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Journal of Integrative Agriculture  2017, Vol. 16 Issue (04): 820-827    DOI: 10.1016/S2095-3119(16)61517-4
Crop Genetics · Breeding · Germplasm Resources Advanced Online Publication | Current Issue | Archive | Adv Search |
Genome-wide identification of the radiation sensitivity protein-23 (RAD23) family members in apple (Malus×domestica Borkh.) and expression analysis of their stress responsiveness
WANG Na, GONG Xiao-qing, MA Feng-wang

State Key Laboratory of Crop Stress Biology for Arid Areas, College of Horticulture, Northwest A&F University, Yangling 712100, P.R.China

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Abstract  Radiation sensitivity proteins-23 (RAD23) are DNA repair factors participate in the ubiquitin/proteasome system (UPS).  Although the genome-wide analysis of RAD23 family members has been conducted in some species, little is known about RAD23 genes in apple (Malus×domestica Borkh.).  We analyzed this gene family in M. domestica in terms of genomic locations, protein and promoter structures, and expressions in response to stresses.  Various members showed a ubiquitous pattern of expression in all selected apple parts.  Their expressions were altered under chilling, heat, and hydrogen peroxide treatments, as well as abscisic acid (ABA) treatment and water deficiency, suggesting their possible roles in plant stress responses.  These results provide essential information about RAD23 genes in apple and will contribute to further functional studies
Keywords:  RAD23      Malus      ubiquitin-like protein      DNA repair protein      heat      stress response  
Received: 16 May 2016   Accepted: 07 April 2017

This work was supported by the National High Technology Research and Development Program of China (863 Program, 2011AA100204) and by the earmarked fund for the China Agriculture Research System (CARS-28).

Corresponding Authors:  MA Feng-wang, Tel/Fax: +86-29-87082648, E-mail:,   

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WANG Na, GONG Xiao-qing, MA Feng-wang. 2017. Genome-wide identification of the radiation sensitivity protein-23 (RAD23) family members in apple (Malus×domestica Borkh.) and expression analysis of their stress responsiveness. Journal of Integrative Agriculture, 16(04): 820-827.

