Like all eukaryotic organisms, plants possess an innate program for controlled cellular demise termed programmed cell death (PCD). Despite the functional conservation of PCD across broad evolutionary distances, an understanding of the molecular machinery underpinning this fundamental program in plants remains largely elusive. As in mammalian PCD, the regulation of plant PCD is critical to development, homeostasis, and proper responses to stress. Evidence is emerging that autophagy is key to the regulation of PCD in plants and that it can dictate the outcomes of PCD execution under various scenarios. Here, we provide a broad and comparative overview of PCD processes in plants, with an emphasis on stress-induced PCD. We also discuss the implications of the paradox that is functional conservation of apoptotic hallmarks in plants in the absence of core mammalian apoptosis regulators, what that means, and whether an equivalent form of death occurs in plants.


Article metrics loading...

Loading full text...

Full text loading...


Literature Cited

  1. Alberti S, Demand J, Esser C, Emmerich N, Schild H, Hohfeld J. 1.  2002. Ubiquitylation of BAG-1 suggests a novel regulatory mechanism during the sorting of chaperone substrates to the proteasome. J. Biol. Chem. 277:45920–27 [Google Scholar]
  2. Alpert P.2.  2005. The limits and frontiers of desiccation-tolerant life. Integr. Comp. Biol. 45:685–95 [Google Scholar]
  3. Arndt V, Daniel C, Nastainczyk W, Alberti S, Hohfeld J. 3.  2005. BAG-2 acts as an inhibitor of the chaperone-associated ubiquitin ligase CHIP. Mol. Biol. Cell 16:5891–900 [Google Scholar]
  4. Baena-González E, Sheen J. 4.  2008. Convergent energy and stress signaling. Trends Plant Sci 13:474–82 [Google Scholar]
  5. Bao Q, Shi Y. 5.  2007. Apoptosome: a platform for the activation of initiator caspases. Cell Death Differ 14:56–65 [Google Scholar]
  6. Bashir Z, Ahmad A, Shafique S, Anjum T, Shafique S, Akram W. 6.  2013. Hypersensitive response—a biophysical phenomenon of producers. Eur. J. Microbiol. Immunol. 3:105–10 [Google Scholar]
  7. Bassham DC, Laporte M, Marty F, Moriyasu Y, Ohsumi Y. 7.  et al. 2006. Autophagy in development and stress responses of plants. Autophagy 2:2–11 [Google Scholar]
  8. Behl C.8.  2016. Breaking BAG: the co-chaperone BAG3 in health and disease. Trends Pharmacol. Sci. 37:672–88 [Google Scholar]
  9. Beilina A, Rudenko IN, Kaganovich A, Civiero L, Chau H. 9.  et al. 2014. Unbiased screen for interactors of leucine-rich repeat kinase 2 supports a common pathway for sporadic and familial Parkinson disease. PNAS 111:2626–31 [Google Scholar]
  10. Blomstedt CK, Griffiths CA, Fredericks DP, Hamill JD, Gaff DF, Neale AD. 10.  2010. The resurrection plant Sporobolus stapfianus: an unlikely model for engineering enhanced plant biomass?. Plant Growth Regul 62:217–32 [Google Scholar]
  11. Bögre L, Henriques R, Magyar Z. 11.  2013. TOR tour to auxin. EMBO J 32:1069–71 [Google Scholar]
  12. Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W. 12.  2010. Sugar signalling and antioxidant network connections in plant cells. FEBS J 277:2022–37 [Google Scholar]
  13. Brive L, Takayama S, Briknarova K, Homma S, Ishida SK. 13.  et al. 2001. The carboxyl-terminal lobe of Hsc70 ATPase domain is sufficient for binding to BAG1. Biochem. Biophys. Res. Commun. 289:1099–105 [Google Scholar]
  14. Burstein E, Ganesh L, Dick RD, van De Sluis B, Wilkinson JC. 14.  et al. 2004. A novel role for XIAP in copper homeostasis through regulation of MURR1. EMBO J 23:244–54 [Google Scholar]
  15. Caldana C, Li Y, Leisse A, Zhang Y, Bartholomaeus L. 15.  et al. 2013. Systemic analysis of inducible target of rapamycin mutants reveal a general metabolic switch controlling growth in Arabidopsis thaliana. Plant J. 73:897–909 [Google Scholar]
  16. Cameron P, Limjuco G, Rodkey J, Bennett C, Schmidt JA. 16.  1985. Amino acid sequence analysis of human interleukin 1 (IL-1). Evidence for biochemically distinct forms of IL-1. J. Exp. Med. 162:790–801 [Google Scholar]
  17. Cerio RJ, Vandergaast R, Friesen PD. 17.  2010. Host insect inhibitor-of-apoptosis SfIAP functionally replaces baculovirus IAP but is differentially regulated by its N-terminal leader. J. Virol. 84:11448–60 [Google Scholar]
  18. Cerretti DP, Kozlosky CJ, Mosley B, Nelson N, Ness KV. 18.  et al. 1992. Molecular cloning of the interleukin-1β converting enzyme. Science 256:97–100 [Google Scholar]
  19. Chaves MM, Maroco JP, Pereira JS. 19.  2003. Understanding plant responses to drought—from genes to the whole plant. Funct. Plant Biol. 30:239–64 [Google Scholar]
  20. Chen S, Dickman MB. 20.  2004. Bcl-2 family members localize to tobacco chloroplasts and inhibit programmed cell death induced by chloroplast-targeted herbicides. J. Exp. Bot. 55:2617–23 [Google Scholar]
