Petal abscission in roses is associated with the activation of a truncated version of the animal PDCD4 homologue, RbPCD1
Introduction
Abscission is a process that results in shedding of various plant parts (leaves, petals, stamens, flowers, fruits) when these are no longer needed. Cell separation occurs due to AZ-specific activation of various cell wall-modifying genes and proteins such as polygalacturonases [[1], [2], [3]], beta-1,4-glucanases [[4], [5], [6]], pectate lyases [7], xyloglucan endotransglucosylase/hydrolases [8,9], expansins [10,11] etc.
The process of separation of the entire organ proceeds within the abscission zone, a small defined zone of cells that are smaller, cytoplasmically denser and morphologically and physiologically distinct from neighbouring cells [[12], [13], [14], [15], [16]]. The AZ cells possess differential sensitivity to hormones like ethylene and auxin and are able to uniquely respond to abscission cues through regulation of a specific set of genes within the abscission zone [[17], [18], [19], [20], [21], [22]].
Since abscission zone cells ultimately undergo cell wall disassembly and cell separation during the process, there has been speculation as to whether AZ cells undergo programmed cell death as observed during senescence. Previous observations have shown indications of PCD during the abscission processes in different plants. In Pelargonium, petal abscission was accompanied with protoplast shrinkage and cell wall degradation in AZ cells [23] while in Chamelaucium uncinatum, cells immediately adjacent to the AZ lost viability [24]. In Prunus, leaf abscission was associated with cell wall degradation and release of cytoplasm followed by cell death [25]. One of the most prominent features of PCD namely DNA degradation, chromatin condensation, loss of cell viability and change in nuclear structure was observed during tomato pedicel abscission [26]. Nucleases such as the LX ribonuclease associated with ethylene responses, senescence and programmed cell death [[27], [28], [29]] were also found to be involved in abscission since antisense LX tomato plants showed delayed abscission of leaves [30]. Similarly, the BIFUNCTIONAL ENDONUCLEASE gene (BFN1), active in the leaf and the fruit abscission zones of both Arabidopsis and tomato, was found to be associated with senescence in Arabidopsis [31] and developmental PCD in tomato [32]. Transcriptomic studies during abscission in apple fruitlets [20] and soybean, tomato and Arabidopsis [33] have identified genes associated with PCD, autophagy and those encoding cysteine proteases and clp proteases.
We are interested in studying the regulation of petal abscission in ethylene-sensitive fragrant roses and the various changes occurring during progression of ethylene-mediated petal abscission [[7], [8], [9],11,22,34]. We have previously shown that rapid transcription of RbCP1 during petal abscission and the expression of a 37 kDa cysteine protease (encoded by RbCP1) resulted in decrease in total protein content during abscission in rose [34] suggesting that petal AZ cells may undergo PCD. In this study, we have identified RbPCD1 as an abscission up-regulated gene, encoding a novel truncated version of the conserved animal PDCD4 proteins that is seedling lethal when expressed in transgenic Arabidopsis. Its ability to suppress transcription and its up-regulation by ethylene in different tissues suggests that it may actively participate to mediate ethylene responses in processes like abscission and senescence.
Section snippets
Plant material, growth and treatments
Flowers of the ethylene-sensitive, early-abscising fragrant rose (Rosa bourboniana var. Gruss an Teplitz) were used to isolate the gene and to examine gene expression. Treatment of flowers of R. bourboniana (ethylene-sensitive, early-abscising) and R. hybrida (var. Opening Night, less ethylene-sensitive, late-abscising) with and without ethylene was carried out essentially as described [7,11]. The petal abscission zone tissue was the 2 mm2 tissue of the petal base in contact with the thalamus [7
Isolation and sequence analysis of RbPCD1
To obtain an insight into the genes that are expressed differentially in the AZ, an analysis of the abscission zone transcriptome was carried out using mRNA differential display. DDRT-PCR was performed as described [49] with minor modifications that included the use of γ32P-ATP for end-labeling of anchor primers to get uniform band intensity, instead of α32P-dCTP at the DDRT-PCR step [37]. One of the genes identified by mRNA differential screening of abscission up-regulated RNAs [50], RbPCD1,
Discussion
Organ abscission is strongly responsive to ethylene and often accompanied with PCD-like features [23,24,30,32,56,57]. The clearest evidence for PCD, however, came from studies in tomato flower and leaf AZ tissues wherein a disruption of nuclear shape and structure was observed in the later stages of abscission, indicating chromatin disorganization [26].
We had previously shown that rose petal abscission was accompanied with the expression of an ethylene-inducible cysteine protease gene, RbCP1 [34
Acknowledgements
We are grateful to Prof. Shucai Wang (Northeast Normal Univ, Changchun, China) for effector and reporter vectors for protoplast transfection study and to Dr Ute Hoecker (Univ of Cologne, Germany) for the gift of the pRTL.2 vector. We thank Dr Sadaf Khan (a former post doc in our lab) and Dr PA Shirke (Dept of Plant Physiology, CSIR-NBRI) for help with the PAM-Imaging. We are grateful to Mr Ram Awadh for taking care of the rose plants. PS, APS, SKT and VK were supported by the Council of
References (72)
- et al.
Transcriptional activation of a pectate lyase gene, RbPel1, during petal abscission in rose
Postharvest Biol. Technol.
(2011) - et al.
