Please wait a minute...
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

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
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:

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:,   

Cite this article: 

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.
[1] CHU Jin-peng, GUO Xin-hu, ZHENG Fei-na, ZHANG Xiu, DAI Xing-long, HE Ming-rong. Effect of delayed sowing on grain number, grain weight, and protein concentration of wheat grains at specific positions within spikes[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2359-2369.
[2] FAN Ting-lu, LI Shang-zhong, ZHAO Gang, WANG Shu-ying, ZHANG Jian-jun, WANG Lei, DANG Yi, CHENG Wan-li. Response of dryland crops to climate change and drought-resistant and water-suitable planting technology: A case of spring maize[J]. >Journal of Integrative Agriculture, 2023, 22(7): 2067-2079.
[3] ZHANG Chong, WANG Dan-dan, ZHAO Yong-jian, XIAO Yu-lin, CHEN Huan-xuan, LIU He-pu, FENG Li-yuan, YU Chang-hao, JU Xiao-tang. Significant reduction of ammonia emissions while increasing crop yields using the 4R nutrient stewardship in an intensive cropping system[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1883-1895.
[4] DU Xiang-bei, XI Min, WEI Zhi, CHEN Xiao-fei, WU Wen-ge, KONG Ling-cong. Raised bed planting promotes grain number per spike in wheat grown after rice by improving spike differentiation and enhancing photosynthetic capacity[J]. >Journal of Integrative Agriculture, 2023, 22(6): 1631-1644.
[5] WU Xian-xin, ZANG Chao-qun, ZHANG Ya-zhao, XU Yi-wei, WANG Shu, LI Tian-ya, GAO Li.

Characterization of wheat monogenic lines with known Sr genes and wheat cultivars for resistance to three new races of Puccinia graminis f. sp. tritici in China [J]. >Journal of Integrative Agriculture, 2023, 22(6): 1740-1749.

[6] DONG Xiu-chun, QIAN Tai-feng, CHU Jin-peng, ZHANG Xiu, LIU Yun-jing, DAI Xing-long, HE Ming-rong. Late sowing enhances lodging resistance of wheat plants by improving the biosynthesis and accumulation of lignin and cellulose[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1351-1365.
[7] ZHANG Zhen-zhen, CHENG Shuang, FAN Peng, ZHOU Nian-bing, XING Zhi-peng, HU Ya-jie, XU Fang-fu, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Effects of sowing date and ecological points on yield and the temperature and radiation resources of semi-winter wheat[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1366-1380.
[8] LI Jiao-jiao, ZHAO Li, LÜ Bo-ya, FU Yu, ZHANG Shu-fa, LIU Shu-hui, YANG Qun-hui, WU Jun, LI Jia-chuang, CHEN Xin-hong. Development and characterization of a novel common wheat–Mexico Rye T1DL·1RS translocation line with stripe rust and powdery mildew resistance[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1291-1307.
[9] ZHAO Xiao-dong, QIN Xiao-rui, LI Ting-liang, CAO Han-bing, XIE Ying-he. Effects of planting patterns plastic film mulching on soil temperature, moisture, functional bacteria and yield of winter wheat in the Loess Plateau of China[J]. >Journal of Integrative Agriculture, 2023, 22(5): 1560-1573.
[10] JIANG Yun, WANG De-li, HAO Ming, ZHANG Jie, LIU Deng-cai.

Development and characterization of wheat–Aegilops kotschyi 1Uk(1A) substitution line with positive dough quality parameters [J]. >Journal of Integrative Agriculture, 2023, 22(4): 999-1008.

[11] Sunusi Amin ABUBAKAR, Abdoul Kader Mounkaila HAMANI, WANG Guang-shuai, LIU Hao, Faisal MEHMOOD, Abubakar Sadiq ABDULLAHI, GAO Yang, DUAN Ai-wang. Growth and nitrogen productivity of drip-irrigated winter wheat under different nitrogen fertigation strategies in the North China Plain[J]. >Journal of Integrative Agriculture, 2023, 22(3): 908-922.
[12] TU Ke-ling, YIN Yu-lin, YANG Li-ming, WANG Jian-hua, SUN Qun. Discrimination of individual seed viability by using the oxygen consumption technique and headspace-gas chromatography-ion mobility spectrometry[J]. >Journal of Integrative Agriculture, 2023, 22(3): 727-737.
[13] TIAN Jin-yu, LI Shao-ping, CHENG Shuang, LIU Qiu-yuan, ZHOU Lei, TAO Yu, XING Zhi-peng, HU Ya-jie, GUO Bao-wei, WEI Hai-yan, ZHANG Hong-cheng. Increasing the appropriate seedling density for higher yield in dry direct-seeded rice sown by a multifunctional seeder after wheat-straw return[J]. >Journal of Integrative Agriculture, 2023, 22(2): 400-416.
[14] Zaid CHACHAR, Siffat Ullah KHAN, ZHANG Xue-huan, LENG Peng-fei, ZONG Na, ZHAO Jun. Characterization of transgenic wheat lines expressing maize ABP7 involved in kernel development[J]. >Journal of Integrative Agriculture, 2023, 22(2): 389-399.
[15] HU Wen-jing, FU Lu-ping, GAO De-rong, LI Dong-sheng, LIAO Sen, LU Cheng-bin. Marker-assisted selection to pyramid Fusarium head blight resistance loci Fhb1 and Fhb2 in a high-quality soft wheat cultivar Yangmai 15[J]. >Journal of Integrative Agriculture, 2023, 22(2): 360-370.
No Suggested Reading articles found!