  21. Chichkova NV, Shaw J, Galiullina RA, Drury GE, Tuzhikov AI. 21.  et al. 2010. Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J 29:1149–61 [Google Scholar]
  22. Coffeen WC, Wolpert TJ. 22.  2004. Purification and characterization of serine proteases that exhibit caspase-like activity and are associated with programmed cell death in Avena sativa. Plant Cell 16:857–73 [Google Scholar]
  23. Coll NS, Vercammen D, Smidler A, Clover C, Van Breusegem F. 23.  et al. 2010. Arabidopsis type I metacaspases control cell death. Science 330:1393–97 [Google Scholar]
  24. Crook NE, Clem RJ, Miller LK. 24.  1993. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67:2168–74 [Google Scholar]
  25. Cui H, Tsuda K, Parker JE. 25.  2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511 [Google Scholar]
  26. Curtis MJ, Wolpert TJ. 26.  2004. 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 38:244–59 [Google Scholar]
  27. Cushman JC, Oliver MJ. 27.  2011. Understanding vegetative desiccation tolerance using integrated functional genomics approaches within a comparative evolutionary framework. Plant Desiccation Tolerance U Lüttge, E Beck, D Bartels 307–38 Ecol. Stud. 215 Berlin: Springer [Google Scholar]
  28. Dai Q, Qian SB, Li HH, McDonough H, Borchers C. 28.  et al. 2005. Regulation of the cytoplasmic quality control protein degradation pathway by BAG2. J. Biol. Chem. 280:38673–81 [Google Scholar]
  29. Das G, Shravage BV, Baehrecke EH. 29.  2012. Regulation and function of autophagy during cell survival and cell death. Cold Spring Harb. Perspect. Biol. 4:a008813 [Google Scholar]
  30. del Pozo O, Lam E. 30.  1998. Caspases and programmed cell death in the hypersensitive response of plants to pathogens. Curr. Biol. 8:1129–32 [Google Scholar]
  31. Demand J, Alberti S, Patterson C, Hohfeld J. 31.  2001. Cooperation of a ubiquitin domain protein and an E3 ubiquitin ligase during chaperone/proteasome coupling. Curr. Biol. 11:1569–77 [Google Scholar]
  32. Deprost D, Truong HN, Robaglia C, Meyer C. 32.  2005. An Arabidopsis homolog of RAPTOR/KOG1 is essential for early embryo development. Biochem. Biophys. Res. Commun. 326:844–50 [Google Scholar]
  33. Deprost D, Yao L, Sormani R, Moreau M, Leterreux G. 33.  et al. 2007. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–70 [Google Scholar]
  34. Desmots F, Russell HR, Lee Y, Boyd K, McKinnon PJ. 34.  2005. The reaper-binding protein scythe modulates apoptosis and proliferation during mammalian development. Mol. Cell. Biol. 25:10329–37 [Google Scholar]
  35. Desmots F, Russell HR, Michel D, McKinnon PJ. 35.  2008. Scythe regulates apoptosis-inducing factor stability during endoplasmic reticulum stress-induced apoptosis. J. Biol. Chem. 283:3264–71 [Google Scholar]
  36. Dickman MB, Fluhr R. 36.  2013. Centrality of host cell death in plant-microbe interactions. Annu. Rev. Phytopathol. 51:543–70 [Google Scholar]
  37. Dickman MB, Park YK, Oltersdorf T, Li W, Clemente T, French R. 37.  2001. Abrogation of disease development in plants expressing animal antiapoptotic genes. PNAS 98:6957–62 [Google Scholar]
  38. Dobrenel T, Caldana C, Hanson J, Robaglia C, Vincentz M. 38.  et al. 2016. TOR signaling and nutrient sensing. Annu. Rev. Plant Biol. 67:261–85 [Google Scholar]
  39. Dobrenel T, Marchive C, Azzopardi M, Clement G, Moreau M. 39.  et al. 2013. Sugar metabolism and the plant target of rapamycin kinase: a sweet operaTOR?. Front. Plant Sci. 4:93 [Google Scholar]
  40. Doukhanina EV, Chen S, van der Zalm E, Godzik A, Reed J, Dickman MB. 40.  2006. Identification and functional characterization of the BAG protein family in Arabidopsis thaliana. J. Biol. Chem. 281:18793–801 [Google Scholar]
  41. Du C, Fang M, Li Y, Li L, Wang X. 41.  2000. Smac, a mitochondrial protein that promotes cytochrome c–dependent caspase activation by eliminating IAP inhibition. Cell 102:33–42 [Google Scholar]
  42. Duckett CS, Nava VE, Gedrich RW, Clem RJ, Van Dongen JL. 42.  et al. 1996. A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 15:2685–94 [Google Scholar]
  43. Dunlop EA, Hunt DK, Acosta-Jaquez HA, Fingar DC, Tee AR. 43.  2011. ULK1 inhibits mTORC1 signaling, promotes multisite Raptor phosphorylation and hinders substrate binding. Autophagy 7:737–47 [Google Scholar]
  44. Dunlop EA, Tee AR. 44.  2014. mTOR and autophagy: a dynamic relationship governed by nutrients and energy. Semin. Cell Dev. Biol. 36:121–29 [Google Scholar]
  45. Egan D, Kim J, Shaw RJ, Guan KL. 45.  2011. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy 7:643–44 [Google Scholar]
  46. Elbein AD, Pan YT, Pastuszak I, Carroll D. 46.  2003. New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R [Google Scholar]
  47. Elmore S.47.  2007. Apoptosis: a review of programmed cell death. Toxicol. Pathol. 35:495–516 [Google Scholar]
