Please wait a minute...
Journal of Integrative Agriculture  2018, Vol. 17 Issue (2): 348-358    DOI: 10.1016/S2095-3119(17)61653-8
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Identification and expression of the CEP gene family in apple (Malus×domestica)
LI Rui1, AN Jian-ping1, YOU Chun-xiang1, SHU Jing2, WANG Xiao-fei1, HAO Yu-jin
1 National Key Laboratory of Crop Biology, National Research Center for Apple Engineering and Technology/College of Horticulture Science and Engineering, Shandong Agricultural University, Tai’an 271018, P.R.China
2 Shandong Agriculture and Engineering University, Jinan 251100, P.R.China
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
Abstract  Plant peptide hormones play important roles in plant growth and development.  Among these hormones, the C-TERMINALLYENCODED PEPTIDE (CEP) belongs to a newly found peptide family that regulates root development in Arabidopsis as well as in other species.  However, nothing is known about the CEP genes in apple (Malus×domestica, MdCEP).  In this study, a total of 27 apple CEP genes were identified through a genome-wide analysis and were phylogenetically divided into three classes (I, II and III).  The predicted MdCEP genes were distributed across 10 of 17 chromosomes with different densities.  Next, the gene structures and motif compositions of the MdCEP genes were analyzed.  Subsequently, the expression analysis suggested that the MdCEP genes were highly activated in roots and that MdCEP23 may play an important role in regulating the growth and development of roots.  Moreover, all of the MdCEP genes were responsive to multiple abiotic stresses, indicating that MdCEP genes may be involved with various aspects of physiological processes in apple.  Nearly one-third of MdCEP genes had a significant response to low nitrogen treatment.  Most of the MdCEP genes were up-regulated under stress, including mannitol, polyethylene glycol (PEG) and abscisic acid (ABA), suggesting that MdCEP genes may be involved in the drought stress response.  This study provides insight into the putative functions of the MdCEP genes using a genome-wide analysis of the CEP gene family. 
Keywords:   peptide signals        CEP gene family        expression analysis        apple  
Received: 02 February 2017   Accepted:
Fund: 

We thank the earmarked fund for the China Agriculture Research System (CARS-28), the National Natural Science Foundation of China (31471854, 31601742), the earmarked fund for the Shandong Province Agriculture Research, China (SDAIT-06-03), the Natural Science Foundation of Shandong Province, China (ZR2011CQ007).

Corresponding Authors:  Correspondence HAO Yu-jin, E-mail: haoyujin@sdau.edu.cn; WANG Xiao-fei, E-mail: xfwang2004@163.com    
About author:  LI Rui,E-mail: liruisdau@163.com

Cite this article: 

LI Rui, AN Jian-ping, YOU Chun-xiang, SHU Jing, WANG Xiao-fei, HAO Yu-jin . 2018. Identification and expression of the CEP gene family in apple (Malus×domestica). Journal of Integrative Agriculture, 17(2): 348-358.

An J P, Li H H, Song L Q, Su L, Liu X, You C X, Hao Y J. 2016. The molecular cloning and functional characterization of MdMYC2, a bHLH transcription factor in apple. Plant Physiology and Biochemistry, 108, 24-31.

Bryan A C, Obaidi A, Wierzba M, Tax F E. 2012. XYLEM INTERMIXED WITH PHLOEM1, a leucine-rich repeat receptor-like kinase required for stem growth and vascular development in Arabidopsis thaliana. Planta, 235, 111-122.

Butenko M A, Vie A K, Brembu T, Aalen R B, Bones A M. 2009. Plant peptides in signalling, looking for new partners. Trends in Plant Science, 14, 255-263.

Cannon S B, Mitra A, Baumgarten A, Young N D, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology, 4, 10.

Cao Z H, Zhang S Z, Wang R K, Zhang R F, Hao Y J. 2013. Genome wide analysis of the apple myb transcription factor family allows the identification of MdoMYB121 gene confering abiotic stress tolerance in plants. PLOS ONE, 8, e69955.

