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Reassessing apoptosis in plants

Abstract

Cell death can be driven by a genetically programmed signalling pathway known as programmed cell death (PCD). In plants, PCD occurs during development as well as in response to environmental and biotic stimuli. Our understanding of PCD regulation in plants has advanced significantly over the past two decades; however, the molecular machinery responsible for driving the system remains elusive. Thus, whether conserved PCD regulatory mechanisms include plant apoptosis remains enigmatic. Animal apoptotic regulators, including Bcl-2 family members, have not been identified in plants but expression of such regulators can trigger or suppress plant PCD. Moreover, plants exhibit nearly all of the biochemical and morphological features of apoptosis. One difference between plant and animal PCD is the absence of phagocytosis in plants. Evidence is emerging that the vacuole may be key to removal of unwanted plant cells, and may carry out functions that are analogous to animal phagocytosis. Here, we provide context for the argument that apoptotic-like cell death occurs in plants.

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Fig. 1: Comparison of apoptotic-like cell death in animal and plant cells.
Fig. 2: Apoptotic bodies in plant PCD and structural conservation of human and Arabidopsis BAG4 BAG domains.

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References

  1. 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).

    Article  CAS  PubMed  Google Scholar 

  2. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  3. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. 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).

    Article  CAS  PubMed  Google Scholar 

  5. 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).

    Article  PubMed  Google Scholar 

  6. 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).

    Article  CAS  PubMed  Google Scholar 

  7. Van Aken, O. & Van Breusegem, F. Licensed to kill: mitochondria, chloroplasts, and cell death. Trends Plant Sci. 20, 754–766 (2015).

    Article  PubMed  Google Scholar 

  8. 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).

    Article  CAS  PubMed  Google Scholar 

  9. 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).

    Article  CAS  PubMed  Google Scholar 

  10. Reape, T. J. & McCabe, P. F. Apoptotic-like programmed cell death in plants. New. Phytol. 180, 13–26 (2008).

    Article  CAS  PubMed  Google Scholar 

  11. Reape, T. J. & McCabe, P. F. Apoptotic-like regulation of programmed cell death in plants. Apoptosis 15, 249–256 (2010).

    Article  CAS  PubMed  Google Scholar 

  12. 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).

    Article  CAS  PubMed  Google Scholar 

  13. 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).

    Article  CAS  PubMed  Google Scholar 

  14. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Wang, J. & Bayles, K. W. Programmed cell death in plants: lessons from bacteria? Trends Plant Sci. 18, 133–139 (2013).

    Article  CAS  PubMed  Google Scholar 

  16. 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).

    Article  CAS  Google Scholar 

  17. Favaloro, B., Allocati, N., Graziano, V., Di Ilio, C. & De Laurenzi, V. Role of apoptosis in disease. Aging 4, 330–349 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dickman, M. B. & Fluhr, R. Centrality of host cell death in plant-microbe interactions. Annu. Rev. Phytopathol. 51, 543–570 (2013).

    Article  CAS  PubMed  Google Scholar 

  19. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. 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).

    CAS  PubMed  Google Scholar 

  21. 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).

    Article  PubMed  Google Scholar 

  22. 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).

    Article  CAS  PubMed  Google Scholar 

  23. van Doorn, W. G. Classes of programmed cell death in plants, compared to those in animals. J. Exp. Bot. 62, 4749–4761 (2011).

    Article  PubMed  Google Scholar 

  24. van Doorn, W. G. et al. Morphological classification of plant cell deaths. Cell Death Differ. 18, 1241–1246 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  25. van Doorn, W. G. & Woltering, E. J. Many ways to exit? Cell death categories in plants. Trends Plant Sci. 10, 117–122 (2005).

    Article  PubMed  Google Scholar 

  26. Dickman, M. B. et al. Abrogation of disease development in plants expressing animal antiapoptotic genes. Proc. Natl Acad. Sci. USA 98, 6957–6962 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Doukhanina, E. V. et al. Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J. Biol. Chem. 281, 18793–18801 (2006).