  48. Farrant PB, Emerson R. 48.  2007. Hyfrecation and curettage as a treatment for fibrofolliculomas in Birt-Hogg-Dube syndrome. Dermatol. Surg. 33:1287–88 [Google Scholar]
  49. Favaloro B, Allocati N, Graziano V, Di Ilio C, De Laurenzi V. 49.  2012. Role of apoptosis in disease. Aging 4:330–49 [Google Scholar]
  50. Fernández MB, Daleo GR, Guevara MG. 50.  2015. Isolation and characterization of a Solanum tuberosum subtilisin-like protein with caspase-3 activity (StSBTc-3). Plant Physiol. Biochem. 86:137–46 [Google Scholar]
  51. Friesen TL, Zhang Z, Solomon PS, Oliver RP, Faris JD. 51.  2008. Characterization of the interaction of a novel Stagonospora nodorum host-selective toxin with a wheat susceptibility gene. Plant Physiol 146:682–93 [Google Scholar]
  52. Froesch BA, Takayama S, Reed JC. 52.  1998. BAG-1L protein enhances androgen receptor function. J. Biol. Chem. 273:11660–66 [Google Scholar]
  53. Gaff DF.53.  1971. Desiccation-tolerant flowering plants in southern Africa. Science 174:1033–34 [Google Scholar]
  54. Gaff DF.54.  1999. Resurrection plants. Plants in Action BJ Atwell, PE Kriedemann, CGN Turnbull, feature essay 15.1 Melbourne: Macmillan Educ. Aust http://plantsinaction.science.uq.edu.au/edition1/?q=content/feature-essay-15-1-resurrection-plants [Google Scholar]
  55. Gaff DF, Bartels D, Gaff JL. 55.  1997. Changes in gene expression during drying in a desiccation-tolerant grass Sporobolus stapfianus and a desiccation-sensitive grass Sporobolus pyramidalis. Aust. J. Plant Physiol. 24:617–22 [Google Scholar]
  56. Gaff DF, Latz PK. 56.  1978. The occurrence of resurrection plants in the Australian flora. Aust. J. Bot. 26:485–92 [Google Scholar]
  57. Gamerdinger M, Hajieva P, Kaya AM, Wolfrum U, Hartl FU, Behl C. 57.  2009. Protein quality control during aging involves recruitment of the macroautophagy pathway by BAG3. EMBO J 28:889–901 [Google Scholar]
  58. Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D. 58.  2012. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell. Mol. Life Sci. 69:3175–86 [Google Scholar]
  59. Gehrmann M, Marienhagen J, Eichholtz-Wirth H, Fritz E, Ellwart J. 59.  et al. 2005. Dual function of membrane-bound heat shock protein 70 (Hsp70), Bag-4, and Hsp40: protection against radiation-induced effects and target structure for natural killer cells. Cell Death Differ 12:38–51 [Google Scholar]
  60. Gilbert BM, Wolpert TJ. 60.  2013. Characterization of the LOV1-mediated, victorin-induced, cell-death response with virus-induced gene silencing. Mol. Plant-Microbe Interact. 26:903–17 [Google Scholar]
  61. Gilchrist DG.61.  1997. Mycotoxins reveal connections between plants and animals in apoptosis and ceramide signaling. Cell Death Differ 4:689–98 [Google Scholar]
  62. Gohre V, Robatzek S. 62.  2008. Breaking the barriers: microbial effector molecules subvert plant immunity. Annu. Rev. Phytopathol. 46:189–215 [Google Scholar]
  63. Griffiths CA, Gaff DF, Neale AD. 63.  2014. Drying without senescence in resurrection plants. Front. Plant Sci. 5:36 [Google Scholar]
  64. Han S, Wang Y, Zheng X, Jia Q, Zhao J. 64.  et al. 2015. Cytoplastic glyceraldehyde-3-phosphate dehydrogenases interact with ATG3 to negatively regulate autophagy and immunity in. Nicotiana benthamiana 27:1316–31 [Google Scholar]
  65. Hanaoka H, Noda T, Shirano Y, Kato T, Hayashi H. 65.  et al. 2002. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol 129:1181–93 [Google Scholar]
  66. Hardie DG.66.  2007. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 8:774–85 [Google Scholar]
  67. Hatsugai N, Iwasaki S, Tamura K, Kondo M, Fuji K. 67.  et al. 2009. A novel membrane fusion-mediated plant immunity against bacterial pathogens. Genes Dev 23:2496–506 [Google Scholar]
  68. Hatsugai N, Kuroyanagi M, Yamada K, Meshi T, Tsuda S. 68.  et al. 2004. A plant vacuolar protease, VPE, mediates virus-induced hypersensitive cell death. Science 305:855–58 [Google Scholar]
  69. He C, Klionsky DJ. 69.  2009. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 43:67–93 [Google Scholar]
  70. Heath MC.70.  2000. Hypersensitive response-related death. Plant Mol. Biol. 44:321–34 [Google Scholar]
  71. Hedbacker K, Carlson M. 71.  2008. SNF1/AMPK pathways in yeast. Front. Biosci. 13:2408–20 [Google Scholar]
  72. Henry E, Fung N, Liu J, Drakakaki G, Coaker G. 72.  2015. Beyond glycolysis: GAPDHs are multi-functional enzymes involved in regulation of ROS, autophagy, and plant immune responses. PLOS Genet 11:e1005199 [Google Scholar]
  73. Hiraiwa N, Nishimura M, Hara-Nishimura I. 73.  1999. Vacuolar processing enzyme is self-catalytically activated by sequential removal of the C-terminal and N-terminal propeptides. FEBS Lett 447:213–16 [Google Scholar]