Chen W, Provart N J, Glazebrook J, Katagiri F, Chang H S, Eulgem T, Mauch F, Luan S, Zou G, Whitham S A, Budworth P R, Tao Y, Xie Z,  Chen X, Lam S, Kreps J A, Harper J F, Ammour A S, Mani B M, Heinlein M, Kobayashi K, Hohn T, Dangl J L, Wang X, Zhua T, et al. 2002. Expression profile matrix of Arabidopsis transcription factor genes suggests their putative functions in response to environmental stresses. The Plant Cell, 14, 559–574.

Czyzewicz N, Yue K, Beeckman T, De Smet I. 2013. Message in a bottle, small signalling peptide outputs during growth and development. Journal of Experimental Botany, 64, 5281–5296.

Delay C, Imin N, Djordjevic M A. 2013. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. Journal of Experimental Botany, 64, 5383–5394.

Dimick P S, Hoskin J C. 1983. Review of apple flavor - state of the art. Critical Reviews in Food Science and Nutrition, 18, 387–409.

Du C, Li X, Chen J, Chen W, Li B, Li C, Wang L, Li J, Zhao X, Lin J. 2016. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 113, 8326–8334.

Edgar R C. 2004. MUSCLE, multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.

Etchells J P, Turner S R. 2010. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development, 137, 767–774.

Glazebrook J. 2001. Genes controlling expression of defense responses in Arabidopsis - 2001 status. Current Opinion in Plant Biology, 4, 301–308.

Hall B G. 2013. Building phylogenetic trees from molecular data with MEGA. Molecular Biology and Evolution, 30, 1229–1235.

Hirakawa Y, Kondo Y, Fukuda H. 2010. Establishment and maintenance of vascular cell communities through local signaling. Current Opinion in Plant Biology, 14, 17–23.

Imin N, Mohd-Radzman N A, Ogilvie H A, Djordjevic M A. 2013. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. Journal of Experimental Botany, 64, 5395–5409.

Katsir L, Davies K A, Bergmann D C, Laux T. 2011. Peptide signaling in plant development. Current Biology, 21, 356–364.

Kidokoro S, Watanabe K, Ohori T, Moriwaki T, Maruyama K, Mizoi J, Myint P S H N, Fujita Y, Sekita S, Shinozaki K. 2015. Soybean DREB1/CBF-type transcription factors function in heat and drought as well as cold stress-responsive gene expression. The Plant Journal, 81, 505–518.

Kondo Y, Hirakawa Y, Kieber J J, Fukuda H. 2011. CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling. Plant & Cell Physiology, 52, 37–48.

Lee J S, De Smet I. 2016. Fine-tuning development through antagonistic peptides, an emerging theme. Trends in Plant Science, 21, 991–993.

Lee J S, Hnilova M, Maes M, Lin Y C, Putarjunan A, Han S K, Avila J, Torii K U. 2015. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature, 522, 439–443.

Lee S Y, Chang S S, Shin J H, Kang D H. 2007. Membrane filtration method for enumeration and isolation of Alicyclobacillus spp. from apple juice. Letters in Applied Microbiology, 45, 540–546.

Li X, Yin X, Wang H, Li J, Guo C. 2015. Genome-wide identification and analysis of the apple (Malus×domestica Borkh.) TIFY gene family. Tree Genetics & Genomes, 11, 1–13.

Mohd-Radzman N A, Binos S, Truong T T, Imin N, Mariani M, Djordjevic M A. 2015. Novel MtCEP1 peptides produced

in vivo differentially regulate root development in Medicago truncatula. Journal of Experimental Botany, 66, 5289–5300.

Mohd-Radzman N A, Laffont C. 2016. Different Pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development. Plant Physiology, 171, 2536–2548.

Murphy E, Smith S, De Smet I. 2012. Small signaling peptides in Arabidopsis development, how cells communicate over a short distance. The Plant Cell, 24, 3198–3217.

Ogilvie H A, Imin N, Djordjevic M A. 2014. Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genomics, 15, 870.

