Ameisen, J. C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ.
9, 367–393 (2002).
Buttner, S. et al. Why yeast cells can undergo apoptosis: death in times of peace, love, and war. J. Cell. Biol.
175, 521–525 (2006).
Dwyer, D. J., Camacho, D. M., Kohanski, M. A., Callura, J. M. & Collins, J. J. Antibiotic-induced bacterial cell death exhibits physiological and biochemical hallmarks of apoptosis. Mol. Cell
46, 561–572 (2012).
Chen, S. & Dickman, M. B. Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J. Exp. Bot.
55, 2617–2623 (2004).
Curtis, M. J. & Wolpert, T. J. The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death. Plant J.
29, 295–312 (2002).
Curtis, M. J. & Wolpert, T. J. The victorin-induced mitochondrial permeability transition precedes cell shrinkage and biochemical markers of cell death, and shrinkage occurs without loss of membrane integrity. Plant J.
38, 244–259 (2004).
Van Aken, O. & Van Breusegem, F. Licensed to kill: mitochondria, chloroplasts, and cell death. Trends Plant Sci.
20, 754–766 (2015).
Zhivotovsky, B. From the nematode and mammals back to the pine tree: on the diversity and evolution of programmed cell death. Cell Death Differ.
9, 867–869 (2002).
Reape, T. J., Kacprzyk, J., Brogan, N., Sweetlove, L. & McCabe, P. F. Mitochondrial markers of programmed cell death in Arabidopsis thaliana. Methods Mol. Biol.
1305, 211–221 (2015).
Reape, T. J. & McCabe, P. F. Apoptotic-like programmed cell death in plants. New. Phytol.
180, 13–26 (2008).
Reape, T. J. & McCabe, P. F. Apoptotic-like regulation of programmed cell death in plants. Apoptosis
15, 249–256 (2010).
Reape, T. J. & McCabe, P. F. Commentary: the cellular condensation of dying plant cells: programmed retraction or necrotic collapse? Plant Sci.
207, 135–139 (2013).
Reape, T. J., Molony, E. M. & McCabe, P. F. Programmed cell death in plants: distinguishing between different modes. J. Exp. Bot.
59, 435–444 (2008).
Wang, H., Li, J., Bostock, R. M. & Gilchrist, D. G. Apoptosis: a functional paradigm for programmed plant cell death induced by a host-selective phytotoxin and invoked during development. Plant Cell
8, 375–391 (1996).
Wang, J. & Bayles, K. W. Programmed cell death in plants: lessons from bacteria? Trends Plant Sci.
18, 133–139 (2013).
Edwards, M. J. Apoptosis, the heat shock response, hyperthermia, birth defects, disease and cancer. Where are the common links? Cell Stress Chap.
3, 213–220 (1998).
Favaloro, B., Allocati, N., Graziano, V., Di Ilio, C. & De Laurenzi, V. Role of apoptosis in disease. Aging
4, 330–349 (2012).
Dickman, M. B. & Fluhr, R. Centrality of host cell death in plant-microbe interactions. Annu. Rev. Phytopathol.
51, 543–570 (2013).
Kerr, J. F., Wyllie, A. H. & Currie, A. R. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer
26, 239–257 (1972).
Maghsoudi, N., Zakeri, Z. & Lockshin, R. A. Programmed cell death and apoptosis-where it came from and where it is going: from Elie Metchnikoff to the control of caspases. Exp. Oncol.
34, 146–152 (2012).
Wallach, D., Kang, T. B., Dillon, C. P. & Green, D. R. Programmed necrosis in inflammation: toward identification of the effector molecules. Science
352, aaf2154 (2016).
Kabbage, M., Kessens, R., Bartholomay, L. C. & Williams, B. The life and death of a plant cell. Annu. Rev. Plant Biol.
68, 375–404 (2017).
van Doorn, W. G. Classes of programmed cell death in plants, compared to those in animals. J. Exp. Bot.
62, 4749–4761 (2011).
van Doorn, W. G. et al. Morphological classification of plant cell deaths. Cell Death Differ.
18, 1241–1246 (2011).
van Doorn, W. G. & Woltering, E. J. Many ways to exit? Cell death categories in plants. Trends Plant Sci.
10, 117–122 (2005).
Dickman, M. B. et al. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc. Natl Acad. Sci. USA
98, 6957–6962 (2001).
