The involvement of ethylene in programmed cell death and climacteric-like behaviour during the remodelling of lace plant (Aponogeton madagascariensis) leaves

Botany ◽  
2012 ◽  
Vol 90 (12) ◽  
pp. 1237-1244 ◽  
Author(s):  
A.N. Dauphinee ◽  
H. Wright ◽  
G. Rantong ◽  
A.H.L.A.N. Gunawardena
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Leaf Development ◽  
Inhibitory Effect ◽  
Ethylene Biosynthesis ◽  
Developmentally Regulated ◽  
Developmental Processes ◽  
Climacteric Fruit ◽  
Signalling Molecule ◽  
Whole Plants

Programmed cell death (PCD) plays an important role in several plant developmental processes. The phytohormone ethylene has been implicated in PCD signalling in many plant systems, but it is also important in developmental processes such as seed germination, flowering, and climacteric fruit ripening. Lace plant (Aponogeton madagascariensis (Mirbel) H. Bruggen) is an aquatic monocot that develops perforated leaves via the deletion of cells through developmentally regulated PCD. The plant is ideal for studying PCD; however, little is known about the regulation of cellular death involved in this system. The current study examines ethylene as a potential signalling molecule in lace plant PCD and investigates climacteric-like behaviour during lace plant leaf development. Whole plants were treated with the ethylene biosynthesis inhibitor aminoethoxyvinylglycine (AVG), the ethylene precursor 1-aminocyclopropane-1-carboxylic acid (ACC), or a combination of both. Subsequently, ethylene levels were monitored, and leaf development was analyzed. The results indicate that ethylene is involved in lace plant PCD signalling. AVG-treated plants had significantly lower ethylene outputs and a significant reduction in perforation formation. The inhibitory effect of AVG was recovered when AVG and ACC were applied simultaneously. The data presented here show for the first time, to our knowledge, climacteric-like behaviour during the remodelling of leaves.

scholarly journals Vacuolar processing enzymes, AmVPE1 and AmVPE2, as potential executors of ethylene regulated programmed cell death in the lace plant (Aponogeton madagascariensis)

Botany ◽  
2018 ◽  
Vol 96 (4) ◽  
pp. 235-247 ◽  
Author(s):  
Gaolathe Rantong ◽  
Arunika H.L.A.N. Gunawardena
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Leaf Development ◽  
Cell Types ◽  
Ethylene Biosynthesis ◽  
Activity Levels ◽  
Developmentally Regulated ◽  
Transcript Levels ◽  
Processing Enzymes ◽  
Laser Capture Microscopy

Perforation formation in Aponogeton madagascariensis (Mirb.) H.Bruggen (lace plant) is an excellent model for studying developmentally regulated programmed cell death (PCD). In this study, we isolated and identified two lace plant vacuolar processing enzymes (VPEs) and investigated their involvement in PCD and throughout leaf development. Lace plant VPE transcript levels were determined during seven different stages of leaf development. PCD and non-PCD cells from “window” stage leaves (in which perforations are forming) were separated through laser-capture microscopy and their transcript levels were also determined. VPE activity was also studied between the cell types, through a VPE activity-based probe JOPD1. Additionally, VPE transcript levels were studied in plants treated with an ethylene biosynthesis inhibitor, aminoethoxyvinylglycine (AVG). The two isolated VPEs, AmVPE1 and AmVPE2, are vegetative type VPEs. AmVPE1 had higher transcript levels during a pre-perforation developmental stage, immediately prior to visible signs of PCD. AmVPE2 transcript levels were higher later during window and late window stages. Both VPEs had higher transcript and activity levels in PCD compared with the non-PCD cells. AVG treatment inhibited PCD and associated increases in VPE transcript levels. Our results suggested that VPEs are involved in the execution of the ethylene-related PCD in the lace plant.

scholarly journals RNA-Seq analysis reveals potential regulators of programmed cell death and leaf remodelling in lace plant (Aponogeton madagascariensis)

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Nathan M. Rowarth ◽  
Bruce A. Curtis ◽  
Anthony L. Einfeldt ◽  
John M. Archibald ◽  
Christian R. Lacroix ◽  
...  
Keyword(s):  
Gene Expression ◽  
Cell Death ◽  
Programmed Cell Death ◽  
Expression Analysis ◽  
Leaf Development ◽  
Anthocyanin Biosynthesis ◽  
Leaf Morphogenesis ◽  
Developmentally Regulated ◽  
Plant Leaf ◽  
Expression Of Genes

