黑麦活性着丝粒特异反转录转座子的筛选及其对逆境胁迫的响应

doi:10.3864/j.issn.0578-1752.2025.14.002

中国农业科学 ›› 2025, Vol. 58 ›› Issue (14): 2720-2738.doi: 10.3864/j.issn.0578-1752.2025.14.002

• 作物遗传育种·种质资源·分子遗传学 • 上一篇下一篇

黑麦活性着丝粒特异反转录转座子的筛选及其对逆境胁迫的响应

吴翠翠¹(), 王若禹¹, 马驰¹, 何美月¹, 尹晓康¹, 冯佳宜¹, 周宾寒¹, 姜宇凡¹, 金汉炳¹, 赵丽丽¹, 孙吉¹, 方正武¹, 程玲¹, 朱展望², 刘易科², 张迎新¹^,^*(), 王书平¹^,^*()

¹ 长江大学农学院/农业农村部长江中游作物绿色高效生产重点实验室（部省共建），湖北荆州 434025
² 湖北省农业科学院粮食作物研究所，武汉 430064

收稿日期:2025-02-05 接受日期:2025-04-02 出版日期:2025-07-17 发布日期:2025-07-17
通信作者:
张迎新，E-mail：zhangyingxin1985@126.com。
王书平，E-mail：wangshuping2003@126.com
联系方式: 吴翠翠，E-mail：13545425232@163.com。
基金资助:
湖北省重点研发计划(2024BBB004); 植物细胞与染色体工程国家重点实验室开放课题(PCCE-KF-2023-10); 粮食作物种质创新与遗传改良湖北省重点实验室开放课题(2024lzjj15)

Screening of Active Centromeric Retrotransposons of Rye and Their Response to Stress

WU CuiCui¹(), WANG RuoYu¹, MA Chi¹, HE MeiYue¹, YIN XiaoKang¹, FENG JiaYi¹, ZHOU BinHan¹, JIANG YuFan¹, JIN HanBing¹, ZHAO LiLi¹, SUN Ji¹, FANG ZhengWu¹, CHENG Ling¹, ZHU ZhanWang², LIU YiKe², ZHANG YingXin¹^,^*(), WANG ShuPing¹^,^*()

¹ College of Agriculture, Yangtze University/Key Laboratory of Green and Efficient Crop Production in the Middle Reaches of the Yangtze River (Co-Construction by Ministry and Province), Ministry of Agriculture and Rural Affairs, Jingzhou 434025, Hubei
² Institute of Food Crops, Hubei Academy of Agricultural Sciences, Wuhan 430064

Received:2025-02-05 Accepted:2025-04-02 Published:2025-07-17 Online:2025-07-17

摘要/Abstract

摘要：

【目的】着丝粒特异反转录转座子（centromeric retrotransposons，CR）家族在维持禾本科染色体稳定中起着重要的作用。黑麦是小麦遗传改良的优良基因供体，具有抗逆和抗病性强等优良特性，其着丝粒区域富集CR等反转录转座子，筛选具有转座活性的黑麦CR（CR of rye，CRR），并解析其在逆境胁迫下的转录和转座规律，为阐明转座子元件在逆境胁迫下对黑麦基因组稳定性的影响机制提供依据。【方法】运用生物信息学方法对黑麦基因组进行转座子元件从头注释，筛选出具有完整结构的CRR；采用半定量方法筛选出在黑麦栽培品种Secale cereal L. Imperial的叶和根中均高表达的CRR；分别采用实时荧光定量PCR（quantitative real-time PCR，qRT-PCR）、甲基化特异PCR（methylmion specific PCR，MSP）和转座子展示（transposon display，TD）技术对其在盐、ABA、H₂O₂、PEG、低温和高温等胁迫下黑麦幼苗期（两叶一心）叶和根中的表达水平、甲基化水平和转座活性进行分析。【结果】共筛选出17个CRR，其中，有7个具有完整结构（CRR1、CRR2、CRR3、CRR4、CRR5、CRR7和CRR11）；半定量结果显示，CRR2、CRR4和CRR7在黑麦叶和根中的表达量均较高，对其结构进行分析，发现这3个CRR均能编码其转座所需的反转录酶、核酸酶H和整合酶，其中，CRR7还编码Gag蛋白；CRR2、CRR4和CRR7在正常条件下均具有基础水平的转录，逆境胁迫能促进其转录，且对CRR7甲基化水平影响最大，其次是CRR2和CRR4；同时，在逆境胁迫下，CRR2、CRR4和CRR7的拷贝数处于动态变化过程，在不同逆境胁迫下，插入和移出基因组频率不同，但整体表现为移出频率大于插入频率。【结论】CRR的5′LTR和3′LTR序列同源性越高，转录活性越强；具有转座活性的CRR在正常条件下具有基础水平的转录，逆境胁迫可促进其转录和转座，且转座主要受转录后调控机制调控；逆境胁迫下基因组重排是影响其在基因组内拷贝数的主要因素。

