干旱条件下玉米转座子插入关联的表观调控分析

doi:10.3864/j.issn.0578-1752.2024.06.002

摘要/Abstract

摘要：

【目的】干旱是全球范围影响玉米生产的最主要胁迫因素之一。解析抗旱性的遗传基础与分子机制为玉米的抗旱改良提供依据。【方法】利用代表性玉米自交系，以叶片相对含水量和散粉-吐丝间隔为指标开展田间抗旱性精准鉴定。筛选2个抗旱性极端差异的自交系，开展基因组重测序分析和转座子插入鉴定；利用全基因组重亚硫酸盐测序（WGBS）方法分析不同水分处理下叶片和根系组织的DNA甲基化水平；同时利用转录组测序方法对相同样品的基因表达进行分析；通过比较分析获得2个材料间的转座子插入缺失变异、差异甲基化区域和差异表达基因，并综合分析这三者间的相关关系。针对前期克隆的玉米抗旱基因ZCN7，分析该基因区域转座子插入缺失变异介导的DNA甲基化和基因表达变化情况。【结果】在田间干旱处理下，自交系H082183的叶片相对含水量和散粉-吐丝间隔均与正常处理没有显著差异，而旅28在所有试验材料中表现最低的叶片相对含水量和最大的散粉-吐丝间隔。利用H082183和旅28这两个抗旱性极端差异的玉米自交系开展基因组重测序和转座子插入分析，分别检测到333 754和333 296个转座子插入，其中，有89 954个转座子插入在2个自交系间具有多态性。基因组DNA甲基化分析表明，转座子、内含子和启动子区域较外显子和非编码区呈现较高的CG和CHG甲基化水平，经差异甲基化分析，在2个自交系间共检测到41 352个差异甲基化区域，其中60%的差异甲基化区域位于转座子插入缺失变异的上下游5 kb范围内。基因表达水平与基因的CG和CHG甲基化水平负相关，在2个自交系干旱下的叶片和根系中分别鉴定到4 196和3 500个差异表达基因，其中19.5%和19.7%与差异甲基化区域关联。通过对抗旱相关基因ZCN7的研究，发现该基因34 kb区间内的3个LTR类转座子插入，造成自交系旅28在干旱和正常处理下的CG和CHG甲基化显著高于抗旱自交系H082183，并且H082183中ZCN7表达量也显著高于旅28。【结论】揭示了转座子介导的表观遗传调控在玉米响应干旱胁迫中的重要作用，进一步扩展了转座子变异和DNA甲基化调控抗旱基因ZCN7表达的分子机制。

关键词: 玉米（Zea mays L.）, 抗旱性, 转座子, DNA甲基化, 转录组

Abstract:

【Objective】 Drought is one of the serious abiotic stresses influencing maize production worldwide. Understanding the molecular mechanisms underlying drought tolerance is of great importance in maize improvement. 【Method】 In the present study, representative maize inbred lines were selected for field drought experiment and the drought tolerance was estimated based on leaf relative water content and anthesis-silking interval. Two inbred lines with contrasting drought tolerance was used for genome resequencing and transposable element insertions were identified. The DNA methylation level of leaf and root tissues under different water treatments of the two lines were measured using Whole Genome Bisulfite Sequencing (WGBS). And the gene expression profiles of these samples were detected by RNA sequencing. The integrative atlas of transposable element insertion/deletion variants, differentially methylated regions and differentially expressed genes in the two lines were constructed. In addition, the transposable element insertion/deletion variant mediated epigenetic regulation of ZCN7, which has been conferred the drought tolerance function in our previous study, was analyzed. 【Result】 The field experiment showed inbred line H082183 showed highest drought tolerance, in which the leaf relative water content and anthesis-silking interval had no significant difference between drought and well-watered treatments. While the Lü28 displayed lowest leaf relative water content and largest anthesis-silking interval under drought. Thus, these two lines were selected for further analysis. A total of 333 754 and 333 296 transposable element insertions were identified in the genome of H082183 and Lü28, respectively. And 89 954 transposable element insertions were polymorphism between two lines. The transposable element insertions, introns and promoters showed higher CG and CHG methylation level than exons and untranslated regions. Furthermore, 41 352 differentially methylated regions were identified between H082183 and Lü28. And 60% of the differentially methylated regions were located in the transposable element insertion\deletion variants and 5 kb flanking regions. The gene expression level showed negatively correlated with CG and CHG methylation. Differentially expression analysis between H082183 and Lü28 obtained 4 196 and 3 500 differentially expressed genes in leaf and root under drought, respectively. The 19.5% and 19.7% of these differentially expressed genes were located in differentially methylated regions. Three LTR transposable element insertions were identified in the 34 kb region of ZCN7 in Lü28 but absent in the genome H082183. And the DNA methylation levels of CG and CHG in this genomic region were significantly higher in Lü28 than H082183 under both drought and well-watered environments, which conferred higher ZCN7 expression in the drought tolerant line H082183. 【Conclusion】 Our results highlight the important role of interplay of transposable element insertions, DNA methylation and gene expression under drought. And gene expression regulation mechanism of ZCN7 relied on the transposable element insertion/deletion variants mediated DNA methylation was proposed.

