1932

Abstract

Programmed cell death (PCD) is a collective term for diverse processes causing an actively induced, tightly controlled cellular suicide. PCD has a multitude of functions in the development and health of multicellular organisms. In comparison to intensively studied forms of animal PCD such as apoptosis, our knowledge of the regulation of PCD in plants remains limited. Despite the importance of PCD in plant development and as a response to biotic and abiotic stresses, the complex molecular networks controlling different forms of plant PCD are only just beginning to emerge. With this review, we provide an update on the considerable progress that has been made over the last decade in our understanding of PCD as an inherent part of plant development. We highlight both functions of developmental PCD and central aspects of its molecular regulation.

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2016-10-06
2024-04-23
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Literature Cited

  1. Alonso-Peral MM, Li J, Li Y, Allen RS, Schnippenkoetter W. et al. 2010. The microRNA159-regulated GAMYB-like genes inhibit growth and promote programmed cell death in Arabidopsis. Plant Physiol. 154:757–71 [Google Scholar]
  2. Amien S, Kliwer I, Márton ML, Debener T, Geiger D. et al. 2010. Defensin-like ZmES4 mediates pollen tube burst in maize via opening of the potassium channel KZM1. PLOS Biol. 8:e1000388 [Google Scholar]
  3. An G, Yi J, Moon S, Lee Y-S, Zhu L. et al. 2016. Defective Tapetum Cell Death 1 (DTC1) regulates ROS levels by binding to metallothionein during tapetum degeneration. Plant Physiol. 170:1611–23 [Google Scholar]
  4. Andème Ondzighi C, Christopher DA, Cho EJ, Chang S-C, Staehelin LA. 2008. Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205–20 [Google Scholar]
  5. Aoki N, Ishibashi Y, Kai K, Tomokiyo R, Yuasa T, Iwaya-Inoue M. 2014. Programmed cell death in barley aleurone cells is not directly stimulated by reactive oxygen species produced in response to gibberellin. J. Plant Physiol. 171:615–18 [Google Scholar]
  6. Bar-Dror T, Dermastia M, Kladnik A, Žnidarič MT, Novak MP. et al. 2011. Programmed cell death occurs asymmetrically during abscission in tomato. Plant Cell 23:4146–63 [Google Scholar]
  7. Beers EP. 1997. Programmed cell death during plant growth and development. Cell Death Differ. 4:649–61 [Google Scholar]
  8. Bethke PC, Libourel IGL, Aoyama N, Chung Y-Y, Still DW, Jones RL. 2007. The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol. 143:1173–88 [Google Scholar]
  9. Blanvillain R, Young B, Cai Y-M, Hecht V, Varoquaux F. et al. 2011. The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J. 30:1173–83 [Google Scholar]
  10. Boex-Fontvieille E, Rustgi S, Reinbothe S, Reinbothe C. 2015. A Kunitz-type protease inhibitor regulates programmed cell death during flower development in Arabidopsis thaliana. J. Exp. Bot. 66:6119–35 [Google Scholar]
  11. Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M. et al. 2009. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136:3279–88 [Google Scholar]
  12. Bollhöner B, Prestele J, Tuominen H. 2012. Xylem cell death: emerging understanding of regulation and function. J. Exp. Bot. 63:1081–94 [Google Scholar]
  13. Bollhöner B, Zhang B, Stael S, Denancé N, Overmyer K. et al. 2013. Post mortem function of AtMC9 in xylem vessel elements. New Phytol. 200:498–510 [Google Scholar]
  14. Bozhkov PV, Filonova LH, Suarez MF, Helmersson A, Smertenko AP. et al. 2004. VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ. 11:175–82 [Google Scholar]
  15. Breeze E, Harrison E, McHattie S, Hughes L, Hickman R. et al. 2011. High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–94 [Google Scholar]
  16. Broderick SR, Wijeratne S, Wijeratn AJ, Chapin LJ, Meulia T, Jones ML. 2014. RNA-sequencing reveals early, dynamic transcriptome changes in the corollas of pollinated petunias. BMC Plant Biol. 14:307 [Google Scholar]
  17. Calderon-Urrea A, Dellaporta SL. 1999. Cell death and cell protection genes determine the fate of pistils in maize. Development 126:435–41 [Google Scholar]
  18. Chen G-H, Sun J-Y, Liu M, Liu J, Yang W-C. 2014. SPOROCYTELESS is a novel embryophyte-specific transcription repressor that interacts with TPL and TCP proteins in Arabidopsis. J. Genet. Genom. 41:617–25 [Google Scholar]
