PCD-otofajinin bitki immünitesiyle korelasyonu

Year 2023, Volume: 60 Issue: 1, 181 - 195, 01.04.2023

Berna Baş

https://doi.org/10.20289/zfdergi.1074706

Abstract

Önemli bir katabolik olay olan otofaji bitkilerin gelişim süreçlerinde ve biyotik/abiyotik strese verdiği tepki sonucunda istenmeyen/hasarlı yapıların/moleküllerin sitoplazmik içerikle beraber vakuollerin içine alınarak litik enzimlerle parçalanması ve nihayet sitoplazmanın tasfiyesiyle hücre ölümü olayıdır. Otofaji konukçu-patojen interaksiyonlarında bitki immünitesinin düzenlenmesinde birçok önemli role sahiptir. Patojen organizmaların yaşam stratejilerine göre bitkilerde otofaji yoluyla hipersensitif reaksiyon (HR) ölümleri ya baskılanmakta ya da teşvik edilmektedir. Aslında otofaji bitki hücrelerinin biyotik faktörlere karşı kendini korumak ve homeostazı stabil tutmak amacıyla patojenleri veya patojene ait yapıları ortadan kaldırmak suretiyle yeni bir adaptasyon yolu olarak da düşünülebilir. HR hücre ölümlerinde otofajinin moleküler mekanizması kesin olarak bilinmese de, otofajiye dahil olan proteolitik enzimlerin HR hücre ölümlerini desteklemesi nedeniyle, bitki ETI (Effector-Triggered Immunity) immün sistemin bileşenlerinden olan HR programlı hücre ölüm kapsamında ele alınmaktadır. Otofaji bitki immünitesinde anti-patojenik yeni bir sistem olmaya aday doğal bir hücresel prosestir. Yeni çalışmalar, bitki immünitesinde HR-PCD (HR-Programmed Cell Death) sürecinde hücre yıkımının otofajiyle bağlantılı olduğunu düşündürmektedir. Bu derleme otofajik sistem ağının bitki immünitesiyle koreleli olduğunu örneklerle açıklamaktadır.

Keywords

Bitki immünitesi, hipersensitif tepki, otofaji, programlı hücre ölümü

Correlation with plant immunity of PCD-autophagy

Abstract

Autophagy, a major catabolic reaction, is cell death by lysis of undesirable/ damaged structures/molecules with some cytoplasmic contents engulfed by vacuoles and result finally in degredation of whole cytoplasm as a part of developmentel processes and to respond biotic/abiotic stresses for homeostasis. Autophagy has multifunctional significant roles in regulation of plant immunity during host-pathogen interactions. Hypersensitive reaction (HR) deaths caused by autophagy can either inhibited or induced depending on life strategies of the pathogen organisms. In fact, autophagy can be considered as a kind of any adaptation way ridding of pathogenes or a section of pathogen properties to maintain the cell itself and for stability of cellular homeostasis versus biotic factors. Although molecular mechanisms of autophagy in HR cell death is unknown, HR that is considered as ETI (Effector-Triggered Immunity) defense from tiered of plant immune system is involved in programmed cell death due to encouraged HR cell death of proteolytic enzymes in autophagy. As a candidate to be novel antipathogenic system in plant immunity, autophagy is already naturally available cellular process. Recent evidences suggest that cell degradation during HR-PCD (HR-Programmed Cell Death) in plant immunity is linked to autophagy process. This review explains with examples that the autophagic system network is correlated with plant immunity.

