Welcome to Acta Agronomica Sinica,

Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (12): 3224-3237.doi: 10.3724/SP.J.1006.2025.54063

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS • Previous Articles     Next Articles

Genome-wide identification of CEP gene family in potato (Solanum tuberosum L.) and functional analysis of StCEP2 in regulating adventitious root growth and salt tolerance

ZHANG Hui-Min,DANG Ya-Ru,SANG Jia-Nan,JIAO Wen-Jing,SUN Chun-Yi,ZHUANG Jia-Mu,WEI Yu-Shu,ZHANG Chao,TIAN Peng,LIU Bai-Lin,SONG Yin*   

  1. College of Agronomy, Northwest A&F University / State key Laboratory for Crop Stress Resistance and High-Efficiency Production, Yangling 712100, Shaanxi, China
  • Received:2025-05-19 Revised:2025-09-10 Accepted:2025-09-10 Online:2025-12-12 Published:2025-09-25
  • Contact: 宋银, E-mail: yin.song@nwafu.edu.cn E-mail:zhanghuimin2022@nwafu.edu.cn
  • Supported by:
    This study was supported by the National Key R&D Program of China (2022YFF1002700), the Key R&D Program in Shaanxi Province (2021LLRH-07 and 2024NC-YBXM-002), and the Undergraduate Training Program for Innovation and Entrepreneurship (S202410712556).

Abstract:

C-terminally encoded peptide (CEP) genes encode a class of secreted small peptides characterized by conserved structural domains near the C-terminus. These genes form a multi-member family that plays crucial roles in regulating various physiological processes in plants, including root development, nitrogen uptake, and responses to environmental stresses. In this study, members of the CEP gene family in potato (Solanum tuberosum, StCEP) were identified and analyzed for their physicochemical properties, conserved motifs, phylogenetic relationships, and promoter cis-acting elements. Expression patterns of StCEP genes were examined across different potato tissues and under various environmental conditions using RNA-seq data. Additionally, the function of salt-induced StCEP genes was validated through exogenous application of synthetic StCEP peptides. A total of 11 StCEP genes were identified in the potato genome, distributed across four chromosomes. The encoded StCEP proteins contained between 1 and 9 CEP motifs, with variability in motif number among members. Phylogenetic analysis revealed that StCEP family members clustered with CEP genes from Arabidopsis thaliana and Solanum lycopersicum, forming two major clades comprising 21 and 26 members, respectively. Synteny analysis showed one syntenic gene pair between potato and A. thaliana, and 12 syntenic pairs between potato and S. lycopersicum. Promoter analysis indicated that StCEP genes are primarily regulated by light-responsive, hormone-responsive, developmental, and stress-related cis-elements. Expression profiling revealed that StCEP genes exhibit tissue-specific expression and are responsive to nitrogen availability, phytohormones (BAP, IAA, GA3, and ABA), and both biotic (e.g., Phytophthora infestans, BABA, BTH) and abiotic (e.g., NaCl) stress factors. Furthermore, exogenous application of the StCEP2 peptide promoted adventitious root formation and enhanced salt tolerance in potato plantlets under in vitro conditions. This study offers valuable insights into the functional roles of StCEP genes in regulating plant development and responses to environmental stress, laying a foundation for future functional genomics and crop improvement research.

Key words: potato, CEP peptide, exogenous peptide assay, adventitious root growth, salt-stress tolerance