Petal abscission in rose (Rosa bourboniana var Gruss an Teplitz) is associated with the enhanced expression of an alpha expansin gene, RbEXPA1
Plant Sci.
(2007) - et al.
Differential and reciprocal regulation of ethylene pathway genes regulates petal abscission in fragrant and non-fragrant roses
Plant Sci.
(2019) - et al.
Anatomy of ethylene-induced petal abscission in Pelargonium× hortorum
Ann. Bot.
(1993) - et al.
Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method
Methods
(2001) - et al.
Differential expression of genes during banana fruit development, ripening and 1-MCP treatment: presence of distinct fruit specific, ethylene induced and ethylene repressed expression
Postharvest Biol. Technol.
(2006) - et al.
Isolation of a novel mouse gene MA-3 that is induced upon programmed cell death
Gene
(1995) - et al.
Cloning of a tomato polygalacturonase expressed in abscission
Plant Mol. Biol.
(1995) - et al.
Expression of polygalacturonases and evidence to support their role during cell separation processes in Arabidopsis thaliana
J. Exp. Bot.
(2007) - et al.
Silencing polygalacturonase expression inhibits tomato petiole abscission
J. Exp. Bot.
(2008)
Flower abscission in mutant tomato plants
Planta
Transgenic analysis of tomato endo‐β‐1, 4‐glucanase gene function. Role of cel1 in floral abscission
Plant J.
Antisense suppression of tomato endo-1, 4-β-glucanase Cel2 mRNA accumulation increases the force required to break fruit abscission zones but does not affect fruit softening
Plant Mol. Biol.
Petal abscission in rose is associated with the differential expression of two ethylene-responsive xyloglucan endotransglucosylase/hydrolase genes, RbXTH1 and RbXTH2
J. Exp. Bot.
Differential expression of several xyloglucan endotransglucosylase/hydrolase genes regulates flower opening and petal abscission in roses
AoB Plants
Changes in expansin activity and gene expression during ethylene-promoted leaflet abscission in Sambucus nigra
J. Exp. Bot.
The positional differentiation of ethylene-responsive cells in rachis abscission zones in leaves of Sambucus nigra and their growth and ultrastructural changes at senescence and separation
Planta
Ethylene-promoted tomato flower abscission and the possible involvement of an inhibitor
Planta
Last exit: senescence, abscission, and meristem arrest in Arabidopsis
Plant Cell
Organ abscission
Annu. Plant Rev.
Steven, Development of the abscission zone
Stewart Postharvest Rev.
Cell wall remodeling in Arabidopsis stamen abscission zones: temporal aspects of control inferred from transcriptional profiling
Plant Signal. Behav.
Ethylene-induced differential gene expression during abscission of citrus leaves
J. Exp. Bot.
Microarray analysis of the abscission-related transcriptome in the tomato flower abscission zone in response to auxin depletion
Plant Physiol.
Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone crosstalk
BMC Plant Biol.
The manipulation of auxin in the abscission zone cells of Arabidopsis flowers reveals that indoleacetic acid signaling is a prerequisite for organ shedding
Plant Physiol.
Anatomy of ethylene-induced floral-organ abscission in Chamelaucium uncinatum (Myrtaceae)
Aus. J. Bot.
Programmed cell death during plant growth and development
Cell Death Differ.
Programmed cell death occurs asymmetrically during abscission in tomato
Plant Cell
Senescence-induced RNases in tomato
Plant Mol. Biol.
Tomato ribonuclease LX with the functional endoplasmic reticulum retention motif HDEF is expressed during programmed cell death processes, including xylem differentiation, germination, and senescence
Plant Physiol.
Tissue-specific expression of tomato Ribonuclease LX during phosphate starvation-induced root growth
J. Exp. Bot.
Suppression of LX ribonuclease in tomato results in a delay of leaf senescence and abscission
Plant Physiol.
Identification of BFN1, a bifunctional nuclease induced during leaf and stem senescence in Arabidopsis
Plant Physiol.
Expression analysis of the BFN1 nuclease gene promoter during senescence, abscission, and programmed cell death-related processes
J. Exp. Bot.
Examination of the abscission-associated transcriptomes for soybean, tomato, and Arabidopsis highlights the conserved biosynthesis of an extensible extracellular matrix and boundary layer
Front. Plant Sci.
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The JA pathway is rapidly down-regulated in petal abscission zones prior to flower opening and affects petal abscission in fragrant roses during natural and ethylene-induced petal abscission
2022, Scientia HorticulturaeCitation Excerpt :Flower buds (unpollinated, loose pointed cylindrical buds with one or two opened petals of the outermost whorl) were picked before sunrise from the field and pedicels placed immediately in water in a beaker. These were then placed in a desiccator and treated with ethylene (0.5 µL L–1) for ∼18 h for R. bourboniana and ∼52 h for R. hybrida at 25±2 °C with 125 μmoles of light intensity from cool white fluorescent tubes (Philips, India) under a light period of 12 h (Sane et al., 2007; VBN 2014; Singh et al., 2019a, Singh et al., 2019b). Regular ventilation changes were carried out every 12 h and ethylene concentration maintained.
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- 1
Current address: National Institute for Plant Genome Research, New Delhi-110067, India.
- 2
Current address: National Centre for Natural Products Research, School of Pharmacy, University of Mississippi, MS 38677, USA.