Keywords

Plant immunity, hypersensitive reaction, autophagy, programmed cell death

References

• Ahmad, R., Y. Zuily-Fodil, C. Passaquet, O. Bethenod, R. Roche & A. Repellin, 2012. Oozone and aging up-regulated type II metacaspase gene expression and global metacaspase activitiy in the leaves of field-grown maize (Zea mays L.) plants. Chemosphere, 87 (7): 789-795. https://doi.org/10.1016/j.chemosphere.2011.12.081
• Aubrey, B.J., G.L. Kelly, A. Janic, M.J. Herold & A. Strasser, 2018. How does p53 induce apoptosis and how does this relate to p53-mediated tumour suppression? Cell Death and Differentiation, 25 (1): 104-113. https://doi.org/10.1038/cdd.2017.169
• B-Debate, 2013. International Center for Scientific Debate Barcelona (Web page. https://www.bdebate.org/en/news/programmed-cell-death-plants-can-help-tackle-increased-food-needs) (Date accessed: Mart 2022)
• Bai, S., J. Liu, C. Chang, L. Zhang, T. Maekawa, Q. Wang, W. Xiao, Y. Liu, J. Chai, F.L. Takken, P. Schulze-Lefert & Q.H. Shen, 2012. Structure-function analysis of barley NLR immune receptor MLA10 reveals its cell compartment specific activity in cell death and disease resistance. PLoS pathogens, 8 (6):e1002752. https://doi.org/10.1371/journal.ppat.1002752
• Balakireva, A.V. & A.A. Zamyatnin, 2018. Indispensable role of proteases in plant innate immunity. International Journal of Molecular Sciences, 19 (2): 629. https://doi.org/10.3390/ijms19020629
• Balakireva, A.V., A.A. Deviatkin, V.G. Zgoda, M.I. Kartashov, N.S. Zhemchuzhina, V.G. Dzhavakhiya, A.V. Golovin & A.A. Zamyatnin, Jr,, 2018. Proteomics analysis reveals that caspase-like and metacaspase-like activities are dispensable for activation of proteases involved in early to biotic stress in Triticum aestivum L. International Journal of Molecular Sciences, 19 (12): 3991. https://doi.org/10.3390/ijms19123991
• Balint-Kurti, P., 2019. The plant hypersensitive response: concepts, control and consequences. Molecular Plant Pathology, 20 (8): 1163-1178. https://doi.org/10.1111/mpp.12821
• Baskett, J.A., 2012. A type II metacaspase interacts with rps1-k-2 in soybean and analysis of the soybean metacaspase gene family. College of Agriculture and Life Sciences, Iowa State University, Thesis. Iowa, USA. 65 pp. https:
• Bernoux, M., T. Ve, S. Williams, C. Warren, D. Hatters, E. Valkov, X. Zhang, J.G. Ellis, B. Kobe & P.N. Dodds, 2011. Structural and functional analysis of a plant resistance protein TIR domain reveals interfaces for self-association, signaling, and autoregulation. Cell Host & Microbe, 9 (3): 200-211. https://doi.org/10.1016/j.chom.2011.02.009
• Bollhöner, B., B. Zhang, S. Stael, N. Denance, K. Overmyer, D. Goffner, F. van Breusegem & H. Tuominen, 2013. Post mortem function of AtMC9 in xylem vessel elements. The New Phytologist, 200 (2): 498-510. https://doi.org/10.1111/nph.12387
• Bollhöner, B., J. Prestele & H. Tuominen, 2012. Xylem cell death: emerging understanding of regulation and function. Journal of Experimental Botany, 63 (3): 1081-1094. https://doi.org/10.1093/jxb/err438
• Bozhkov, P.V., 2018. Plant autophagy: mechanisms and functions. Journal of Experimental Botany, 69 (6): 1281–1285. https://doi.org/10.1093/jxb/ery070
• Chang, H.X., L.L. Domier, O. Radwan, C.R. Yendrek, M.E. Hudson & G.L. Hartman, 2016. Identification of multiple phytotoxins produced by Fusarium virguliforme including a phytotoxic effector (FvNIS1) associated with sudden death syndrome foliar symptoms. Molecular plant-microbe interactions: MPMI, 29 (2): 96-108. https://doi.org/10.1094/MPMI-09-15-0219-R
• Chichkova, N.V., A.I. Tuzhikov, M. Taliansky & A.B. Vartapetian, 2012. Plant phytaspases and animal caspases: structurally unrelated death proteases with a common role and specificity. Physiologia Plantarum, 145 (1): 77-84. https://doi.org/10.1111/j.1399-3054.2011.01560.x
