps in Autophagy (Animal) Membran e precursor Phagophore PAS Isolation membrane Macromolecules Eg: protein Autophagosome Lysosome Autolysosome
- 29. 29
- 30. 30 Nutrient deprived condition/Starvation Growth factors Eg: Hormones Defective or in excess, cytotoxic protein aggregates Radiations – Damaged Excess organelles upregulated during senescence under nitrogen or fixed-carbon starvation hypersensitive response following pathogen (Li et al., 2014) Factors/Conditions stimulating autophagy
- 31. ATG1-ATG13 kinase complex Induction of Autophagy 31 Farré and Suresh Subramani , 1.Induction
- 32. Key Regulators of Autophagy 32 Nutrient and growth factor-sensitive signalling pathways mammalian target of rapamycin (mTOR)/ plant TOR 5'-adenosine monophosphate (AMP)-activated protein kinase (AMPK)/SNF1/SnRK1 signaling pathways Autophagy-related Genes/proteins (ATGs) Xin et al., 2014
- 33. TOR – Target of Rapamycin • 270 kDA • mTORC1 and mTORC2 complex 33 TORC1complex mTOR + RAPTOR (regulatory- associated protein of TOR) + mLST8 (Lethal with Sec Thirteen 8). RAPTOR – phosphorylation and LST8 – Stabilization. RAPTOR - Recruitment This complex functions as a nutrient/energy sensor and controls protein synthesis Rapamycin, insulin, growth factors, certain amino acids and their mechanical stimuli, and oxidative stress Crozet et al., 2014 TOR Complex 2 (TORC2) TOR + RICTOR (rapamycin-insensitive companion of MTOR) + LST8, and mammalian stress-activated protein kinase interacting protein 1 (mSIN1)
- 34. 34 Rexin et al., 2015
- 35. 35 Yeast - 34 Autophagy Related Genes (ATG) Rice – 33 (Arabidopsis, Wheat, soya.....) APG, AUT, CVT,GSA, PAG,PDD etc. 2003 – Yeast researchers Nomenclature ‘ATG’ Xin et al., 2014 Autophagy-related Genes/proteins (ATGs)
- 36. 3 classes 36 i) ATG1-ATG13 kinase complex ii) ATG6/vps30 complex iii) ATG5-ATG12 complex and ATG8-PE complex (two ubiquitin like conjugation systems)
- 37. 37 ATG1-ATG13 kinase complex (Cycling Complex) PI3 kinase complex ATG6/vps30 complex ATG5-ATG12 complex and ATG8-PE Avin-Wittenberg et al., 2012
- 38. 1.Induction - ATG1-ATG13 kinase complex Induction of Autophagy Recruitment of core Atg proteins for PAS organisation ATG1-ATG13 kinase complex Induction of Autophagy Activates PI3K 1 VPS34 Atg6/ VPS30 Atg14 VPS15 VPS34 PI3K 1 complex Phagophore formation P PI3KP Produces
- 39. 2. Expansion & 3. Maturation Atg2 Atg18 Atg9 Atg9 complex Lipids recruitment Atg6/ VPS30 Atg14 VPS15 VPS34 PI3K 1 complex Phagophore formation P PI3KP Produces Atg6/ VPS30 VPS34 Atg14 membrane phospholipid Phagophore ER, PM, Golgi, M’condria Two ubiquitin like Conjugation systems Atg9 Atg12 Atg5 Atg7 Atg16 Atg10 E1 E2 1st Atg7 PE Atg4 Atg8 Atg8 Atg8
- 41. 41 Selective Autophagy ATG8 dependent Many selective substrates have ATG8-interacting motifs (AIMs) which bind to ATG8 on autophagic membranes
- 42. Mechanism of Selective Autophagy 42
- 43. 43 Batoko et al., 201
- 44. Techniques to Study Autophagy Transmission electron microscopy (TEM) analysis remains “the golden standard,”. 44 Electron micrographs of representative Arabidopsis cells grown for 12 h in (A) control medium supplemented with 1.5% sucrose (B) in sucrose-free medium 1. Electron microscopy
- 45. 2.Molecular Markers • Proteins involved in autophagy • autophagy-related phenotypes under different experimental conditions - caused by ATG gene modifications in Arabidopsis thaliana 45 Mitou et al., 2009