Chen L, Madura K. 2002. Rad23 promotes the targeting of proteolytic substrates to the proteasome. Molecular and Cellular Biology, 22, 4902–4913.
Dantuma N P, Heinen C, Hoogstraten D. 2009. The ubiquitin receptor Rad23: at the crossroads of nucleotide excision repair and proteasomal degradation. DNA Repair, 8, 449–460.
Elsasser S, Chandler-Militello D, Muller B, Hanna J, Finley D. 2004. Rad23 and Rpn10 serve as alternative ubiquitin receptors for the proteasome. The Journal of Biological Chemistry, 279, 26817–26822.
Elsasser S, Finley D. 2005. Delivery of ubiquitinated substrates to protein-unfolding machines. Nature Cell Biology, 7, 742–749.
Farmer L M, Book A J, Lee K H, Lin Y L, Fu H Y, Vierstra R D, 2010. The RAD23 family provides an essential connection between the 26S proteasome and ubiquitylated proteins in Arabidopsis. The Plant Cell, 22, 124–142.
Gambino G, Perrone I, Gribaudo I. 2008. A rapid and effective method for RNA extraction from different tissues of grapevine and other woody plants. Phytochemical Analysis, 19, 520–525.
Guo W, Chen R, Gong Z, Yin Y, Li D. 2013. Suppression subtractive hybridization analysis of genes regulated by application of exogenous abscisic acid in pepper plant (Capsicum annuum L.) leaves under chilling stress. PLOS ONE, 8, e66667.
Guzder S N, Sung P, Prakash L, Prakash S. 1998. Affinity of yeast nucleotide excision repair factor 2, consisting of the Rad4 and Rad23 proteins, for ultraviolet damaged DNA. The Journal of Biological Chemistry, 273, 31541–31546.
Haglund K, Dikic I. 2005. Ubiquitylation and cell signaling. The EMBO Journal, 24, 3353–3359.
Hershko A, Ciechanover A. 1998. The ubiquitin system. Annual Review of Biochemistry, 67, 425–479.
Hoeijmakers J H. 2001. Genome maintenance mechanisms for preventing cancer. Nature, 411, 366–374.
Huang X, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Research, 9, 868–877.
Liang R Y, Chen L, Ko B T, Shen Y H, Li Y T, Chen B R, Lin K T, Madura K, Chuang S M. 2014. Rad23 interaction with the proteasome is regulated by phosphorylation of its ubiquitin-like (UbL) domain. Journal of Molecular Cell Biology, 426, 4049–4060.
Liu R H, Meng J L. 2003. MapDraw: a microsoft excel macro for drawing genetic linkage maps based on given genetic linkage data. Hereditas, 25, 317–321. (in Chinese)
Livak K, Schmittgen T. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25, 402–408.
Madura K, Prakash S. 1990. Transcript levels of the Saccharomyes cerevisiae DNA repair gene RAD23 increase in response to UV light and in meiosis but remain constant in the mitotic cell cycle. Nucleic Acids Research, 8, 4737–4742.
Masutani C, Sugasawa K, Yanagisawa J, Sonoyama T, Ui M, Enomoto T, Takio K, Tanaka K, van der Spek P J, Bootsma D, Hoeijmakers H J, Hanaoka F. 1994. Purification and cloning of a nucleotide excision repair complex involving the Xeroderma pigmentosum group C protein and a human homolog of yeast RAD23. The EMBO Journal, 13, 1831–1843.
Mukhopadhyay D, Riezman H. 2007. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science, 315, 201–205.
Ning D L, Lu T C, Liu G F, Yang C P, Wang B C. 2013. Proteomic analysis points to a role for RAD23 in apical dominance in Pinus sylvestris var. mongolica. Plant Molecular Biology Report, 31, 1283–1292.
Pickart C M. 2001. Mechanisms underlying ubiquitination. Annual Review of Biochemistry, 70, 503–533.
Postel D, Vanlemmens P, Gode P, Ronco G, Villa P. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.
Rao H, Sastry A. 2002. Recognition of specific ubiquitin conjugates is important for the proteolytic functions of the ubiquitin-associated domain proteins Dsk2 and Rad23. Journal of Biological Chemistry, 277, 11691–11695.
Reed H, Gillette T G. 2007. Nucleotide excision repair and the ubiquitin proteasome pathway-do all roads lead to Rome? DNA Repair, 6, 149–156.
Rombauts S, Déhais P, van Montagu M, Rouzé P. 1999. PlantCARE, a plant cis-acting regulatory element database. Nucleic Acids Research, 27, 295–296.
Schauber C, Chen L, Tongaonkar P, Vega I, Lambertson D, Potts W, Madura K. 1998. Rad23 links DNA repair to the ubiquitin/proteasome pathway. Nature, 391, 715–718.
Schultz T F, Quatrano R S. 1997. Characterization and expression of a rice RAD23 gene. Plant Molecular Biology, 34, 557–562.
Sturm A, Lienhard S. 1998. Two isoforms of plant RAD23 complement a UV-sensitive rad23 mutant in yeast. The Plant Journal, 13, 815–821.
Troggio M, Gleave A, Salvi S, Chagné D, Cestaro A, Kumar S, Crowhurst R N, Gardiner S E. 2012. Apple, from genome to breeding. Tree Genetics & Genomes, 8, 509–529.
Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar S K, Troggio M,  Pruss D, Salvi S, Pindo M, Baldi P, Castelletti S, Cavaiuolo M, Coppola G, Costa F, Cova V, Dal Ri A, Goremykin V, et al. 2010. The genome of the domesticated apple (Malus×domestica Borkh.). Nature Genetics, 42, 833–839.
Voges D, Zwickl P, Baumeister W. 1999. The 26S proteasome: a molecular machine designed for controlled proteolysis. Annual Review of Biochemistry, 68, 1015–1068.
Wang N, Yue Z, Liang D, Ma F. 2014. Genome-wide identification of members in the YTH domain-containing RNA-binding protein family in apple and expression analysis of their responsiveness to senescence and abiotic stresses. Gene, 538, 292–305.
Watkins J F, Sung P, Prakash L, Prakash S. 1993. The Saccharomyces cerevisiae DNA repair gene RAD23 encodes a nuclear protein containing a ubiquitin-like domain required for biological function. Molecular and Cellular Biology, 13, 7757–7765.
Zhang X, Garreton V, Chua N H. 2005. The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes & Development, 19, 1532–1543.
Zuo Z, Mahajan P B. 2005. Recombinant expression of maize nucleotide excision repair protein Rad23 in Escherichia coli. Protein Expression and Purification, 41, 287–297.
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