Key words: maize (Zea mays L.), drought tolerance, transposable element, DNA methylation, transcriptome

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.

GAO ChenXi, HAO LuYang, HU Yue, LI YongXiang, ZHANG DengFeng, LI ChunHui, SONG YanChun, SHI YunSu, WANG TianYu, LI Yu, LIU XuYang. Analysis of Transposable Element Associated Epigenetic Regulation under Drought in Maize[J]. Scientia Agricultura Sinica, 2024, 57(6): 1034-1048.

图/表 7

图1

表1

图2

图3

图4

图5

图6

参考文献 58

[1]	WALLACE J G, RODGERS-MELNICK E, BUCKLER E S. On the road to breeding 4.0: Unraveling the good, the bad, and the boring of crop quantitative genomics. Annual Review of Genetics, 2018, 52: 421-444. doi: 10.1146/annurev-genet-120116-024846 pmid: 30285496
[2]	ZHU J K. Abiotic stress signaling and responses in plants. Cell, 2016, 167(2): 313-324. doi: 10.1016/j.cell.2016.08.029
[3]	YANG Z R, CAO Y B, SHI Y T, QIN F, JIANG C F, YANG S H. Genetic and molecular exploration of maize environmental stress resilience: Toward sustainable agriculture. Molecular Plant, 2023, 16(10): 1496-1517. doi: 10.1016/j.molp.2023.07.005
[4]	HOCHHOLDINGER F, BALDAUF J A. Heterosis in plants. Current Biology, 2018, 28(18): R1089-R1092. doi: 10.1016/j.cub.2018.06.041
[5]	LOBELL D B, ROBERTS M J, SCHLENKER W, BRAUN N, LITTLE B B, REJESUS R M, HAMMER G L. Greater sensitivity to drought accompanies maize yield increase in the U.S. Midwest. Science, 2014, 344(6183): 516-519. doi: 10.1126/science.1251423 pmid: 24786079
[6]	CHEN Q Y, LI W Y, TAN L B, TIAN F. Harnessing knowledge from maize and rice domestication for new crop breeding. Molecular Plant, 2021, 14(1): 9-26. doi: 10.1016/j.molp.2020.12.006 pmid: 33316465
[7]	DOEBLEY J, STEC A, HUBBARD L. The evolution of apical dominance in maize. Nature, 1997, 386(6624): 485-488. doi: 10.1038/386485a0
[8]	STUDER A, ZHAO Q, ROSS-IBARRA J, DOEBLEY J. Identification of a functional transposon insertion in the maize domestication gene tb1. Nature Genetics, 2011, 43(11): 1160-1163. doi: 10.1038/ng.942
[9]	HUNG H Y, SHANNON L M, TIAN F, BRADBURY P J, CHEN C, FLINT-GARCIA S A, MCMULLEN M D, WARE D, BUCKLER E S, DOEBLEY J F, HOLLAND J B. ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(28): E 1913-E1921.
[10]	YANG Q, LI Z, LI W Q, KU L X, WANG C, YE J R, LI K, YANG N, LI Y P, ZHONG T, LI J S, CHEN Y H, YAN J B, YANG X H, XU M L. CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the postdomestication spread of maize. Proceedings of the National Academy of Sciences of the United States of America, 2013, 110(42): 16969-16974.
[11]	HUANG C, SUN H Y, XU D Y, CHEN Q Y, LIANG Y M, WANG X F, XU G H, TIAN J G, WANG C L, LI D, WU L S, YANG X H, JIN W W, DOEBLEY J F, TIAN F. ZmCCT9 enhances maize adaptation to higher latitudes. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(2): E334-E341.
