Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen

Thomas, Steven G.; Huang, Shanjin; Li, Shutian; Staiger, Christopher J.; Franklin‐Tong, Vernonica E.

doi:10.1083/jcb.200604011

Cited by 139 publications

(149 citation statements)

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“…If ataxin-2 is overexpressed in yeast it causes premature cell death due to defects in actin filament formation (Satterfield et al 2002). Actin depolymerisation has been shown to be an adequate cause of cell death in pollen tubes (Thomas et al 2006), suggesting that the relation between cell death and lack of actin structure is also present in angiosperms. It is not clear if the presently observed induction of ataxin-2 in Ipomoea petals is also an essential part of the process leading to cell death.…”

Section: Appearance Of Senescence Parameters Compared With Gene Exprementioning

confidence: 99%

Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers

et al. 2007

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We isolated several senescence-associated genes (SAGs) from the petals of morning glory (Ipomoea nil) flowers, with the aim of furthering our understanding of programmed cell death. Samples were taken from the closed bud stage to advanced visible senescence. Actinomycin D, an inhibitor of transcription, if given prior to 4 h after opening, suppressed the onset of visible senescence, which occurred at about 9 h after flower opening. The isolated genes all showed upregulation. Two cell-wall related genes were upregulated early, one encoding an extensin and one a caffeoyl-CoA-3-O-methyltransferase, involved in lignin production. A pectinacetylesterase was upregulated after flower opening and might be involved in cell-wall degradation. Some identified genes showed high homology with published SAGs possibly involved in remobilisation processes: an alcohol dehydrogenase and three cysteine proteases. One transcript encoded a leucine-rich repeat receptor protein kinase, putatively involved in signal transduction. Another transcript encoded a 14-3-3 protein, also a protein kinase. Two genes have apparently not been associated previously with senescence: the first encoded a putative SEC14, which is required for Golgi vesicle transport, the second was a putative ataxin-2, which has been related to RNA metabolism. Induction of the latter has been shown to result in cell death in yeast, due to defects in actin filament formation. The possible roles of these genes in programmed cell death are discussed.

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Section: Appearance Of Senescence Parameters Compared With Gene Exprementioning

confidence: 99%

Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers

et al. 2007

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“…SI activates PCD specifically in incompatible pollen, thereby preventing self-fertilization. Recent investigations revealed that alterations in actin dynamics can push pollen tubes into PCD (Thomas et al, 2006), and an SI-activated mitogen-activated protein kinase (Rudd et al, 1996) is implicated in signaling to PCD . These data suggest that in Papaver, these components contribute to an integrated SI signaling network to achieve inhibition and death of incompatible pollen.…”

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confidence: 99%

Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen

2008

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Perception and integration of signals into responses is of crucial importance to cells. Both the actin and microtubule cytoskeleton are known to play a role in mediating diverse stimulus responses. Self-incompatibility (SI) is an important mechanism to prevent self-fertilization. SI in Papaver rhoeas triggers a Ca 21 -dependent signaling network to trigger programmed cell death (PCD), providing a neat way to inhibit and destroy incompatible pollen. We previously established that SI stimulates F-actin depolymerization and that altering actin dynamics can push pollen tubes into PCD. Very little is known about the role of microtubules in pollen tubes. Here, we investigated whether the pollen tube microtubule cytoskeleton is a target for the SI signals. We show that SI triggers very rapid apparent depolymerization of cortical microtubules, which, unlike actin, does not reorganize later. Actin depolymerization can trigger microtubule depolymerization but not vice versa. Moreover, although disruption of microtubule dynamics alone does not trigger PCD, alleviation of SI-induced PCD by taxol implicates a role for microtubule depolymerization in mediating PCD. Together, our data provide good evidence that SI signals target the microtubule cytoskeleton and suggest that signal integration between microfilaments and microtubules is required for triggering of PCD.

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“…This fi nding suggested that disturbance of actin polymer dynamics could trigger PCD in pollen. Data implicated actin depolymerization being functionally involved in the initiation of SI-induced PCD and established a causal link between actin polymerization status and initiation of PCD in plant cells (Thomas et al 2006 ). Thus, the rapid and substantial actin depolymerization triggered by SI signaling not only results in the rapid inhibition of incompatible pollen tip growth, but it also activates a caspase-3-like/ DEVDase activity, triggering PCD (see Fig.…”

Section: Involvement Of Actin Signaling In Si-mediated Pcdmentioning

confidence: 99%

“…Both actin and microtubule alterations are implicated in mediating PCD (Thomas et al 2006 ;Poulter et al 2008 ). A number of studies have shown that either actin depolymerization or stabilization can infl uence whether a eukaryotic cell enters into an apoptotic pathway; see (Franklin-Tong and Gourlay 2008 ;Smertenko and Franklin-Tong 2011 ).…”

Section: Involvement Of Actin Signaling In Si-mediated Pcdmentioning

confidence: 99%

“…Investigations examining the effect of the actin-depolymerizing drug, latrunculin B (LatB), and the actin-stabilizing/polymerizing drug, jasplakinolide (Jasp), in Papaver pollen revealed that both treatments stimulated high levels of DNA fragmentation, which was mediated by a caspase-3 like/DEVDase activity (Thomas et al 2006 ). This fi nding suggested that disturbance of actin polymer dynamics could trigger PCD in pollen.…”

Section: Involvement Of Actin Signaling In Si-mediated Pcdmentioning

confidence: 99%

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Papaver rhoeas S-Determinants and the Signaling Networks They Trigger

Franklin‐Tong

2014

Sexual Reproduction in Animals and Plants

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Higher plants use specifi c interactions between pollen and pistil to achieve pollination. Self-incompatibility (SI) is an important mechanism used by many species to prevent inbreeding. It is controlled by a multi-allelic S locus. "Self" (incompatible) pollen is discriminated from "non-self" (compatible) pollen by interaction of pollen and pistil S locus components and is subsequently inhibited. Our studies of the SI system in Papaver rhoeas have revealed that the pistil S locus protein, PrsS, is a small novel secreted protein that interacts with the pollen S locus protein, PrpS, which is a small novel transmembrane protein. This interaction of PrsS with incompatible pollen induces a SI response, involving a Ca 2+ -dependent signaling network, resulting in pollen inhibition and programmed cell death; this provides a neat way to destroy "self"-pollen. Several SI-induced events have been identifi ed, including Ca 2+ and K + infl ux, increases in cytosolic free Ca 2+ , activation of a MAP kinase, alterations to the cytoskeleton, and phosphorylation of a soluble inorganic pyrophosphatase. Here we present an overview of our knowledge of the novel cell-cell recognition S -determinants and the signals, targets, and mechanisms triggered by an incompatible interaction. We hope this review is of interest to those involved in the origins and evolution of cell-cell recognition systems involved in discrimination between "self" and "non-self," which include histocompatibility systems in primitive chordates and vertebrates as well as plant self-incompatibility.

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Actin depolymerization is sufficient to induce programmed cell death in self-incompatible pollen

Cited by 139 publications

References 50 publications

Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers

Gene expression in opening and senescing petals of morning glory (Ipomoea nil) flowers

Microtubules Are a Target for Self-Incompatibility Signaling in Papaver Pollen

Papaver rhoeas S-Determinants and the Signaling Networks They Trigger

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