  19. Chen J, Yi Q, Song Q, Gu Y, Zhang J. et al. 2015. A highly efficient maize nucellus protoplast system for transient gene expression and studying programmed cell death–related processes. Plant Cell Rep. 34:1239–51 [Google Scholar]
  20. Chen W-H, Li P-F, Chen M-K, Lee Y-I, Yang C-H. 2015. FOREVER YOUNG FLOWER negatively regulates ethylene response DNA-binding factors by activating an ethylene-responsive factor to control Arabidopsis floral organ senescence and abscission. Plant Physiol. 168:1666–83 [Google Scholar]
  21. Cheng X-X, Yu M, Zhang N, Zhou Z-Q, Xu Q-T. et al. 2016. Reactive oxygen species regulate programmed cell death progress of endosperm in winter wheat (Triticum aestivum L.) under waterlogging. Protoplasma 253:311–27 [Google Scholar]
  22. Christensen CA, Gorsich SW, Brown RH, Jones LG, Brown J. et al. 2002. Mitochondrial GFA2 is required for synergid cell death in Arabidopsis. Plant Cell 14:2215–32 [Google Scholar]
  23. Claessen D, Rozen DE, Kuipers OP, Søgaard-Andersen L, van Wezel GP. 2014. Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies. Nat. Rev. Microbiol. 12:115–24 [Google Scholar]
  24. Crawford BCW, Ditta G, Yanofsky MF. 2007. The NTT gene is required for transmitting-tract development in carpels of Arabidopsis thaliana. Curr. Biol. 17:1101–8 [Google Scholar]
  25. Crawford BCW, Yanofsky MF. 2011. HALF FILLED promotes reproductive tract development and fertilization efficiency in Arabidopsis thaliana. Development 138:2999–3009 [Google Scholar]
  26. Cronshaw J, Bouck GB. 1965. The fine structure of differentiating xylem elements. J. Cell Biol. 24:415–31 [Google Scholar]
  27. Dauphinee AN, Wright H, Rantong G, Gunawardena AHLAN. 2012. The involvement of ethylene in programmed cell death and climacteric-like behaviour during the remodelling of lace plant (Aponogeton madagascariensis) leaves. Botany 90:1237–44 [Google Scholar]
  28. de Graaf BHJ, Vatovec S, Juárez-Díaz JA, Chai L, Kooblall K. et al. 2012. The Papaver self-incompatibility pollen S-determinant, PrpS, functions in Arabidopsis thaliana. Curr. Biol. 22:154–59 [Google Scholar]
  29. DeLong A, Calderon-Urrea A, Dellaporta SL. 1993. Sex determination gene TASSELSEED 2 of maize encodes a short-chain alcohol dehydrogenase required for stage-specific floral organ abortion. Cell 74:757–68 [Google Scholar]
  30. Demesa-Arévalo E, Vielle-Calzada J-P. 2013. The classical arabinogalactan protein AGP18 mediates megaspore selection in Arabidopsis. Plant Cell 25:1274–87 [Google Scholar]
  31. Denay G, Creff A, Moussu S, Wagnon P, Thévenin J. et al. 2014. Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1. Development 141:1222–27 [Google Scholar]
  32. Denton D, Aung-Htut MT, Lorensuhewa N, Nicolson S, Zhu W. et al. 2013. UTX coordinates steroid hormone–mediated autophagy and cell death. Nat. Commun. 4:2916 [Google Scholar]
  33. Domínguez F, Cejudo FJ. 2006. Identification of a nuclear-localized nuclease from wheat cells undergoing programmed cell death that is able to trigger DNA fragmentation and apoptotic morphology on nuclei from human cells. Biochem. J. 397:529–36 [Google Scholar]
  34. Domínguez F, Cejudo FJ. 2014. Programmed cell death (PCD): an essential process of cereal seed development and germination. Front. Plant Sci. 5:366 [Google Scholar]
  35. Domínguez F, Moreno J, Cejudo FJ. 2001. The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213:352–60 [Google Scholar]
  36. Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L. et al. 2014. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Commun. 5:3129 [Google Scholar]
  37. Eaves DJ, Flores-Ortiz C, Haque T, Lin Z, Teng N, Franklin-Tong VE. 2014. Self-incompatibility in Papaver: advances in integrating the signalling network. Biochem. Soc. Trans. 42:370–76 [Google Scholar]
  38. Endo H, Yamaguchi M, Tamura T, Nakano Y, Nishikubo N. et al. 2015. Multiple classes of transcription factors regulate the expression of VASCULAR-RELATED NAC-DOMAIN7, a master switch of xylem vessel differentiation. Plant Cell Physiol. 56:242–54 [Google Scholar]
  39. Escamez S, André D, Zhang B, Bollhöner B, Pesquet E, Tuominen H. 2016. METACASPASE9 modulates autophagy to confine cell death to the target cells during Arabidopsis vascular xylem differentiation. Biol. Open 5:122–29 [Google Scholar]