关键词: 黑麦, 着丝粒, 转座子元件, 逆境胁迫, 甲基化, 转座活性

Abstract:

【Objective】Centromeric retrotransposons (CR) play an important role in maintaining chromosomal stability of Poaceae species. Rye (Secale cereale L. cv. Imperial), a valuable genetic donor for wheat improvement, showed enhanced stress tolerance and disease resistance, the centromeric regions of which are enriched with CR. Screen active rye specific CR (CR of Rye, CRR) and study their transposition patterns under stress conditions, would help elucidate the mechanisms of the possible influence of transposable elements (TEs) transposition on genome stability of rye under stress conditions. 【Method】To identify intact CRR, the rye genome was subjected to de novo annotation of TEs using bioinformatics tools. Semi-quantitative analysis was applied to screen highly expressed CRR in both leaves and roots of rye. Quantitative real-time PCR (qRT-PCR), methylation-specific PCR (MSP), and transposon display (TD) techniques were used to analyze the expression and methylation level, and transposition activity of the screened CRR in leaves and roots of abiotic stressed rye seedlings (at the one-tip-two-leaf stage), including salt, ABA, H₂O₂, PEG, low temperature, and high temperature. 【Result】Seventeen CRR were identified, and seven have intact structure (CRR1, CRR2, CRR3, CRR4, CRR5, CRR7, and CRR11). Semi-quantitative analysis revealed CRR2, CRR4, and CRR7 were highly expressed in both leaves and roots. Structural analysis of the three CRR indicated that they could encode all the enzymes necessary for TE transposition (reverse transcriptase, ribonuclease H, and integrase), with CRR7 also encoded a Gag protein. Under normal conditions, CRR2, CRR4, and CRR7 were basically expressed, which were upregulated by stress treatments, the methylation level of CRR7 changed most under stressed conditions, followed by CRR2 and CRR4. Additionally, the copy number of the three CRR was dynamically changed under stress conditions. Under different stress conditions, the insertion and excision frequency of CRR was different under different stress conditions, but the overall excision frequency was higher than the insertion frequency.【Conclusion】The higher of the sequence homology between the 5’ and 3’ LTRs of CRR, the higher of the transcriptional activity of CRR; active CRR have basical transcriptional level under normal conditions, the transcription and transposition activity of which were upregulated by stress stimuli, which were primarily regulated by post-transcriptional regulatory mechanisms. Genomic rearrangement might be the main factor affecting the copy number of CRR in stress conditions.

Key words: rye, centromere, transposon element, adversity stress, methylation, transposition activity

吴翠翠, 王若禹, 马驰, 何美月, 尹晓康, 冯佳宜, 周宾寒, 姜宇凡, 金汉炳, 赵丽丽, 孙吉, 方正武, 程玲, 朱展望, 刘易科, 张迎新, 王书平. 黑麦活性着丝粒特异反转录转座子的筛选及其对逆境胁迫的响应[J]. 中国农业科学, 2025, 58(14): 2720-2738.