  74. Hoang TML, Moghaddam L, Williams B, Khanna H, Dale J, Mundree SG. 74.  2015. Development of salinity tolerance in rice by constitutive-overexpression of genes involved in the regulation of programmed cell death. Front. Plant Sci. 6:175 [Google Scholar]
  75. Hoang TML, Williams B, Khanna H, Dale J, Mundree SG. 75.  2014. Physiological basis of salt stress tolerance in rice expressing the antiapoptotic gene SfIAP. Funct. Plant Biol. 41:1168–77 [Google Scholar]
  76. Hofius D, Munch D, Bressendorff S, Mundy J, Petersen M. 76.  2011. Role of autophagy in disease resistance and hypersensitive response-associated cell death. Cell Death Differ 18:1257–62 [Google Scholar]
  77. Ingram J, Bartels D. 77.  1996. The molecular basis of dehydration tolerance in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:377–403 [Google Scholar]
  78. Ishida H, Yoshimoto K, Izumi M, Reisen D, Yano Y. 78.  et al. 2008. Mobilization of Rubisco and stroma-localized fluorescent proteins of chloroplasts to the vacuole by an ATG gene-dependent autophagic process. Plant Physiol 148:142–55 [Google Scholar]
  79. Itakura E, Kishi C, Inoue K, Mizushima N. 79.  2008. Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19:5360–72 [Google Scholar]
  80. Iwaya-Inoue M, Nonami H. 80.  2003. Effects of trehalose on flower senescence from the view point of physical states of water. Environ. Control Biol. 41:3–15 [Google Scholar]
  81. Jiang Y, Woronicz JD, Liu W, Goeddel DV. 81.  1999. Prevention of constitutive TNF receptor 1 signaling by silencer of death domains. Science 283:543–46 [Google Scholar]
  82. Kabbage M, Dickman MB. 82.  2008. The BAG proteins: a ubiquitous family of chaperone regulators. Cell. Mol. Life Sci. 65:1390–402 [Google Scholar]
  83. Kabbage M, Li W, Chen S, Dickman MB. 83.  2010. The E3 ubiquitin ligase activity of an insect anti-apoptotic gene (SfIAP) is required for plant stress tolerance. Physiol. Mol. Plant Pathol. 74:351–62 [Google Scholar]
  84. Kabbage M, Williams B, Dickman MB. 84.  2013. Cell death control: the interplay of apoptosis and autophagy in the pathogenicity of Sclerotinia sclerotiorum. PLOS Pathog 9:e1003287 [Google Scholar]
  85. Kacprzyk J, Daly CT, McCabe PF. 85.  2011. The botanical dance of death: programmed cell death in plants. Advances in Botanical Research 60 J-C Kader, M Delsney 168–261 London: Academic [Google Scholar]
  86. Kadota Y, Watanabe T, Fujii S, Higashi K, Sano T. 86.  et al. 2004. Crosstalk between elicitor-induced cell death and cell cycle regulation in tobacco BY-2 cells. Plant J 40:131–42 [Google Scholar]
  87. Kalia SK, Lee S, Smith PD, Liu L, Crocker SJ. 87.  et al. 2004. BAG5 inhibits parkin and enhances dopaminergic neuron degeneration. Neuron 44:931–45 [Google Scholar]
  88. Kang CH, Jung WY, Kang YH, Kim JY, Kim DG. 88.  et al. 2006. AtBAG6, a novel calmodulin-binding protein, induces programmed cell death in yeast and plants. Cell Death Differ 13:84–95 [Google Scholar]
  89. Karbaschi MR, Williams B, Taji A, Mundree SG. 89.  2016. Tripogon loliiformis elicits a rapid physiological and structural response to dehydration for desiccation tolerance. Funct. Plant Biol. 43:643–55 [Google Scholar]
  90. Kim J, Kundu M, Viollet B, Guan KL. 90.  2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat. Cell Biol. 13:132–41 [Google Scholar]
  91. Kim J, Lee H, Lee HN, Kim SH, Shin KD, Chung T. 91.  2013. Autophagy-related proteins are required for degradation of peroxisomes in Arabidopsis hypocotyls during seedling growth. Plant Cell 25:4956–66 [Google Scholar]
  92. Kim KS, Min JY, Dickman MB. 92.  2008. Oxalic acid is an elicitor of plant programmed cell death during Sclerotinia sclerotiorum disease development. Mol. Plant-Microbe Interact. 21:605–12 [Google Scholar]
  93. Kim SM, Bae C, Oh SK, Choi D. 93.  2013. A pepper (Capsicum annuum L.) metacaspase 9 (Camc9) plays a role in pathogen-induced cell death in plants. Mol. Plant Pathol. 14:557–66 [Google Scholar]
  94. Kim WY, Lee SY, Jung YJ, Chae HB, Nawkar GM. 94.  et al. 2011. 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. 286:42670–78 [Google Scholar]
  95. Knapp RT, Wong MJ, Kollmannsberger LK, Gassen NC, Kretzschmar A. 95.  et al. 2014. Hsp70 cochaperones HspBP1 and BAG-1M differentially regulate steroid hormone receptor function. PLOS ONE 9:e85415 [Google Scholar]
  96. Kullmann M, Schneikert J, Moll J, Heck S, Zeiner M. 96.  et al. 1998. RAP46 is a negative regulator of glucocorticoid receptor action and hormone-induced apoptosis. J. Biol. Chem. 273:14620–25 [Google Scholar]
  97. Kumar S.97.  2007. Caspase function in programmed cell death. Cell Death Differ 14:32–43 [Google Scholar]
  98. Kuroyanagi M, Yamada K, Hatsugai N, Kondo M, Nishimura M, Hara-Nishimura I. 98.  2005. Vacuolar processing enzyme is essential for mycotoxin-induced cell death in Arabidopsis thaliana. J. Biol. Chem. 280:32914–20 [Google Scholar]