  40. Escamez S, Tuominen H. 2014. Programmes of cell death and autolysis in tracheary elements: when a suicidal cell arranges its own corpse removal. J. Exp. Bot. 65:1313–21 [Google Scholar]
  41. Farage-Barhom S, Burd S, Sonego L, Mett A, Belausov E. et al. 2011. Localization of the Arabidopsis senescence- and cell death–associated BFN1 nuclease: from the ER to fragmented nuclei. Mol. Plant 4:1062–73 [Google Scholar]
  42. Farage-Barhom S, Burd S, Sonego L, Perl-Treves R, Lers A. 2008. Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death–related processes. J. Exp. Bot. 59:3247–58 [Google Scholar]
  43. Fath A, Bethke PC, Jones RL. 2001. Enzymes that scavenge reactive oxygen species are down-regulated prior to gibberellic acid–induced programmed cell death in barley aleurone. Plant Physiol. 126:156–66 [Google Scholar]
  44. Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M. et al. 2014. Programmed cell death controlled by ANAC033/SOMBRERO determines root cap organ size in Arabidopsis. Curr. Biol. 24:931–40 [Google Scholar]
  45. Feng B, Lu D, Ma X, Peng Y, Sun Y. et al. 2012. Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72:612–24 [Google Scholar]
  46. Fernández Gómez J, Talle B, Wilson ZA. 2015. Anther and pollen development: a conserved developmental pathway. J. Integr. Plant Biol. 57:876–91 [Google Scholar]
  47. Fuchs Y, Steller H. 2011. Programmed cell death in animal development and disease. Cell 147:742–58 [Google Scholar]
  48. Fuchs Y, Steller H. 2015. Live to die another way: modes of programmed cell death and the signals emanating from dying cells. Nat. Rev. Mol. Cell Biol. 16:329–44 [Google Scholar]
  49. Ge X, Dietrich C, Matsuno M, Li G, Berg H, Xia Y. 2005. An Arabidopsis aspartic protease functions as an anti-cell-death component in reproduction and embryogenesis. EMBO Rep. 6:282–88 [Google Scholar]
  50. Gremski K, Ditta G, Yanofsky MF. 2007. The HECATE genes regulate female reproductive tract development in Arabidopsis thaliana. Development 134:3593–601 [Google Scholar]
  51. Grimault A, Gendrot G, Chamot S, Widiez T, Rabillé H. et al. 2015. ZmZHOUPI, an endosperm-specific basic helix-loop-helix transcription factor involved in maize seed development. Plant J. 84:574–86 [Google Scholar]
  52. Groover A, DeWitt N, Heidel A, Jones A. 1997. Programmed cell death of plant tracheary elements differentiating in vitro. Protoplasma 196:197–211 [Google Scholar]
  53. Groß-Hardt R, Kägi C, Baumann N, Moore JM, Baskar R. et al. 2007. LACHESIS restricts gametic cell fate in the female gametophyte of Arabidopsis. PLOS Biol. 5:e47 [Google Scholar]
  54. Gubler F, Chandler PM, White RG, Llewellyn DJ, Jacobsen JV. 2002. Gibberellin signaling in barley aleurone cells. Control of SLN1 and GAMYB expression. Plant Physiol. 129:191–200 [Google Scholar]
  55. Gunawardena AHLAN. 2008. Programmed cell death and tissue remodelling in plants. J. Exp. Bot. 59:445–51 [Google Scholar]
  56. Gunawardena AHLAN, Greenwood JS, Dengler NG. 2004. Programmed cell death remodels lace plant leaf shape during development. Plant Cell 16:60–73 [Google Scholar]
  57. Hatsugai N, Yamada K, Goto-Yamada S, Hara-Nishimura I. 2015. Vacuolar processing enzyme in plant programmed cell death. Front. Plant Sci. 6:234 [Google Scholar]
  58. He D, Wang Q, Wang K, Yang P. 2015. Genome-wide dissection of the microRNA expression profile in rice embryo during early stages of seed germination. PLOS ONE 10:e0145424 [Google Scholar]
  59. Hierl G, Höwing T, Isono E, Lottspeich F, Gietl C. 2014. Ex vivo processing for maturation of Arabidopsis KDEL-tailed cysteine endopeptidase 2 (AtCEP2) pro-enzyme and its storage in endoplasmic reticulum derived organelles. Plant Mol. Biol. 84:605–20 [Google Scholar]
  60. Holloway SJ, Friedman WE. 2008. Embryological features of Tofieldia glutinosa and their bearing on the early diversification of monocotyledonous plants. Ann. Bot. 102:167–82 [Google Scholar]
  61. Imai A, Hanzawa Y, Komura M, Yamamoto KT, Komeda Y, Takahashi T. 2006. The dwarf phenotype of the Arabidopsis acl5 mutant is suppressed by a mutation in an upstream ORF of a bHLH gene. Development 133:3575–85 [Google Scholar]
  62. Ishibashi Y, Kasa S, Sakamoto M, Aoki N, Kai K. et al. 2015. A role for reactive oxygen species produced by NADPH oxidases in the embryo and aleurone cells in barley seed germination. PLOS ONE 10:e0143173 [Google Scholar]