WU CuiCui, WANG RuoYu, MA Chi, HE MeiYue, YIN XiaoKang, FENG JiaYi, ZHOU BinHan, JIANG YuFan, JIN HanBing, ZHAO LiLi, SUN Ji, FANG ZhengWu, CHENG Ling, ZHU ZhanWang, LIU YiKe, ZHANG YingXin, WANG ShuPing. Screening of Active Centromeric Retrotransposons of Rye and Their Response to Stress[J]. Scientia Agricultura Sinica, 2025, 58(14): 2720-2738.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2025.14.002

https://www.chinaagrisci.com/CN/Y2025/V58/I14/2720

图/表 8

图1

图2

图3

图4

图5

图6

图7

图8

参考文献 50

[1]	SANAN-MISHRA N, ABDUL KADER JAILANI A, MANDAL B, MUKHERJEE S K. Secondary siRNAs in plants: Biosynthesis, various functions, and applications in virology. Frontiers in Plant Science, 2021, 12: 610283.
[2]	HAN M, PERKINS M H, NOVAES L S, XU T, CHANG H. Advances in transposable elements: from mechanisms to applications in mammalian genomics. Frontiers in Genetics, 2023, 14: 1290146.
[3]	HAYWARD A, GILBERT C. Transposable elements. Current Biology, 2022, 32(17): R904-R909.
[4]	MILLER J T, DONG F, JACKSON S A, SONG J, JIANG J. Retrotransposon-related DNA sequences in the centromeres of grass chromosomes. Genetics, 1998, 150(4): 1615-1623. doi: 10.1093/genetics/150.4.1615 pmid: 9832537
[5]	ANANIEV E V, PHILLIPS R L, RINES H W. Chromosome-specific molecular organization of maize (Zea mays L.) centromeric regions. Proceedings of the National Academy of Sciences of the United States of America, 1998, 95(22): 13073-13078.
[6]	ZHONG C X, MARSHALL J B, TOPP C, MROCZEK R, KATO A, NAGAKI K, BIRCHLER J A, JIANG J M, DAWE R K. Centromeric retroelements and satellites interact with maize kinetochore protein CENH₃. The Plant Cell, 2002, 14(11): 2825-2836.
[7]	PIETZENUK B, MARKUS C, GAUBERT H, BAGWAN N, MEROTTO A, BUCHER E, PECINKA A. Recurrent evolution of heat-responsiveness in Brassicaceae COPIA elements. Genome Biology, 2016, 17(1): 209.
[8]	ELLINGHAUS D, KURTZ S, WILLHOEFT U. LTRharvest, an efficient and flexible software for de novo detection of LTR retrotransposons. BMC Bioinformatics, 2008, 9: 18.
[9]	VICIENT C M, CASACUBERTA J M. Impact of transposable elements on polyploid plant genomes. Annals of Botany, 2017, 120(2): 195-207. doi: 10.1093/aob/mcx078 pmid: 28854566
[10]	CAPY P. Classification and nomenclature of retrotransposable elements. Cytogenetic and Genome Research, 2005, 110(1/2/3/4): 457-461.
[11]	LLORENS C, FUTAMI R, COVELLI L, DOMÍNGUEZ-ESCRIBÁ L, VIU J M, TAMARIT D, AGUILAR-RODRÍGUEZ J, VICENTE- RIPOLLES M, FUSTER G, BERNET G P, et al. The Gypsy Database (GyDB) of mobile genetic elements: Release 2.0. Nucleic Acids Research, 2011, 39(Database issue): D70-D74.
[12]	NEUMANN P, NAVRÁTILOVÁ A, KOBLÍŽKOVÁ A, KEJNOVSKÝ E, HŘIBOVÁ E, HOBZA R, WIDMER A, DOLEŽEL J, MACAS J. Plant centromeric retrotransposons: A structural and cytogenetic perspective. Mobile DNA, 2011, 2(1): 4. doi: 10.1186/1759-8753-2-4 pmid: 21371312