Doukhanina, E. V. et al. Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J. Biol. Chem.
281, 18793–18801 (2006).
Fukuda, H. Programmed cell death of tracheary elements as a paradigm in plants. Plant. Mol. Biol.
44, 245–253 (2000).
Hatsugai, N. et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science
305, 855–858 (2004).
Kim, K. S., Min, J. Y. & Dickman, M. B. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant Microbe Interact.
21, 605–612 (2008).
Lorang, J. et al. Tricking the guard: exploiting plant defense for disease susceptibility. Science
338, 659–662 (2012).
Williams, B. & Dickman, M. Plant programmed cell death: can’t live with it; can’t live without it. Mol. Plant. Path.
9, 531–544 (2008).
Williams, B., Kabbage, M., Kim, H. J., Britt, R. & Dickman, M. B. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLoS Pathog.
7, e1002107 (2011).
Watanabe, N. & Lam, E. Two Arabidopsis metacaspases AtMCP1b and AtMCP2b are arginine/lysine-specific cysteine proteases and activate apoptosis-like cell death in yeast. J. Biol. Chem.
280, 14691–14699 (2005).
Kumar, S. Caspase function in programmed cell death. Cell Death Differ.
14, 32–43 (2007).
Shalini, S., Dorstyn, L., Dawar, S. & Kumar, S. Old, new and emerging functions of caspases. Cell Death Differ.
22, 526–539 (2015).
Fink, S. L. & Cookson, B. T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun.
73, 1907–1916 (2005).
Rojo, E. et al. VPEγ exhibits a caspase-like activity that contributes to defense against pathogens. Curr. Biol.
14, 1897–1906 (2004).
Ge, Y. et al. Inhibition of cathepsin B by caspase-3 inhibitors blocks programmed cell death in Arabidopsis. Cell Death Differ.
23, 1493–1501 (2016).
Coffeen, W. C. & Wolpert, T. J. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell
16, 857–873 (2004).
Chichkova, N. V., Galiullina, R. A., Beloshistov, R. E., Balakireva, A. V. & Vartapetian, A. B. Phytaspases: aspartate-specific proteases involved in plant cell death. Bioorganicheskaia Khimiia
40, 658–664 (2014).
Galiullina, R. A. et al. substrate specificity and possible heterologous targets of phytaspase, a plant cell death protease. J. Biol. Chem.
290, 24806–24815 (2015).
Li, Y., Kabbage, M., Liu, W. & Dickman, M. B. Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants. Plant Cell
28, 233–247 (2016).
Uren, A. G. et al. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell
6, 961–967 (2000).
Vercammen, D. et al. Type II metacaspases Atmc4 and Atmc9 of Arabidopsis thaliana cleave substrates after arginine and lysine. J. Biol. Chem.
279, 45329–45336 (2004).
Carmona-Gutierrez, D., Frohlich, K. U., Kroemer, G. & Madeo, F. Metacaspases are caspases. Doubt no more. Cell Death Differ.
17, 377–378 (2010).
Enoksson, M. & Salvesen, G. S. Metacaspases are not caspases – always doubt. Cell Death Differ.
17, 1221 (2010).
Sundstrom, J. F. et al. Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat. Cell Biol.
11, 1347–1354 (2009).
Filonova, L. H. et al. Two waves of programmed cell death occur during formation and development of somatic embryos in the gymnosperm, Norway spruce. J. Cell Sci.
113, 4399–4411 (2000).
Nunez, R., Sancho-Martinez, S. M., Novoa, J. M. & Lopez-Hernandez, F. J. Apoptotic volume decrease as a geometric determinant for cell dismantling into apoptotic bodies. Cell Death Differ.
17, 1665–1671 (2010).
Flannagan, R. S., Jaumouille, V. & Grinstein, S. The cell biology of phagocytosis. Annu. Rev. Pathol.
7, 61–98 (2012).
Li, W. & Dickman, M. B. Abiotic stress induces apoptotic-like features in tobacco that is inhibited by expression of human Bcl-2. Biotechnol. Lett.
26, 87–95 (2004).
Li, W., Kabbage, M. & Dickman, M. B. Transgenic expression of an insect inhibitor of apoptosis gene, SfIAP, confers abiotic and biotic stress tolerance and delays tomato fruit ripening. Physiol. Mol. Plant Pathol.
