TaPCNA plays a role in programmed cell death after UV-B exposure in wheat (Triticum aestivum)
Meiting Du A , Ying Zhang A , Huize Chen
A B and Rong Han A B
+ Author Affiliations
- Author Affiliations
A Higher Education Key Laboratory of Plant Molecular and Environment Stress Response (Shanxi Normal University) in Shanxi Province, Linfen City, Shanxi Province, China.
B Corresponding authors. Emails: chenhuize@hotmail.com; snuchen@snu.ac.kr
Functional Plant Biology 48(10) 1029-1038 https://doi.org/10.1071/FP21013
Submitted: 14 January 2021 Accepted: 7 June 2021 Published: 9 July 2021
Journal compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
Ultraviolet (UV)-B is a component of sunlight and shows a significant effect on DNA damage, which can be regulated by proliferating cell nuclear antigen (PCNA). The role of TaPCNA in wheat (Triticum aestivum L.) programmed cell death (PCD) under UV-B has not been investigated previously. Here, we explored the function of TaPCNA in wheat exposed to UV-B utilising Barley Stripe Mosaic Virus–virus-induced gene silencing (VIGS). The results showed that the expression of TaPCNA was downregulated, and curly wheat leaves with several spots were determined by VIGS. The growth rate and mesophyll cell length were significantly inhibited after TaPCNA was silenced. The activity of superoxide dismutase and the contents of soluble sugar and soluble protein decreased, whereas the activities of peroxidase and catalase and malondialdehyde content increased in TaPCNA-silenced and UV-B treatment groups. DNA laddering and propidium iodide staining results showed that DNA fragments and micronucleus accumulated after TaPCNA silencing with or without UV-B. Thus, TaPCNA participates in plant growth and DNA damage and PCD under UV-B. This study suggests an idea for the exploration of the function of certain genes in such complex wheat genomes and offers a theoretical basis to improve wheat agronomic traits.
Keywords: programmed cell death, gene silencing, wheat, UV-B radiation, proliferating cell nuclear antigen, Triticum aestivum L.
References
Abdel-Latif A, Osman G (2017) Comparison of three genomic DNA extraction methods to obtain high DNA quality from maize. Plant Methods 13, 1–9.| Comparison of three genomic DNA extraction methods to obtain high DNA quality from maize.Crossref | GoogleScholarGoogle Scholar | 28053646PubMed |
Bruce G, Gu M, Shi N, Liu Y, Hong Y (2011) Influence of retinoblastoma-related gene silencing on the initiation of DNA replication by African cassava mosaic virus Rep in cells of mature leaves in Nicotiana benthamiana plants. Virology Journal 8, 561
| Influence of retinoblastoma-related gene silencing on the initiation of DNA replication by African cassava mosaic virus Rep in cells of mature leaves in Nicotiana benthamiana plants.Crossref | GoogleScholarGoogle Scholar | 22204717PubMed |
Bruuinsma J (1963) The quantitative analysis of chlorophylls a and b in plant extracts. Photochemistry and Photobiology 2, 241–249.
| The quantitative analysis of chlorophylls a and b in plant extracts.Crossref | GoogleScholarGoogle Scholar |
Chen K, Gao C (2015) Targeted gene mutation in plants. In ‘Somatic Genome Manipulation’. Eds Li, Xiu-Qing, Donnelly, Danielle J., Jensen, Thomas G. pp. 253–272. (Springer)
De Gara L (2004) Class III peroxidases and ascorbate metabolism in plants. Phytochemistry Reviews 3, 195–205.
| Class III peroxidases and ascorbate metabolism in plants.Crossref | GoogleScholarGoogle Scholar |
Essers J, Theil AF, Baldeyron C, van Cappellen WA, Houtsmuller AB, Kanaar R, Vermeulen W (2005) Nuclear dynamics of PCNA in DNA replication and repair. Molecular and Cellular Biology 25, 9350–9359.
| Nuclear dynamics of PCNA in DNA replication and repair.Crossref | GoogleScholarGoogle Scholar | 16227586PubMed |
Hopkins L, Bond M, Tobin A (2002) Ultraviolet‐B radiation reduces the rates of cell division and elongation in the primary leaf of wheat (Triticum aestivum L. cv Maris Huntsman). Plant, Cell & Environment 25, 617–624.
| Ultraviolet‐B radiation reduces the rates of cell division and elongation in the primary leaf of wheat (Triticum aestivum L. cv Maris Huntsman).Crossref | GoogleScholarGoogle Scholar |
Kelman Z (1997) PCNA: structure, functions and interactions. Oncogene 14, 629–640.
| PCNA: structure, functions and interactions.Crossref | GoogleScholarGoogle Scholar | 9038370PubMed |
Kuhlmann F, Müller C (2010) UV-B impact on aphid performance mediated by plant quality and plant changes induced by aphids. Plant Biology 12, 676–684.
| UV-B impact on aphid performance mediated by plant quality and plant changes induced by aphids.Crossref | GoogleScholarGoogle Scholar | 20636911PubMed |
Leung W, Baxley RM, Moldovan G-L, Bielinsky A-K (2018) Mechanisms of DNA damage tolerance: Post-translational regulation of PCNA. Genes 10, 10
| Mechanisms of DNA damage tolerance: Post-translational regulation of PCNA.Crossref | GoogleScholarGoogle Scholar |
Li Y, Liu Y, Qi F, Deng C, Lu C, Huang H, Dai S (2020) Establishment of virus-induced gene silencing system and functional analysis of ScbHLH17 in Senecio cruentus. Plant Physiology and Biochemistry 147, 272–279.
