Programmed cell death of secretory cavity cells of citrus fruits is associated with Ca2+ accumulation in the nucleus

Zheng, Ping; Bai, Mei; Chen, Y.; Liu, P. W.; Liang, Shejian; Wu, Hong

doi:10.1007/s00468-014-1024-z

Cited by 13 publications

(11 citation statements)

References 31 publications

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“…This change would cause failure in pollen maturation for germination. Additionally, Zheng et al suggested that the PCD process of secretory cavity cells in citrus fruits is associated with Ca 2 + accumulation in the nucleus, which initiates PCD [74]. In our study, we noted that the tapetum was decomposed into small pieces in MT plants (Fig.…”

Section: Deps Related To Ca 2+ Bindingmentioning

confidence: 72%

iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.)

Pang

Wei

et al. 2015

Journal of Proteomics

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Section: Deps Related To Ca 2+ Bindingmentioning

confidence: 72%

iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.)

Pang

Wei

et al. 2015

Journal of Proteomics

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“…PCD creating aerenchyma in water logged plants involves ethylene and calcium, while changes in local ROS production might also play a role under low oxygen conditions in e.g., maize roots (Evans, 2003 ; Verboven et al, 2012 ; Yamauchi et al, 2013 ; Van Hautegem et al, 2014 ; Broughton et al, 2015 ). PCD has been observed in fruit under external stress (Chen et al, 2014 ; Zheng et al, 2014 ) but evidence of the phenomenon has not yet been given for pore formation during fruit growth. To our knowledge no studies have yet been conducted on PCD during growth of fruit organs.…”

Section: Discussionmentioning

confidence: 99%

Spatial development of transport structures in apple (Malus × domestica Borkh.) fruit

et al. 2015

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The void network and vascular system are important pathways for the transport of gases, water and solutes in apple fruit (Malus × domestica Borkh). Here we used X-ray micro-tomography at various spatial resolutions to investigate the growth of these transport structures in 3D during fruit development of “Jonagold” apple. The size of the void space and porosity in the cortex tissue increased considerably. In the core tissue, the porosity was consistently lower, and seemed to decrease toward the end of the maturation period. The voids in the core were more narrow and fragmented than the voids in the cortex. Both the void network in the core and in the cortex changed significantly in terms of void morphology. An automated segmentation protocol underestimated the total vasculature length by 9–12% in comparison to manually processed images. Vascular networks increased in length from a total of 5 m at 9 weeks after full bloom, to more than 20 m corresponding to 5 cm of vascular tissue per cubic centimeter of apple tissue. A high degree of branching in both the void network and vascular system and a complex three-dimensional pattern was observed across the whole fruit. The 3D visualizations of the transport structures may be useful for numerical modeling of organ growth and transport processes in fruit.

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“…Some studies have shown that the mechanisms are similar to those in animal cells, not only in terms of morphological and biochemical changes, but also in terms the regulation involved ( Reape and McCabe, 2010 ). For example, cytochemical and immunocytochemical experiments have demonstrated that caspase 3-like and calcium ions are involved in chromatin agglutination and DNA degradation in the apoptosis of citrus fruit secretory vesicles ( Liu et al , 2012 ; Zheng et al , 2014 ). Ca 2+ may play a role in hypersensitive PCD by activating caspase 3-like activity ( Zuppini et al , 2005 ), or it may enter the cytoplasm from the extracellular space, increasing intracellular calcium levels and causing vacuole rupture ( Fukuda, 2000 ).…”

Section: Introductionmentioning

confidence: 99%

“…Subsequently, Chen and Wu (2010) used TUNEL assays to show that PCD is involved in the dissolution of secretory cavity cells. Further studies have demonstrated that both caspase 3-like and Ca 2+ are involved in the degradation of the nuclear structure and of chromatin during the PCD of secretory cavity cells ( Liu et al , 2012 ; Zheng et al , 2014 ). Thus, PCD has been confirmed to be involved in the formation of secretory cavities during Citrus fruit schizolysigeny ( Chen and Wu, 2010 ; Liu et al , 2012 ).…”

Section: Introductionmentioning

confidence: 99%

“…Thus, PCD has been confirmed to be involved in the formation of secretory cavities during Citrus fruit schizolysigeny ( Chen and Wu, 2010 ; Liu et al , 2012 ). In addition, Zheng et al (2014) found that the spatio-temporal localization of Ca 2+ is closely related to nuclear morphological changes, and hence it is presumably involved in regulating the degradation of the nuclear structure and nuclear chromatin during the PCD. However, the mechanism underlying the involvement of Ca 2+ remains unknown.…”

Section: Introductionmentioning

confidence: 99%

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Ca2+-dependent nuclease is involved in DNA degradation during the formation of the secretory cavity by programmed cell death in fruit of Citrus grandis ‘Tomentosa’

Bai

Liang

Huai

et al. 2020

Journal of Experimental Botany

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The secretory cavity is a typical structure in Citrus fruit and is formed by schizolysigeny. Previous reports have indicated that programmed cell death (PCD) is involved in the degradation of secretory cavity cells in the fruit, and that the spatio-temporal location of calcium is closely related to nuclear DNA degradation in this process; however, the molecular mechanisms underlying this Ca2+ regulation remain largely unknown. Here, we identified CgCaN that encodes a Ca2+-dependent DNase in the fruit of Citrus grandis ‘Tomentosa’, the function of which was studied using calcium ion localization, DNase activity assays, in situ hybridization, and protein immunolocalization. The results suggested that the full-length cDNA of CgCaN contains an ORF of 1011 bp that encodes a protein 336 amino acids in length with a SNase-like functional domain. CgCaN digests dsDNA at neutral pH in a Ca2+-dependent manner. In situ hybridization signals of CgCaN were particularly distributed in the secretory cavity cells. Ca2+ and Ca2+-dependent DNases were mainly observed in the condensed chromatin and in the nucleolus. In addition, spatio-temporal expression patterns of CgCaN and its protein coincided with the time-points that corresponded to chromatin degradation and nuclear rupture during the PCD in the development of the fruit secretory cavity. Taken together, our results suggest that Ca2+-dependent DNases play direct roles in nuclear DNA degradation during the PCD of secretory cavity cells during Citrus fruit development. Given the consistency of the expression patterns of genes regulated by calmodulin (CaM) and calcium-dependent protein kinases (CDPK) and the dynamics of calcium accumulation, we speculate that CaM and CDPK proteins might be involved in Ca2+ transport from the extracellular walls through the cytoplasm and into the nucleus to activate CgCaN for DNA degradation.

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Programmed cell death of secretory cavity cells of citrus fruits is associated with Ca2+ accumulation in the nucleus

Cited by 13 publications

References 31 publications

iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.)

iTRAQ-facilitated proteomic profiling of anthers from a photosensitive male sterile mutant and wild-type cotton (Gossypium hirsutum L.)

Spatial development of transport structures in apple (Malus × domestica Borkh.) fruit

Ca2+-dependent nuclease is involved in DNA degradation during the formation of the secretory cavity by programmed cell death in fruit of Citrus grandis ‘Tomentosa’

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