  99. La Farge C, Williams KH, England JH. 99.  2013. Regeneration of Little Ice Age bryophytes emerging from a polar glacier with implications of totipotency in extreme environments. PNAS 110:9839–44 [Google Scholar]
  100. Li F, Vierstra RD. 100.  2012. Autophagy: a multifaceted intracellular system for bulk and selective recycling. Trends Plant Sci 17:526–37 [Google Scholar]
  101. Li L, Xing Y, Chang D, Fang S, Cui B. 101.  et al. 2016. CaM/BAG5/Hsc70 signaling complex dynamically regulates leaf senescence. Sci. Rep. 6:31889 [Google Scholar]
  102. Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M. 102.  et al. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell 91:479–89 [Google Scholar]
  103. Li W, Kabbage M, Dickman MB. 103.  2010. 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. 74:363–75 [Google Scholar]
  104. Li Y, Kabbage M, Liu W, Dickman MB. 104.  2016. Aspartyl protease-mediated cleavage of BAG6 is necessary for autophagy and fungal resistance in plants. Plant Cell 28:233–47 [Google Scholar]
  105. Liu R, Takayama S, Zheng Y, Froesch B, Chen GQ. 105.  et al. 1998. Interaction of BAG-1 with retinoic acid receptor and its inhibition of retinoic acid-induced apoptosis in cancer cells. J. Biol. Chem. 273:16985–92 [Google Scholar]
  106. Liu Y, Bassham DC. 106.  2012. Autophagy: pathways for self-eating in plant cells. Annu. Rev. Plant Biol. 63:215–37 [Google Scholar]
  107. Lu CA, Lin CC, Lee KW, Chen JL, Huang LF. 107.  et al. 2007. The SnRK1A protein kinase plays a key role in sugar signaling during germination and seedling growth of rice. Plant Cell 19:2484–99 [Google Scholar]
  108. Lu H, Chandrasekar B, Oeljeklaus J, Misas-Villamil JC, Wang Z. 108.  et al. 2015. Subfamily-specific fluorescent probes for cysteine proteases display dynamic protease activities during seed germination. Plant Physiol 168:1462–75 [Google Scholar]
  109. Marshall RS, Li F, Gemperline DC, Book AJ, Vierstra RD. 109.  2015. Autophagic degradation of the 26S proteasome is mediated by the dual ATG8/ubiquitin receptor RPN10 in Arabidopsis. Mol. Cell 58:1053–66 [Google Scholar]
  110. Matsuzawa S, Takayama S, Froesch BA, Zapata JM, Reed JC. 110.  1998. p53-inducible human homologue of Drosophila seven in absentia (Siah) inhibits cell growth: suppression by BAG-1. EMBO J 17:2736–47 [Google Scholar]
  111. McGee SL, Hargreaves M. 111.  2008. AMPK and transcriptional regulation. Front. Biosci. 13:3022–33 [Google Scholar]
  112. McKersie BD, Lesheim Y. 112.  2013. Stress and Stress Coping in Cultivated Plants Dordrecht, Neth.: Springer [Google Scholar]
  113. Meikrantz W, Schlegel R. 113.  1995. Apoptosis and the cell cycle. J. Cell Biochem. 58:160–74 [Google Scholar]
  114. Menand B, Meyer C, Robaglia C. 114.  2004. Plant growth and the TOR pathway. Curr. Top. Microbiol. Immunol. 279:97–113 [Google Scholar]
  115. Michaeli S, Galili G, Genschik P, Fernie AR, Avin-Wittenberg T. 115.  2016. Autophagy in plants—what's new on the menu?. Trends Plant Sci 21:134–44 [Google Scholar]
  116. Michaeli S, Honig A, Levanony H, Peled-Zehavi H, Galili G. 116.  2014. Arabidopsis ATG8-INTERACTING PROTEIN1 is involved in autophagy-dependent vesicular trafficking of plastid proteins to the vacuole. Plant Cell 26:4084–101 [Google Scholar]
  117. Mills K, Daish T, Harvey KF, Pfleger CM, Hariharan IK, Kumar S. 117.  2006. The Drosophila melanogaster Apaf-1 homologue ARK is required for most, but not all, programmed cell death. J. Cell Biol. 172:809–15 [Google Scholar]
  118. Minina EA, Sanchez-Vera V, Moschou PN, Suarez MF, Sundberg E. 118.  et al. 2013. Autophagy mediates caloric restriction-induced lifespan extension in Arabidopsis. Aging Cell 12:327–29 [Google Scholar]
  119. Mock JY, Chartron JW, Zaslaver M, Xu Y, Ye Y, Clemons WM Jr. 119.  2015. Bag6 complex contains a minimal tail-anchor-targeting module and a mock BAG domain. PNAS 112:106–11 [Google Scholar]
  120. Mufti AR, Burstein E, Csomos RA, Graf PC, Wilkinson JC. 120.  et al. 2006. XIAP is a copper binding protein deregulated in Wilson's disease and other copper toxicosis disorders. Mol. Cell 21:775–85 [Google Scholar]
  121. Munné-Bosch S, Alegre L. 121.  2004. Die and let live: leaf senescence contributes to plant survival under drought stress. Funct. Plant Biol. 31:203–16 [Google Scholar]
  122. Nakaune S, Yamada K, Kondo M, Kato T, Tabata S. 122.  et al. 2005. A vacuolar processing enzyme, δVPE, is involved in seed coat formation at the early stage of seed development. Plant Cell 17:876–87 [Google Scholar]
  123. Oliver MJ, Guo L, Alexander DC, Ryals JA, Wone BW, Cushman JC. 123.  2011. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell 23:1231–48 [Google Scholar]
  124. Oliver MJ, Woods AJ, O'Mahoney P. 124.  1998. “To dryness and beyond”—preparation for the dried state and rehydration in vegetative desiccation-tolerant plants. Plant Growth Regul 24:193–201 [Google Scholar]