Ohyama K, Ogawa M, Matsubayashi Y. 2008. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. The Plant Journal, 55, 152–160.

Okamoto S, Tabata R, Matsubayashi Y. 2016. Long-distance peptide signaling essential for nutrient homeostasis in plants. Current Opinion in Plant Biology, 34, 35–40.

Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W, De Cokere S, Mispelaere M, De Smet I, Beeckman T. 2013. The CEP family in land plants, evolutionary analyses, expression studies, and role in Arabidopsis shoot development. Journal of Experimental Botany, 64, 5371–5381.

Roberts I, Smith S, Stes E, De Rybel B, Staes A, Van De Cotte B, Njo M F, Dedeyne L, Demol H, Lavenus J, Audenaert D, Gevaert K, Beeckman T, Smet L D. 2016. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. Journal of Experimental Botany, 67, 4889–4899.

Song W, Liu L, Wang J, Wu Z, Zhang H, Tang J, Lin G, Wang Y, Wen X, Li W, Han Z, Guo H, Chai J. 2016. Signature motif-guided identification of receptors for peptide hormones essential for root meristem growth. Cell Research, 26, 674–685.

Su H, Zhang S, Yuan X, Chen C, Wang X F, Hao Y J. 2013. Genome-wide analysis and identification of stress-responsive genes of the NAM-ATAF1, 2-CUC2 transcription factor family in apple. Plant Physiology and Biochemistry, 71, 11–21.

Sui Z, Wang T, Li H, Zhang M, Li Y, Xu R, Xing G, Ni Z, Xin M. 2016. Overexpression of peptide-encoding OsCEP6.1 results in pleiotropic effects on growth in rice (O. sativa). Frontiers in Plant Science, 7, 228.

Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science, 346, 343–346.

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.

Wang J, Guo M Z, Xing L L. 2012. FastJoin, an improved neighbor-joining algorithm. Genetics and Molecular Research, 11, 1909–1922.

Wang X, Zhang S, Su L, Liu X, Hao Y. 2013. A genome-wide analysis of the LBD (LATERAL ORGAN BOUNDARIES Domain) gene family in Malus domestica with a functional characterization of MdLBD11. PLOS ONE, 8, e57044.

Xu J, Xing S, Zhang Z, Chen X, Wang X. 2016. Genome-wide identification and expression analysis of the tubby-like protein family in the Malus domestica genome. Frontiers in Plant Science, 7, e25198.

Zhao T, Liang D, Wang P, Liu J, Ma F. 2012. Genome-wide analysis and expression profiling of the DREB transcription factor gene family in Malus under abiotic stress. Molecular Genetics and Genomics, 287, 423–436.
 