    Article  CAS  PubMed  Google Scholar 

  28. Fukuda, H. Programmed cell death of tracheary elements as a paradigm in plants. Plant. Mol. Biol. 44, 245–253 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. Hatsugai, N. et al. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305, 855–858 (2004).

    Article  CAS  PubMed  Google Scholar 

  30. 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).

    Article  CAS  PubMed  Google Scholar 

  31. Lorang, J. et al. Tricking the guard: exploiting plant defense for disease susceptibility. Science 338, 659–662 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. 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).

    Article  CAS  Google Scholar 

  33. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. 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).

    Article  CAS  PubMed  Google Scholar 

  35. Kumar, S. Caspase function in programmed cell death. Cell Death Differ. 14, 32–43 (2007).

    Article  CAS  PubMed  Google Scholar 

  36. Shalini, S., Dorstyn, L., Dawar, S. & Kumar, S. Old, new and emerging functions of caspases. Cell Death Differ. 22, 526–539 (2015).

    Article  CAS  PubMed  Google Scholar 

  37. Fink, S. L. & Cookson, B. T. Apoptosis, pyroptosis, and necrosis: mechanistic description of dead and dying eukaryotic cells. Infect. Immun. 73, 1907–1916 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rojo, E. et al. VPEγ exhibits a caspase-like activity that contributes to defense against pathogens. Curr. Biol. 14, 1897–1906 (2004).

    Article  CAS  PubMed  Google Scholar 

  39. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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).

    CAS  PubMed  Google Scholar 

  42. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 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).

    CAS  PubMed  Google Scholar 

  45. 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).

    Article  CAS  PubMed  Google Scholar 

  46. Carmona-Gutierrez, D., Frohlich, K. U., Kroemer, G. & Madeo, F. Metacaspases are caspases. Doubt no more. Cell Death Differ. 17, 377–378 (2010).

    Article  CAS  PubMed  Google Scholar 

  47. Enoksson, M. & Salvesen, G. S. Metacaspases are not caspases – always doubt. Cell Death Differ. 17, 1221 (2010).

    Article  CAS  PubMed  Google Scholar 

  48. 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).

    Article  PubMed  Google Scholar 

  49. 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).

    CAS  PubMed  Google Scholar 

  50. 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).

    Article  CAS  PubMed  Google Scholar 

  51. Flannagan, R. S., Jaumouille, V. & Grinstein, S. The cell biology of phagocytosis. Annu. Rev. Pathol. 7, 61–98 (2012).

    Article  CAS  PubMed  Google Scholar 

  52. 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).

    Article  CAS  PubMed  Google Scholar 

  53. 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).

    Article  CAS  Google Scholar 

  54. 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).

    Article  CAS  Google Scholar 

  55. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 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).

    Article  CAS  PubMed  Google Scholar 

  57. 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).

    Article  CAS  PubMed  Google Scholar 

  58. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Schendel, S. L., Montal, M. & Reed, J. C. Bcl-2 family proteins as ion-channels. Cell Death Differ. 5, 372–380 (1998).

    Article  CAS  PubMed  Google Scholar 

  60. Stroud, R. M., Reiling, K., Wiener, M. & Freymann, D. Ion-channel-forming colicins. Curr. Opin. Struct. Biol. 8, 525–533 (1998).

    Article  CAS  PubMed  Google Scholar 

  61. 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).

    Article  CAS  PubMed  Google Scholar 

  62. 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).

    Article  CAS  PubMed  Google Scholar 

  63. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. 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).

    Article  CAS  PubMed  Google Scholar 

  65. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. 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).

    Article  CAS  PubMed  Google Scholar 

  67. Billen, L. P., Shamas-Din, A. & Andrews, D. W. Bid: a Bax-like BH3 protein. Oncogene 27, S93–S104 (2008).

    Article  CAS  PubMed  Google Scholar 

  68. 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).