- 46. Tests of Lysosomal/Vacuolar Activity Lysotracker - visualize acidic compartments - specific markers of autophagy Concanamycin A - a compound that blocks the degradation of autophagic bodies within the central vacuole Acridine Orange (AO) - fluorescent basic dye accumulates in acidic compartments, where it forms aggregates that fluoresce bright red. • In acridine orange-stained cells, cytoplasm and nucleolus emit bright green fluorescence, whereas acidic compartments fluoresce in bright red. Monodansylcadaverine (MDC). The autofluorescent substance MDC is commonly used to detect autophagic vacuoles in plants and in other organisms E64d - inhibit autophagy, autophagic vesicles accumulates inside vacuoles 46
- 47. Role of Autophagy in Human Diseases 47 Autophagy can both inhibit and promote cancer formation through different mechanisms, depending on the stage of tumour Autophagy has multiple roles during tumorigenesis
- 48. 48 Liu and Ryan, 2012
- 49. 49 Role of autophagy in various metabolic diseases Choi et al., 2014
- 50. Physiological Roles of Autophagy in plants50 1. Autophagy in Nutrient Starvation sucrose, carbon and nitrogen - activate autophagy AtATG7, AtATG8, and AtATG9 yellowing of leaves expression of AtSEN1, a senescence marker gene, accelerate senescence Involved in Root hair formation and root elongation under nutrient starvation conditions - Li et al.,2015
- 51. 2. Autophagy in the Oxidative Stress Response 51 Reactive oxygen species (ROS) Activated derivatives of oxygen Highly toxic materials - accumulate in large amounts under various environmental stress conditions and/or during developmental stages Cell death - Damage to carbohydrates, DNA, lipids, and proteins Reduction in degradation efficiency DSSP
- 52. 3. Autophagy in Development 52 Cell growth and differentiation Root hair formation and root elongation under nutrient starvation conditions ATG2 and ATG5 Autophagy induction - not observe in the root tips in response to sucrose deprivation AtAtg6 - Arabidopsis homolog of yeast Atg6/Vps30 and tobacco Beclin 1 proteins, lead to pollen germination defects when disrupted – Qin et al., 2007 ATG8-interacting proteins (ATI1 and ATI2) over expressed or suppressed in both ATI1 and ATI2, respectively, stimulates or inhibits seed germination Honig et al., 2012
- 53. 4. Autophagy as a defence against intracellular pathogens 53 Xenophagy – pathway HR in which plant cells at the site of infection are killed by programmed cell death, ATG6 - uncontrolled HR Autophagy has also been reported to play important roles in suppression of cell death and defense response to, the powdery mildew fungus through AtATG2 and AtATG18 in Arabidopsis - Wang et al., 2011 An orthologue of the ATG6 gene was studied in Nicotiana benthamiana. Silencing of the ATG6 gene by RNA interference in plants resulted in reduced autophagy and uncontrolled HR upon infection with tobacco mosaic
- 54. 4. Autophagy in Programmed Cell Death 54 Autophagy is a mechanism that facilitates cell survival in response to abiotic and biotic stresses and controls PCD by degrading toxic cellular components Mariño et al., 2014 Functional relationship between autophagy and
- 55. 55 Li et al.,2015, 468: 800- 806 Identified an SiATG8a, from foxtail millet SiATG8a is mainly expressed in stems and its expression was induced by drought stress and nitrogen starvation Objective : To analyse the effect of autophagy during nitrogen starvation and to drought stress
- 56. 56 For the nitrogen starvation - Seeds were germinated on MS medium and 15 days old seedlings were treated with N-deficient liquid medium For the drought stress treatments, 3-week-old seedlings were treated with 6% PEG for 1 h, 6 h, 24 h, 36 h, and 48 h MDA (malondialdehyde) MDA: marker for stress.
