title: Self-incompatibility-induced programmed cell death in field poppy pollen involves dramatic acidification of the incompatible pollen tube cytosol.
abstract: Self-incompatibility (SI) is an important genetically controlled mechanism to prevent inbreeding in higher plants. SI involves highly specific interactions during pollination, resulting in the rejection of incompatible (self) pollen. Programmed cell death (PCD) is an important mechanism for destroying cells in a precisely regulated manner. SI in field poppy (Papaver rhoeas) triggers PCD in incompatible pollen. During SI-induced PCD, we previously observed a major acidification of the pollen cytosol. Here, we present measurements of temporal alterations in cytosolic pH ([pH]cyt); they were surprisingly rapid, reaching pH 6.4 within 10 min of SI induction and stabilizing by 60 min at pH 5.5. By manipulating the [pH]cyt of the pollen tubes in vivo, we show that [pH]cyt acidification is an integral and essential event for SI-induced PCD. Here, we provide evidence showing the physiological relevance of the cytosolic acidification and identify key targets of this major physiological alteration. A small drop in [pH]cyt inhibits the activity of a soluble inorganic pyrophosphatase required for pollen tube growth. We also show that [pH]cyt acidification is necessary and sufficient for triggering several key hallmark features of the SI PCD signaling pathway, notably activation of a DEVDase/caspase-3-like activity and formation of SI-induced punctate actin foci. Importantly, the actin binding proteins Cyclase-Associated Protein and Actin-Depolymerizing Factor are identified as key downstream targets. Thus, we have shown the biological relevance of an extreme but physiologically relevant alteration in [pH]cyt and its effect on several components in the context of SI-induced events and PCD.
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
authors: Katie A
authors: KA
authors: Wilkins
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
authors: Maurice
authors: M
authors: Bosch
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
authors: Tamanna
authors: T
authors: Haque
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
authors: Nianjun
authors: N
authors: Teng
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom.
authors: Natalie S
authors: NS
authors: Poulter
authors: School of Biosciences, University of Birmingham, Edgbaston, Birmingham B15 2TT, United Kingdom V.E.Franklin-Tong@bham.ac.uk.
authors: Vernonica E
authors: VE
authors: Franklin-Tong
mesh_terms: D000199:Actins / Q000378:metabolism; D017209:Apoptosis / Q000187:drug effects*; D000001:Calcimycin / Q000494:pharmacology; D002118:Calcium / Q000494:pharmacology; D053148:Caspase 3 / Q000378:metabolism; D003600:Cytosol / Q000187:drug effects / Q000378:metabolism*; D006863:Hydrogen-Ion Concentration; D043564:Inorganic Pyrophosphatase / Q000378:metabolism; D007476:Ionophores / Q000494:pharmacology; D010207:Papaver / Q000166:cytology* / Q000378:metabolism; D010447:Peptide Hydrolases / Q000378:metabolism; D010940:Plant Proteins / Q000378:metabolism; D053205:Pollen Tube / Q000166:cytology* / Q000187:drug effects; D011422:Propionates / Q000494:pharmacology*; D060436:Self-Incompatibility in Flowering Plants / Q000187:drug effects*; D012995:Solubility; D014617:Vacuoles / Q000187:drug effects / Q000378:metabolism
chemical_list: D000199:Actins; D007476:Ionophores; D010940:Plant Proteins; D011422:Propionates; D000001:Calcimycin; D010447:Peptide Hydrolases; D053148:Caspase 3; C108711:DEVDase; D043564:Inorganic Pyrophosphatase; C029658:propionic acid; D002118:Calcium
references: Plant Physiol. 2001 Feb;125(2):615-26
references: 11161019
references: J Cell Biochem. 2003 Apr 1;88(5):1066-76
references: 12616543
references: Proc Natl Acad Sci U S A. 1994 Mar 15;91(6):2265-9
references: 8134385
references: Plant Physiol. 2008 Mar;146(3):1358-67
references: 18192439
references: Proc Natl Acad Sci U S A. 2007 Nov 13;104(46):18327-32
references: 17989229
references: Cell Death Differ. 2011 Aug;18(8):1241-6
references: 21494263
references: J Exp Bot. 2011 Oct;62(14):4749-61
references: 21778180
references: Cell Death Differ. 2004 Feb;11(2):175-82
references: 14576770
references: Nature. 2004 May 20;429(6989):305-9
references: 15152254
references: Trends Cell Biol. 1993 Oct;3(10):340-5
references: 14731903
references: J Exp Bot. 2003 Jan;54(380):141-8
references: 12456764
references: Plant Cell. 2001 Apr;13(4):907-21
references: 11283344
references: J Cell Sci. 2013 Aug 1;126(Pt 15):3249-58
references: 23908377
references: Plant Cell. 2002 Nov;14(11):2915-27