Abstract Background The lace plant (Aponogeton madagascariensis) is an aquatic monocot that develops leaves with uniquely formed perforations through the use of a developmentally regulated process called programmed cell death (PCD). The process of perforation formation in lace plant leaves is subdivided into several developmental stages: pre-perforation, window, perforation formation, perforation expansion and mature. The first three emerging “imperforate leaves” do not form perforations, while all subsequent leaves form perforations via developmentally regulated PCD. PCD is active in cells called “PCD cells” that do not retain the antioxidant anthocyanin in spaces called areoles framed by the leaf veins of window stage leaves. Cells near the veins called “NPCD cells” retain a red pigmentation from anthocyanin and do not undergo PCD. While the cellular changes that occur during PCD are well studied, the gene expression patterns underlying these changes and driving PCD during leaf morphogenesis are mostly unknown. We sought to characterize differentially expressed genes (DEGs) that mediate lace plant leaf remodelling and PCD. This was achieved performing gene expression analysis using transcriptomics and comparing DEGs among different stages of leaf development, and between NPCD and PCD cells isolated by laser capture microdissection. Results Transcriptomes were sequenced from imperforate, pre-perforation, window, and mature leaf stages, as well as PCD and NPCD cells isolated from window stage leaves. Differential expression analysis of the data revealed distinct gene expression profiles: pre-perforation and window stage leaves were characterized by higher expression of genes involved in anthocyanin biosynthesis, plant proteases, expansins, and autophagy-related genes. Mature and imperforate leaves upregulated genes associated with chlorophyll development, photosynthesis, and negative regulators of PCD. PCD cells were found to have a higher expression of genes involved with ethylene biosynthesis, brassinosteroid biosynthesis, and hydrolase activity whereas NPCD cells possessed higher expression of auxin transport, auxin signalling, aspartyl proteases, cysteine protease, Bag5, and anthocyanin biosynthesis enzymes. Conclusions RNA sequencing was used to generate a de novo transcriptome for A. madagascariensis leaves and revealed numerous DEGs potentially involved in PCD and leaf remodelling. The data generated from this investigation will be useful for future experiments on lace plant leaf development and PCD in planta.

scholarly journals Hsp70 plays a role in programmed cell death during the remodelling of leaves of the lace plant (Aponogeton madagascariensis)

2019 ◽  
Author(s):  
Nathan M Rowarth ◽  
Adrian N Dauphinee ◽  
Georgia L Denbigh ◽  
Arunika Hlan Gunawardena
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Leaf Development ◽  
Anthocyanin Content ◽  
Plant Leaves ◽  
Antioxidant Treatment ◽  
Plant Leaf ◽  
Whole Plants ◽  
Shock Proteins

Abstract Lace plant leaves utilize programmed cell death (PCD) to form perforations during development. The role of heat shock proteins (Hsps) in PCD during lace plant leaf development is currently unknown. Hsp70 amounts were measured throughout lace plant leaf development, and the results indicate that it is highest before and during PCD. Increased Hsp70 amounts correlate with raised anthocyanin content and caspase-like protease (CLP) activity. To investigate the effects of Hsp70 on leaf development, whole plants were treated with either of the known regulators of PCD [reactive oxygen species (ROS) or antioxidants] or an Hsp70 inhibitor, chlorophenylethynylsulfonamide (PES-Cl). ROS treatment significantly increased Hsp70 2-fold and CLP activity in early developing leaves, but no change in anthocyanin and the number of perforations formed was observed. Antioxidant treatment significantly decreased Hsp70, anthocyanin, and CLP activity in early leaves, resulting in the fewest perforations. PES-Cl (25 μM) treatment significantly increased Hsp70 4-fold in early leaves, while anthocyanin, superoxide, and CLP activity significantly declined, leading to fewer perforations. Results show that significantly increased (4-fold) or decreased Hsp70 amounts lead to lower anthocyanin and CLP activity, inhibiting PCD induction. Our data support the hypothesis that Hsp70 plays a role in regulating PCD at a threshold in lace plant leaf development. Hsp70 affects anthocyanin content and caspase-like protease activity, and helps regulate PCD during the remodelling of leaves of lace plant, Aponogeton madagascariensis.