• Chichkova, N.V., J. Shaw, R.A. Galiullina, G.E. Drury, A.I. Tuzhikov, S.H. Kim, M. Kalkum, T.B. Hong, E.N. Gorshkova, L. Torrance, A.B. Vartapetian & M. Taliansky, 2010. Phytaspase, a relocalisable cell death promoting plant protease with protease with caspase specificity. The EMBO Journal, 29 (6): 1149-1161. https://doi.org/10.1038/emboj.2010.1
• Coll, N.S., A. Smidler, M. Puigvert, C. Popa, M. Valls & J.L. Dangl, 2014. The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy. Cell death and differentiation. 21 (9): 1399-1408. https://doi.org/10.1038/cdd.2014.50
• Coll, N.S., D. Vercammen, A. Smidler, C. Clover, F. van Breusegem, J.L. Dangl & P. Epple, 2010. Arabidopsis type I metacaspases control cell death. Science, 330 (6009):1393-1397. https://doi.org/10.1126/science.1194980
• Coll, N.S., P. Epple & J.L. Dangl, 2011. Programmed cell death in the plant immune system. Cell Death and Differentiation. 18 (8): 1247-1256. https://doi.org/10.1038/cdd.2011.37
• Daskalov, A., B. Habenstein, R. Sabaté, M. Berbon, D. Martinez, S. Chaignepain, B. Coulary-Salin, K. Hofmann, A. Loquet & S.J. Saupe, 2016. Identification of a novel cell death-inducing domain reveals that fungal amyloid-controlled programmed cell death is related to necroptosis. Proceedings of the National Academy of Sciences of the United States of America, 113 (10): 2720-2725. https://doi.org/10.1073/pnas.1522361113
• Daskalov, A., J. Heller, S. Herzog, A. Fleißner & N.L. Glass, 2017. Molecular mechanisms regulating cell fusion and heterokaryon formation in filamentous fungi. Microbiology Spectrum, 5 (2): FUNK0015-2016. https://doi.org/10.1128/microbiolspec.FUNK-0015-2016
• Dickman, M.B. & P. de Figueiredo, 2013. Death be not proud-cell death control in plant fungal interactions. PLoS Pathogens, 9 (9): e1003542. https://doi.org/10.1371/journal.ppat.1003542
• Domínguez, F., J. Moreno & F.J. Cejudo, 2012. The scutellum of germinated wheat grains undergoes programmed cell death: identification of an acidic nuclease involved in nucleus dismantling. Journal of Experimental Botany, 63 (15): 5475-5485. https://doi.org/10.1093/jxb/ers199
• Fang, Y., K. Xie & L. Xiong, 2014. Conserved miR164-targeted NAC genes negatively regulate drought resistance in rice. Journal of Experimental Botany, 65 (8): 2119-2135. https://doi.org/10.1093/jxb/eru072
• Faris, J.D. & T.L. Friesen, 2020. Plant genes hijacked by necrotrophic fungal pathogens. Current Opinion in Plant Biology, 56: 74-80. https://doi.org/10.1016/j.pbi.2020.04.003
• Fendrych, M., T. van Hautegem, M. van Durme, Y. Olvera-Carrillo, M. Huysmans, M. Karimi, S. Lippens, C.J. Guérin, M. Krebs, K. Schumacker & M.K. Nowack, 2014. Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Current Biology, 24 (9): 931-940. https://doi.org/10.1016/j.cub.2014.03.025
• Fernández, M.B., G.R. Daleo & M.G. Guevara, 2012. DEVDase activity is induced in potato leaves during Phytophthora infestans infection. Plant Physiology and Biochemistry, 61: 197-203. https://doi.org/10.1016/j.plaphy.2012.10.007
• Filomeni, G., D. De Zio & F. Cecconi, 2015. Oxidative stress and autophagy: the clash between damage and metabolic needs. Cell Death & Differentiation, 22 (3): 377-388. https://doi.org/10.1038/cdd.2014.150
• Frank, D. & J.E. Vince, 2019. Pyroptosis versus necroptosis: similarities, differences, and crosstalk. Cell Death and Differentiation, 26 (1): 99-114. https://doi.org/10.1038/s41418-018-0212-6
• Fuchs, Y. & H. Steller, 2011. Programmed cell death in animal development and disease. Cell, 147 (4): 742-758. https://doi.org/10.1016/j.cell.2011.10.033
• Galluzzi, L., I. Vitale, S.A. Aaronson, J.M. Abrams, D. Adam, P. Agostinis, E.S. Alnemri, L. Altucci, I. Amelio, D.W. Andrewset al. & G. Kroemer, 2018. Molecular mechanisms of cell death: recommendations of the nomenclature committee on cell death. Cell Death & Differentiation, 25 (3): 486-541. https://doi.org/10.1038/s41418-017-0012-4
• Giraldo, M.C. & B. Valent, 2013. Filamentous plant pathogen effectors in action. Nature Reviews Microbiology, 11 (11): 800-814. https://doi.org/10.1038/nrmicro3119