74, 363–375 (2010).
McCabe, P. F., Levine, A., Meijer, P.-J., Tapon, N. A. & Pennell, R. I. A programmed cell death pathway activated in carrot cells cultured at low cell density. Plant J.
12, 267–280 (1997).
Chiou, S. K., Tseng, C. C., Rao, L. & White, E. Functional complementation of the adenovirus E1B 19-kilodalton protein with Bcl-2 in the inhibition of apoptosis in infected cells. J. Virol.
68, 6553–6566 (1994).
Huang, D. C., Cory, S. & Strasser, A. Bcl-2, Bcl-XL and adenovirus protein E1B19kD are functionally equivalent in their ability to inhibit cell death. Oncogene
14, 405–414 (1997).
Qiao, J. et al. Enhanced resistance to salt, cold and wound stresses by overproduction of animal cell death suppressors Bcl-xL and Ced-9 in tobacco cells - their possible contribution through improved function of organella. Plant Cell Physiol.
43, 992–1005 (2002).
Lacomme, C. & Santa Cruz, S. Bax-induced cell death in tobacco is similar to the hypersensitive response. Proc. Natl Acad. Sci. USA
96, 7956–7961 (1999).
Schendel, S. L., Montal, M. & Reed, J. C. Bcl-2 family proteins as ion-channels. Cell Death Differ.
5, 372–380 (1998).
Stroud, R. M., Reiling, K., Wiener, M. & Freymann, D. Ion-channel-forming colicins. Curr. Opin. Struct. Biol.
8, 525–533 (1998).
Baek, D. et al. Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Mol. Biol.
56, 15–27 (2004).
Balk, J., Chew, S. K., Leaver, C. J. & McCabe, P. F. The intermembrane space of plant mitochondria contains a DNase activity that may be involved in programmed cell death. Plant J.
34, 573–583 (2003).
Balk, J. & Leaver, C. J. The PET1-CMS mitochondrial mutation in sunflower is associated with premature programmed cell death and cytochrome c release. Plant Cell
13, 1803–1818 (2001).
Balk, J., Leaver, C. J. & McCabe, P. F. Translocation of cytochrome c from the mitochondria to the cytosol occurs during heat-induced programmed cell death in cucumber plants. FEBS Lett.
463, 151–154 (1999).
Vacca, R. A. et al. Cytochrome c is released in a reactive oxygen species-dependent manner and is degraded via caspase-like proteases in tobacco Bright-Yellow 2 cells en route to heat shock-induced cell death. Plant Physiol.
141, 208–219 (2006).
Yao, N., Eisfelder, B. J., Marvin, J. & Greenberg, J. T. The mitochondrion - an organelle commonly involved in programmed cell death in Arabidopsis thaliana. Plant J.
40, 596–610 (2004).
Billen, L. P., Shamas-Din, A. & Andrews, D. W. Bid: a Bax-like BH3 protein. Oncogene
27, S93–S104 (2008).
Takayama, S. et al. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell
80, 279–284 (1995).
Takayama, S., Xie, Z. & Reed, J. C. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem.
274, 781–786 (1999).
Kabbage, M. & Dickman, M. B. The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci.
65, 1390–1402 (2008).
Li, Y. & Dickman, M. Processing of AtBAG6 triggers autophagy and fungal resistance. Plant Signal. Behav.
11, e1175699 (2016).
Williams, B., Kabbage, M., Britt, R. & Dickman, M. B. AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. Proc. Natl Acad. Sci. USA
107, 6088–6093 (2010).
Li, Y., Williams, B. & Dickman, M. Arabidopsis B-cell lymphoma2 (Bcl-2)-associated athanogene 7 (BAG7)-mediated heat tolerance requires translocation, sumoylation and binding to WRKY29. New Phytol.
214, 695–705 (2017).
Minina, E. A., Smertenko, A. P. & Bozhkov, P. V. Vacuolar cell death in plants: metacaspase releases the brakes on autophagy. Autophagy
10, 928–929 (2014).
Hara-Nishimura, I. & Hatsugai, N. The role of vacuole in plant cell death. Cell. Death Differ.
18, 1298–1304 (2011).
Hatsugai, N., Kuroyanagi, M., Nishimura, M. & Hara-Nishimura, I. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis
11, 905–911 (2006).