- 57. Expression patterns of SiATG8a gene 57
- 58. 58 Overexpression of SiATG8a in transgenic Arabidopsis enhanced tolerance to nitrogen starvation
- 59. 59 Overexpression of SiATG8a enhanced tolerance to drought stress in transgenic Arabidopsis.
- 60. Future perspectives of autophagy in plants 60 Poorly understood - no suitable molecular marker to trace when and where autophagy is induced in plants Only a few autophagy and autophagy-related mutants have been identified in plants Approaches and methods for analyzing autophagy reported in the literature are not always appropriate
- 61. Future perspectives 61 Crosstalk between autophagy and photosynthesis Transcriptional and post-transcriptional regulation The lipid composition of autophagosomal membranes, and the way lipids are mobilized, delivered and assembled within them Mechanisms and physiological roles of granulophagy and ribophagy in plants The role of autophagy in cell remodelling during cell differentiation Manipulation of autophagy for better nutrient management at the whole-plant level. Metabolic checkpoints in autophagy regulation in source and sink tissues
- 63. REFERENCES 63 Floyd, B. E., Pu, Y., Soto-Burgos, J. and Bassham, D. C, 2015, To live or die: autophagy in plants. Springer,Switzerland, pp.269-300. DOI: 10.1007/978-3-319-21033-9_11. Li, W., Chen, M., Zhong, L., Liu, J., Xu, Z., Li, L., Zhou, Y., Guo, C. and Ma, Y., 2015, Overexpression of the autophagy- related gene SiATG8a from foxtail millet (Setaria italica L.) confers tolerance to both nitrogen starvation and drought stress in Arabidopsis. Biochem. Biophys. Res. Commun, 468: 800-806. Ryabovol, V. V. and Minibayeva, F. V, 2016, Molecular mechanisms of autophagy in plants: Role of ATG8 proteins in formation and functioning of autophagosomes. Biochemistry, 81(4): 348-363. Wen, X. and Klionsky, D. J., 2016, An overview of macroautophagy in yeast. J Mol Biol, 428(9): 1681-1699 White, E., 2013, Deconvoluting the context-dependent role for autophagy in cancer. Nat Rev Cancer, 12(6): 401–410. Xin, L., Xiaojun, P., Gongwei, Q., Tong, Z. and Honghui, L., 2014, The roles of autophagy in development and stress responses in Arabidopsis thaliana. Apoptosis, 19: 905-921 https://www.nobelprize.org/prizes/medicine/2016/press-release/ https://en.wikipedia.org/wiki/Yoshinori_Ohsumi https://www.nobelprize.org/prizes/medicine/2016/ohsumi/lecture/
- 64. 64
Editor's Notes
- Although proteins are marginally stable and exhibit a level of mutational robustness, they do misfold under excessive environmental stresses or mutations. Prompt degradation of irreversibly damaged proteins is essential to preserve normal cellular function Cells maintain their homeostasis through continuous synthesis and degradation of their components.
- neurodegenerative diseases such as Alzheimer’s, Huntington, Parkinson’s, and the prion maladies.
- Ubiquitination requires three types of enzyme: ubiquitinactivating enzymes, ubiquitin-conjugating enzymes, and ubiquitin ligases, known as E1s, E2s, and E3s, respectively.
- The other major pathway of protein degradation in eukaryotic cells involves the uptake of proteins by lysosomes
- Autophagy is a process in which a eukaryotic (but not prokaryotic) cell destroys its own components through the lysosomal machinery.