• Gobert, A., Y. Quan, M. Arrivé, F. Waltz, N. Da Silva, L. Jomat, M. Cohen, I. Jupin & P. Giegé, 2021. Towards plant resistance to viruses using protein-only RNase P. Nature Communications, 12 (1): 1007. https://doi.org/10.1038/s41467-021-21338-6
• Gonçalves, A.P., J. Heller, A. Daskalov, A. Videira & N.L. Glass, 2017. Regulated forms of cell death in fungi. Frontiers in Microbiology, 8: 1837. https://doi.org/10.3389/fmicb.2017.01837
• Grilo, A.L. & A. Mantalaris, 2019. Apoptosis: A mammalian cell bioprocessing perspective. Biotechnology Advances, 37 (3): 459-475. https://doi.org/10.1016/j.biotechadv.2019.02.012
• Hatsugai, N., K. Yamada, S. Goto-Yamada & I. Hara-Nishimura, 2015. Vascuolar processing enzyme in plant programmed cell death. Frontiers in Plant Science, 6: 234. https://doi.org/10.3389/fpls.2015.00234
• Hatsugai, N., S. Iwasaki, K. Tamura, M. Kondo, K. Fuji, K. Ogasawara, M. Nishimura & I. Hara-Nishimura, 2009. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes & Development, 23 (21): 2496-2506. https://doi.org/10.1101/gad.1825209
• Hauenstein, A.V., L. Zhang & H. Wu, 2015. The hierarchical structural architecture of inflammasomes, supramolecular inflammatory machines. Current Opinion in Structural Biology, 31: 75-83. https://doi.org/10.1016/j.sbi.2015.03.014
• He, R., G.E. Drury, V.I. Rotari, A. Gordon, M. Willer, T. Farzaneh, E.J. Woltering & P. Gallois, 2008. Metacaspase-8 modulates programmed cell death induced by ultraviolet light and H2O2 in Arabidopsis. The Journal of Biological Chemistry, 283 (2): 774-783. https://doi.org/10.1074/jbc.M704185200
• Kabbage, M., B. Williams & M.B. Dickman, 2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLoS Pathogens, 9 (4):e1003287. https://doi.org/10.1371/journal.ppat.1003287
• Kaneda, T., Y. Taga, R. Takai, M. Iwano, H. Matsui, S. Takayama, A. Isogai & F.S. Che, 2009. The transcription factor OsNAC4 is a key positive regulator of plant hypersensitive cell death. The EMBO Journal, 28 (7): 926-936. https://doi.org/10.1038/emboj.2009.39
• Kim, S.M., C. Bae, S.K. Oh, & D. Choi, 2013. A pepper (Capsicum annuum L.) metacaspase 9 (Camc9) plays a role in pathogen-induced cell death in plants. Molecular Plant Pathology, 14 (6): 557-566. https://doi.org/10.1111/mpp.12027
• Kumar, G.N.M., C.G. Kannangara & N.R. Knowles, 2022. Nucleases are upregulated in potato tubers afflicted with zebra chip disease. Planta, 255 (3): 54. https://doi.org/10.1007/s00425-022-03832-3
• Kumar, G.N.M., L.O. Knowles & N.R. Knowles, 2017. Zebra chip disease enhances respiration and oxidative stress of potato tubers (Solanum tuberosum L.). Planta, 246 (4): 625-639. https://doi.org/10.1007/s00425-017-2714-8
• Kumar, S., M. Kinoshita, M. Noda, N.G. Copeland & N.A. Jenkins, 1994. Induction of apoptosis by the mouse Nedd2 gene, which encodes a protein similar to the product of the Caenorhabditis elegans cell death gene ced-3 and the mammalian IL-1 beta-converting enzyme. Genes and Development, 8 (14): 1613-1626. https://doi.org/10.1101/gad.8.14.1613
• Kumar, S., Y. Tomooka & M. Noda, 1992. Identification of a set of genes with developmentally down-regulated expression in the mouse brain. Biochemical and Biophysical Research Communications, 182 (3): 1155-1161. https://doi.org/10.1016/0006-291x(92)91747-e
• Kuroyanagi, M., K. Yamada, N. Hatsugai, M. Kondo, M. Nishimura & I. Hara-Nishimura, 2005. Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. The Journal of Biological Chemistry, 280 (38): 32914-32920. https://doi.org/10.1074/jbc.M504476200
• Kwon, S.I. & D.J. Hwang, 2013. Expression analysis of the metacaspase gene family in Arabidopsis. Journal of Plant Biology, 56 (6): 391-398. https://doi.org/10.1007/s12374-013-0290-4
• Latrasse, D., M. Benhamed, C. Bergounioux, C. Raynaud & M. Delarue, 2016. Plant programmed cell death from a chromatin point of view. Journal of Experimental Botany, 67 (20): 5887-5900. https://doi.org/10.1093/jxb/erw329
• Lee, M.H., H.S. Jeon, H.G. Kim & O.K. Park, 2017. An Arabidopsis NAC transcription factor NAC4 promotes pathogen-induced cell death under negative regulation by microRNA164. The New Phytologist, 214 (1): 343-360. https://doi.org/10.1111/nph.14371