  63. Ito J, Fukuda H. 2002. ZEN1 is a key enzyme in the degradation of nuclear DNA during programmed cell death of tracheary elements. Plant Cell 14:3201–11 [Google Scholar]
  64. Iwano M, Ngo QA, Entani T, Shiba H, Nagai T. et al. 2012. Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development 139:4202–9 [Google Scholar]
  65. Jiang L, Yang S-L, Xie L-F, Puah CS, Zhang X-Q. et al. 2005. VANGUARD1 encodes a pectin methylesterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 17:584–96 [Google Scholar]
  66. Jung K-H, Han M-J, Lee Y-S, Kim Y-W, Hwang I. et al. 2005. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–22 [Google Scholar]
  67. Kägi C, Baumann N, Nielsen N, Stierhof Y-D, Groß-Hardt R. 2010. The gametic central cell of Arabidopsis determines the lifespan of adjacent accessory cells. PNAS 107:22350–55 [Google Scholar]
  68. Kasaras A, Kunze R. 2010. Expression, localisation and phylogeny of a novel family of plant-specific membrane proteins. Plant Biol. 12:140–52 [Google Scholar]
  69. Kerr JFR, Wyllie AH, Currie AR. 1972. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br. J. Cancer 26:239–57 [Google Scholar]
  70. Kessler SA, Grossniklaus U. 2011. She's the boss: signaling in pollen tube reception. Curr. Opin. Plant Biol. 14:622–27 [Google Scholar]
  71. Kim HJ, Hong SH, Kim YW, Lee IH, Jun JH. et al. 2014. Gene regulatory cascade of senescence-associated NAC transcription factors activated by ETHYLENE-INSENSITIVE2-mediated leaf senescence signalling in Arabidopsis. J. Exp. Bot. 65:4023–36 [Google Scholar]
  72. Kim JH, Woo HR, Kim J, Lim PO, Lee IC. et al. 2009. Trifurcate feed-forward regulation of age-dependent cell death involving miR164 in Arabidopsis. Science 323:1053–57 [Google Scholar]
  73. Kim S-H, Kwon C, Lee J-H, Chung T. 2012. Genes for plant autophagy: functions and interactions. Mol. Cells 34:413–23 [Google Scholar]
  74. Klimešová J, Nobis MP, Herben T. 2015. Senescence, ageing and death of the whole plant: morphological prerequisites and constraints of plant immortality. New Phytol. 206:14–18 [Google Scholar]
  75. Ko S-S, Li M-J, Sun-Ben Ku M, Ho Y-C, Lin Y-J. et al. 2014. The bHLH142 transcription factor coordinates with TDR1 to modulate the expression of EAT1 and regulate pollen development in rice. Plant Cell 26:2486–504 [Google Scholar]
  76. Kobayashi H, Ikeda TM, Nagata K. 2013. Spatial and temporal progress of programmed cell death in the developing starchy endosperm of rice. Planta 237:1393–400 [Google Scholar]
  77. Koyama T. 2014. The roles of ethylene and transcription factors in the regulation of onset of leaf senescence. Front. Plant Sci. 5:650 [Google Scholar]
  78. Kumpf RP, Nowack MK. 2015. The root cap: a short story of life and death. J. Exp. Bot. 66:5651–62 [Google Scholar]
  79. Kuriyama H. 1999. Loss of tonoplast integrity programmed in tracheary element differentiation. Plant Physiol. 121:763–74 [Google Scholar]
  80. Lam E, Zhang Y. 2012. Regulating the reapers: activating metacaspases for programmed cell death. Trends Plant Sci. 17:487–94 [Google Scholar]
  81. Lers A, Sonego L, Green PJ, Burd S. 2006. Suppression of LX ribonuclease in tomato results in a delay of leaf senescence and abscission. Plant Physiol. 142:710–21 [Google Scholar]
  82. Leydon AR, Beale KM, Woroniecka K, Castner E, Chen J. et al. 2013. Three MYB transcription factors control pollen tube differentiation required for sperm release. Curr. Biol. 23:1209–14 [Google Scholar]
  83. Leydon AR, Tsukamoto T, Dunatunga D, Qin Y, Johnson MA, Palanivelu R. 2015. Pollen tube discharge completes the process of synergid degeneration that is initiated by pollen tube–synergid interaction in Arabidopsis. Plant Physiol. 169:485–96 [Google Scholar]
  84. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W. et al. 2011. PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol. 156:615–30 [Google Scholar]
  85. Li N, Zhang D-S, Liu H-S, Yin C-S, Li X-x. et al. 2006. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014 [Google Scholar]
  86. Liang Y, Tan Z-M, Zhu L, Niu Q-K, Zhou J-J. et al. 2013. MYB97, MYB101 and MYB120 function as male factors that control pollen tube–synergid interaction in Arabidopsis thaliana fertilization. PLOS Genet. 9:e1003933 [Google Scholar]
