Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (6): 1034-1048.doi: 10.3864/j.issn.0578-1752.2024.06.002

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

Analysis of Transposable Element Associated Epigenetic Regulation under Drought in Maize

GAO ChenXi(), HAO LuYang, HU Yue, LI YongXiang, ZHANG DengFeng, LI ChunHui, SONG YanChun, SHI YunSu, WANG TianYu, LI Yu(), LIU XuYang()   

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/State Key Laboratory of Crop Gene Resources and Breeding, Beijing 100081
  • Received:2023-08-30 Accepted:2023-10-23 Online:2024-03-25 Published:2024-03-25
  • Contact: LI Yu, LIU XuYang

RichHTML

15

PDF

101

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

Fig. 1

Drought tolerance-related phenotype and genomic distribution of variable transposable element insertions and DNA methylation levels A: The leaf relative water content performance of eight lines in different water treatments. *: P<0.05, **: P<0.01; NS: No significant difference. WS and WW are drought and well-watered treatments, respectively. B: The anthesis-silking interval of eight lines in different water treatments. C: The genomic distribution of transposable element (TE) insertion presence/absence variations (PAVs), methylation levels and differentially methylated regions (DMRs) in 3 Mb size sliding widow were plotted. The blue bars and lines were for H082183, and the red ones were for Lü28"

Table 1

Transposable element insertions of each superfamily in H082183 and Lü28 genomes"

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
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

Fig. 2

DNA methylation levels in different genomic regions A: The average percentage of CG, CHG and CHH methylation sites in all methylation C sites of all libraries. B-D show the methylation levels of the CG (B), CHG (C) and CHH (D) contexts in terms of different genomic regions. L_HC and L_HD mean leaf of H082183 under control and drought, respectively. L_LC and L_LD mean leaf of Lü28 under control and drought, respectively. R_HC, R_HD, R_LC and R_LD are the corresponding samples of root. The same as below"

Fig. 3

DNA methylation levels around transposable element and differentially methylated regions A: Genome wide distribution of CG and CHG methylation levels in relation to the transposable element insertion. The X-axis is 100 kb flanking regions of transposable element insertion sites and Y-axis is density of normalized scores of average methylation levels. B: The total numbers of differentially methylated regions (DMRs) detected in leaf or root between H082183 and Lü28. C: The proportions of DMRs identified in genes, 2 kb upstream promoters or intergenic regions. D: The proportions of differentially methylated regions located in transposable element insertion (TEI) PAVs, 5 kb flank regions of TEI PAVs or other regions"

Fig. 4

Comparison analysis of differentially methylated regions and differentially expressed genes A: Distribution of methylation levels with genes in different expression levels. The different methylation levels were defined based on the Quartile1 (Q1, 25%) and Quartile3 (Q3, 75%) of the distribution of gene expression. B: Correlation of CG/CHG methylation differences with gene expression differences. C: Differentially expressed genes associated with methylation variation under drought. The overlap of genotypic differentially expressed genes and differentially methylated regions in leaf or root. The mH+ presents the mCG or mCHG methylation level were higher in H082183 and vice versa. The eH+ presents gene showed higher expression level in H082183 under drought and vice versa. D: GO analysis of the differentially expressed genes associated with differentially methylated regions. The top five most significant GO terms are showed"

Fig. 5

Expression levels of DNA methyltransferase and demethylase genes ** and * represent significant level of FDR<0.01 and FDR<0.05, respectively. The ns means non-significant. The H and L in x-axis are H082183 and Lü28, and D and C are drought and well-watered control treatments, respectively"

Fig. 6

Transposable element insertion associated epigenetic regulation of ZCN7 A: The transposable element insertions and DNA methylation near ZCN7. The dots present single base CG and CHG methylation levels. The green dots revealed higher methylation in Lü28 and orange dot showed higher methylation in H082183. The pink regions present regions with higher methylation in Lü28 and the green regions were higher methylated in H082183. B: The gene expression of ZCN7 in H082183 and Lü28 obtained by RNA-Seq. C: The gene expression of ZCN7 based on another indipendant experiment using RT-qPCR. D: The co-expressed genes with ZCN7 in maize leaves. The gene co-expression networks were constructed using WGCNA and the top 30 genes that were co-expressed with ZCN7 were shown. E: The transposable element insertion/deletion variant mediated epigenetic regulation of ZCN7 based on the results of the present study"