• Levine, A., R.I. Pennell, M.E. Alvarez, R. Palmer & C. Lamb, 1996. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Current Biology, 6 (4): 427-437. https://doi.org/10.1016/s0960-9822(02)00510-9
• Li, F. & R.D.Vierstra, 2012. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends in Plant Sciences, 17 (9): 526-537. https://doi.org/10.1016/j.tplants.2012.05.006
• Liu, Y. & D.C. Bassham, 2012. Autophagy: pathways for self-eating in plant cells. Annual Review of Plant Biology, 63: 215-237. https://doi.org/10.1146/annurev-arplant-042811-105441
• Liu, Y., M. Schiff, K. Czymmek, Z. Tallóczy, B. Levine & S.P. Dinesh-Kumar, 2005. Autophagy regulates programmed cell death during the plant innate immune response. Cell, 121 (4): 567-577. https://doi.org/10.1016/j.cell.2005.03.007
• Liu, Z., Z. Zhang, J.D. Faris, R.P. Oliver, R. Syme, M.C. McDonald, B.A. McDonald, P.S. Solomon, S. Lu, W.L. Shelver, S. Xu & T.L. Friesen, 2012. The cysteine rich necrotrophic effector SnTox1 produced by Stagonospora nodorum triggers susceptibility of wheat lines harboring Snn1. PLoS pathogens, 8 (1):e1002467. https://doi.org/10.1371/journal.ppat.1002467
• Locato, V. & L. De Gara, 2018. ‛‛Programmed Cell Death in Plants: An Overview, 1-8’’. In: Programmed Cell Death Methods and Protocol, 1st ed. (Ed: De Gara L, Locato V.) Vol. 1743. Humana Press, New York, NY, 198 pp. https://doi.org/10.1007/978-1-4939-7668-3_1
• Lord, C.E. & A.H. Gunawardena, 2012. Programmed cell death in C. elegans, mammals and plants. European journal of cell biology, 91 (8): 603-613. https://doi.org/10.1016/j.ejcb.2012.02.002
• Mendes, G.C., P.A. Reis, I.P. Calil, H.H. Carvalho, F.J. Aragao & E.P. Fontes, 2013. GmNAC30 and GmNAC81 integrate the endoplasmic retikulum stress- and osmotic stress-induced cell death responses through a vacuolar processing enzyme. Proceedings of the National Academy of Sciences of the United States of America,110 (48): 19627-19632. https://doi.org/10.1073/pnas.1311729110
• Mengiste, T., 2012. Plant Immunity to necrotrophs. Annual Review of Phytopathology, 50: 267-294. https://doi.org/10.1146/annurev-phyto-081211-172955
• Minina, E.A., L.H. Filonova, K. Fukada, E.I. Savenkov, V. Gogvadze, D. Clapham, V. Sanchez-Vera M.F. Suarez, B. Zhivotovsky, G. Daniel, A. Smertenko & P.V. Bozhkov, 2013. Autophagy and metacaspase determine the mode of cell death in plants. The Journal of Cell Biology, 203 (6):917–927. https://doi.org/10.1083/jcb.201307082
• Minina, E.A., P.V. Bozhkov & D. Hofius, 2014. Autophagy as initiator or executioner of cell death. Trends in Plant Science, 19 (11): 692-697. https://doi.org/10.1016/j.tplants.2014.07.007
• Misas-Villamil, J.C., G. Toenges, I. Kolodziejek, A.M. Sadaghiani, F. Kaschani, T. Colby, M. Bogyo & R.A. van der Hoorn, 2013. Acivity profiling of vacuolar processing enzymes reveals a role for VPE during oomycete infection. The Plant Journal, 73 (4): 689-700. https://doi.org/10.1111/tpj.12062
• Misas-Villamil, J.C., R.A. van der Hoorn & G. Doehlemann, 2016. Papain-like cysteine proteases as hubs in plant immunity. The New Phytologist, 212 (4): 902-907. https://doi.org/10.1111/nph.14117
• Mittler R., L. Simon & E. Lam, 1997. Pathogen-induced programmed cell death in tobacco. Journal of Cell Sciences, 110 (11): 13333-1344. https://doi.org/10.1242/jcs.110.11.1333
• Moyano, L., M.D. Correa, L.C. Favre, F.S. Rodríguez, S. Maldonado & M.P. López-Fernández, 2018. Activation of nucleases, PCD and mobilization of reserves in Araucaria angustifolia megagametophyte during germination. Frontiers of Plant Science, 9: 1275. https://doi.org/10.3389/fpls.2018.01275
• Moyano, L., M.P. Lopéz-Fernández, A. Carrau, J.M. Nannini, S. Petrocelli, E.G. Orellano & S. Maldonado, 2020. Red light delays programmed cell death in non-host interaction between Pseudomonas syringae pv tomato DC3000 and tobacco plants. Plant Science: an international journal of experimental plant biology, 291: 110361. https://doi.org/10.1016/j.plantsci.2019.110361