references: 12417710
references: Mol Biol Cell. 2006 Nov;17(11):4645-55
references: 16914523
references: Plant Physiol. 2007 Sep;145(1):236-45
references: 17660353
references: Mol Plant. 2008 Nov;1(6):879-87
references: 19825589
references: Biochemistry. 1993 Sep 28;32(38):9994-10004
references: 8399168
references: FEBS Lett. 2003 Jul 17;547(1-3):223-7
references: 12860418
references: Plant Physiol. 1999 Dec;121(4):1291-8
references: 10594116
references: Nature. 2006 Nov 23;444(7118):490-3
references: 17086195
references: Genome Biol. 2002;3(5):reviews3007
references: 12049672
references: J Cell Sci. 1997 Aug;110 ( Pt 15):1729-40
references: 9264460
references: Plant Cell. 1996 Apr;8(4):713-724
references: 12239397
references: J Cell Biol. 1997 Mar 24;136(6):1307-22
references: 9087445
references: Plant Cell. 2006 Sep;18(9):2182-93
references: 16920777
references: Plant Physiol. 2005 Mar;137(3):841-7
references: 15761210
references: Curr Biol. 2004 Nov 9;14(21):1897-906
references: 15530390
references: Plant Cell. 2002 Oct;14(10):2613-26
references: 12368508
references: Trends Cell Biol. 1999 Sep;9(9):364-70
references: 10461190
references: Plant Physiol. 2004 Mar;134(3):1227-39
references: 14988481
references: J Biol Chem. 2012 Oct 12;287(42):35722-32
references: 22904322
references: Curr Opin Plant Biol. 2005 Aug;8(4):404-8
references: 15939660
references: Trends Plant Sci. 2005 Mar;10(3):117-22
references: 15749469
references: Plant Cell Physiol. 2007 Oct;48(10):1414-25
references: 17704529
references: J Cell Sci. 2007 Aug 1;120(Pt 15):2609-18
references: 17635992
references: Plant Cell. 2004 Apr;16(4):857-73
references: 15020745
references: Mol Biol Cell. 2007 Aug;18(8):3002-14
references: 17538023
references: Ann Bot. 2011 Sep;108(4):659-75
references: 21320881
references: Plant Physiol. 1989 Jul;90(3):1102-7
references: 16666858
references: Mol Plant. 2013 Sep;6(5):1419-37
references: 23702593
references: Bioarchitecture. 2012 May 1;2(3):75-87
references: 22880146
references: Biochemistry. 1993 Sep 28;32(38):9985-93
references: 8399167
references: Curr Biol. 1998 Oct 8;8(20):1129-32
references: 9778530
references: J Exp Bot. 2010 Apr;61(7):2015-25
references: 20097844
references: J Biol Chem. 1985 Nov 25;260(27):14410-2
references: 4055781
references: Plant Mol Biol. 2000 Oct;44(3):245-53
references: 11199386
references: Plant Cell. 2002 Sep;14(9):2175-90
references: 12215514
references: J Biol Chem. 2004 Jan 2;279(1):779-87
references: 14573611
references: Science. 1994 Mar 11;263(5152):1419-21
references: 17776513
references: Cell Death Differ. 2011 Aug;18(8):1263-70
references: 21566662
references: Plant Physiol. 2010 Mar;152(3):1274-83
references: 20081043
references: Trends Cell Biol. 2002 Dec;12(12):598-605
references: 12495849
references: Proc Natl Acad Sci U S A. 1986 Dec;83(23):8992-5
references: 16593782
references: Mol Biol Cell. 1997 Feb;8(2):367-85
references: 9190214
references: J Cell Sci. 1997 May;110 ( Pt 10):1187-98
references: 9191043
references: Plant Physiol. 2001 Jan;125(1):94-7
references: 11154305
references: J Exp Bot. 2014 Mar;65(5):1331-42
references: 24449385
references: J Cell Biol. 1999 Feb 8;144(3):483-96
references: 9971743
references: Mol Biol Cell. 2005 May;16(5):2275-84
references: 15728723
references: J Cell Biol. 2004 Mar 15;164(6):803-9
references: 15024029
references: J Cell Sci. 2008 Sep 1;121(Pt 17):2913-20
references: 18716285
references: Science. 2004 Aug 6;305(5685):855-8
references: 15297671
references: Plant Physiol. 2011 May;156(1):404-16
references: 21386034
references: Plant Physiol. 1998 Oct;118(2):349-64
references: 9765521
references: Plant Methods. 2010 Nov 30;6:27
references: 21118545
references: J Cell Biol. 2006 Jul 17;174(2):221-9
references: 16831890
references: Development. 1998 Aug;125(15):2925-34
references: 9655814
references: FEBS Lett. 2000 Jun 16;475(2):139-44
references: 10858505
references: Curr Biol. 2014 May 5;24(9):931-40
references: 24726156
references: Cell Mol Life Sci. 1999 Feb;55(2):214-32
references: 24481914
references: Plant Physiol. 2011 Feb;155(2):963-73
references: 21177472
references: Plant Cell. 2002 Jan;14(1):149-63
references: 11826305
references: Biochem J. 2008 Aug 1;413(3):389-404
references: 18613816
references: Bioessays. 2001 Jan;23(1):86-94
references: 11135313
references: Plant Physiol. 2009 Jun;150(2):815-24
references: 19346440
references: Cell Death Differ. 2011 Aug;18(8):1298-304
references: 21637288
references: Plant Physiol. 2001 Sep;127(1):119-30
references: 11553740
references: J Exp Bot. 2010 Apr;61(7):1969-86
references: 20159884