A conserved core of PCD indicator genes discriminates developmentally and environmentally induced programmed cell death in plants

Olvera-Carrillo, Yadira; Bel, Michiel Van; Hautegem, Tom Van; Fendrych, Matyáš; Huysmans, Marlies; Šimášková, Mária; Durme, Matthias Van; Buscaill, Pierre; Rivas, Susana; Coll, Núria S.; Coppens, Frederik; Maere, Steven; Nowack, Moritz K.

doi:10.1104/pp.15.00769

Cited by 124 publications

(199 citation statements)

References 62 publications

(79 reference statements)

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“…To identify cell death markers with relative specificity for the endosperm, we therefore interrogated available in silico resources and the literature. We identified two genes expressed prior to cell death in the lateral root cap as potentially useful pre-cell death markers in endosperm: PASPA3 and BFN1 (Olvera-Carrillo et al, 2015;Fendrych et al, 2014). In silico expression profiles (Le et al, 2010;Winter et al, 2007) for these genes are shown in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…Although in animals, the molecular control of dPCD pathways is well characterised and relatively conserved (recently reviewed by Suzanne and Steller, 2013), almost every reported instance of plant dPCD seems to involve unique molecular players, with the triggers of plant dPCD being particularly diverse (recently reviewed by Van Hautegem et al, 2015). Interestingly, however, a conserved set of indicator genes expressed prior to multiple plant dPCD processes has recently been defined (Olvera-Carrillo et al, 2015). These include the aspartate protease-encoding PASPA3 gene, which has no known function, but is a very early marker of cells destined for dPCD, and the bifunctional nuclease-encoding BFN1 gene, expression of which has been shown to pave the way for nuclear corpse clearance during lateral root cap cell death (Fendrych et al, 2014;Van Durme and Nowack, 2016).…”

Section: Introductionmentioning

confidence: 99%

“…The genetically controlled elimination of unwanted cells is a common occurrence during both animal and plant development. The term developmental programmed cell death (dPCD) has been used to describe such processes (Olvera-Carrillo et al, 2015). Although in animals, the molecular control of dPCD pathways is well characterised and relatively conserved (recently reviewed by Suzanne and Steller, 2013), almost every reported instance of plant dPCD seems to involve unique molecular players, with the triggers of plant dPCD being particularly diverse (recently reviewed by Van Hautegem et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds

et al. 2016

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Seed development in angiosperms demands the tightly coordinated development of three genetically distinct structures. The embryo is surrounded by the endosperm, which is in turn enclosed within the maternally derived seed coat. In Arabidopsis, final seed size is determined by early expansion of the coenocytic endosperm, which then cellularises and subsequently undergoes developmental programmed cell death, breaking down as the embryo grows. Endosperm breakdown requires the endospermspecific basic helix-loop-helix transcription factor ZHOUPI. However, to date, the mechanism underlying the Arabidopsis endosperm breakdown process has not been elucidated. Here, we provide evidence that ZHOUPI does not induce the developmental programmed cell death of the endosperm directly. Instead ZHOUPI indirectly triggers cell death by regulating the expression of cell wall-modifying enzymes, thus altering the physical properties of the endosperm to condition a mechanical environment permitting the compression of the cellularised endosperm by the developing embryo.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds

et al. 2016

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“…Distinct from animals, most mutant plants with single-gene mutations of conserved PCD components are viable, indicating the regulations of plant PCD are usually quantitative or are regulated in response to both developmental cues and environmental signals (Bozhkov and Lam, 2011). Recently, promoter-reporter lines, including PASPA3, RNS3, SCPL48, CEP1, and DMP4, have been successfully generated for visualizing cells ready for developmentally regulated PCD, which will largely facilitate the temporal and spatial observation of plant PCD process during development (Olvera-Carrillo et al, 2015). However, the underlying cellular mechanisms in regulating tapetal PCD remain elusive.…”