[13]	ZHANG Y X, FAN C M, LI S S, CHEN Y H, WANG R R, ZHANG X Q, HAN F P, HU Z M. The diversity of sequence and chromosomal distribution of new transposable element-related segments in the rye genome revealed by FISH and lineage annotation. Frontiers in Plant Science, 2017, 8: 1706. doi: 10.3389/fpls.2017.01706 pmid: 29046683
[14]	NAISH M, ALONGE M, WLODZIMIERZ P, TOCK A J, ABRAMSON B W, SCHMÜCKER A, MANDÁKOVÁ T, JAMGE B, LAMBING C, KUO P, et al. The genetic and epigenetic landscape of the Arabidopsis centromeres. Science, 2021, 374(6569): eabi7489.
[15]	WLODZIMIERZ P, RABANAL F A, BURNS R, NAISH M, PRIMETIS E, SCOTT A, MANDÁKOVÁ T, GORRINGE N, TOCK A J, HOLLAND D, et al. Cycles of satellite and transposon evolution in Arabidopsis centromeres. Nature, 2023, 618(7965): 557-565.
[16]	周芳. 黄瓜着丝粒重复序列的组成与分布分析[D]. 南京: 南京农业大学, 2022.
	ZHOU F. Composition and distribution of centromeric repeats in cucumber[D]. Nanjing: Nanjing Agricultural University, 2022. (in Chinese)
[17]	HEUBERGER M, KOO D H, AHMED H I, TIWARI V K, ABROUK M, POLAND J, KRATTINGER S G, WICKER T. Evolution of Einkorn wheat centromeres is driven by the mutualistic interplay of two LTR retrotransposons. Mobile DNA, 2024, 15(1): 16. doi: 10.1186/s13100-024-00326-9 pmid: 39103880
[18]	SHARMA A, PRESTING G G. Centromeric retrotransposon lineages predate the maize/rice divergence and differ in abundance and activity. Molecular Genetics and Genomics, 2008, 279(2): 133-147. doi: 10.1007/s00438-007-0302-5 pmid: 18000683
[19]	NEUMANN P, YAN H H, JIANG J M. The centromeric retrotransposons of rice are transcribed and differentially processed by RNA interference. Genetics, 2007, 176(2): 749-761. doi: 10.1534/genetics.107.071902 pmid: 17409063
[20]	NEUMANN P, NOVÁK P, HOŠTÁKOVÁ N, MACAS J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mobile DNA, 2019, 10: 1. doi: 10.1186/s13100-018-0144-1 pmid: 30622655
[21]	SU H D, LIU Y L, LIU C, SHI Q H, HUANG Y H, HAN F P. Centromere satellite repeats have undergone rapid changes in polyploid wheat subgenomes. The Plant Cell, 2019, 31(9): 2035-2051. doi: 10.1105/tpc.19.00133 pmid: 31311836
[22]	ROQUIS D, ROBERTSON M, YU L, THIEME M, JULKOWSKA M, BUCHER E. Genomic impact of stress-induced transposable element mobility in Arabidopsis. Nucleic Acids Research, 2021, 49(18): 10431-10447.
[23]	MILYAEVA P A, KUKUSHKINA I V, KIM A I, NEFEDOVA L N. Stress induced activation of LTR retrotransposons in the Drosophila melanogaster genome. Life, 2023, 13(12): 2272.
[24]	International Wheat Genome Sequencing Consortium (IWGSC). Shifting the limits in wheat research and breeding using a fully annotated reference genome. Science, 2018, 361(6403): eaar7191.
[25]	LING H Q, MA B, SHI X L, LIU H, DONG L L, SUN H, CAO Y H, GAO Q, ZHENG S S, LI Y, et al. Genome sequence of the progenitor of wheat A subgenome Triticum urartu. Nature, 2018, 557(7705): 424-428.