[1] ZHANG Qiang-qiang, GAO Xi-xi, Nazir Muhammad ABDULLAHI, WANG Yue, HUO Xue-xi. Asset specificity and farmers’ intergenerational succession willingness of apple management[J]. >Journal of Integrative Agriculture, 2023, 22(8): 2553-2566.
[2] WANG Chu-kun, ZHAO Yu-wen, HAN Peng-liang, YU Jian-qiang, HAO Yu-jin, XU Qian, YOU Chun-xiang, HU Da-gang. Auxin response factor gene MdARF2 is involved in ABA signaling and salt stress response in apple[J]. >Journal of Integrative Agriculture, 2022, 21(8): 2264-2274.
[3] XUAN Zhi-you, ZHANG Song, LI Ping, YANG Fang-yun, CHEN Hong-ming, LIU Ke-hong, ZHOU Yan, LI Zhong-an, ZHOU Chang-yong, CAO Meng-ji. Apple stem grooving virus is associated with leaf yellow mottle mosaic disease on Citrus grandis cv. Huangjinmiyou in China[J]. >Journal of Integrative Agriculture, 2022, 21(7): 2031-2041.
[4] HU Ling-yu, YUE Hong, ZHANG Jing-yun, LI Yang-tian-su, GONG Xiao-qing, ZHOU Kun, MA Feng-wang. Overexpression of MdMIPS1 enhances drought tolerance and water-use efficiency in apple[J]. >Journal of Integrative Agriculture, 2022, 21(7): 1968-1981.
[5] WANG Er-peng, AN Ning, GENG Xian-hui, Zhifeng GAO, Emmanuel KIPROP. Consumers’ willingness to pay for ethical consumption initiatives on e-commerce platforms[J]. >Journal of Integrative Agriculture, 2021, 20(4): 1012-1020.
[6] HU Guo-jun, DONG Ya-feng, ZHANG Zun-ping, FAN Xu-dong, REN Fang. Molecular characterization of Apple necrotic mosaic virus identified in crabapple (Malus spp.) tree of China[J]. >Journal of Integrative Agriculture, 2019, 18(3): 698-704.
[7] LI Liu, ZHENG Meng-meng, MA Xiao-fang, LI Yuan-jun, LI Qing-yu, WANG Guo-ping, HONG Ni . Molecular, serological and biological characterization of a novel Apple stem pitting virus strain from a local pear variety grown in China[J]. >Journal of Integrative Agriculture, 2019, 18(11): 2549-2560.
[8] LIU Xuan, LIANG Wei, LI Yu-xing, LI Ming-jun, MA Bai-quan, LIU Chang-hai, MA Feng-wang, LI Cui-ying. Transcriptome analysis reveals the effects of alkali stress on root system architecture and endogenous hormones in apple rootstocks[J]. >Journal of Integrative Agriculture, 2019, 18(10): 2264-2271.
[9] ZHANG Lei, ZHENG Xing-wei, QIAO Lin-yi, QIAO Ling, ZHAO Jia-jia, WANG Jian-ming, ZHENG Jun. Analysis of three types of resistance gene analogs in PmU region from Triticum urartu[J]. >Journal of Integrative Agriculture, 2018, 17(12): 2601-2611.
[10] TANG Yu-jin, WANG Qian, XUE Jing-yi, LI Yan, LI Rui-min, Steve Van Nocker, WANG Yue-jin, ZHANG Chao-hong. Gene cloning and expression analyses of WBC genes in the developing grapevine seeds[J]. >Journal of Integrative Agriculture, 2018, 17(06): 1348-1359.
[11] YU Tong-ying, LU Ming-xing, CUI Ya-dong. Characterization of T-complex polypeptide 1 (TCP-1) from the Chilo suppressalis HSP60 family and its expression in response to temperature stress[J]. >Journal of Integrative Agriculture, 2018, 17(05): 1032-1039.
[12] WANG Yan-xiu, HU Ya, CHEN Bai-hong, ZHU Yan-fang, Mohammed Mujitaba Dawuda, Sofkova Svetla. Physiological mechanisms of resistance to cold stress associated with 10 elite apple rootstocks[J]. >Journal of Integrative Agriculture, 2018, 17(04): 857-866.
[13] CUI Li, NIU Li-ying, LI Da-jing, LIU Chun-quan, LIU Ying-ping, LIU Chun-ju, SONG Jiang-feng. Effects of different drying methods on quality, bacterial viability and storage stability of probiotic enriched apple snacks[J]. >Journal of Integrative Agriculture, 2018, 17(01): 247-255.
[14] ZHANG Kun-xi, WEN Tian, DONG Jun, MA Feng-wang, BAI Tuan-hui, WANG Kun, LI Cui-ying. Comprehensive evaluation of tolerance to alkali stress by 17 genotypes of apple rootstocks[J]. >Journal of Integrative Agriculture, 2016, 15(7): 1499-1509.
[15] DOU Ling-ling, GUO Ya-ning, Ondati Evans, PANG Chao-you, WEI Heng-ling, SONG Mei-zhen, FAN Shu-li, YU Shu-xun. Identification and expression analysis of group III WRKY transcription factors in cotton[J]. >Journal of Integrative Agriculture, 2016, 15(11): 2469-2480.
No Suggested Reading articles found!