PMCCPMCCPMCC

Search tips
Search criteria 

Advanced

 
Logo of plantsigLink to Publisher's site
 
Plant Signal Behav. 2016 June; 11(6): e1176820.
Published online 2016 April 20. doi:  10.1080/15592324.2016.1176820
PMCID: PMC4973761

AtPDCD5 plays a role during dark-senescence in Arabidopsis

ABSTRACT

In this work, we investigated the role of an Arabidopsis protein, AtPDCD5, during senescence after a 24h-dark period. Previously, we demonstrated that AtPDCD5 participates in programmed cell death (PCD) after UV-B exposure and in age-induced senescence. The results presented here, together with previous data, demonstrate that AtPDCD5 not only plays an important role during DNA damage responses induced by UV-B radiation, but also takes part in PCD programs such as dark-induced senescence in Arabidopsis.

KEYWORDS: Darkness, PDCD5, programmed cell death, senescence, UV-B radiation

Abbreviations

PCD
Programmed Cell Death
OE
Overexpressing

Programmed cell death (PCD) is an essential process of life. In animals and plants, PCD is involved in different aspects of development, shaping structures or eliminating unwanted tissues.1,2 In plants, PCD occurs as an essential part of development but also as a reaction to biotic and abiotic environmental challenges.3 During stress conditions, abiotic stresses such as heat, salt, UV radiation or extended darkness; or biotic stresses such as pathogen attacks can lead to cell death.4,5 On the other hand, differentiation induced PCD occurs as a final differentiation step in specific cell types, for instance, in xylem tracheary elements, the root cap, or the anther tapetum layer;6-8 but also age-induced PCD takes place as the last step of organ senescence that occurs in all tissues of an organ or even the entire plant at the end of its life cycle.9 Leaf senescence involves different physiological, biochemical, and molecular changes, including a decline in photosynthetic efficiency, decreases in chlorophyll and protein contents, and increases in membrane ion leakage and expression of senescence-associated genes.10 Although senescence occurs in an age-dependent manner and it is controlled by an innate genetic program; unfavorable environmental stresses, such as darkness, can also trigger senescence during leaf development. Plant growth and development requires light, and plants require photoreceptors to adapt to ambient light conditions throughout development. Interestingly, plants that overexpress the photoreceptors phytochrome A or B show delayed leaf yellowing,11,12 while the knockout phyB mutant is hyposensitive to a dark treatment,13 suggesting that phytochromes participate in the regulation of leaf senescence. Photoactivated phytochromes move from the cytosol to the nucleus, where they interact with regulators of light signaling such as the transcription factors PIF4 and PIF5 that are positive factors of dark-induced senescence in Arabidopsis.14

Previously, we reported that an Arabidopsis protein, Programmed Cell Death protein 5 (AtPDCD5), which is highly similar to the human PDCD5 protein, is induced by UV-B radiation and participates in PCD in UV-B DNA damage response.15 In humans, PDCD5 binds to the histone acetyltransferase TIP60 to enhance its activity to repair DNA damage and it also regulates different types of PCD; for example the translocation of Bax, a pro-apototic factor, from the cytosol to the mitochondria, inducing cytochrome c release and an activation of caspase-3 activity, which are early events of the beginning of apoptosis.16 On the other hand, HsPDCD5 participates in the PCD pathway regulated by the Tumor Necrosis Factor Receptor TNFRSF19, a paraptosis-like cell death pathway.17 In Arabidopsis, AtPDCD5 transcripts are increased after UV-B exposure, and transgenic plants overexpressing this protein show increased cell death in roots after UV-B exposure, while mutants in this gene are less affected by the treatment than WT plants.15 pdcd5 mutants also have an altered antioxidant metabolism and accumulate higher levels of DNA damage after UV-B exposure; while plants overexpressing AtPDCD5 show less DNA damage. Interestingly, AtPDCD5 also participates in age-induced programmed cell death. Plants deficient in AtPDCD5 expression exhibit a delayed leaf senescence characterized by higher chlorophyll content compared to WT plants, whereas PDCD5 OE plants show lower levels of total chlorophylls in the leaves than WT plants.15 Interestingly, while WT plants show a significant decrease in both chlorophyll a and b after a 24-h darkness period compared to levels in plants that were kept under a 16-h-light/8-h-dark photoperiod (Fig. 1A and B), pdcd5 mutants have a lower although still significant decrease in chlorophyll content after an extended period of darkness. This lower decrease in chlorophyll content in pdcd5 mutants was similar as that measured after UV-B exposure,15 suggesting that PDCD5 may participate not only in PCD after UV-B exposure, but also in dark-induced senescence. Although PDCD5 overexpressing plants (PDCD5 OE) were more chlorotic than WT plants as already reported,15 the decrease in chlorophylls after 24 h of darkness was similar as that measured in WT plants (Fig. 1A and B).