[1] Matsubayashi Y. Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol, 2014, 65: 385–413.
[2] Tavormina P, De Coninck B, Nikonorova N, De Smet I, Cammue B P A. The plant peptidome: an expanding repertoire of structural features and biological functions. Plant Cell, 2015, 27: 2095–2118.
[3] Olsson V, Joos L, Zhu S S, Gevaert K, Butenko M A, De Smet I. Look closely, the beautiful may be small: precursor-derived peptides in plants. Annu Rev Plant Biol, 2019, 70: 153–186.
[4] Hou S G, Liu D R, He P. Phytocytokines function as immunological modulators of plant immunity. Stress Biol, 2021, 1: 8.
[5] 吕倩雯, 杨永芳. 植物小肽信号生物学功能及其在作物改良中研究进展. 遗传, 2023, 45: 813–828.
Lyu Q W, Yang Y F. The biological functions of peptide signaling in plant and the advances on its utilization for crop improvement. Hereditas (Beijing), 2023, 45: 813–828 (in Chinese with English abstract).
[6] Tan W Y, Nian H, Tran L P, Jin J, Lian T X. Small peptides: novel targets for modulating plant-rhizosphere microbe interactions. Trends Microbiol, 2024, 32: 1072–1083.
[7] Zhang Y W, Duan X L, Xie Y M, Xuan W. Uncovering the function of peptides: bridging hormone signaling, microbial interactions, and root development in plants. New Crops, 2024, 1: 100011.
[8] Ji C, Li H, Zhang Z L, Peng S Y, Liu J P, Zhou Y, Yang Y X, Han H B. The power of small signaling peptides in crop and horticultural plants. Crop J, 2025, 13: 656–667.
[9] Xiao F, Zhou H P, Lin H H. Decoding small peptides: regulators of plant growth and stress resilience. J Integr Plant Biol, 2025, 67: 596–631.
[10] Zhang Z, Han H, Zhao J, Liu Z, Deng L, Wu L, Niu J, Guo Y, Wang G, Gou X, et al. Peptide hormones in plants. Mol Hortic, 2025, 5: 7.
[11] Ohyama K, Ogawa M, Matsubayashi Y. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J, 2008, 55: 152–160.
[12] Delay C, Imin N, Djordjevic M A. CEP genes regulate root and shoot development in response to environmental cues and are specific to seed plants. J Exp Bot, 2013, 64: 5383–5394.
[13] Roberts I, Smith S, De Rybel B, Van Den Broeke J, Smet W, De Cokere S, Mispelaere M, De Smet I, Beeckman T. The CEP family in land plants: evolutionary analyses, expression studies, and role in Arabidopsis shoot development. J Exp Bot, 2013, 64: 5371–5381.
[14] Sui Z P, Wang T Y, Li H J, Zhang M, Li Y Y, Xu R B, Xing G F, Ni Z F, Xin M M. Overexpression of peptide-encoding OsCEP6.1 results in pleiotropic effects on growth in rice (O. sativa). Front Plant Sci, 2016, 7: 228.
[15] de Bang T C, Lundquist P K, Dai X B, Boschiero C, Zhuang Z H, Pant P, Torres-Jerez I, Roy S, Nogales J, Veerappan V, et al. Genome-wide identification of Medicago peptides involved in macronutrient responses and nodulation. Plant Physiol, 2017, 175: 1669–1689.
[16] 曾祥翠, 杨永念, 李如月, 蒋学乾, 蒋旭, 徐嫣然, 刘忠宽, 龙瑞才, 康俊梅, 杨青川, 等. 紫花苜蓿MsCEP基因家族的鉴定及其调控根系生长发育功能的分析. 中国农业科学, 2024, 57: 4839–4853.
Zeng X C, Yang Y N, Li R Y, Jiang X Q, Jiang X, Xu Y R, Liu Z K, Long R C, Kang J M, Yang Q C, et al. Identification of alfalfa (Medicago sativa) MsCEP genes and functional analysis of its regulation in root growth and development. Sci Agric Sin, 2024, 57: 4839–4853 (in Chinese with English abstract).
[17] Li R, An J P, You C X, Shu J, Wang X F, Hao Y J. Identification and expression of the CEP gene family in apple (Malus × domestica). J Integr Agric, 2018, 17: 348–358.
[18] Xu R B, Li Y F, Sui Z P, Lan T Y, Song W J, Zhang M, Zhang Y R, Xing J W. A C-terminal encoded peptide, ZmCEP1, is essential for kernel development in maize. J Exp Bot, 2021, 72: 5390–5406.
[19] Zhang L, Ren Y, Xu Q, Wan Y M, Zhang S Z, Yang G D, Huang J G, Yan K, Zheng C C, Wu C G. SiCEP3, a C-terminally encoded peptide from Setaria italica, promotes ABA import and signaling. J Exp Bot, 2021, 72: 6260–6273.