• Nanson, J.D., B. Kobe & T. Ve, 2019. Death, TIR, and RHIM: Self-assembling domains involved in innate immunity and cell-death signaling. Journal of Leukocyte Biololgy, 105 (2): 363-375. https://doi.org/10.1002/JLB.MR0318-123R
• Nirmala, J.G. & M. Lopus, 2020. Cell death mechanisms in eukaryotes. Cell Biology and Toxicology, 36 (2): 145-164. https://doi.org/10.1007/s10565-019-09496-2
• Nuruzzaman, M., R. Manimekalai, A.M. Sharoni, K. Satoh, H. Kondoh, H. Ooka & S. Kikuchi, 2010. Genome-wide analysis of NAC transcription factor family in rice. Gene, 465 (1-2): 30-44. https://doi.org/10.1016/j.gene.2010.06.008
• Ogata, T., Y. Kida, T. Arai, Y. Kishi, Y. Manago, M. Murai & Y. Matsushita, 2012. Overexpression of tobacco ethylene response factor NtERF3 gene and its homologues from tobacco and rice induces hypersensitive response-like cell death in tobacco. Journal of General Plant Pathology,78 (1): 8-17. https://doi.org/10.1007/s10327-011-0355-5
• Ogita, N., Y. Okushima, M. Tokizawa, Y.Y. Yamamoto, M. Tanaka, M. Seki, Y. Makita, M. Matsui, K. Okamoto-Yoshiyama, T. Sakamoto, T. Kurata, K. Hiruma, Y. Saijo, N. Takahashi & M. Umeda, 2018. Identifying the target genes of SUPPRESSOR OF GAMMA RESPONSE 1, a master transcription factor controlling DNA damage response in Arabidopsis. The Plant Journal: for cell and molecular biology, 94 (3): 439-453. https://doi.org/10.1111/tpj.13866
• Ootsubo, Y., T. Hibino, T. Wakazono, Y. Mukai & F.S. Che, 2016. IREN, a novel EF-hand motif-containing nuclease functions in the degradation of nuclear DNA during hypersensitive response cell death in rice. Bioscience, Biotechnology and Biochemistry, 80 (4): 748-760. https://doi.org/10.1080/09168451.2015.1123610
• Paoletti, M, 2016. Vegetative incompatibility in fungi: from recognition to cell death, whatever does the trick. Fungal Biology Reviews, 30 (4): 152-162. https://doi.org/10.1016/j.fbr.2016.08.002
• Paoletti, M. & C. Clavé, 2007. The fungus-specific HET domain mediates programmed cell death in Podospora anserina. Eukaryotic Cell, 6 (11): 2001-2008. https://doi.org/10.1128/EC.00129-07
• Pérez-Pérez, M.E., S.D. Lemaire, S.D. & J.L. Crespo, 2012. Reactive oxygen species and autophagy in plants and algae. Plant Physiology, 160 (1): 156-164. https://doi.org/10.1104/pp.112.199992
• Petrov, V., J. Hille, B. Mueller-Roeber & T.S. Gechev, 2015. ROS-mediated abiotic stress-induced programmed cell death in plants. Frontiers in Plant Science, 6: 69. https://doi.org/10.3389/fpls.2015.00069
• Pitsili, E., U.J. Phukan & N.S. Coll, 2020. Cell Death in Plant Immunity. Cold Springer Harbor Perspectives in Biology, 12 (6): a036483. https://doi.org/10.1101/cshperspect.a036483
• Plackett, A.R., S.G. Thomas, Z.A. Wilson & P. Hedden, 2011. Gibberelin control of stamen development: a fertile field. Trends in Plant Science. 16: (10): 568-578. https://doi.org/10.1016/j.tplants.2011.06.007
• Ramirez, M. & G.S. Salvesen, 2018. A primer on caspase mechanisms. Seminars in cell & developmental biology, 82: 79–85. https://doi.org/10.1016/j.semcdb.2018.01.002
• Salguero-Linares, J. & N.S. Coll, 2019. Plant proteases in the control of the hypersensitive response. Journal of Experimental Botany. 70 (7): 2087-2095. https://doi.org/10.1093/jxb/erz030
• Salvesen, G.S., A. Hempel & N.S. Coll, 2016. Protease signaling in animal and plant-regulated cell death. The FEBS journal, 283 (14): 2577–2598. https://doi.org/10.1111/febs.13616
• Schulmeyer, K.H. & T.L. Yahr, 2017. Post-transcriptional regulation of type III secretion in plant and animal pathogens. Current Opinion in Microbiology, 36: 30-36. https://doi.org/10.1016/j.mib.2017.01.009
• Sharma, B., D. Joshi, P.K. Yadav, A.K. Gupta & T.K. Bhatt, 2016. Role of Ubiquitin-Mediated Degradation System in Plant Biology. Frontiers in Plant Sciences, 7: 806. https://doi.org/10.3389/fpls.2016.00806