[12]	MAO H D, WANG H W, LIU S X, LI Z G, YANG X H, YAN J B, LI J S, TRAN L S P, QIN F. A transposable element in a NAC gene is associated with drought tolerance in maize seedlings. Nature Communications, 2015, 6: 8326. doi: 10.1038/ncomms9326 pmid: 26387805
[13]	WANG X L, WANG H W, LIU S X, FERJANI A, LI J S, YAN J B, YANG X H, QIN F. Genetic variation in ZmVPP1 contributes to drought tolerance in maize seedlings. Nature Genetics, 2016, 48(10): 1233-1241. doi: 10.1038/ng.3636
[14]	SUN X P, XIANG Y L, DOU N N, ZHANG H, PEI S R, FRANCO A V, MENON M, MONIER B, FEREBEE T, LIU T, LIU S Y, GAO Y C, WANG J B, TERZAGHI W, YAN J B, HEARNE S, LI L, LI F, DAI M Q. The role of transposon inverted repeats in balancing drought tolerance and yield-related traits in maize. Nature Biotechnology, 2023, 41(1): 120-127. doi: 10.1038/s41587-022-01470-4
[15]	SEBERG O, PETERSEN G. A unified classification system for eukaryotic transposable elements should reflect their phylogeny. Nature Reviews Genetics, 2009, 10(4): 276. doi: 10.1038/nrg2165-c3 pmid: 19238178
[16]	HÉNAFF E, ZAPATA L, CASACUBERTA J M, OSSOWSKI S. Jitterbug: Somatic and germline transposon insertion detection at single-nucleotide resolution. BMC Genomics, 2015, 16: 768. doi: 10.1186/s12864-015-1975-5 pmid: 26459856
[17]	CHEN K, WALLIS J W, MCLELLAN M D, LARSON D E, KALICKI J M, POHL C S, MCGRATH S D, WENDL M C, ZHANG Q Y, LOCKE D P, SHI X Q, FULTON R S, LEY T J, WILSON R K, DING L, MARDIS E R. BreakDancer: An algorithm for high resolution mapping of genomic structural variation. Nature Methods, 2009, 6(9): 677-681. doi: 10.1038/nmeth.1363
[18]	ZHUANG J L, WANG J, THEURKAUF W, WENG Z P. TEMP: A computational method for analyzing transposable element polymorphism in populations. Nucleic Acids Research, 2014, 42(11): 6826-6838. doi: 10.1093/nar/gku323 pmid: 24753423
[19]	ROBB S M C, LU L, VALENCIA E, BURNETTE J M, OKUMOTO Y, WESSLER S R, STAJICH J E. The use of RelocaTE and unassembled short reads to produce high-resolution snapshots of transposable element generated diversity in rice. Genes Genomes Genetics, 2013, 3(6): 949-957.
[20]	JIANG C, CHEN C, HUANG Z Y, LIU R Y, VERDIER J. ITIS, a bioinformatics tool for accurate identification of transposon insertion sites using next-generation sequencing data. BMC Bioinformatics, 2015, 16(1): 72. doi: 10.1186/s12859-015-0507-2
[21]	CARPENTIER M C, MANFROI E, WEI F J, WU H P, LASSERRE E, LLAURO C, DEBLADIS E, AKAKPO R, HSING Y I, PANAUD O. Retrotranspositional landscape of Asian rice revealed by 3000 genomes. Nature Communications, 2019, 10: 24. doi: 10.1038/s41467-018-07974-5
[22]	ZHANG H M, LANG Z B, ZHU J K. Dynamics and function of DNA methylation in plants. Nature Reviews Molecular Cell Biology, 2018, 19(8): 489-506. doi: 10.1038/s41580-018-0016-z pmid: 29784956