Hatsugai, N., Yamada, K., Goto-Yamada, S. & Hara-Nishimura, I. Vacuolar processing enzyme in plant programmed cell death. Front. Plant Sci. 10.3389/fpls.2015.00234 (2015).
Wertman, J., Lord, C. E., Dauphinee, A. N. & Gunawardena, A. H. The pathway of cell dismantling during programmed cell death in lace plant (Aponogeton madagascariensis) leaves. BMC Plant Biol.
12, 115 (2012).
Hatsugai, N. et al. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev.
23, 2496–2506 (2009).
Gijzen, M. & Nurnberger, T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry
67, 1800–1807 (2006).
Wei, Z. M. et al. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science
257, 85–88 (1992).
Lampl, N., Alkan, N., Davydov, O. & Fluhr, R. Set-point control of RD21 protease activity by AtSerpin1 controls cell death in Arabidopsis. Plant J.
74, 498–510 (2013).
Lampl, N. et al. Arabidopsis AtSerpin1, crystal structure and in vivo interaction with its target protease RESPONSIVE TO DESICCATION-21 (RD21). J. Biol. Chem.
285, 13550–13560 (2010).
Lema Asqui, S. et al. AtSERPIN1 is an inhibitor of the metacaspase AtMC1-mediated cell death and autocatalytic processing in planta. http://dx.doi.org/10.1111/nph.14446 (2017).
Alavian, K. N. et al. Bcl-xL regulates metabolic efficiency of neurons through interaction with the mitochondrial F1FO ATP synthase. Nat. Cell Biol.
13, 1224–1233 (2011).
Shabala, S., Cuin, T. A., Prismall, L. & Nemchinov, L. G. Expression of animal CED-9 anti-apoptotic gene in tobacco modifies plasma membrane ion fluxes in response to salinity and oxidative stress. Planta
227, 189–197 (2007).
Robert, G., Munoz, N., Melchiorre, M., Sanchez, F. & Lascano, R. Expression of animal anti-apoptotic gene Ced-9 enhances tolerance during Glycine max L.–Bradyrhizobium japonicum interaction under saline stress but reduces nodule formation. PLoS ONE
9, e101747 (2014).
He, C. & Levine, B. The Beclin 1 interactome. Curr. Opin. Cell Biol.
22, 140–149 (2010).
Crook, N. E., Clem, R. J. & Miller, L. K. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol.
67, 2168–2174 (1993).
Takahashi, R. et al. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem.
273, 7787–7790 (1998).
Yang, Y. L. & Li, X. M. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell. Res.
10, 169–177 (2000).
Kim, W. Y. et al. Inhibitor of apoptosis (IAP)-like protein lacks a baculovirus IAP repeat (BIR) domain and attenuates cell death in plant and animal systems. J. Biol. Chem.
286, 42670–42678 (2011).
Houot, V. et al. Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J. Exp. Bot.
52, 1721–1730 (2001).
Levine, A., Pennell, R. I., Alvarez, M. E., Palmer, R. & Lamb, C. Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr. Biol.
6, 427–437 (1996).
Wang, M., Oppedijk, B. J., Lu, X., Van Duijn, B. & Schilperoort, R. A. Apoptosis in barley aleurone during germination and its inhibition by abscisic acid. Plant Mol. Biol.
32, 1125–1134 (1996).
Yao, N. et al. Novel evidence for apoptotic cell response and differential signals in chromatin condensation and DNA cleavage in victorin-treated oats. Plant J.
28, 13–26 (2001).
Min, K. et al. Peroxisome function is required for virulence and survival of Fusarium graminearum. Mol. Plant Microbe Interact.
25, 1617–1627 (2012).
Navarre, D. A. & Wolpert, T. J. Victorin induction of an apoptotic/senescence–like response in oats. Plant Cell
11, 237–249 (1999).
Woltering, E. J., van der Bent, A. & Hoeberichts, F. A. Do plant caspases exist? Plant. Physiol.
130, 1764–1769 (2002).
Xu, Q. & Zhang, L. Plant caspase-like proteases in plant programmed cell death. Plant Signal. Behav.
4, 902–904 (2009).
Higaki, T. et al. Elicitor-induced cytoskeletal rearrangement relates to vacuolar dynamics and execution of cell death: in vivo imaging of hypersensitive cell death in tobacco BY-2 cells. Plant Cell Physiol.
48, 1414–1425 (2007).