  87. Lin Z, Eaves DJ, Sanchez-Moran E, Franklin FCH, Franklin-Tong VE. 2015. The Papaver rhoeas S determinants confer self-incompatibility to Arabidopsis thaliana in planta. Science 350:684–87 [Google Scholar]
  88. Liu L, Fan X-D. 2013. Tapetum: regulation and role in sporopollenin biosynthesis in Arabidopsis. Plant Mol. Biol. 83:165–75 [Google Scholar]
  89. Lombardi L, Casani S, Ceccarelli N, Galleschi L, Picciarelli P, Lorenzi R. 2007. Programmed cell death of the nucellus during Sechium edule Sw. seed development is associated with activation of caspase-like proteases. J. Exp. Bot. 58:2949–58 [Google Scholar]
  90. Lombardi L, Ceccarelli N, Picciarelli P, Sorce C, Lorenzi R. 2010. Nitric oxide and hydrogen peroxide involvement during programmed cell death of Sechium edule nucellus. Physiol. Plant. 140:89–102 [Google Scholar]
  91. López-Fernández MP, Maldonado S. 2015. Programmed cell death in seeds of angiosperms. J. Integr. Plant Biol. 57:996–1002 [Google Scholar]
  92. Lord CEN, Dauphinee AN, Watts RL, Gunawardena AHLAN. 2013. Unveiling interactions among mitochondria, caspase-like proteases, and the actin cytoskeleton during plant programmed cell death (PCD). PLOS ONE 8:e57110 [Google Scholar]
  93. Lord CEN, Gunawardena AHLAN. 2012. Programmed cell death in C. elegans, mammals and plants. Eur. J. Cell Biol. 91:603–13 [Google Scholar]
  94. Maruyama D, Hamamura Y, Takeuchi H, Susaki D, Nishimaki M. et al. 2013. Independent control by each female gamete prevents the attraction of multiple pollen tubes. Dev. Cell 25:317–23 [Google Scholar]
  95. Maruyama D, Völz R, Takeuchi H, Mori T, Igawa T. et al. 2015. Rapid elimination of the persistent synergid through a cell fusion mechanism. Cell 161:907–18 [Google Scholar]
  96. Matallana-Ramirez LP, Rauf M, Farage-Barhom S, Dortay H, Xue G-P. et al. 2013. NAC transcription factor ORE1 and senescence-induced BIFUNCTIONAL NUCLEASE1 (BFN1) constitute a regulatory cascade in Arabidopsis. Mol. Plant 6:1432–52 [Google Scholar]
  97. Ménard D, Pesquet E. 2015. Cellular interactions during tracheary elements formation and function. Curr. Opin. Plant Biol. 23:109–15 [Google Scholar]
  98. Milhinhos A, Miguel CM. 2013. Hormone interactions in xylem development: a matter of signals. Plant Cell Rep. 32:867–83 [Google Scholar]
  99. Moll C, Von Lyncker L, Zimmermann S, Kägi C, Baumann N. et al. 2008. CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 56:913–21 [Google Scholar]
  100. Morris K, Linkies A, Müller K, Oracz K, Wang X. et al. 2011. Regulation of seed germination in the close Arabidopsis relative Lepidium sativum: a global tissue-specific transcript analysis. Plant Physiol. 155:1851–70 [Google Scholar]
  101. Muñiz L, Minguet EG, Singh SK, Pesquet E, Vera-Sirera F. et al. 2008. ACAULIS5 controls Arabidopsis xylem specification through the prevention of premature cell death. Development 135:2573–82 [Google Scholar]
  102. Munné-Bosch S. 2015. Senescence: Is it universal or not?. Trends Plant Sci. 20:713–20 [Google Scholar]
  103. Nakaune S, Yamada K, Kondo M, Kato T, Tabata S. 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]
  104. Nehme R, Conradt B. 2009. egl-1: a key activator of apoptotic cell death in C. elegans. Oncogene 27:S30–40 [Google Scholar]
  105. Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U. 2014. A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev. Cell 29:491–500 [Google Scholar]
  106. Niu N, Liang W, Yang X, Jin W, Wilson ZA. et al. 2013. EAT1 promotes tapetal cell death by regulating aspartic proteases during male reproductive development in rice. Nat. Commun. 4:1445 [Google Scholar]
  107. Nogueira FCS, Palmisano G, Soares EL, Shah M, Soares AA. et al. 2012. Proteomic profile of the nucellus of castor bean (Ricinus communis L.) seeds during development. J. Proteom. 75:1933–39 [Google Scholar]
  108. Noh Y-S, Amasino RM. 1999. Identification of a promoter region responsible for the senescence-specific expression of SAG12. Plant Mol. Biol. 41:181–94 [Google Scholar]
  109. Obara K, Kuriyama H, Fukuda H. 2001. Direct evidence of active and rapid nuclear degradation triggered by vacuole rupture during programmed cell death in Zinnia. Plant Physiol. 125:615–26 [Google Scholar]
  110. Olvera-Carrillo Y, Van Bel M, Van Hautegem T, Fendrych M, Huysmans M. et al. 2015. A conserved core of programmed cell death indicator genes discriminates developmentally and environmentally induced programmed cell death in plants. Plant Physiol. 169:2684–99 [Google Scholar]