Section: Discussionmentioning

confidence: 99%

MONENSIN SENSITIVITY1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-Mediated Rab7 Activation Regulates Tapetal Programmed Cell Death and Pollen Development

et al. 2016

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Programmed cell death (PCD)-triggered degradation of plant tapetum is essential for microspore development and pollen coat formation; however, little is known about the cellular mechanism regulating tapetal PCD. Here, we demonstrate that Rab7-mediated vacuolar transport of tapetum degradation-related cysteine proteases is crucial for tapetal PCD and pollen development in Arabidopsis (Arabidopsis thaliana), with the following evidence: (1) The monensin sensitivity1 (mon1) mutants, which are defective in Rab7 activation, showed impaired male fertility due to a combined defect in both tapetum and male gametophyte development. (2) In anthers, MON1 showed preferential high level expression in tapetal cell layers and pollen. (3) The mon1 mutants exhibited delayed tapetum degeneration and tapetal PCD, resulting in abnormal pollen coat formation and decreased male fertility. (4) MON1/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-mediated Rab7 activation was indispensable for vacuolar trafficking of tapetum degradation-related cysteine proteases, supporting that PCD-triggered tapetum degeneration requires Rab7-mediated vacuolar trafficking of these cysteine proteases. (5) MON1 mutations also resulted in defective pollen germination and tube growth. Taken together, tapetal PCD and pollen development require successful MON1/CCZ1-mediated vacuolar transport in Arabidopsis.

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“…The LeLX gene that encodes RNase LX is an orthologue of Arabidopsis RNS3 , which was recently linked to developmental PCD (Olvera‐Carrillo et al . 2015). LeLX expression has been detected at the distal side of the mature tomato leaf petiole abscission zone, where the RNase LX protein is localised and where prominent ultrastructural hallmarks of PCD have been observed (Bar‐Dror et al .…”

Section: Introductionmentioning

confidence: 99%

The pattern of 1‐aminocyclopropane‐1‐carboxylate oxidase induction in the tomato leaf petiole abscission zone is independent of expression of the ribonuclease‐LX‐encoding LeLX gene

et al. 2018

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The abscission of tomato leaves occurs in the petiole abscission zone, and its late stage includes two spatially divided processes: cell separation and programmed cell death (PCD). Both of these processes are regulated by ethylene. The last step in ethylene biosynthesis is conversion of 1‐aminocyclopropane‐1‐carboxylic acid to ethylene, which is catalysed by the enzyme 1‐aminocyclopropane‐1‐carboxylate oxidase (ACO); however, the location of ACO in the leaf petiole abscission zone is not known. The tomato gene LeLX encodes ribonuclease LX, which is a marker for PCD and is induced by ethylene during abscission, but its association with ACO has not been explored.In a tomato transgenic line 1‐7 with inhibited expression of LeLX showing delayed leaf abscission, the morphology and ultrastructure of the leaf petiole abscission zone was examined. In this zone of the cv.’VF36’ and of a transgenic line 1‐7, spatiotemporal differences in expression of LeACO1 and LeACO4 were analysed and ACO protein was detected immunohistochemically.In comparison to wild‐type plants, there were no obvious morphological and ultrastructural features in the abscission zone of plants of a transgenic line 1‐7 before and after abscission induction. LeACO1 expression was low before abscission induction, and increased 24 h after induction, although with no apparent spatial pattern. In contrast, LeACO4 was expressed before abscission induction, and its transcript level declined 24 h after induction on the distal side of the abscission zone fracture. In the LeLX‐inhibited transgenic line, there were no significant differences in LeACO1 and LeACO4 expression in the petiole abscission zone, in comparison to wild‐type plants. In addition, the ACO protein was immunolocalised to the vascular tissues that traverse the petiole abscission zone in plants of wild type and of a transgenic line 1‐7; and additionally in the plane of future abscission zone fracture of transgenic‐line plants.The results suggest temporal differential expression of the LeACO genes in tomato leaf petioles and vascular localisation of ACO1 protein. Additionally, the results indicate that expression of LeACO genes is not affected by suppression of the LeLX expression.

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A conserved core of PCD indicator genes discriminates developmentally and environmentally induced programmed cell death in plants

Cited by 124 publications

References 62 publications

Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds

Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds

MONENSIN SENSITIVITY1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-Mediated Rab7 Activation Regulates Tapetal Programmed Cell Death and Pollen Development

The pattern of 1‐aminocyclopropane‐1‐carboxylate oxidase induction in the tomato leaf petiole abscission zone is independent of expression of the ribonuclease‐LX‐encoding LeLX gene

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