Autoregulation of Shh expression and Shh induction of cell death suggest a mechanism for modulating polarising activity during chick limb development

Development ◽  
2000 ◽  
Vol 127 (22) ◽  
pp. 4811-4823 ◽  
Author(s):  
J.J. Sanz-Ezquerro ◽  
C. Tickle
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Sonic Hedgehog ◽  
Limb Development ◽  
Retroviral Vector ◽  
Cellular Mechanism ◽  
Limb Bud ◽  
Drug Induced ◽  
Signalling Molecule ◽  
Vertebrate Limb

The polarising region expresses the signalling molecule sonic hedgehog (Shh), and is an embryonic signalling centre essential for outgrowth and patterning of the vertebrate limb. Previous work has suggested that there is a buffering mechanism that regulates polarising activity. Little is known about how the number of Shh-expressing cells is controlled but, paradoxically, the polarising region appears to overlap with the posterior necrotic zone, a region of programmed cell death. We have investigated how Shh expression and cell death respond when levels of polarising activity are altered, and show an autoregulatory effect of Shh on Shh expression and that Shh affects cell death in the posterior necrotic zone. When we increased Shh signalling, by grafting polarising region cells or applying Shh protein beads, this led to a reduction in the endogenous Shh domain and an increase in posterior cell death. In contrast, cells in other necrotic regions of the limb bud, including the interdigital areas, were rescued from death by Shh protein. Application of Shh protein to late limb buds also caused alterations in digit morphogenesis. When we reduced the number of Shh-expressing cells in the polarising region by surgery or drug-induced killing, this led to an expansion of the Shh domain and a decrease in the number of dead cells. Furthermore, direct prevention of cell death using a retroviral vector expressing Bcl2 led to an increase in Shh expression. Finally, we provide evidence that the fate of some of the Shh-expressing cells in the polarising region is to undergo apoptosis and contribute to the posterior necrotic zone during normal limb development. Taken together, these results show that there is a buffering system that regulates the number of Shh-expressing cells and thus polarising activity during limb development. They also suggest that cell death induced by Shh could be the cellular mechanism involved. Such an autoregulatory process based on cell death could represent a general way for regulating patterning signals in embryos.

scholarly journals MazF-Mediated Cell Death in Escherichia coli: a Point of No Return

2004 ◽  
Vol 186 (24) ◽  
pp. 8295-8300 ◽  
Author(s):  
Shahar Amitai ◽  
Yussuf Yassin ◽  
Hanna Engelberg-Kulka
Keyword(s):  
Escherichia Coli ◽  
Cell Death ◽  
Programmed Cell Death ◽  
Inhibitory Effect ◽  
Luria Bertani ◽  
E Coli ◽  
Ectopic Overexpression ◽  
Point Of No Return ◽  
The Rich ◽  
Overexpression System

ABSTRACT mazEF is a stress-induced toxin-antitoxin module, located on the chromosome of Escherichia coli, that we have previously described to be responsible for programmed cell death in E. coli. mazF specifies a stable toxin, and mazE specifies a labile antitoxin. Recently, it was reported that inhibition of translation and cell growth by ectopic overexpression of the toxin MazF can be reversed by the action of the antitoxin MazE ectopically overexpressed at a later time. Based on these results, it was suggested that rather than inducing cell death, mazF induces a state of reversible bacteriostasis (K. Pederson, S. K. Christensen, and K. Gerdes, Mol. Microbiol. 45:501-510, 2002). Using a similar ectopic overexpression system, we show here that overexpression of MazE could reverse MazF lethality only over a short window of time. The size of that window depended on the nature of the medium in which MazF was overexpressed. Thus, we found “a point of no return,” which occurred sooner in minimal M9 medium than it did in the rich Luria-Bertani medium. We also describe a state in which the effect of MazF on translation could be separated from its effect on cell death: MazE overproduction could completely reverse the inhibitory effect of MazF on translation, while not affecting the bacteriocidic effect of MazF at all. Our results reported here support our view that the mazEF module mediates cell death and is part of a programmed cell death network.

scholarly journals The role of auxin in developmentally regulated programmed cell death in lace plant