  111. Pagnussat GC, Alandete-Saez M, Bowman JL, Sundaresan V. 2009. Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324:1684–89 [Google Scholar]
  112. Papini A, Mosti S, Milocani E, Tani G, Di Falco P, Brighigna L. 2011. Megasporogenesis and programmed cell death in Tillandsia (Bromeliaceae). Protoplasma 248:651–62 [Google Scholar]
  113. Pei H, Ma N, Chen J, Zheng Y, Tian J. et al. 2013. Integrative analysis of miRNA and mRNA profiles in response to ethylene in rose petals during flower opening. PLOS ONE 8:e64290 [Google Scholar]
  114. Petrov V, Hille J, Mueller-Roeber B, Gechev TS. 2015. ROS-mediated abiotic stress–induced programmed cell death in plants. Front. Plant Sci. 6:69 [Google Scholar]
  115. Phan HA, Iacuone S, Li SF, Parish RW. 2011. The MYB80 transcription factor is required for pollen development and the regulation of tapetal programmed cell death in Arabidopsis thaliana. Plant Cell 23:2209–24 [Google Scholar]
  116. Phan HA, Li SF, Parish RW. 2012. MYB80, a regulator of tapetal and pollen development, is functionally conserved in crops. Plant Mol. Biol. Rep. 78:171–83 [Google Scholar]
  117. Plackett ARG, Thomas SG, Wilson ZA, Hedden P. 2011. Gibberellin control of stamen development: a fertile field. Trends Plant Sci. 16:568–78 [Google Scholar]
  118. Putcha GV, Johnson EM Jr. 2004. ‘Men are but worms’: neuronal cell death in C. elegans and vertebrates. Cell Death Differ. 11:38–48 [Google Scholar]
  119. Qiao H, Shen Z, Huang S-sC, Schmitz RJ, Urich MA. et al. 2012. Processing and subcellular trafficking of ER-tethered EIN2 control response to ethylene gas. Science 338:390–93 [Google Scholar]
  120. Radchuk V, Borisjuk L, Radchuk R, Steinbiss H-H, Rolletschek H. et al. 2006. Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell 18:1652–66 [Google Scholar]
  121. Radchuk V, Weier D, Radchuk R, Weschke W, Weber H. 2011. Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J. Exp. Bot. 62:1217–27 [Google Scholar]
  122. Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K. et al. 2011. Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol. 190:351–68 [Google Scholar]
  123. Rantong G, Evans R, Gunawardena AHLAN. 2015. Lace plant ethylene receptors, AmERS1a and AmERS1c, regulate ethylene-induced programmed cell death during leaf morphogenesis. Plant Mol. Biol. 89:215–27 [Google Scholar]
  124. Rauf M, Arif M, Dortay H, Matallana-Ramírez LP, Waters MT. et al. 2013. ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription. EMBO Rep. 14:382–88 [Google Scholar]
  125. Roberts IN, Caputo C, Criado MV, Funk C. 2012. Senescence-associated proteases in plants. Physiol. Plant. 145:130–39 [Google Scholar]
  126. Rogers HJ. 2013. From models to ornamentals: How is flower senescence regulated?. Plant Mol. Biol. Rep. 82:563–74 [Google Scholar]
  127. Sabelli PA, Liu Y, Dante RA, Lizarraga LE, Nguyen HN. et al. 2013. Control of cell proliferation, endoreduplication, cell size, and cell death by the retinoblastoma-related pathway in maize endosperm. PNAS 110:E1827–36 [Google Scholar]
  128. Savitskaya MA, Onishchenko GE. 2015. Mechanisms of apoptosis. Biochemistry 80:1393–417 [Google Scholar]
  129. Schiøtt M, Romanowsky SM, Bækgaard L, Jakobsen MK, Palmgren MG, Harper JF. 2004. A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. PNAS 101:9502–7 [Google Scholar]
  130. Schippers JHM. 2015. Transcriptional networks in leaf senescence. Curr. Opin. Plant Biol. 27:77–83 [Google Scholar]
  131. Senatore A, Trobacher CP, Greenwood JS. 2009. Ricinosomes predict programmed cell death leading to anther dehiscence in tomato. Plant Physiol. 149:775–90 [Google Scholar]
  132. Shahri W, Tahir I. 2014. Flower senescence: some molecular aspects. Planta 239:277–97 [Google Scholar]
  133. Shibuya K, Niki T, Ichimura K. 2013. Pollination induces autophagy in petunia petals via ethylene. J. Exp. Bot. 64:1111–20 [Google Scholar]
  134. Shibuya K, Shimizu K, Niki T, Ichimura K. 2014. Identification of a NAC transcription factor, EPHEMERAL1, that controls petal senescence in Japanese morning glory. Plant J. 79:1044–51 [Google Scholar]
  135. Smertenko A, Bozhkov PV. 2014. Somatic embryogenesis: life and death processes during apical-basal patterning. J. Exp. Bot. 65:1343–60 [Google Scholar]