[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
[1] ZHAO ZhenJian, WANG Kai, CHEN Dong, SHEN Qi, YU Yang, CUI ShengDi, WANG JunGe, CHEN ZiYang, YU ShiXin, CHEN JiaMiao, WANG XiangFeng, TANG GuoQing. Integrated Aanalysis of Genome and DNA Methylation for Screening Key Genes Related to Pork Quality Traits [J]. Scientia Agricultura Sinica, 2024, 57(7): 1394-1406.
[2] XIAO Tao, LI Hui, LUO Wei, YE Tao, YU Huan, CHEN YouBo, SHI YuShi, ZHAO DePeng, WU Yun. Screening of Candidate Genes for Green Shell Egg Shell Color Traits in Chishui Black Bone Chicken Based on Transcriptome Sequencing [J]. Scientia Agricultura Sinica, 2023, 56(8): 1594-1605.
[3] LI Hui, ZHANG YuFeng, LI XiaoGang, WANG ZhongHua, LIN Jing, CHANG YouHong. Identification of Salt-Tolerant Transcription Factors in the Roots of Pyrus betulaefolia by the Association Analysis of Genome-Wide DNA Methylation and Transcriptome [J]. Scientia Agricultura Sinica, 2023, 56(7): 1377-1390.
[4] LI YiPu, TONG LiXiu, LIN YaNan, SU ZhiJun, BAO HaiZhu, WANG FuGui, LIU Jian, QU JiaWei, HU ShuPing, SUN JiYing, WANG ZhiGang, YU XiaoFang, XU MingLiang, GAO JuLin. Investigation of Low Nitrogen Tolerance of ZmCCT10 in Maize [J]. Scientia Agricultura Sinica, 2023, 56(6): 1035-1044.
[5] QU Qing, LIU Ning, ZOU JinPeng, ZHANG YaXuan, JIA Hui, SUN ManLi, CAO ZhiYan, DONG JinGao. Screening of Differential Genes and Analysis of Metabolic Pathways in the Interaction Between Fusarium verticillioides and Maize Kernels [J]. Scientia Agricultura Sinica, 2023, 56(6): 1086-1101.
[6] WANG JianFeng, CHENG JiaXin, SHU WeiXue, ZHANG YanRu, WANG XiaoJie, KANG ZhenSheng, TANG ChunLei. Functional Analysis of Effector Hasp83 in the Pathogenicity of Puccinia striiformis f. sp. tritici [J]. Scientia Agricultura Sinica, 2023, 56(5): 866-878.
[7] YI ZeHui, ZHAO Jing, MAO LiPing. Development and Transferability of EST-SSR Markers Based on Transcriptome Data from Asparagus officinalis [J]. Scientia Agricultura Sinica, 2023, 56(22): 4490-4505.
[8] CHEN MinDong, WANG Bin, LIU JianTing, LI YongPing, BAI ChangHui, YE XinRu, QIU BoYin, WEN QingFang, ZHU HaiSheng. Screening Regulatory Genes Related to Luffa Fruit Length and Diameter Development Based on Transcriptome and WGCNA [J]. Scientia Agricultura Sinica, 2023, 56(22): 4506-4522.
[9] WANG Qian, DONG KongJun, XUE YaPeng, LIU ShaoXiong, WANG RuoNan, YANG JiaQi, LU Ping, WANG RuiYun, YANG TianYu, LIU MinXuan. Identification and Evaluation of Drought Tolerance and Screening of Drought-Tolerant Germplasm for Core Germplasms in Proso Millet at Adult Stage [J]. Scientia Agricultura Sinica, 2023, 56(21): 4163-4174.
[10] LU YanQing, LIN YanJin, WANG XianDa, LU XinKun. A Transcriptome Analysis Identifies Candidate Genes Related to Fruit Cracking in Pomelo Fruits [J]. Scientia Agricultura Sinica, 2023, 56(20): 4087-4101.
[11] ZHANG Xin, YANG XingYu, ZHANG ChaoRan, ZHANG Chong, ZHENG HaiXia, ZHANG XianHong. Identification and Expression Analysis of Heat Shock Protein Superfamily Genes in Callosobruchus chinensis [J]. Scientia Agricultura Sinica, 2023, 56(19): 3814-3828.
[12] LI Yan, TAO KeYu, HU Yue, LI YongXiang, ZHANG DengFeng, LI ChunHui, HE GuanHua, SONG YanChun, SHI YunSu, LI Yu, WANG TianYu, ZOU HuaWen, LIU XuYang. Function of Maize ZCN7 in Regulating Drought Resistance at Flowering Stage [J]. Scientia Agricultura Sinica, 2023, 56(16): 3051-3061.
[13] LIU ZiGang, WEI JiaPing, CUI JunMei, WU ZeFeng, FANG Yan, DONG XiaoYun, ZHENG GuoQiang. Status, Existing Problems and Strategy Discussion on Northward Expansion of Winter Rapeseed in China [J]. Scientia Agricultura Sinica, 2023, 56(15): 2854-2862.
[14] CHEN YuMei, ZHANG CongCong, HU LiRong, FANG Hao, DOU JinHuan, GUO Gang, WANG Yan, LIU QiaoXiang, WANG YaChun, XU Qing. Effect of Heat Stress on DNA Methylation of GNAS Promoter Region in Dairy Cows [J]. Scientia Agricultura Sinica, 2023, 56(12): 2395-2406.
[15] ZHANG Rui,ZHANG TianLiu,FAN TingTing,ZHU Bo,ZHANG LuPei,XU LingYang,GAO HuiJiang,LI JunYa,CHEN Yan,GAO Xue. Evolutionary Relationship Between Transposable Elements and Tandem Repeats in Bovinae Species [J]. Scientia Agricultura Sinica, 2022, 55(9): 1859-1867.
Viewed
Full text


Abstract

Cited
  Shared   
  Discussed   
No Suggested Reading articles found!
京ICP备09089781号-30
Copyright 2018 © Editorial office of Scientia Agricultura Sinica
Tel: 86-010-82106279    E-mail: zgnykx@mail.caas.net.cn
Supported by Beijing Magtech Co.Ltd