[20] Liu Y T, Zuo T T, Qiu Z W, Zhuang K Q, Hu S P, Han H B. Genome-wide identification reveals the function of CEP peptide in cucumber root development. Plant Physiol Biochem, 2021, 169: 119–126.
[21] Lebedeva M A, Gancheva M S, Kulaeva O A, Zorin E A, Dobychkina D A, Romanyuk D A, Sulima A S, Zhukov V A, Lutova L A. Identification and expression analysis of the C-TERMINALLY ENCODED PEPTIDE family in Pisum sativum L. Int J Mol Sci, 2022, 23: 14875.
[22] Qiu Z W, Zhuang K Q, Liu Y T, Ge X M, Chen C, Hu S P, Han H B. Functional characterization of C-TERMINALLY ENCODED PEPTIDE (CEP) family in Brassica rapa L. Plant Signal Behav, 2022, 17: 2021365.
[23] Liu D, Shen Z P, Zhuang K Q, Qiu Z W, Deng H M, Ke Q L, Liu H J, Han H B. Systematic annotation reveals CEP function in tomato root development and abiotic stress response. Cells, 2022, 11: 2935.
[24] Xu K X, Tian D D, Wang T J, Zhang A J, Elsadek M A Y, Liu W H, Chen L P, Guo Y F. Small secreted peptides (SSPs) in tomato and their potential roles in drought stress response. Mol Hortic, 2023, 3: 17.
[25] Pan X L, Deng Z C, Wu R R, Yang Y L, Akher S A, Li W, Zhang Z L, Guo Y F. Identification of CEP peptides encoded by the tobacco (Nicotiana tabacum) genome and characterization of their roles in osmotic and salt stress responses. Plant Physiol Biochem, 2024, 209: 108525.
[26] Mei Z Y, Li B, Zhu S H, Li Y, Yao J B, Pan J W, Zhang Y S, Chen W. A genome-wide analysis of the CEP gene family in cotton and a functional study of GhCEP46-D05 in plant development. Int J Mol Sci, 2024, 25: 4231.
[27] Taleski M, Jin M, Chapman K, Taylor K, Winning C, Frank M, Imin N, Djordjevic M A. CEP hormones at the nexus of nutrient acquisition and allocation, root development, and plant-microbe interactions. J Exp Bot, 2024, 75: 538–552.
[28] Imin N, Mohd-Radzman N A, Ogilvie H A, Djordjevic M A. The peptide-encoding CEP1 gene modulates lateral root and nodule numbers in Medicago truncatula. J Exp Bot, 2013, 64: 5395–5409.
[29] Zhu F G, Deng J, Chen H, Liu P, Zheng L H, Ye Q Y, Li R, Brault M, Wen J Q, Frugier F, et al. A CEP peptide receptor-like kinase regulates auxin biosynthesis and ethylene signaling to coordinate root growth and symbiotic nodulation in Medicago truncatula. Plant Cell, 2020, 32: 2855–2877.
[30] Zhu F G, Ye Q Y, Chen H, Dong J L, Wang T. Multigene editing reveals that MtCEP1/2/12 redundantly control lateral root and nodule number in Medicago truncatula. J Exp Bot, 2021, 72: 3661–3676.
[31] Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science, 2014, 346: 343–346.
[32] Nadiatul A Mohd-Radzman C L. Different pathways act downstream of the CEP peptide receptor CRA2 to regulate lateral root and nodule development. Plant Physiol, 2016, 171: 2536–2548.
[33] Luo Z P, Wang J, Li F Y, Lu Y T, Fang Z J, Fu M D, Mysore K S, Wen J Q, Gong J M, Murray J D, et al. The small peptide CEP1 and the NIN-like protein NLP1 regulate NRT2.1 to mediate root nodule formation across nitrate concentrations. Plant Cell, 2023, 35: 776–794.
[34] Roy S, Griffiths M, Torres-Jerez I, Sanchez B, Antonelli E, Jain D, Krom N, Zhang S L, York L M, Scheible W R, et al. Application of synthetic peptide CEP1 increases nutrient uptake rates along plant roots. Front Plant Sci, 2021, 12: 793145.
[35] Hsieh Y H, Wei Y H, Lo J C, Pan H Y, Yang S Y. Arbuscular mycorrhizal symbiosis enhances tomato lateral root formation by modulating CEP2 peptide expression. New Phytol, 2022, 235: 292–305.