  125. Osuna D, Usadel B, Morcuende R, Gibon Y, Blasing OE. 125.  et al. 2007. Temporal responses of transcripts, enzyme activities and metabolites after adding sucrose to carbon-deprived Arabidopsis seedlings. Plant J 49:463–91 [Google Scholar]
  126. Padmanabhan MS, Ma S, Burch-Smith TM, Czymmek K, Huijser P, Dinesh-Kumar SP. 126.  2013. Novel positive regulatory role for the SPL6 transcription factor in the N TIR-NB-LRR receptor-mediated plant innate immunity. PLOS Pathog 9:e1003235 [Google Scholar]
  127. Parrish AB, Freel CD, Kornbluth S. 127.  2013. Cellular mechanisms controlling caspase activation and function. Cold Spring Harb. Perspect. Biol. 5:a008672 [Google Scholar]
  128. Peters S, Mundree SG, Thomson JA, Farrant JM, Keller F. 128.  2007. Protection mechanisms in the resurrection plant Xerophyta viscosa (Baker): both sucrose and raffinose family oligosaccharides (RFOs) accumulate in leaves in response to water deficit. J. Exp. Bot. 58:1947–56 [Google Scholar]
  129. Preston JC, Hileman LC. 129.  2013. Functional evolution in the plant SQUAMOSA-PROMOTER BINDING PROTEIN-LIKE (SPL) gene family. Front. Plant Sci. 4:80 [Google Scholar]
  130. Reape TJ, McCabe PF. 130.  2008. Apoptotic-like programmed cell death in plants. New Phytol 180:13–26 [Google Scholar]
  131. Reape TJ, McCabe PF. 131.  2013. Commentary: the cellular condensation of dying plant cells: programmed retraction or necrotic collapse?. Plant Sci 207:135–39 [Google Scholar]
  132. Ren M, Venglat P, Qiu S, Feng L, Cao Y. 132.  et al. 2012. Target of rapamycin signaling regulates metabolism, growth, and life span in Arabidopsis. Plant Cell 24:4850–74 [Google Scholar]
  133. Riedl SJ, Shi Y. 133.  2004. Molecular mechanisms of caspase regulation during apoptosis. Nat. Rev. Mol. Cell Biol. 5:897–907 [Google Scholar]
  134. Rodriguez MC, Edsgard D, Hussain SS, Alquezar D, Rasmussen M. 134.  et al. 2010. Transcriptomes of the desiccation-tolerant resurrection plant Craterostigma plantagineum. Plant J 63:212–28 [Google Scholar]
  135. Rojo E, Martıín R, Carter C, Zouhar J, Pan S. 135.  et al. 2004. VPEγ exhibits a caspase-like activity that contributes to defense against pathogens. Curr. Biol. 14:1897–906 [Google Scholar]
  136. Rosati A, Graziano V, De Laurenzi V, Pascale M, Turco MC. 136.  2011. BAG3: a multifaceted protein that regulates major cell pathways. Cell Death Disease 2:e141 [Google Scholar]
  137. Rose TL, Bonneau L, Der C, Marty-Mazars D, Marty F. 137.  2006. Starvation-induced expression of autophagy-related genes in Arabidopsis. Biol. Cell 98:53–67 [Google Scholar]
  138. Rothe M, Pan MG, Henzel WJ, Ayres TM, Goeddel DV. 138.  1995. The TNFR2-TRAF signaling complex contains two novel proteins related to baculoviral inhibitor of apoptosis proteins. Cell 83:1243–52 [Google Scholar]
  139. Ruckenstuhl C, Netzberger C, Entfellner I, Carmona-Gutierrez D, Kickenweiz T. 139.  et al. 2014. Lifespan extension by methionine restriction requires autophagy-dependent vacuolar acidification. PLOS Genet 10:e1004347 [Google Scholar]
  140. Sarkar S, Davies JE, Huang Z, Tunnacliffe A, Rubinsztein DC. 140.  2007. Trehalose, a novel mTOR-independent autophagy enhancer, accelerates the clearance of mutant huntingtin and α-synuclein. J. Biol. Chem. 282:5641–52 [Google Scholar]
  141. Schepetilnikov M, Dimitrova M, Mancera-Martinez E, Geldreich A, Keller M, Ryabova LA. 141.  2013. TOR and S6K1 promote translation reinitiation of uORF-containing mRNAs via phosphorylation of eIF3h. EMBO J 32:1087–102 [Google Scholar]
  142. Schile AJ, García-Fernández M, Steller H. 142.  2008. Regulation of apoptosis by XIAP ubiquitin-ligase activity. Genes Dev 22:2256–66 [Google Scholar]
  143. Shalini S, Dorstyn L, Dawar S, Kumar S. 143.  2015. Old, new and emerging functions of caspases. Cell Death Differ 22:526–39 [Google Scholar]
  144. Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF. 144.  et al. 2011. Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLOS Pathog 7:e1002185 [Google Scholar]
  145. Singh S, Ambastha V, Levine A, Sopory SK, Yadava PK. 145.  et al. 2015. Anhydrobiosis and programmed cell death in plants: commonalities and differences. Curr. Plant Biol. 2:12–20 [Google Scholar]
  146. Smith AM, Stitt M. 146.  2007. Coordination of carbon supply and plant growth. Plant Cell Environ 30:1126–49 [Google Scholar]
  147. Song J, Takeda M, Morimoto RI. 147.  2001. Bag1-Hsp70 mediates a physiological stress signalling pathway that regulates Raf-1/ERK and cell growth. Nat. Cell Biol. 3:276–82 [Google Scholar]
  148. Srinivasula SM, Ashwell JD. 148.  2008. IAPs: What's in a name?. Mol. Cell 30:123–35 [Google Scholar]
  149. Stone JM, Liang X, Nekl ER, Stiers JJ. 149.  2005. Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant J 41:744–54 [Google Scholar]