[23]	NOSHAY J M, ANDERSON S N, ZHOU P, JI L X, RICCI W, LU Z F, STITZER M C, CRISP P A, HIRSCH C N, ZHANG X Y, SCHMITZ R J, SPRINGER N M. Monitoring the interplay between transposable element families and DNA methylation in maize. PLoS Genetics, 2019, 15(9): e1008291. doi: 10.1371/journal.pgen.1008291
[24]	KANKEL M W, RAMSEY D E, STOKES T L, FLOWERS S K, HAAG J R, JEDDELOH J A, RIDDLE N C, VERBSKY M L, RICHARDS E J. Arabidopsis MET1 cytosine methyltransferase mutants. Genetics, 2003, 163(3): 1109-1122. doi: 10.1093/genetics/163.3.1109
[25]	LINDROTH A M, CAO X, JACKSON J P, ZILBERMAN D, MCCALLUM C M, HENIKOFF S, JACOBSEN S E. Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science, 2001, 292(5524): 2077-2080. doi: 10.1126/science.1059745
[26]	DU J M, ZHONG X H, BERNATAVICHUTE Y V, STROUD H, FENG S H, CARO E, VASHISHT A A, TERRAGNI J, CHIN H G, TU A, HETZEL J, WOHLSCHLEGEL J A, PRADHAN S, PATEL D J, JACOBSEN S E. Dual binding of chromomethylase domains to H3K9me2-containing nucleosomes directs DNA methylation in plants. Cell, 2012, 151(1): 167-180. doi: 10.1016/j.cell.2012.07.034 pmid: 23021223
[27]	HUETTEL B, KANNO T, DAXINGER L, AUFSATZ W, MATZKE A J M, MATZKE M. Endogenous targets of RNA-directed DNA methylation and Pol IV in Arabidopsis. The EMBO Journal, 2006, 25(12): 2828-2836. doi: 10.1038/sj.emboj.7601150
[28]	TIAN T, WANG S H, YANG S P, YANG Z R, LIU S X, WANG Y J, GAO H J, ZHANG S S, YANG X H, JIANG C F, QIN F. Genome assembly and genetic dissection of a prominent drought-resistant maize germplasm. Nature Genetics, 2023, 55(3): 496-506. doi: 10.1038/s41588-023-01297-y pmid: 36806841
[29]	XU J, CHEN G, HERMANSON P J, XU Q, SUN C S, CHEN W Q, KAN Q X, LI M Q, CRISP P A, YAN J B, LI L, SPRINGER N M, LI Q. Population-level analysis reveals the widespread occurrence and phenotypic consequence of DNA methylation variation not tagged by genetic variation in maize. Genome Biology, 2019, 20(1): 243. doi: 10.1186/s13059-019-1859-0 pmid: 31744513
[30]	XU Q, WU L M, LUO Z X, ZHANG M, LAI J S, LI L, SPRINGER N M, LI Q. DNA demethylation affects imprinted gene expression in maize endosperm. Genome Biology, 2022, 23(1): 77. doi: 10.1186/s13059-022-02641-x pmid: 35264226
[31]	XU G, LYU J, LI Q, LIU H, WANG D F, ZHANG M, SPRINGER N M, ROSS-IBARRA J, YANG J L. Evolutionary and functional genomics of DNA methylation in maize domestication and improvement. Nature Communications, 2020, 11(1): 5539. doi: 10.1038/s41467-020-19333-4 pmid: 33139747
[32]	ZHANG X J, LIU X Y, ZHANG D F, TANG H J, SUN B C, LI C H, HAO L Y, LIU C, LI Y X, SHI Y S, XIE X Q, SONG Y C, WANG T Y, LI Y. Genome-wide identification of gene expression in contrasting maize inbred lines under field drought conditions reveals the significance of transcription factors in drought tolerance. PLoS ONE, 2017, 12(7): e0179477. doi: 10.1371/journal.pone.0179477