Figure 1.
PDCD5 participates in dark-induced leaf senescence in Arabidopsis. Arabidopsis plants were grown in a growth chamber under a 16-h-light/8-h-dark photoperiod; after 3 weeks, a set of plants were kept under dark conditions for 24 h; while ...

In order to confirm a putative role of AtPDCD5 in dark senescence, we evaluated the integrity of the cells by measuring the electrolyte leakage of leaves. Previously, we found that PDCD5 OE lines exhibited a higher increase in electrolyte leakage than WT plants after a UV-B treatment, while the opposite was observed in pdcd5 mutants.15 A similar result was obtained when WT and plants with altered PDCD5 expression levels were kept in the darkness for 24h. Fig. 1C shows that, while electrolyte leakage was similar in the different set of plants kept under a 16-h-light/8-h-dark photoperiod; after 24 h of darkness, the PDCD5 OE line showed a significantly higher increase in electrolyte leakage than WT plants, whereas pdcd5 plants showed a significantly lower increase than WT plants. In addition, fully expanded leaf #4 from WT, pdcd5 and PDCD5 OE plants were stained with trypan blue to visualize the presence of death cells after 24 h of darkness. Fig. 1D shows that leaf #4 from both WT and PDCD5 OE plants are considerably stained after extended darkness (mainly in veins and surrounding cells, Fig 1D, magnification), while leaves from pdcd5 mutants in the dark display similar stain intensity as leaves from control plants under a 16-h-light/8-h-dark photoperiod. Taking together, our results suggest that, besides its role in cell death after UV-B exposure and age-induced senescence as described in Falcone Ferreyra et al. (2016),15 AtPDCD5 also participates in dark-induced senescence in Arabidopsis. Interestingly, Arabidopsis seedlings changed to darkness conditions at midday showed an increase in ribosome-bound PDCD5 mRNAs, suggesting that PDCD5 expression would be regulated at post-transcriptional and/or translational levels in response to light deprivation.18,19 Moreover, PDCD5 transcript levels are significantly higher in senescing leaves than in young and developed rosette leaves (Fig 1E), demonstrating that PDCD5 plays a role in senescence programs in Arabidopsis plants.

Disclosure of potential conflicts of interest

No potential conflicts of interest were disclosed.

Funding

This work was financed by FONCyT grants PICT 2012-00267 and PICT 2013-268. M.L.F.F. and P.C. are members of the Researcher Career of the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET).