  136. Song X, Yuan L, Sundaresan V. 2014. Antipodal cells persist through fertilization in the female gametophyte of Arabidopsis. Plant Reprod. 27:197–203 [Google Scholar]
  137. Sorensen A-M, Kröber S, Unte US, Huijser P, Dekker K, Saedler H. 2003. The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J. 33:413–23 [Google Scholar]
  138. Sundström JF, Vaculova A, Smertenko AP, Savenkov EI, Golovko A. 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]
  139. Takahashi H, Yamauchi T, Colmer TD, Nakazono M. 2014. Aerenchyma formation in plants. Plant Cell Monogr. 21:247–65 [Google Scholar]
  140. Takahashi H, Yamauchi T, Rajhi I, Nishizawa NK, Nakazono M. 2015. Transcript profiles in cortical cells of maize primary root during ethylene-induced lysigenous aerenchyma formation under aerobic conditions. Ann. Bot. 115:879–94 [Google Scholar]
  141. Tata JR. 1966. Requirement for RNA and protein synthesis for induced regression of the tadpole tail in organ culture. Dev. Biol. 13:77–94 [Google Scholar]
  142. Thongkum M, Burns P, Bhunchoth A, Warin N, Chatchawankanphanich O, van Doorn WG. 2015. Ethylene and pollination decrease transcript abundance of an ethylene receptor gene in Dendrobium petals. J. Plant Physiol. 176:96–100 [Google Scholar]
  143. Trobacher CP, Senatore A, Holley C, Greenwood JS. 2013. Induction of a ricinosomal-protease and programmed cell death in tomato endosperm by gibberellic acid. Planta 237:665–79 [Google Scholar]
  144. Tsiatsiani L, Timmerman E, De Bock P-J, Vercammen D, Stael S. et al. 2013. The Arabidopsis metacaspase9 degradome. Plant Cell 25:2831–47 [Google Scholar]
  145. Tsuji H, Aya K, Ueguchi-Tanaka M, Shimada Y, Nakazono M. et al. 2006. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. Plant J. 47:427–44 [Google Scholar]
  146. Van Durme M, Nowack MK. 2016. Mechanisms of developmentally controlled cell death in plants. Curr. Opin. Plant Biol. 29:29–37 [Google Scholar]
  147. Van Hautegem T, Waters AJ, Goodrich J, Nowack MK. 2015. Only in dying, life: programmed cell death during plant development. Trends Plant Sci. 20:102–13 [Google Scholar]
  148. Vanden Berghe T, Linkermann A, Jouan-Lanhouet S, Walczak H, Vandenabeele P. 2014. Regulated necrosis: the expanding network of non-apoptotic cell death pathways. Nat. Rev. Mol. Cell Biol. 15:135–47 [Google Scholar]
  149. Vera-Sirera F, Minguet EG, Singh SK, Ljung K, Tuominen H. et al. 2010. Role of polyamines in plant vascular development. Plant Physiol. Biochem. 48:534–39 [Google Scholar]
  150. Vizcay-Barrena G, Wilson ZA. 2006. Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J. Exp. Bot. 57:2709–17 [Google Scholar]
  151. Vogelmann K, Drechsel G, Bergler J, Subert C, Philippar K. et al. 2012. Early senescence and cell death in Arabidopsis saul1 mutants involves the PAD4-dependent salicylic acid pathway. Plant Physiol. 159:1477–87 [Google Scholar]
  152. Wagstaff C, Yang TJW, Stead AD, Buchanan-Wollaston V, Roberts JA. 2009. A molecular and structural characterization of senescing Arabidopsis siliques and comparison of transcriptional profiles with senescing petals and leaves. Plant J. 57:690–705 [Google Scholar]
  153. Wang H, Wu H-M, Cheung AY. 1996. Pollination induces mRNA poly(A) tail-shortening and cell deterioration in flower transmitting tissue. Plant J. 9:715–27 [Google Scholar]
  154. Wilkins KA, Bosch M, Haque T, Teng N, Poulter NS, Franklin-Tong VE. 2015. Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol. Plant Physiol. 167:766–79 [Google Scholar]
  155. Wilkins KA, Poulter NS, Franklin-Tong VE. 2014. Taking one for the team: self-recognition and cell suicide in pollen. J. Exp. Bot. 65:1331–42 [Google Scholar]
  156. Willemse MTM. 1981. Polarity during megasporogenesis and megagametogenesis. Phytomorphology 31:125–35 [Google Scholar]
  157. Wilson ZA, Song J, Taylor B, Yang C. 2011. The final split: the regulation of anther dehiscence. J. Exp. Bot. 62:1633–49 [Google Scholar]
  158. Woriedh M, Wolf S, Márton ML, Hinze A, Gahrtz M. et al. 2013. External application of gametophyte-specific ZmPMEI1 induces pollen tube burst in maize. Plant Reprod. 26:255–66 [Google Scholar]
  159. Wu L, Chen H, Curtis C, Fu ZQ. 2014. Go in for the kill: how plants deploy effector-triggered immunity to combat pathogens. Virulence 5:710–21 [Google Scholar]