[36] Smith S, Zhu S S, Joos L, Roberts I, Nikonorova N, Vu L D, Stes E, Cho H, Larrieu A, Xuan W, et al. The CEP5 peptide promotes abiotic stress tolerance, as revealed by quantitative proteomics, and attenuates the AUX/IAA equilibrium in Arabidopsis. Mol Cell Proteom, 2020, 19: 1248–1262.
[37] Rzemieniewski J, Leicher H, Lee H K, Broyart C, Nayem S, Wiese C, Maroschek J, Camgöz Z, Olsson Lalun V, Djordjevic M A, et al. CEP signaling coordinates plant immunity with nitrogen status. Nat Commun, 2024, 15: 10686.
[38] Wang X Y, Yu W L, Yuan Q, Chen X Y, He Y X, Zhou J G, Xun Q Q, Wang G D, Li J, Meng X Z. The pathogen-induced peptide CEP14 is perceived by the receptor-like kinase CEPR2 to promote systemic disease resistance in Arabidopsis. Plant Physiol, 2024, 197: kiae549.
[39] 徐建飞, 金黎平. 马铃薯遗传育种研究: 现状与展望. 中国农业科学, 2017, 50: 990–1015.
Xu J F, Jin L P. Advances and perspectives in research of potato genetics and breeding. Sci Agric Sin, 2017, 50: 990–1015 (in Chinese with English abstract).
[40] Qu L, Huang X Q, Su X, Zhu G Q, Zheng L L, Lin J, Wang J W, Xue H W. Potato: from functional genomics to genetic improvement. Mol Hortic, 2024, 4: 34.
[41] 赵朋, 陈广侠, 张宴萍, 杨晓慧, 刘芳, 董道峰. 马铃薯苗期耐碱性鉴定方法及86份种质资源耐碱性综合评价. 作物学报, 2023, 49: 923–2934.
Zhao P, Chen G X, Zhang Y P, Yang X H, Liu F, Dong D F. Alkaline tolerance identification method of potato seedlings and comprehensive assessment of alkaline tolerance of 86 kinds of potato germplasms. Acta Agron Sin, 2023, 49: 2923–2934 (in Chinese with English abstract).
[42] Ogilvie H A, Imin N, Djordjevic M A. Diversification of the C-TERMINALLY ENCODED PEPTIDE (CEP) gene family in angiosperms, and evolution of plant-family specific CEP genes. BMC Genomics, 2014, 15: 870.
[43] Shen Z P, Zuo T T, Xia H L, Ai S C, Tao Q, Zeng C, Guo X P, Han H B. Synthetic CsCEP3 peptide attenuates salinity stress via ROS and ABA signaling in cucumber primary root. Horticulturae, 2023, 9: 921.
[44] Aggarwal S, Rathore R S, Rakhi R, Kumari S, Singla-Pareek S L, Mustafiz A. OsCEP8-mediated abiotic stress response is associated with auxin and sugar homeostasis in plants. Environ Exp Bot, 2025, 229: 106082.
[45] Chen C J, Wu Y, Li J W, Wang X, Zeng Z H, Xu J, Liu Y L, Feng J T, Chen H, He Y H, et al. TBtools-II: a “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant, 2023, 16: 1733–1742.
[46] Tiwari J K, Buckseth T, Zinta R, Saraswati A, Singh R K, Rawat S, Dua V K, Chakrabarti S K. Transcriptome analysis of potato shoots, roots and stolons under nitrogen stress. Sci Rep, 2020, 10: 1152.
[47] Jing Q K, Hou H L, Meng X K, Chen A R, Wang L X, Zhu H S, Zheng S, Lyu Z Y, Zhu X B. Transcriptome analysis reveals the proline metabolic pathway and its potential regulation TF-hub genes in salt-stressed potato. Front Plant Sci, 2022, 13: 1030138.
[48] Taleski M, Imin N, Djordjevic M A. CEP peptide hormones: key players in orchestrating nitrogen-demand signalling, root nodulation, and lateral root development. J Exp Bot, 2018, 69: 1829–1836.
[49] Roberts I, Smith S, Stes E, De Rybel B, Staes A, van de Cotte B, Njo M F, Dedeyne L, Demol H, Lavenus J, et al. CEP5 and XIP1/CEPR1 regulate lateral root initiation in Arabidopsis. J Exp Bot, 2016, 67: 4889–4899.
[1] ZHUO Feng-Qi, TANG Zhen-San, LEI Yu-Jun, CHENG Li-Xiang, ZHAO Tian-Tian, LYU Tai, YANG Chen, ZHANG Feng. Screening of low glycemic potato varieties (lines) based on cooking methods and regeneration temperature [J]. Acta Agronomica Sinica, 2025, 51(9): 2538-2546.
[2] ZHU Jin-Cheng, YANG Qiu-Hua, CHENG Li-Xiang, LI Wen-Li, SHI Ming-Ming, LI Hui-Xia, ZHANG Feng. Screening of potato germplasm for resistance to Meloidogyne incognita and analysis of related physiological responses [J]. Acta Agronomica Sinica, 2025, 51(9): 2307-2317.