References

1. Fuchs Y, Steller H. Programmed cell death in animal development and disease. Cell 2011; 147:742-58; PMID:22078876; http://dx.doi.org/10.1016/j.cell.2011.10.033 [PMC free article] [PubMed] [Cross Ref]
2. Van Hautegem T, Waters AJ, Goodrich J, Nowack MK. Only in dying, life: programmed cell death during plant development. Trends Plant Sci 2015; 20:102-13; PMID:25457111; http://dx.doi.org/10.1016/j.tplants.2014.10.003 [PubMed] [Cross Ref]
3. Lam E. Controlled cell death, plant survival and development. Nat Rev Mol Cell Biol 2004; 5:305-15; PMID:15071555; http://dx.doi.org/2334405910.1038/nrm1358 [PubMed] [Cross Ref]
4. Nawkar GM, Maibam P, Park JH, Sahi VP, Lee SY, Kang CH. UV Induced cell death in plants. Int J Mol Sci 2013; 14:1608-28; PMID:23344059; http://dx.doi.org/10.3390/ijms14011608 [PMC free article] [PubMed] [Cross Ref]
5. Petrov V, Hille J, Mueller-Roeber B, Gechev TS. ROS-mediated abiotic stress-induced programmed cell death in plants. Front Plant Sci 2015; 6:69; PMID:25741354; http://dx.doi.org/10.3389/fpls.2015.00069 [PMC free article] [PubMed] [Cross Ref]
6. Plackett ARG, Thomas SG, Wilson ZA, Hedden P. Gibberellin control of stamen development: a fertile field. Trends Plant Sci 2011; 16: 568-78; PMID:21824801; http://dx.doi.org/10.1016/j.tplants.2011.06.007 [PubMed] [Cross Ref]
7. Bollhöner B, Zhang B, Stael S, Denancé N, Overmyer K, Goffner D, Van Breusegem F, Tuominen H. Post mortem function of AtMC9 in xylem vessel elements. New Phytol 2013; 200:498-510; PMID:23834670; http://dx.doi.org/10.1111/nph.12387 [PubMed] [Cross Ref]
8. Fendrych M, Van Hautegem T, Van Durme M, Olvera-Carrillo Y, Huysmans M, Karimi M, Lippens S, Guérin CJ, Krebs M, Schumacher K, et al. Programmed cell death controlled by ANAC033/ SOMBRERO determines root cap organ size in Arabidopsis. Curr Biol 2014; 24:931-40; PMID:24726156; http://dx.doi.org/; PMID:23176101; http://dx.doi.org/2345391610.1016/j.cub.2014.03.02510.1111/nph.12047 [PubMed] [Cross Ref]
9. Thomas H. Senescence, ageing and death of the whole plant. New Phytol 2013; 197:696-711 [PubMed]
10. Sarwat M, Naqvi AR, Ahmad P, Ashraf M, Akram NA. Phytohormones and microRNAs as sensors and regulators of leaf senescence: assigning macro roles to small molecules. Biotechnol Adv 2013; 31:1153-71; PMID:23453916; http://dx.doi.org/10.1016/j.biotechadv.2013.02.003 [PubMed] [Cross Ref]
11. Rousseaux MC, Ballaré CL, Jordan ET, Vierstra RD Directed overexpression of PHYA locally suppresses stem elongation and leaf senescence responses to far-red radiation. Plant Cell Environ 1997; 20:1551-58; PMID:24604733; http://dx.doi.org/1031868510.1046/j.1365-3040.1997.d01-51.x [Cross Ref]
12. Thiele A, Herold M, Lenk I, Quail PH, Gatz C. Heterologous expression of Arabidopsis phytochrome B in transgenic potato influences photosynthetic per-formance and tuber development. Plant Physiol 1999; 120:73-82; PMID:10318685; http://dx.doi.org/10.1104/pp.120.1.73 [PubMed] [Cross Ref]
13. Brouwer B, Gardeström P, Keech O In response to partial plant shading, the lack of phytochrome A does not directly induce leaf senescence but alters the fine-tuning of chlorophyll biosynthesis. J Exp Bot 2014; 65:4037-49; http://dx.doi.org/10.1093/jxb/eru060 [PMC free article] [PubMed] [Cross Ref]
14. Song Y, Yang C, Gao S, Zhang W, Li L, Kuai B. Age-triggered and dark-induced leaf senescence require the bHLH transcription factors PIF3, 4, and 5. Mol Plant 2014; 7:1776-87; PMID:25296857; http://dx.doi.org/10.1093/mp/ssu109 [PMC free article] [PubMed] [Cross Ref]
15. Falcone Ferreyra ML, Casadevall R, D´Andrea L, AbdElgawad H, Beemster GTS, Casati P AtPDCD5 Plays a Role in Programmed Cell Death after UV-B Exposure in Arabidopsis. Plant Physiol 2016 [PubMed]
16. Chen LN, Wang Y, Chen YY. Short interfering RNA against the PDCD5 attenuates cell apoptosis and caspase-3 activity induced by Bax overexpression. Apoptosis 2006; 11:101-11; PMID:16374546; http://dx.doi.org/10.1007/s10495-005-3134-y [PubMed] [Cross Ref]
17. Wang Y, Li X, Wang L, Ding P, Zhang Y, Han W, Ma D. An alternative form of paraptosis-like cell death, triggered by TAJ/TROY and enhanced by PDCD5 overexpression. J Cell Sci 2004; 117:1525-32; PMID:15020679; http://dx.doi.org/10.1242/jcs.00994 [PubMed] [Cross Ref]
18. Juntawong P, Bailey-Serres J Dynamic light regulation of translation status in Arabidopsis thaliana. Front Plant Sci 2012; 3:66;PMID:22645595; http://dx.doi.org/10.3389/fpls.2012.00066 [PMC free article] [PubMed] [Cross Ref]
19. Zimmermann P, Hirsch-Hoffmann M, Hennig L, Gruissem W GENEVESTIGATOR. Arabidopsis microarray database and analysis toolbox. Plant Physiol 2004; 136:2621-32; http://dx.doi.org/10.1104/pp.104.046367 [PubMed] [Cross Ref]

Articles from Plant Signaling & Behavior are provided here courtesy of Taylor & Francis