[26]	MASCHER M, GUNDLACH H, HIMMELBACH A, BEIER S, TWARDZIOK S O, WICKER T, RADCHUK V, DOCKTER C, HEDLEY P E, RUSSELL J, et al. A chromosome conformation capture ordered sequence of the barley genome. Nature, 2017, 544(7651): 427-433.
[27]	LI G W, WANG L J, YANG J P, HE H, JIN H B, LI X M, REN T H, REN Z L, LI F, HAN X, et al. A high-quality genome assembly highlights rye genomic characteristics and agronomically important genes. Nature Genetics, 2021, 53(4): 574-584. doi: 10.1038/s41588-021-00808-z pmid: 33737755
[28]	LIU C, HUANG Y H, GUO X R, YI C Y, LIU Q, ZHANG K B, ZHU C L, LIU Y, HAN F P. Young retrotransposons and non-B DNA structures promote the establishment of dominant rye centromere in the 1RS.1BL fused centromere. New Phytologist, 2024, 241(2): 607-622.
[29]	EVTUSHENKO E V, LEVITSKY V G, ELISAFENKO E A, GUNBIN K V, BELOUSOV A I, ŠAFÁŘ J, DOLEŽEL J, VERSHININ A V. The expansion of heterochromatin blocks in rye reflects the co-amplification of tandem repeats and adjacent transposable elements. BMC Genomics, 2016, 17: 337. doi: 10.1186/s12864-016-2667-5 pmid: 27146967
[30]	BIMPONG D, ZHAO L L, RAN M Y, ZHAO X Z, WU C C, LI Z Q, WANG X, CHENG L, FANG Z W, HU Z M, et al. Transcriptomic analysis reveals the regulatory mechanisms of messenger RNA (mRNA) and long non-coding RNA (lncRNA) in response to waterlogging stress in rye (Secale cereale L.). BMC Plant Biology, 2024, 24(1): 534.
[31]	NIAN L L, LIU X L, YANG Y B, ZHU X L, YI X F, HAIDER F U. Genome-wide identification, phylogenetic, and expression analysis under abiotic stress conditions of LIM gene family in Medicago sativa L. PLoS ONE, 2021, 16(6): e0252213.
[32]	MANI B, AGARWAL M, KATIYAR-AGARWAL S. Comprehensive expression profiling of rice tetraspanin genes reveals diverse roles during development and abiotic stress. Frontiers in Plant Science, 2015, 6: 1088. doi: 10.3389/fpls.2015.01088 pmid: 26697042
[33]	周宾寒, 杨竹, 王书平, 方正武, 胡赞民, 徐兆师, 张迎新. 小麦幼苗活性LTR反转录转座子筛选及其对非生物胁迫的响应. 作物学报, 2023, 49(4): 966-977. doi: 10.3724/SP.J.1006.2023.21023
	ZHOU B H, YANG Z, WANG S P, FANG Z W, HU Z M, XU Z S, ZHANG Y X. Screening of active LTR retrotransposons in wheat (Triticum aestivum L.) seedlings and analysis of their responses to abiotic stresses. Acta Agronomica Sinica, 2023, 49(4): 966-977. (in Chinese)
[34]	TAMURA K, STECHER G, KUMAR S. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 2021, 38(7): 3022-3027. doi: 10.1093/molbev/msab120 pmid: 33892491
[35]	BAILEY T L, JOHNSON J, GRANT C E, NOBLE W S. The MEME suite. Nucleic Acids Research, 2015, 43(W1): W39-W49.
[36]	CHEN C J, CHEN H, ZHANG Y, THOMAS H R, FRANK M H, HE Y H, XIA R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 2020, 13(8): 1194-1202. doi: S1674-2052(20)30187-8 pmid: 32585190
[37]	ZHOU Y B, LI Y, QI X L, LIU R B, DONG J H, JING W H, GUO M M, SI Q L, XU Z S, LI L C, et al. Overexpression of V-type H⁺ pyrophosphatase gene EdVP 1 from Elymus dahuricus increases yield and potassium uptake of transgenic wheat under low potassium conditions. Scientific Reports, 2020, 10(1): 5020.