[3] YIN Li-Na, ZHANG Rui, CHEN Guo-Huan, BAI Lei, LI Jun, GUO Hua-Chun, YANG Fang. Comparison of wound healing capacity of tubers of different potato varieties [J]. Acta Agronomica Sinica, 2025, 51(9): 2399-2411.
[4] ZHANG Hai-Yan, XIE Bei-Tao, DONG Shun-Xu, ZHANG Li-Ming, DUAN Wen-Xue. Effects of different types and ratios of water-soluble fertilizers on the yield and quality of table-use sweet potato [Ipomoea batatas (L.) Lam.] under drip irrigation [J]. Acta Agronomica Sinica, 2025, 51(9): 2485-2500.
[5] JIA Xiao-Xia, QI En-Fang, WEN Guo-Hong, MA Sheng, HUANG Wei, LYU He-Ping, LI Jian-Wu, QU Ya-Ying, DING Ning. Establishment of regeneration system and creation of glufosinate-resistant germplasm for early-mid maturing potato ‘Longshu 20’ [J]. Acta Agronomica Sinica, 2025, 51(9): 2285-2294.
[6] LI Qiu-Yun, LI Shi-Gui, FAN Jun-Liang, LIU Hao-Tian, ZHAO Xiao-Bin, LYU Shuo, WANG Yan-Hao, YUE Yun, ZHANG Ning, SI Huai-Jun. Effects of ionic zinc and nano-zinc on physiological characteristics, yield, and quality of potato [J]. Acta Agronomica Sinica, 2025, 51(7): 1838-1849.
[7] YIN Yu-Meng, WANG Yan-Nan, KANG Zhi-He, QIAO Shou-Chen, BIAN Qian-Qian, LI Ya-Wei, CAO Guo-Zheng, ZHAO Guo-Rui, XU Dan-Dan, YANG Yu-Feng. Cloning and functional analysis of glutathione S-transferase gene IbGSTU7 in sweetpotato [J]. Acta Agronomica Sinica, 2025, 51(7): 1736-1746.
[8] SHAO Shun-Wei, CHEN Zhuo, LAN Zhen-Dong, CAI Xing-Kui, ZOU Hua-Fen, LI Chen-Xi, TANG Jing-Hua, ZHU Xi, ZHANG Yu, DONG Jian-Ke, JIN Hui, SONG Bo-Tao. QTL mapping of tuber eye depth based on BSA-seq technique [J]. Acta Agronomica Sinica, 2025, 51(7): 1725-1735.
[9] YANG Shuang, BAI Lei, GUO Hua-Chun, MIAO Ya-Sheng, LI Jun. Morphological characteristics, types, and developmental process of potato leaf trichomes [J]. Acta Agronomica Sinica, 2025, 51(6): 1582-1598.
[10] XU Jie, XIA Lu-Lu, TANG Zhen-San, LI Wen-Li, ZHAO Tian-Tian, CHENG Li-Xiang, ZHANG Feng. Odor quality analysis of potato tuber after steaming and baking [J]. Acta Agronomica Sinica, 2025, 51(5): 1409-1420.
[11] ZHAO Xi-Juan, ZHANG Fan, LIU Sheng-Xuan, QIN Jun, CHEN Hui-Lan, LIN Yuan, LUO Hong-Bing, LIU Yi, SONG Bo-Tao, HU Xin-Xi, WANG En-Shuang. Optimization of extraction methods for four endogenous hormones in potatoes and analysis of their content during the process of releasing dormancy in tubers [J]. Acta Agronomica Sinica, 2025, 51(4): 1050-1060.
[12] YANG Xin-Yue, XIAO Ren-Hao, ZHANG Lin-Xi, TANG Ming-Jun, SUN Guang-Yan, DU Kang, LYU Chang-Wen, TANG Dao-Bin, WANG Ji-Chun. Effects of waterlogging at different growth stages on the stress-resistance physiological characteristics and yield formation of sweet potato [J]. Acta Agronomica Sinica, 2025, 51(3): 744-754.
[13] SU Ming, WU Jia-Rui, HONG Zi-Qiang, LI Fan-Guo, ZHOU Tian, WU Hong-Liang, KANG Jian-Hong. Response of potato tuber starch formation and yield to phosphorus fertilizer reduction in the semi-arid region of Northwest China [J]. Acta Agronomica Sinica, 2025, 51(3): 713-727.
[14] HUO Ru-Xue, GE Xiang-Han, SHI Jia, LI Xue-Rui, DAI Sheng-Jie, LIU Zhen-Ning, LI Zong-Yun. Functional analysis of the sweetpotato histidine kinase protein IbHK5 in response to drought and salt stresses [J]. Acta Agronomica Sinica, 2025, 51(3): 650-666.
[15] WANG Yu-Xin, CHEN Tian-Yu, ZHAI Hong, ZHANG Huan, GAO Shao-Pei, HE Shao-Zhen, ZHAO Ning, LIU Qing-Chang. Cloning and characterization of drought tolerance function of kinase gene IbHT1 in sweetpotato [J]. Acta Agronomica Sinica, 2025, 51(2): 301-311.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
No Suggested Reading articles found!