  160. Wu X, Knapp S, Stamp A, Stammers DK, Jörnvall H. et al. 2007. Biochemical characterization of TASSELSEED 2, an essential plant short-chain dehydrogenase/reductase with broad spectrum activities. FEBS J. 274:1172–82 [Google Scholar]
  161. Xie H-T, Wan Z-Y, Li S, Zhang Y. 2014. Spatiotemporal production of reactive oxygen species by NADPH oxidase is critical for tapetal programmed cell death and pollen development in Arabidopsis. Plant Cell 26:2007–23 [Google Scholar]
  162. Xing Q, Creff A, Waters A, Tanaka H, Goodrich J, Ingram GC. 2013. ZHOUPI controls embryonic cuticle formation via a signalling pathway involving the subtilisin protease ABNORMAL LEAF-SHAPE1 and the receptor kinases GASSHO1 and GASSHO2. Development 140:770–79 [Google Scholar]
  163. Xu B, Ohtani M, Yamaguchi M, Toyooka K, Wakazaki M. et al. 2014. Contribution of NAC transcription factors to plant adaptation to land. Science 343:1505–8 [Google Scholar]
  164. Xu Y, Hanson MR. 2000. Programmed cell death during pollination-induced petal senescence in petunia. Plant Physiol. 122:1323–33 [Google Scholar]
  165. Xu Y, Iacuone S, Li SF, Parish RW. 2014. MYB80 homologues in Arabidopsis, cotton and Brassica: regulation and functional conservation in tapetal and pollen development. BMC Plant Biol. 14:278 [Google Scholar]
  166. Xuan W, Band LR, Kumpf RP, Van Damme D, Parizot B. et al. 2016. Cyclic programmed cell death stimulates hormone signaling and root development in Arabidopsis. Science 351:384–87 [Google Scholar]
  167. Yamada T, Ichimura K, Kanekatsu M, van Doorn WG. 2009. Homologs of genes associated with programmed cell death in animal cells are differentially expressed during senescence of Ipomoea nil petals. Plant Cell Physiol. 50:610–25 [Google Scholar]
  168. Yamaguchi M, Goué N, Igarashi H, Ohtani M, Nakano Y. et al. 2010. VASCULAR-RELATED NAC-DOMAIN6 and VASCULAR-RELATED NAC-DOMAIN7 effectively induce transdifferentiation into xylem vessel elements under control of an induction system. Plant Physiol. 153:906–14 [Google Scholar]
  169. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T. 2011. VASCULAR-RELATED NAC-DOMAIN 7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J. 66:579–90 [Google Scholar]
  170. Yang W-C, Sundaresan V. 2000. Genetics of gametophyte biogenesis in Arabidopsis. Curr. Opin. Plant Biol. 3:53–57 [Google Scholar]
  171. Yin L-L, Xue H-W. 2012. The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–65 [Google Scholar]
  172. Yoo Y-H, Choi H-K, Jung K-H. 2015. Genome-wide identification and analysis of genes associated with lysigenous aerenchyma formation in rice roots. J. Plant Biol. 58:117–27 [Google Scholar]
  173. Young TE, Gallie DR. 2000. Programmed cell death during endosperm development. Plant Mol. Biol. 44:283–301 [Google Scholar]
  174. Young TE, Gallie DR, DeMason DA. 1997. Ethylene-mediated programmed cell death during maize endosperm development of wild-type and shrunken2 genotypes. Plant Physiol. 115:737–51 [Google Scholar]
  175. Yu X-H, Perdue TD, Heimer YM, Jones AM. 2002. Mitochondrial involvement in tracheary element programmed cell death. Cell Death Differ. 9:189–98 [Google Scholar]
  176. Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D. 2010. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol. 154:149–62 [Google Scholar]
  177. Zhang D, Liu D, Lv X, Wang Y, Xun Z. et al. 2014. The cysteine protease CEP1, a key executor involved in tapetal programmed cell death, regulates pollen development in Arabidopsis. Plant Cell 26:2939–61 [Google Scholar]
  178. Zhao C, Avci U, Grant EH, Haigler CH, Beers EP. 2008. XND1, a member of the NAC domain family in Arabidopsis thaliana, negatively regulates lignocellulose synthesis and programmed cell death in xylem. Plant J. 53:425–36 [Google Scholar]
  179. Zhao P, Zhou X-M, Zhang L-Y, Wang W, Ma L-g. et al. 2013. A bipartite molecular module controls cell death activation in the basal cell lineage of plant embryos. PLOS Biol. 11:e1001655 [Google Scholar]
  180. Zhong R, Lee C, Ye Z-H. 2010. Global analysis of direct targets of secondary wall NAC master switches in Arabidopsis. Mol. Plant Breed. 3:1087–103 [Google Scholar]
  181. Zhu J, Chen H, Li H, Gao J-F, Jiang H. et al. 2008. Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55:266–77 [Google Scholar]
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