[33]	CHEN S F, ZHOU Y Q, CHEN Y R, GU J. Fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 2018, 34(17): i884-i890. doi: 10.1093/bioinformatics/bty560
[34]	SCHNABLE P S, WARE D, FULTON R S, STEIN J C, WEI F S, PASTERNAK S, LIANG C Z, ZHANG J W, FULTON L, GRAVES T A, MINX P, REILY A D, COURTNEY L, KRUCHOWSKI S S, TOMLINSON C, STRONG C, DELEHAUNTY K, FRONICK C, COURTNEY B, ROCK S M, BELTER E, DU F Y, KIM K, ABBOTT R M, COTTON M, LEVY A, MARCHETTO P, OCHOA K, JACKSON S M, GILLAM B, CHEN W Z, YAN L, HIGGINBOTHAM J, CARDENAS M, WALIGORSKI J, APPLEBAUM E, PHELPS L, FALCONE J, KANCHI K, THANE T, SCIMONE A, THANE N, HENKE J, WANG T, RUPPERT J, SHAH N, ROTTER K, HODGES J, INGENTHRON E, CORDES M, KOHLBERG S, SGRO J, DELGADO B, MEAD K, CHINWALLA A, LEONARD S, CROUSE K, COLLURA K, KUDRNA D, CURRIE J, HE R F, ANGELOVA A, RAJASEKAR S, MUELLER T, LOMELI R, SCARA G, KO A, DELANEY K, WISSOTSKI M, LOPEZ G, CAMPOS D, BRAIDOTTI M, ASHLEY E, GOLSER W, KIM H, LEE S, LIN J K, DUJMIC Z, KIM W, TALAG J, ZUCCOLO A, FAN C Z, SEBASTIAN A, KRAMER M, SPIEGEL L, NASCIMENTO L, ZUTAVERN T, MILLER B, AMBROISE C, MULLER S, SPOONER W, NARECHANIA A, REN L Y, WEI S, KUMARI S, BEN F G, LEVY M J, MCMAHAN L, VAN BUREN P, VAUGHN M W, YING K, YEH C T, EMRICH S J, JIA Y, KALYANARAMAN A, HSIA A P, BARBAZUK W B, BAUCOM R S, BRUTNELL T P, CARPITA N C, CHAPARRO C, CHIA J M, DERAGON J M, ESTILL J C, FU Y, JEDDELOH J A, HAN Y J, LEE H, LI P H, LISCH D R, LIU S Z, LIU Z J, NAGEL D H, MCCANN M C, SANMIGUEL P, MYERS A M, NETTLETON D, NGUYEN J, PENNING B W, PONNALA L, SCHNEIDER K L, SCHWARTZ D C, SHARMA A, SODERLUND C, SPRINGER N M, SUN Q, WANG H, WATERMAN M, WESTERMAN R, WOLFGRUBER T K, YANG L X, YU Y, ZHANG L F, ZHOU S G, ZHU Q H, BENNETZEN J L, DAWE R K, JIANG J M, JIANG N, PRESTING G G, WESSLER S R, ALURU S, MARTIENSSEN R A, CLIFTON S W, MCCOMBIE W R, WING R A, WILSON R K. The B73 maize genome: complexity, diversity, and dynamics. Science, 2009, 326(5956): 1112-1115. doi: 10.1126/science.1178534 pmid: 19965430
[35]	KRUEGER F, ANDREWS S R. Bismark: a flexible aligner and methylation caller for Bisulfite-Seq applications. Bioinformatics, 2011, 27(11):1571-1572. doi: 10.1093/bioinformatics/btr167 pmid: 21493656
[36]	WU H, XU T L, FENG H, CHEN L, LI B, YAO B, QIN Z H, JIN P, CONNEELY K N. Detection of differentially methylated regions from whole-genome bisulfite sequencing data without replicates. Nucleic Acids Research, 2015, 43(21): e141.
[37]	AKALIN A, KORMAKSSON M, LI S, GARRETT-BAKELMAN F E, FIGUEROA M E, MELNICK A, MASON C E. methylKit: A comprehensive R package for the analysis of genome-wide DNA methylation profiles. Genome Biology 2012, 13(10): R87. doi: 10.1186/gb-2012-13-10-r87