2020 ◽  
Vol 107 (4) ◽  
pp. 577-586
Author(s):  
Georgia L. Denbigh ◽  
Adrian N. Dauphinee ◽  
Meredith S. Fraser ◽  
Christian R. Lacroix ◽  
Arunika H. L. A. N. Gunawardena
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Developmentally Regulated

scholarly journals Somatic piRNAs and Transposons are Differentially Expressed Coincident with Skeletal Muscle Atrophy and Programmed Cell Death

2021 ◽  
Vol 12 ◽  
Author(s):  
Junko Tsuji ◽  
Travis Thomson ◽  
Christine Brown ◽  
Subhanita Ghosh ◽  
William E. Theurkauf ◽  
...  
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Skeletal Muscle Atrophy ◽  
Rna Seq ◽  
Developmentally Regulated ◽  
Transposon Silencing ◽  
Ping Pong ◽  
Somatic Tissues ◽  
Oxidation Resistant ◽  
Pirna Pathway

PIWI-interacting RNAs (piRNAs) are small single-stranded RNAs that can repress transposon expression via epigenetic silencing and transcript degradation. They have been identified predominantly in the ovary and testis, where they serve essential roles in transposon silencing in order to protect the integrity of the genome in the germline. The potential expression of piRNAs in somatic cells has been controversial. In the present study we demonstrate the expression of piRNAs derived from both genic and transposon RNAs in the intersegmental muscles (ISMs) from the tobacco hawkmoth Manduca sexta. These piRNAs are abundantly expressed, ∼27 nt long, map antisense to transposons, are oxidation resistant, exhibit a 5’ uridine bias, and amplify via the canonical ping-pong pathway. An RNA-seq analysis demonstrated that 19 piRNA pathway genes are expressed in the ISMs and are developmentally regulated. The abundance of piRNAs does not change when the muscles initiate developmentally-regulated atrophy, but are repressed coincident with the commitment of the muscles undergo programmed cell death at the end of metamorphosis. This change in piRNA expression is correlated with the repression of several retrotransposons and the induction of specific DNA transposons. The developmentally-regulated changes in the expression of piRNAs, piRNA pathway genes, and transposons are all regulated by 20-hydroxyecdysone, the steroid hormone that controls the timing of ISM death. Taken together, these data provide compelling evidence for the existence of piRNA in somatic tissues and suggest that they may play roles in developmental processes such as programmed cell death.

Drosophila caspases involved in developmentally regulated programmed cell death of peptidergic neurons during early metamorphosis

2010 ◽  
Vol 519 (1) ◽  
pp. 34-48 ◽  
Author(s):  
Gyunghee Lee ◽  
Zixing Wang ◽  
Ritika Sehgal ◽  
Chun-Hong Chen ◽  
Keiko Kikuno ◽  
...  
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Peptidergic Neurons ◽  
Developmentally Regulated

Calcium inhibition halts developmental programmed cell death in the lace plant, Aponogeton madagascariensis?

Botany ◽  
2010 ◽  
Vol 88 (2) ◽  
pp. 206-210 ◽  
Author(s):  
Anna Elliott ◽  
Arunika H.L.A.N. Gunawardena
Keyword(s):  
Cell Death ◽  
Programmed Cell Death ◽  
Leaf Growth ◽  
Indirect Evidence ◽  
Ruthenium Red ◽  
Leaf Length ◽  
Leaf Morphogenesis ◽  
Whole Plants

This study examined the effect of the calcium channel blocker ruthenium red (RR) on developmental programmed cell death (PCD) and perforation formation in leaves of the aquatic lace plant ( Aponogeton madagascariensis (Mirbel) H. Bruggen). Plant immersion experiments were conducted using various concentrations (0, 10, 20, 30, and 40 µmol·L–1) of RR applied to whole plants over a 3 to 4 week period. The ratio of number of leaf perforations per centimetre of leaf length along with leaf length were used to assess treatment effect. While the ratio of number of perforations per centimetre of leaf length was significantly reduced with RR treatment, leaf length was not, overall, significantly affected by RR. Therefore, it was concluded that RR was able to inhibit calcium movement and halt PCD, thus reducing perforation formation without having detrimental effects on leaf growth. The present research provides indirect evidence of the possible role of calcium in developmental PCD in vivo during leaf morphogenesis in the lace plant. Furthermore, it suggests the usefulness of the lace plant as a model system for pharmacological studies involving developmental PCD.

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