  150. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J. 150.  2005. Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol 137:13–30 [Google Scholar]
  151. Sundstrom JF, Vaculova A, Smertenko AP, Savenkov EI, Golovko A. 151.  et al. 2009. Tudor staphylococcal nuclease is an evolutionarily conserved component of the programmed cell death degradome. Nat. Cell Biol. 11:1347–54 [Google Scholar]
  152. Suttangkakul A, Li F, Chung T, Vierstra RD. 152.  2011. The ATG1/ATG13 protein kinase complex is both a regulator and a target of autophagic recycling in Arabidopsis. Plant Cell 23:3761–79 [Google Scholar]
  153. Takahashi R, Deveraux Q, Tamm I, Welsh K, Assa-Munt N. 153.  et al. 1998. A single BIR domain of XIAP sufficient for inhibiting caspases. J. Biol. Chem. 273:7787–90 [Google Scholar]
  154. Takayama S, Reed JC. 154.  2001. Molecular chaperone targeting and regulation by BAG family proteins. Nat. Cell Biol. 3:E237–41 [Google Scholar]
  155. Takayama S, Sato T, Krajewski S, Kochel K, Irie S. 155.  et al. 1995. Cloning and functional analysis of BAG-1: a novel Bcl-2-binding protein with anti-cell death activity. Cell 80:279–84 [Google Scholar]
  156. Takayama S, Xie Z, Reed JC. 156.  1999. An evolutionarily conserved family of Hsp70/Hsc70 molecular chaperone regulators. J. Biol. Chem. 274:781–86 [Google Scholar]
  157. Tardieu F.157.  2005. Plant tolerance to water deficit: physical limits and possibilities for progress. C. R. Geosci. 337:57–67 [Google Scholar]
  158. Tenev T, Zachariou A, Wilson R, Paul A, Meier P. 158.  2002. Jafrac2 is an IAP antagonist that promotes cell death by liberating Dronc from DIAP1. EMBO J 21:5118–29 [Google Scholar]
  159. Thomma BP, Nurnberger T, Joosten MH. 159.  2011. Of PAMPs and effectors: the blurred PTI-ETI dichotomy. Plant Cell 23:4–15 [Google Scholar]
  160. Thornberry NA, Bull HG, Calaycay JR, Chapman KT, Howard AD. 160.  et al. 1992. A novel heterodimeric cysteine protease is required for interleukin-1β processing in monocytes. Nature 356:768–74 [Google Scholar]
  161. Thress K, Evans EK, Kornbluth S. 161.  1999. Reaper-induced dissociation of a Scythe-sequestered cytochrome c-releasing activity. EMBO J 18:5486–93 [Google Scholar]
  162. Thress K, Henzel W, Shillinglaw W, Kornbluth S. 162.  1998. Scythe: a novel reaper-binding apoptotic regulator. EMBO J 17:6135–43 [Google Scholar]
  163. Tran V, Weier D, Radchuk R, Thiel J, Radchuk V. 163.  2014. Caspase-like activities accompany programmed cell death events in developing barley grains. PLOS ONE 9:e109426 [Google Scholar]
  164. Tschopp J, Martinon F, Hofmann K. 164.  1999. Apoptosis: silencing the death receptors. Curr. Biol. 9:R381–84 [Google Scholar]
  165. Tsiatsiani L, Timmerman E, De Bock PJ, Vercammen D, Stael S. 165.  et al. 2013. The Arabidopsis METACASPASE9 degradome. Plant Cell 25:2831–47 [Google Scholar]
  166. Tsiatsiani L, Van Breusegem F, Gallois P, Zavialov A, Lam E, Bozhkov PV. 166.  2011. Metacaspases. Cell Death Differ 18:1279–88 [Google Scholar]
  167. Twiddy D, Cohen GM, Macfarlane M, Cain K. 167.  2006. Caspase-7 is directly activated by the approximately 700-kDa apoptosome complex and is released as a stable XIAP-caspase-7 approximately 200-kDa complex. J. Biol. Chem. 281:3876–88 [Google Scholar]
  168. Uren AG, O'Rourke K, Aravind LA, Pisabarro MT, Seshagiri S. 168.  et al. 2000. Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma. Mol. Cell 6:961–67 [Google Scholar]
  169. Usadel B, Blasing OE, Gibon Y, Retzlaff K, Hohne M. 169.  et al. 2008. Global transcript levels respond to small changes of the carbon status during progressive exhaustion of carbohydrates in Arabidopsis rosettes. Plant Physiol 146:1834–61 [Google Scholar]
  170. van Doorn WG.170.  2011. Classes of programmed cell death in plants, compared to those in animals. J. Exp. Bot. 62:4749–61 [Google Scholar]
  171. van Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P. 171.  et al. 2011. Morphological classification of plant cell deaths. Cell Death Differ 18:1241–46 [Google Scholar]
  172. Van Hautegem T, Waters AJ, Goodrich J, Nowack MK. 172.  2015. Only in dying, life: programmed cell death during plant development. Trends Plant Sci 20:102–13 [Google Scholar]
  173. Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM. 173.  et al. 2000. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell 102:43–53 [Google Scholar]
  174. Wang HG, Takayama S, Rapp UR, Reed JC. 174.  1996. Bcl-2 interacting protein, BAG-1, binds to and activates the kinase Raf-1. PNAS 93:7063–68 [Google Scholar]
  175. Wang X, Guo J, Fei E, Mu Y, He S. 175.  et al. 2014. BAG5 protects against mitochondrial oxidative damage through regulating PINK1 degradation. PLOS ONE 9:e86276 [Google Scholar]