[38]	KIM D, PAGGI J M, PARK C, BENNETT C, SALZBERG S L. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nature Biotechnology, 2019, 37(8): 907-915. doi: 10.1038/s41587-019-0201-4 pmid: 31375807
[39]	LIAO Y, SMYTH G K, SHI W. featureCounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics, 2014, 30(7): 923-930. doi: 10.1093/bioinformatics/btt656 pmid: 24227677
[40]	LOVE M I, HUBER W, ANDERS S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology, 2014, 15(12): 550. doi: 10.1186/s13059-014-0550-8
[41]	LANGFELDER P, HORVATH S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 2008, 9: 559. doi: 10.1186/1471-2105-9-559 pmid: 19114008
[42]	YOUNG M D, WAKEFIELD M J, SMYTH G K, OSHLACK A. Gene ontology analysis for RNA-seq: Accounting for selection bias. Genome Biology, 2010, 11(2): R14. doi: 10.1186/gb-2010-11-2-r14
[43]	李燕, 陶柯宇, 胡悦, 李永祥, 张登峰, 李春辉, 何冠华, 宋燕春, 石云素, 黎裕, 王天宇, 邹华文, 刘旭洋. 玉米ZCN7在调控花期抗旱性中的作用. 中国农业科学, 2023, 56(16): 3051-3061. doi: 10.3864/j.issn.0578-1752.2023.16.001.
	LI Y, TAO K Y, HU Y, LI Y X, ZHANG D F, LI C H, HE G H, SONG Y C, SHI Y S, LI Y, WANG T Y, ZOU H W, LIU X Y. Function of maize ZCN7 in regulating drought resistance at flowering stage. Scientia Agricultura Sinica, 2023, 56(16): 3051-3061. doi: 10.3864/j.issn.0578-1752.2023.16.001. (in Chinese)
[44]	MCCLINTOCK B. The origin and behavior of mutable loci in maize. Proceedings of the National Academy of Sciences of the United States of America, 1950, 36(6): 344-355.
[45]	ANDERSON S N, STITZER M C, BROHAMMER A B, ZHOU P, NOSHAY J M, O'CONNOR C H, HIRSCH C D, ROSS-IBARRA J, HIRSCH C N, SPRINGER N M. Transposable elements contribute to dynamic genome content in maize. The Plant Journal, 2019, 100(5): 1052-1065. doi: 10.1111/tpj.14489 pmid: 31381222
[46]	CASTELLETTI S, TUBEROSA R, PINDO M, SALVI S. A MITE transposon insertion is associated with differential methylation at the maize flowering time QTL Vgt1. Genes Genomes Genetics, 2014, 4(5): 805-812.
[47]	LAZAROW K, DOLL M L, KUNZE R. Molecular biology of maize Ac/Ds elements: An overview. Methods in Molecular Biology, 2013, 1057: 59-82.
[48]	LISCH D. Mutator and MULE transposons. Microbiology Spectrum, 2015, 3(2): MDNA3-0032-2014.
[49]	LIANG L, ZHOU L, TANG Y P, LI N K, SONG T, SHAO W, ZHANG Z R, CAI P, FENG F, MA Y F, YAO D S, FENG Y, MA Z Y, ZHAO H, SONG R T. A sequence-indexed Mutator insertional library for maize functional genomics study. Plant Physiology, 2019, 181(4): 1404-1414. doi: 10.1104/pp.19.00894
[50]	LI J K, FU J J, CHEN Y, FAN K J, HE C, ZHANG Z Q, LI L, LIU Y J, ZHENG J, REN D T, WANG G Y. The U6 biogenesis-like 1 plays an important role in maize kernel and seedling development by affecting the 3' end processing of U6 snRNA. Molecular Plant, 2017, 10(3): 470-482. doi: 10.1016/j.molp.2016.10.016