- Foundation stone was kept by the discovery of Lysosome, of Ignition to the mechanism of Autophagy given by Christien duve
- Historical landmarks of autophagy research
- Micropexophagy is a selective microautophagic pathway that engulfs a cluster of damaged and/or superfluous peroxisomes Process of non-selective microautophagy can be observed in all types of eucaryotic cells.
- Microautophagy, as well as macroautophagy, helps cells to withstand prolonged starvation by ceaseless recycle of nutrients and energy
- A unique feature of this pathway is that all substrate proteins contain in their amino acid sequence a motif, biochemically related to the pentapeptide KFERQ,
- Selectively degrade viral proteins bacterial proteins, prions, fungal proteins etc.
- Autophagy appears to be a highly conserved process, since it has been found in all eukaryotic organisms
- Plant cells employ multiple catabolic mechanisms to remove dysfunctional and unneeded constituents and to recycle intracellular nutrients. A major route involves macroautophagy (hereafter referred to as autophagy), which encapsulates and delivers cytoplasmic material to the vacuole for breakdown (reviewed in . Central to this process is the de novo formation of a cup-shaped vesicle called the phagophore (or isolation membrane) by a set of AUTOPHAGY-RELATED (ATG) proteins that localize within a common phagophore assembly site (PAS). The phagophore elongates, engulfs cytoplasmic material, and eventually seals to create a double membrane-enclosed compartment called the autophagosome, which subsequently fuses with the vacuole/lysosome to release the internal vesicle as an autophagic body. The autophagic body and its cargo are then degraded by vacuolar hydrolases, and the resulting metabolites are exported back to the cytoplasm for reuse.
- defective or in excess, cytotoxic protein aggregates (aggrephagy), and even invading pathogens (xenophagy) (Johansen and Lamark, 2011).
- The scaffold proteins have several roles. First, they interact with and recruit other core autophagy machinery components, such as the Atg1 complex38 (FIG. 3c–f); during starvation, typically both Atg11 and Atg17 are involved. During nutrient deprivation, the target of rapamycin complex 1 (TORC1), which is a protein kinase, is inactivated, resulting in hypophosphorylation of Atg13 (REF. 39) (FIG. 1). The hypophosphorylated Atg13–Atg1 complex is then bound by the Atg17–Atg29–Atg31 complex and recruited to form the PAS38,40,41. Interestingly, Atg11 can recruit Atg17 to the PAS in the absence of Atg1 and Atg13 through interactions with the Atg29–Atg31 complex42. transmembrane protein ATG9 which helps deliver lipids to the expanding phagophore in conjunction with the peripheral ATG2 and ATG18 proteins. Active Atg1 phosphorylates itself as well as the autophagy-related integral membrane protein Atg9, which recruits the Atg2–Atg18 complex to initiate phagophore membrane elongation4 The transmembrane protein Atg9 cycles between the mitochondria and the pre-autophagosomal structure, which is the site of autophagosome biogenesis. Atg9 is thought to mediate the delivery of membrane to the forming autophagosome.
- In all organisms studied, under high-nutrient conditions, TOR activates protein synthesis and growth pathways and inhibits autophagy, whereas under low-nutrient conditions, growth is blocked and autophagy is activated. TOR is so named because it was identified in screens for yeast mutants that are resistant to the effects of rapamycin. TOR is a member of the phosphatidylinositol kinase-related kinase family based on its sequence but functionally is a serine/ threonine protein kinase
- In budding yeast Saccharomyces cerevisiae, to date 34 Autophagy Related Genes (ATG)
- ATG genes have also been identified in various crop plants, such as soya, tomatoes, tobacco, wheat, rice, maize, etc. ryabovol 2016
- The scaffold proteins have several roles. First, they interact with and recruit other core autophagy machinery components, such as the Atg1 complex38 (FIG. 3c–f); during starvation, typically both Atg11 and Atg17 are involved. During nutrient deprivation, the target of rapamycin complex 1 (TORC1), which is a protein kinase, is inactivated, resulting in hypophosphorylation of Atg13 (REF. 39) (FIG. 1). The hypophosphorylated Atg13–Atg1 complex is then bound by the Atg17–Atg29–Atg31 complex and recruited to form the PAS38,40,41. Interestingly, Atg11 can recruit Atg17 to the PAS in the absence of Atg1 and Atg13 through interactions with the Atg29–Atg31 complex42. transmembrane protein ATG9 which helps deliver lipids to the expanding phagophore in conjunction with the peripheral ATG2 and ATG18 proteins. Active Atg1 phosphorylates itself as well as the autophagy-related integral membrane protein Atg9, which recruits the Atg2–Atg18 complex to initiate phagophore membrane elongation4 The transmembrane protein Atg9 cycles between the mitochondria and the pre-autophagosomal structure, which is the site of autophagosome biogenesis. Atg9 is thought to mediate the delivery of membrane to the forming autophagosome.