| Establishment of virus-induced gene silencing system and functional analysis of ScbHLH17 in Senecio cruentus.Crossref | GoogleScholarGoogle Scholar | 31891861PubMed |
Liu W, Xu F, Lv T, Zhou W, Chen Y, Jin C, Lu L, Lin X (2018) Spatial responses of antioxidative system to aluminum stress in roots of wheat (Triticum aestivum L.) plants. The Science of the Total Environment 627, 462–469.
| Spatial responses of antioxidative system to aluminum stress in roots of wheat (Triticum aestivum L.) plants.Crossref | GoogleScholarGoogle Scholar | 29426169PubMed |
Lizana XC, Hess S, Calderini DF (2009) Crop phenology modifies wheat responses to increased UV-B radiation. Agricultural and Forest Meteorology 149, 1964–1974.
| Crop phenology modifies wheat responses to increased UV-B radiation.Crossref | GoogleScholarGoogle Scholar |
Maga G, Hübscher U (2003) Proliferating cell nuclear antigen (PCNA): a dancer with many partners. Journal of Cell Science 116, 3051–3060.
| Proliferating cell nuclear antigen (PCNA): a dancer with many partners.Crossref | GoogleScholarGoogle Scholar | 12829735PubMed |
Mailand N, Gibbs-Seymour I, Bekker-Jensen S (2013) Regulation of PCNA–protein interactions for genome stability. Nature Reviews. Molecular Cell Biology 14, 269–282.
| Regulation of PCNA–protein interactions for genome stability.Crossref | GoogleScholarGoogle Scholar | 23594953PubMed |
Nawkar GM, Maibam P, Park JH, Sahi VP, Lee SY, Kang CH (2013) UV-Induced cell death in plants. International Journal of Molecular Sciences 14, 1608–1628.
| UV-Induced cell death in plants.Crossref | GoogleScholarGoogle Scholar | 23344059PubMed |
Paunesku T, Mittal S, Protić M, Oryhon J, Korolev S, Joachimiak A, Woloschak G (2001) Proliferating cell nuclear antigen (PCNA): ringmaster of the genome. International Journal of Radiation Biology 77, 1007–1021.
| Proliferating cell nuclear antigen (PCNA): ringmaster of the genome.Crossref | GoogleScholarGoogle Scholar | 11682006PubMed |
Qian J, Chen Y, Xu Y, Zhang X, Kang Z, Jiao J, Zhao J (2019) Interactional similarities and differences in the protein complex of PCNA and DNA replication factor C between rice and Arabidopsis. BMC Plant Biology 19, 257
| Interactional similarities and differences in the protein complex of PCNA and DNA replication factor C between rice and Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 31200645PubMed |
Ries G, Heller W, Puchta H, Sandermann H, Seidlitz HK, Hohn B (2000) Elevated UV-B radiation reduces genome stability in plants. Nature 406, 98–101.
| Elevated UV-B radiation reduces genome stability in plants.Crossref | GoogleScholarGoogle Scholar | 10894550PubMed |
Ripley BM, Gildenberg MS, Washington MT (2020) Control of DNA damage bypass by ubiquitylation of PCNA. Genes 11, 138
| Control of DNA damage bypass by ubiquitylation of PCNA.Crossref | GoogleScholarGoogle Scholar |
Schulz P, Neukermans J, Van Der Kelen K, Mühlenbock P, Van Breusegem F, Noctor G, et al (2012) Chemical PARP inhibition enhances growth of Arabidopsis and reduces anthocyanin accumulation and the activation of stress protective mechanisms. PLoS One 7, e37287
| Chemical PARP inhibition enhances growth of Arabidopsis and reduces anthocyanin accumulation and the activation of stress protective mechanisms.Crossref | GoogleScholarGoogle Scholar | 22662141PubMed |
Shewry PR (2009) Wheat. Journal of Experimental Botany 60, 1537–1553.
| Wheat.Crossref | GoogleScholarGoogle Scholar | 19386614PubMed |
Strzalka W, Ziemienowicz A (2011) Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation. Annals of Botany 107, 1127–1140.
| Proliferating cell nuclear antigen (PCNA): a key factor in DNA replication and cell cycle regulation.Crossref | GoogleScholarGoogle Scholar | 21169293PubMed |
Yin R, Ulm R (2017) How plants cope with UV-B: from perception to response. Current Opinion in Plant Biology 37, 42–48.
| How plants cope with UV-B: from perception to response.Crossref | GoogleScholarGoogle Scholar | 28411583PubMed |
Yuan C, Li C, Yan L, Jackson AO, Liu Z, Han C, Yu J, Li D (2011) A high throughput barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots. PLoS One 6, e26468
| A high throughput barley stripe mosaic virus vector for virus induced gene silencing in monocots and dicots.Crossref | GoogleScholarGoogle Scholar | 22195048PubMed |
Zhao S, Huang Q, Yang P, Zhang J, Jia H, Jiao Z (2012) Effects of ion beams pretreatment on damage of UV-B radiation on seedlings of winter wheat (Triticum aestivum L.). Applied Biochemistry and Biotechnology 168, 2123–2135.
| Effects of ion beams pretreatment on damage of UV-B radiation on seedlings of winter wheat (Triticum aestivum L.).Crossref | GoogleScholarGoogle Scholar | 23054823PubMed |