[38]	LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-ΔΔC_Tmethod. Methods, 2001, 25(4): 402-408.
[39]	FELDMAN M, LEVY A A. Genome evolution due to allopolyploidization in wheat. Genetics, 2012, 192(3): 763-774. doi: 10.1534/genetics.112.146316 pmid: 23135324
[40]	MA M X, LIU J H, SONG Y J, LI L, LI Y F. TaqMan MGB probe fluorescence real-time quantitative PCR for rapid detection of Chinese Sacbrood virus. PLoS ONE, 2013, 8(2): e52670.
[41]	KOLACSEK O, IZSVÁK Z, IVICS Z, SARKADI B, ORBÁN T I. Quantitative analysis of DNA transposon-mediated gene delivery:The Sleeping Beauty system as an example. Iconcept Press Ltd, 2014, 7(1): 112-123.
[42]	SHAN X H, LIU Z L, DONG Z Y, WANG Y M, CHEN Y, LIN X Y, LONG L K, HAN F P, DONG Y S, LIU B. Mobilization of the active MITE transposons mPing and Pong in rice by introgression from wild rice (Zizania latifolia Griseb.). Molecular Biology and Evolution, 2005, 22(4): 976-990.
[43]	PAN Y P, BO K L, CHENG Z H, WENG Y Q. The loss-of-function GLABROUS3mutation in cucumber is due to LTR-retrotransposon insertion in a class IV HD-ZIP transcription factor gene CsGL3 that is epistatic over CsGL1. BMC Plant Biology, 2015, 15(1): 302.
[44]	MERIÇ S, AYAN A, GÜNDÜZ B, ÖZPIRINÇCI C, ÇELIK Ö, ATAK Ç. Investigation of Tos17 LTR retrotransposon movements in rice (Oryza sativa L.) under nickel and boron stress. Cereal Research Communications, 2024, 52(4): 1299-1312.
[45]	YANG L L, ZHANG X Y, WANG L Y, LI Y G, LI X T, YANG Y, SU Q, CHEN N, ZHANG Y L, LI N, DENG C L, LI S F, GAO W J. Lineage-specific amplification and epigenetic regulation of LTR- retrotransposons contribute to the structure, evolution, and function of Fabaceae species. BMC Genomics, 2023, 24(1): 423.
[46]	OKAMOTO H, HIROCHIKA H. Silencing of transposable elements in plants. Trends in Plant Science, 2001, 6(11): 527-534. pmid: 11701381
[47]	ZHANG P P, MBODJ A, SOUNDIRAMOURTTY A, LLAURO C, GHESQUIÈRE A, INGOUFF M, KEITH SLOTKIN R, PONTVIANNE F, CATONI M, MIROUZE M. Extrachromosomal circular DNA and structural variants highlight genome instability in Arabidopsis epigenetic mutants. Nature Communications, 2023, 14(1): 5236.
[48]	GASPAROTTO E, BURATTIN F V, DI GIOIA V, PANEPUCCIA M, RANZANI V, MARASCA F, BODEGA B. Transposable elements co-option in genome evolution and gene regulation. International Journal of Molecular Sciences, 2023, 24(3): 2610.
[49]	MIYAO A, YAMANOUCHI U. Transposable element finder (TEF): Finding active transposable elements from next generation sequencing data. BMC Bioinformatics, 2022, 23(1): 500. doi: 10.1186/s12859-022-05011-3 pmid: 36418944
[50]	MA J X, JACKSON S A. Retrotransposon accumulation and satellite amplification mediated by segmental duplication facilitate centromere expansion in rice. Genome Research, 2006, 16(2): 251-259. pmid: 16354755