- The first mechanism is ATG8 dependent (Fig. 3a). Many selective substrates have LC3-interacting regions (LIRs, also known as ATG8-interacting motifs (AIMs)) or GABARAP-interacting motifs (GIMs), which bind to ATG8 (LC3s and GABARAPs in mammals) on autophagic membranes71,72
- Fig. 3 | Potential mechanisms of selective macroautophagy. a, Selective substrates (such as proteins, organelles and bacteria) have or recruit autophagy receptors (for example, SQSTM1/p62, NBR1 and optineurin), which are recognized by ATG8 (LC3 and GABARAP in mammals) family proteins on the autophagosomal membrane. To recruit receptors, substrates are often ubiquitinated and bind to the ubiquitin-binding regions in autophagy receptors. b, Autophagy receptors recruit the autophagy initiation complex (ATG1 and ULK complexes in yeast and mammals, respectively) either directly or indirectly to induce autophagy. c, Selective substrates (for example, ubiquitinated proteins, damaged organelles or bacteria) may accumulate at the site of autophagosome formation and are engulfed by autophagosomes even without direct recognition. d, Autophagic membranes may elongate by wetting on the surface of intracellular condensates (liquid/fluid droplets) generated by liquid–liquid phase separation.
- Understanding and exploiting autophagy signaling in plants
- Proteins that are involved in the autophagy process or that are degraded specifically through autophagy have been used to monitor autophagic activity. Several of them are already in use in plants. Plants knockout and transgenic for these markers are useful tools to study autophagy-related phenotypes under different experimental conditions
- - The autofluorescent substance MDC is commonly used to detect autophagic vacuoles in plants and in other organisms - Spherical structures were observed by fluorescence microscopy
- Reactive oxidative species (ROS) are highly toxic materials that accumulate in large amounts under various environmental stress conditions and/or during developmental stages ROS can lead to cell death by causing damage to carbohydrates, DNA, lipids, and proteins Oxidized proteins also accumulate in those plants due to a reduction in degradation efficiency Oxidized proteins also accumulate in those plants due to a reduction in degradation efficiency (Xiong et al., 2007a). These results demonstrate that oxidized and damaged cellular components produced during oxidative stress are transferred to the vacuole for autophagic degradation
- Wild-type and transgenic Arabidopsis seedlings grown under nitrogen starvation conditions. Lateral root numbers (B), the total surface area of roots (C), the total surface area of leaves (D), root length (E), nitrogen content (F), and protein content (G) of wild-type and transgenic plants. Values are means ± standard deviation (SD) (n ¼ 3 independent experiments, t-test; identical and different letters represent, respectively, non-significant and significant differences).
- Reactive oxygen species degrade polyunsaturated lipids, forming malondialdehyde - The production of this aldehyde is used as a biomarker to measure the level of oxidative stress in an organism
- The molecular mechanism and physiological role of autophagy in plants, however, is still poorly understood No suitable molecular marker to trace when and where autophagy is induced in plants and only a few autophagy and autophagy-related mutants have been identified in plants
- The following are key topics for future research into plant autophagy