[51]	LI H C, WANG L J, LIU M S, DONG Z B, LI Q F, FEI S L, XIANG H T, LIU B S, JIN W W. Maize plant architecture is regulated by the ethylene biosynthetic gene ZmACS7. Plant Physiology, 2020, 183(3): 1184-1199. doi: 10.1104/pp.19.01421
[52]	CHEN G, WANG R L, JIANG Y Z, DONG X X, XU J, XU Q, KAN Q X, LUO Z X, SPRINGER N M, LI Q. A novel active transposon creates allelic variation through altered translation rate to influence protein abundance. Nucleic Acids Research, 2023, 51(2): 595-609. doi: 10.1093/nar/gkac1195 pmid: 36629271
[53]	KOBAYASHI Y, KAYA H, GOTO K, IWABUCHI M, ARAKI T. A pair of related genes with antagonistic roles in mediating flowering signals. Science, 1999, 286(5446): 1960-1962. doi: 10.1126/science.286.5446.1960 pmid: 10583960
[54]	KARDAILSKY I, SHUKLA V K, AHN J H, DAGENAIS N, CHRISTENSEN S K, NGUYEN J T, CHORY J, HARRISON M J, WEIGEL D. Activation tagging of the floral inducer FT. Science, 1999, 286(5446): 1962-1965. doi: 10.1126/science.286.5446.1962
[55]	DANILEVSKAYA O N, MENG X, HOU Z L, ANANIEV E V, SIMMONS C R. A genomic and expression compendium of the expanded PEBP gene family from maize. Plant Physiology, 2008, 146(1): 250-264. doi: 10.1104/pp.107.109538 pmid: 17993543
[56]	GUO L, WANG X H, ZHAO M, HUANG C, LI C, LI D, YANG C J, YORK A M, XUE W, XU G H, LIANG Y M, CHEN Q Y, DOEBLEY J F, TIAN F. Stepwise cis-regulatory changes in ZCN8 contribute to maize flowering-time adaptation. Current Biology, 2018, 28(18): 3005-3015. e4. doi: 10.1016/j.cub.2018.07.029
[57]	LIANG Y M, LIU Q, WANG X F, HUANG C, XU G H, HEY S, LIN H Y, LI C, XU D Y, WU L S, WANG C L, WU W H, XIA J L, HAN X, LU S J, LAI J S, SONG W B, SCHNABLE P S, TIAN F. ZmMADS69 functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to maize flowering time adaptation. The New Phytologist, 2019, 221(4): 2335-2347. doi: 10.1111/nph.2019.221.issue-4
[58]	MASCHERETTI I, TURNER K, BRIVIO R S, HAND A, COLASANTI J, ROSSI V. Florigen-encoding genes of day-neutral and photoperiod-sensitive maize are regulated by different chromatin modifications at the floral transition. Plant Physiology, 2015, 168(4): 1351-1363. doi: 10.1104/pp.15.00535 pmid: 26084920

转座子分类 Subclass	转座子家族 Superfamily	简写代码 Code	H082183基因组数量 No. in H082183 genome	旅28基因组数量 No. in Lü28 genome	2个基因组共有数量 No. in both genomes
Retrotransposons
LTR	Copia	RLC	123957	121858	108237
	Gypsy	RLG	170353	165861	140809
	Unkown LTR	RLX	26778	25969	21611
LINE	L1	RIL	1545	1529	1306
LINE	RTE	RIT	600	570	502
SINE	RST	RST	638	575	439
DNA transposons
TIR	hAT	DTA	14696	13966	11300
	CACTA	DTC	22130	21366	17714
	PIF-Harbinger	DTH	5295	4965	3671
	Mutator	DTM	6197	5915	4967
	Tc1-Mariner	DTT	542	526	352
Helitron	Helitron	DHH	3621	3451	2803