黑麦活性着丝粒特异反转录转座子的筛选及其对逆境胁迫的响应

Screening of Active Centromeric Retrotransposons of Rye and Their Response to Stress

RichHTML

PDF

赞

可视化

摘要/Abstract

引用本文

使用本文

图/表 8

参考文献 50

相关文章 15

Metrics

本文评价

推荐阅读 0

[1]	赵真坚, 王凯, 陈栋, 申琦, 余杨, 崔晟頔, 王俊戈, 陈子旸, 禹世欣, 陈佳苗, 王翔枫, 唐国庆. 基因组和DNA甲基化组联合分析筛选猪肉质性状关键基因[J]. 中国农业科学, 2024, 57(7): 1394-1406.
[2]	高晨曦, 郝陆洋, 胡悦, 李永祥, 张登峰, 李春辉, 宋燕春, 石云素, 王天宇, 黎裕, 刘旭洋. 干旱条件下玉米转座子插入关联的表观调控分析[J]. 中国农业科学, 2024, 57(6): 1034-1048.
[3]	苏小雨, 谭政委, 李春明, 李磊, 鲁丹丹, 余永亮, 董薇, 安素妨, 杨青, 孙瑶, 许兰杰, 杨红旗, 梁慧珍. 高温胁迫下芝麻全基因组甲基化差异及关联基因表达分析[J]. 中国农业科学, 2024, 57(24): 4825-4838.
[4]	李慧, 张雨峰, 李晓刚, 王中华, 蔺经, 常有宏. 全基因组DNA甲基化和转录组联合分析鉴定杜梨耐盐相关转录因子[J]. 中国农业科学, 2023, 56(7): 1377-1390.
[5]	陈玉梅, 张聪聪, 胡丽蓉, 房浩, 窦金焕, 郭刚, 王炎, 刘巧香, 王雅春, 徐青. 热应激对奶牛GNAS启动子区DNA甲基化水平的影响[J]. 中国农业科学, 2023, 56(12): 2395-2406.
[6]	杨昕冉,马鑫浩,杜嘉伟,昝林森. m⁶A甲基化酶相关基因在牛骨骼肌生成中的表达[J]. 中国农业科学, 2023, 56(1): 165-178.
[7]	束婧婷,单艳菊,姬改革,章明,屠云洁,刘一帆,巨晓军,盛中伟,唐燕飞,李华,邹剑敏. 广西麻鸡m6A甲基转移酶基因表达与肌纤维类型及成肌分化的关系[J]. 中国农业科学, 2022, 55(3): 589-601.
[8]	冯俊杰,赵文达,张新全,刘英杰,袁帅,董志晓,熊毅,熊艳丽,凌瑶,马啸. 引种日本多花黑麦草标准品种DUS性状变异分析及应用[J]. 中国农业科学, 2022, 55(12): 2447-2460.
[9]	张方方,马宁博,岳善超,李世清. 基于不同方法的汉中盆地稻麦轮作土壤供氮能力评价[J]. 中国农业科学, 2020, 53(19): 3996-4009.
[10]	魏志标，柏兆海，马林，张福锁. 中国苜蓿、黑麦草和燕麦草产量差及影响因素[J]. 中国农业科学, 2018, 51(3): 507-522.
[11]	张涛, 司福会, 张玉喜, 盖树鹏. 外源GA₃影响牡丹花芽DNA甲基化水平和相关酶基因的表达分析[J]. 中国农业科学, 2018, 51(18): 3561-3569.
[12]	刘欢，张新全，马啸，张瑞珍，何光武，潘玲，金梦雅. 基于荧光检测技术的多花黑麦草EST-SSR指纹图谱的构建[J]. 中国农业科学, 2017, 50(3): 437-450.
[13]	黄婷，马啸，张新全，张新跃，张瑞珍，符开欣. 多花黑麦草DUS测定中SSR标记品种鉴定比较分析[J]. 中国农业科学, 2015, 48(2): 381-389.
[14]	沈丹，谢雨琇，李庆平，薛松磊，史云强，王赛赛，陈才，钱跃，高波，崔恒宓，宋成义. 多转座子载体的构建及转座特性比较研究[J]. 中国农业科学, 2015, 48(11): 2270-2278.
[15]	朱红菊，刘文革，赵胜杰，路绪强，何楠，豆峻岭，高磊. NaCl胁迫下二倍体和同源四倍体西瓜幼苗DNA甲基化差异分析[J]. 中国农业科学, 2014, 47(20): 4045-4055.