• Sueldo, D.J. & R. van der Hoorn, 2017. Plant life needs cell death, but does plant cell death need Cys proteases?.The FEBS Journal, 284 (10): 1577-1585. https://doi.org/10.1111/febs.14034
• Sugawara, T., E.A. Trifonova, A.V. Kochetov & Y. Kanayama, 2016. Expression of an extracellular ribonuclease gene increases resistance to Cucumber mosaic virus in tobacco. BMC Plant Biology, 16 (Suppl 3): 246. https://doi.org/10.1186/s12870-016-0928-8
• Thomas, E.L. & R. van der Hoorn, 2018. Ten Prominent Host Proteases in Plant-Pathogen Interactions. International Journal of Molecular Sciences, 19 (2): 639. https://doi.org/10.3390/ijms19020639
• Thomas, H., 2013. Senescence, ageing and death of the whole plant. The New Phytologist, 197 (3): 696-711. https://doi.org/10.1111/nph.12047
• Tsiatsiani, L., E. Timmerman, P.J. De Bock, D. Vercammen, S. Stael, B. van de Cotte, A. Staes, M. Goethals, T. Beunens, P. van Damme, K. Gevaert & F. van Breusegem, 2013. The Arabidopsis metacaspase9 degradome. The Plant Cell, 25 (8): 2831-2847. https://doi.org/10.1105/tpc.113.115287
• Urbach, J.M. & F.M. Ausubel, 2017. The NBS-LRR architectures of plant R-proteins and metazoan NLRs evolved in independent events. Proceedings of the National Academy of Sciences of the United States of America, 114 (5): 1063-1068. https://doi.org/10.1073/pnas.1619730114
• Valandro, F., P.K. Menguer, C. Cabreira-Cagliari, M. Margis-Pinheiro & A. Cagliari, 2020. Programmed cell death (PCD) control in plants: New insights from the Arabidopsis thaliana deathosome. Plant Science: an international journal of experimental plant biology, 299: 110603. https://doi.org/10.1016/j.plantsci.2020.110603
• van Doorn W.G. & A. Papini, 2013. Ultrastructure of autophagy in plant cells: a review. Autophagy, 9 (12): 1922-1936. https://doi.org/10.4161/auto.26275
• van Doorn W.G., 2011. Classes of programmed cell death in plants, compared to those in animals. Journal of Experimental Botany, 62 (14): 4749-4761. https://doi.org/10.1093/jxb/err196
• van Doorn, W.G., E.P. Beers, J.L. Dangl, V.E. Franklin-Tong, P. Gallois, I. Hara-Nishimura, A.M. Jones, M. Kawai-Yamada, E. Lam, J. Mundy, L.A. Mur, M. Petersen, A. Smertenko, M. Taliansky, F. van Breusegem, T. Wolpert, E. Woltering, B. Zhivotovsky & P.V. Bozhkov, 2011. Morphological classification of plant cell deaths. Cell Death and Differentiation, 18 (8): 1241-1246. https://doi.org/10.1038/cdd.2011.36
• van Durme, M. & M.K. Nowack, 2016. Mechanisms of developmentally controlled cell death in plants. Current Opinion in Plant Biology, 29: 29-37. https://doi.org/10.1016/j.pbi.2015.10.013
• van Hautegem, T., A.J. Waters, J. Goodrich & M.K. Nowack, 2015. Only in dying, life: programmed cell death during plant development. Trends in Plant Science, 20 (2): 102-113. https://doi.org/10.1016/j.tplants.2014.10.003
• Ve, T., P.R. Vajjhala, A. Hedger, T. Croll, F. DiMaio, S. Horsefield, X. Yu, P. Lavrencic, Z. Hassan, G.P. Morgan, A. Mansell, M. Mobli, A. O’Carroll, B. Chauvin, Y. Gambin, E. Sierecki, M.J. Landsberg, K.J. Stacey, E.H. Egelman & B. Kobe, 2017. Structural basis of TIR-domain-assembly formation in MAL- and MyD88-dependent TLR4 signaling. Nature Structural & Molecular Biology. 24 (9): 743-751. https://doi.org/10.1038/nsmb.3444
• Wang, L. & H. Zhang, 2014. Genomewide survey and characterization of metacaspase gene family in rice (Oryza sativa). Journal of Genetics, 93 (1): 93-102. https://doi.org/10.1007/s12041-014-0343-6
• Wang, X., R. Guo, M. Tu, D. Wang, C. Guo, R. Wan, Z. Li & X. Wang, 2017. Ectopic expression of the wild grape WRKY transcription factor VqWRKY52 in Arabidopsis thaliana enhances resistance to the biotrophic pathogen powdery mildew but not to the necrotrophic pathogen Botrytis cinerea. Frontiers in Plant Sciences, 8: 97. https://doi.org/10.3389/fpls.2017.00097
• Wang, X., X. Wang, H. Feng, C. Tang, P. Bai, G. Wei, L. Huang & Z. Kang, 2012. TaMCA4, a novel wheat metacaspase gene functions in programmed cell death induced by the fungal pathogen Puccinia striiformis f. sp. tritici. Molecular plant-microbe interactions: MPMI, 25 (6): 755-764. https://doi.org/10.1094/MPMI-11-11-0283-R