    Article  CAS  PubMed  Google Scholar 

  69. Takayama, S., Xie, Z. & Reed, J. C. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem. 274, 781–786 (1999).

    Article  CAS  PubMed  Google Scholar 

  70. Kabbage, M. & Dickman, M. B. The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65, 1390–1402 (2008).

    Article  CAS  PubMed  Google Scholar 

  71. Li, Y. & Dickman, M. Processing of AtBAG6 triggers autophagy and fungal resistance. Plant Signal. Behav. 11, e1175699 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  72. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. 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).

    Article  CAS  PubMed  Google Scholar 

  74. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Hara-Nishimura, I. & Hatsugai, N. The role of vacuole in plant cell death. Cell. Death Differ. 18, 1298–1304 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Hatsugai, N., Kuroyanagi, M., Nishimura, M. & Hara-Nishimura, I. A cellular suicide strategy of plants: vacuole-mediated cell death. Apoptosis 11, 905–911 (2006).

    Article  CAS  PubMed  Google Scholar 

  77. 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).

  78. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  79. Hatsugai, N. et al. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev. 23, 2496–2506 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Gijzen, M. & Nurnberger, T. Nep1-like proteins from plant pathogens: recruitment and diversification of the NPP1 domain across taxa. Phytochemistry 67, 1800–1807 (2006).

    Article  CAS  PubMed  Google Scholar 

  81. Wei, Z. M. et al. Harpin, elicitor of the hypersensitive response produced by the plant pathogen Erwinia amylovora. Science 257, 85–88 (1992).

    Article  CAS  PubMed  Google Scholar 

  82. 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).

    Article  CAS  PubMed  Google Scholar 

  83. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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).

  85. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. 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).

    Article  CAS  PubMed  Google Scholar 

  87. 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).

    Article  PubMed  PubMed Central  Google Scholar 

  88. He, C. & Levine, B. The Beclin 1 interactome. Curr. Opin. Cell Biol. 22, 140–149 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. 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).

    CAS  PubMed  PubMed Central  Google Scholar 

  90. Takahashi, R. et al. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem. 273, 7787–7790 (1998).

    Article  CAS  PubMed  Google Scholar 

  91. Yang, Y. L. & Li, X. M. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell. Res. 10, 169–177 (2000).

    Article  CAS  PubMed  Google Scholar 

  92. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. 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).

    CAS  PubMed  Google Scholar 

  94. 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).

    Article  CAS  PubMed  Google Scholar 

  95. 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).

    Article  CAS  PubMed  Google Scholar 

  96. 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).

    Article  CAS  PubMed  Google Scholar 

  97. Min, K. et al. Peroxisome function is required for virulence and survival of Fusarium graminearum. Mol. Plant Microbe Interact. 25, 1617–1627 (2012).

    Article  CAS  PubMed  Google Scholar 

  98. Navarre, D. A. & Wolpert, T. J. Victorin induction of an apoptotic/senescence–like response in oats. Plant Cell 11, 237–249 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  99. Woltering, E. J., van der Bent, A. & Hoeberichts, F. A. Do plant caspases exist? Plant. Physiol. 130, 1764–1769 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Xu, Q. & Zhang, L. Plant caspase-like proteases in plant programmed cell death. Plant Signal. Behav. 4, 902–904 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. 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).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

Research in the Dickman lab is supported by BARD and NSF. B.W. is supported by a QUT Vice Chancellor’s Research Fellowship. P.d.F. is supported by grants from the Texas A&M University – CAPES program, the Texas A&M - Conacyt program, the National Science Foundation, the National Institutes of Health and the Qatar National Research Foundation. T.J.W. is supported in part by the Agriculture and Food Research Initiative Competitive Grants Program Grant no. 2016-67013-24736 from the USDA National Institute of Food and Agriculture.

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M.D., B.W., Y.L., P.d.F. and T.W. wrote the article. P.d.F., B.W. and Y.L. prepared the figures.

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Correspondence to Martin Dickman or Brett Williams.

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Dickman, M., Williams, B., Li, Y. et al. Reassessing apoptosis in plants. Nature Plants 3, 773–779 (2017). https://doi.org/10.1038/s41477-017-0020-x

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