  176. Watanabe N, Lam E. 176.  2011. Arabidopsis metacaspase 2d is a positive mediator of cell death induced during biotic and abiotic stresses. Plant J 66:969–82 [Google Scholar]
  177. Whittaker A, Martinelli T, Bochicchio A, Vazzana C, Farrant J. 177.  2004. Comparison of sucrose metabolism during the rehydration of desiccation-tolerant and desiccation-sensitive leaf material of Sporobolus stapfianus. Physiol. Plant. 122:11–20 [Google Scholar]
  178. Whittaker A, Martinelli T, Farrant JM, Bochicchio A, Vazzana C. 178.  2007. Sucrose phosphate synthase activity and the co-ordination of carbon partitioning during sucrose and amino acid accumulation in desiccation-tolerant leaf material of the C4 resurrection plant Sporobolus stapfianus during dehydration. J. Exp. Bot. 58:3775–87 [Google Scholar]
  179. Williams B, Kabbage M, Britt R, Dickman MB. 179.  2010. AtBAG7, an Arabidopsis Bcl-2-associated athanogene, resides in the endoplasmic reticulum and is involved in the unfolded protein response. PNAS 107:6088–93 [Google Scholar]
  180. Williams B, Kabbage M, Kim HJ, Britt R, Dickman MB. 180.  2011. Tipping the balance: Sclerotinia sclerotiorum secreted oxalic acid suppresses host defenses by manipulating the host redox environment. PLOS Pathog 7:e1002107 [Google Scholar]
  181. Williams B, Njaci I, Moghaddam L, Long H, Dickman MB. 181.  et al. 2015. Trehalose accumulation triggers autophagy during plant desiccation. PLOS Genet 11:e1005705 [Google Scholar]
  182. Williams B, Verchot J, Dickman MB. 182.  2014. When supply does not meet demand-ER stress and plant programmed cell death. Front. Plant Sci. 5:211 [Google Scholar]
  183. Wrzaczek M, Brosche M, Kollist H, Kangasjarvi J. 183.  2009. Arabidopsis GRI is involved in the regulation of cell death induced by extracellular ROS. PNAS 106:5412–17 [Google Scholar]
  184. Wu G, Chai J, Suber TL, Wu J-W, Du C. 184.  et al. 2000. Structural basis of IAP recognition by Smac/DIABLO. Nature 408:1008–12 [Google Scholar]
  185. Yamada T, Takatsu Y, Manabe T, Kasumi M, Marubashi W. 185.  2003. Suppressive effect of trehalose on apoptotic cell death leading to petal senescence in ethylene-insensitive flowers of gladiolus. Plant Sci 164:213–21 [Google Scholar]
  186. Yang YL, Li XM. 186.  2000. The IAP family: endogenous caspase inhibitors with multiple biological activities. Cell Res 10:169–77 [Google Scholar]
  187. Yang Z, Klionsky DJ. 187.  2010. Eaten alive: a history of macroautophagy. Nat. Cell Biol. 12:814–22 [Google Scholar]
  188. Ye CM, Chen S, Payton M, Dickman MB, Verchot J. 188.  2013. TGBp3 triggers the unfolded protein response and SKP1-dependent programmed cell death. Mol. Plant Pathol. 14:241–55 [Google Scholar]
  189. Yobi A, Wone BW, Xu W, Alexander DC, Guo L. 189.  et al. 2012. Comparative metabolic profiling between desiccation-sensitive and desiccation-tolerant species of Selaginella reveals insights into the resurrection trait. Plant J 72:983–99 [Google Scholar]
  190. Yobi A, Wone BW, Xu W, Alexander DC, Guo L. 190.  et al. 2013. Metabolomic profiling in Selaginella lepidophylla at various hydration states provides new insights into the mechanistic basis of desiccation tolerance. Mol. Plant 6:369–85 [Google Scholar]
  191. Young AR, Chan EY, Hu XW, Kochl R, Crawshaw SG. 191.  et al. 2006. Starvation and ULK1-dependent cycling of mammalian Atg9 between the TGN and endosomes. J. Cell Sci. 119:3888–900 [Google Scholar]
  192. Yu X, Wang L, Acehan D, Wang X, Akey CW. 192.  2006. Three-dimensional structure of a double apoptosome formed by the Drosophila Apaf-1 related killer. J. Mol. Biol. 355:577–89 [Google Scholar]
  193. Yuan J, Shaham S, Ledoux S, Ellis HM, Horvitz HR. 193.  1993. The C. elegans cell death gene ced-3 encodes a protein similar to mammalian interleukin-1β-converting enzyme. Cell 75:641–52 [Google Scholar]
  194. Zhang H, Dong S, Wang M, Wang W, Song W. 194.  et al. 2010. The role of vacuolar processing enzyme (VPE) from Nicotiana benthamiana in the elicitor-triggered hypersensitive response and stomatal closure. J. Exp. Bot. 61:3799–812 [Google Scholar]
  195. Zimmermann D, Gomez-Barrera JA, Pasule C, Brack-Frick UB, Sieferer E. 195.  et al. 2016. Cell death control by matrix metalloproteinases. Plant Physiol 171:1456–69 [Google Scholar]
  196. Zipfel C, Robatzek S. 196.  2010. Pathogen-associated molecular pattern-triggered immunity: veni, vidi…?. Plant Physiol 154:551–54 [Google Scholar]
  197. Zou H, Henzel WJ, Liu X, Lutschg A, Wang X. 197.  1997. Apaf-1, a human protein homologous to C.elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90:405–13 [Google Scholar]
  198. Zou H, Li Y, Liu X, Wang X. 198.  1999. An APAF-1·cytochrome c multimeric complex is a functional apoptosome that activates procaspase-9. J. Biol. Chem. 274:11549–56 [Google Scholar]

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error