• Watanabe, N. & E. Lam, 2011. Arabidopsis metacaspase 2d is positive mediator of cell death induced during biotic and abiotic stresses. The Plant Journal, 66 (6): 969-982. https://doi.org/10.1111/j.1365-313X.2011.04554.x
• Williams, S.J., K.H. Sohn, L. Wan, M. Bernoux, P.F. Sarris, C. Segonzac, T. Ve, Y. Ma, S.B. Saucet, D.J. Ericsson, L.W. Casey, T. Lonhienne, D.J. Winzor, X. Zhang, A. Coerdt, J.E. Parker, P.N. Dodds, B. Kobe & J.D. Jones, 2014. Structural basis for assembly and function of a heterodimeric plant immune receptor. Science, 344 (6181): 299-303. https://doi.org/10.1126/science.1247357
• Wu, L., H. Chen, C. Curtis & Z.Q. Fu, 2014. Go in for the kill: How plants deploy effector-trigered immunity to combat pathogens. (Corrected). Virulence, 5 (7): 710-721. https://doi.org/10.4161/viru.29755
• Yang, Z.T., M.J. Wang, L. Sun, S.J. Lu, D.L. Bi, L. Sun, Z.T. Song, S.S. Zhang, S.F. Zhou & J.X. Liu, 2014. The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genetics, 10 (3): e1004243. https://doi.org/10.1371/journal.pgen.1004243
• Yao, C., Y. Wu, H. Nie & D. Tang, 2012. RPN1a, a 26S proteasome subunit, is required for innate immunity in Arabidopsis. The Plant Journal, 71 (6): 1015-1028. https://doi.org/10.1111/j.1365-313X.2012.05048.x
• Yao, S., S. Luo, C. Pan, W. Xiong, D. Xiao, A. Wang, J. Zhan & L. He, 2020. Metacaspase MC1 enhances aluminum-induced programmed cell death of root tip cells in Peanut. Plant and Soil, 448 (1): 479-494. https://doi.org/10.1007/s11104-020-04448-w
• Yuan, J., S. Shaham S, S. Ledoux, H.M. Ellis & H.R. Horvitz, 1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1 beta-converting enzyme. Cell, 75 (4): 641-652. https://doi.org/10.1016/0092-8674 (93) 90485-9
• Yuan, X., H. Wang, J. Cai, D. Li & F. Song, 2019. NAC transcription factors in plant immunity. Phytopathology Research, 1 (1): 1-13. https://doi.org/10.1186/s42483-018-0008-0
• Zamyatnin, A.A.Jr., 2015. Plant proteases involved in regulated cell death. Biochemsitry (Mosc). Biokhimiia, 80 (13): 1701-1715. https://doi.org/10.1134/S0006297915130064
• Zhai, Z., N. Ha, F. Papagiannouli, A. Hamacher-Brady, N. Brady, S. Sorge, D. Bezdan & I. Lohmann, 2012. Antagonistic regulation of apoptosis and differentiation by the cut transcription factor represents a tumor-suppressing mechanism in drosophila. PLoS Genetics, 8 (3): e1002582. https://doi.org/10.1371/journal.pgen.1002582
• Zhang, B., O. van Aken, L. Thatcher, I. De Clercq, O. Duncan, S.R. Law, M.W. Murcha, M. van der Merwe, H.S. Seifi, C. Carrie, C. Cazzonelli, J. Radomiljac, M. Höfte, K.B. Singh, F. van Breusegem & J. Whelan, 2014. The mitochondrial outer membrane AAA ATPase AtOM66 affects cell death and pathogen resistance in Arabidopsis thaliana. The Plant Journal: for cell and molecular biology, 80 (4): 709-727. https://doi.org/10.1111/tpj.12665
• Zhang, C., P. Gong, R. Wei, S. Li, X. Zhang, Y. Yu & Y. Wang, 2013. The metacaspase gene family of Vitis vinifera L.: characterization and differential expression during ovule abortion in stenospermocarpic seedless grapes. Gene, 528 (2): 267-276. https://doi.org/10.1016/j.gene.2013.06.062
• Zhang, H., S. Dong, M. Wang, W. Wang, W. Song, X. Dou, X. Zheng & Z. Zhang, 2010. The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. Journal of Experimental Botany, 61 (13): 3799-3812. https://doi.org/10.1093/jxb/erq189
• Zhang, X., M. Bernoux, A.R. Bentham, T.E. Newman, T. Ve, L.W. Casey, T.M. Raaymakers, J. Hu, T.I. Croll, K.J. Schreiber, B.J. Staskawicz, P.A. Anderson, K.H. Sohn, S.J. Williams, P.N. Dodds & B. Kobe, 2017. Multiple functional self-association interfaces in plant TIR domains. The Proceedings of the National Academy of Sciences of the United States of America, 114 (10): E2046-E2052. https://doi.org/10.1073/pnas.1621248114
• Zhou, J.M., 2016. Plant Pathology: A Life and Death Struggle in Rice Blast Disease. Current Biology: CB, 26 (18): R843-R845. https://doi.org/10.1016/j.cub.2016.08.038