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Acta Agronomica Sinica ›› 2023, Vol. 49 ›› Issue (9): 2398-2411.doi: 10.3724/SP.J.1006.2023.22059

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

Dynamic change profile of histone H3K18cr on rice whole genome under cold stress

LIU Kai1(), CHEN Ji-Jin1, LIU Shuai2, CHEN Xu1, ZHAO Xin-Ru2, SUN Shang2, XUE Chao2, GONG Zhi-Yun1,2,*()   

  1. 1Jiangsu Key Laboratory of Crop Genomics and Molecular Breeding / Key Laboratory of Plant Functional Genomics of the Ministry of Education / Jiangsu Key Laboratory of Crop Genetics and Physiology, Agricultural College of Yangzhou University, Yangzhou 225009, Jiangsu, China
    2Jiangsu Co-innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou 225009, Jiangsu, China
  • Received:2022-10-07 Accepted:2023-02-10 Online:2023-09-12 Published:2023-02-27
  • Supported by:
    National Natural Science Foundation of China(31871232)

Abstract:

Histone modifications play an important role in response to abiotic stresses in rice. Crotonylation is a novel histone modification, and the changes of crotonylation in rice subjected to low temperature stress are rarely reported. In this study, RNA-seq and ChIP-seq were performed on normal-grown and cold-treated rice seedlings of rice variety ‘Nipponbare’, followed by combined analysis of the regulatory characteristics of the crotonylation modification at the histone H3 lysine 18-specific site (H3K18cr) on gene expression under cold stress. The results showed that H3K18cr was mainly enriched in the first exon and intergenic region and had positive correlation with gene expression and gene length. The global distribution of H3K18cr in rice genome did not change under cold stress, but WB and ChIP-seq results indicated that the overall modification level decreased. The differential modification analysis revealed that there were significant increase and decrease of 899 genes and 409 genes in the modification after cold stress, respectively. Association analysis with RNA-seq showed that a total of 199 genes had increased levels of H3K18cr modification and up-regulated expression levels. GO enrichment revealed that these genes were mainly involved in the processes such as the regulation of transcriptional activity. Further analysis indicated that histone H3K18cr was involved in the response process of cold stress by regulating the expression of transcription factors such as OsDREB1A, OsEATB, OsAP2-39, and OsNAC9 in rice. The results provide a theoretical basis for further understanding the epigenetic mechanisms of histone crotonylation in response to cold stress in plants.

Key words: rice, cold stress, H3K18cr, gene expression

Table 1

Primers used in this study"

引物名称
Primer name
引物序列
Primer sequence (5'-3')
引物名称
Primer name
引物序列
Primer sequence (5'-3')
OsDREB1A-F GACGTCCTGAGTGACATGG OsTPS1-F CATCGTGTCAGAGTTTGTCG
OsDREB1A-R CTAGTAGCTCCAGAGTGGGA OsTPS1-R TCACGTACCTGTAGTGCTTC
OsDREB1B-F GTCCACACTTTTCAGTGCGAG OsLEA5-F CTCACCTACACCCTCAAGTG
OsDREB1B-R AATCTCGCACTGAAAAGTGTGG OsLEA5-R CGAGATGAGGAAGTCGTAGG
OsMYBS3-F CAAGAACCAGAGACCCAAGT OsV5A-F CTTCTGCTGAGAATGGACCT
OsMYBS3-R AAGCTGGAACAATCACTGGA OsV5A-R GAGGGTGGGATGATGAATGT
OsMADS57-F GTTCCAGCACTCCATACAGC ONAC095-F CAGGAGGAGAGGTGGAGG
OsMADS57-R GGCAGATGAAGTCCCAGTTCT ONAC095-R GGGGATGATGTCGAACTTGA

Fig. 1

H3K18cr variations of seedlings for rice variety ‘Nipponbare’ under cold stress rice A: phenotypes of two-week-old rice seedlings after 10 hours of normal and cold (4℃) treatments; B: protein immunoassay of H3K18cr under normal and cold stress. ImageJ software was used to quantify the band intensities.; C: the genome-wide distribution of H3K18cr peaks under normal and cold stress; D: the distribution pattern of H3K18cr on different types of genes under normal and cold stress. X-axis indicates the normalization of different length genes into percentages, including the upstream and downstream 1 kb regions of the gene. Y-axis represents the normalized reads count of H3K18cr."

Table 2

ChIP-seq data alignment"

样品名
Sample name
重复数
Replicate
总序列数
Total clean reads
比对序列数
Total aligned reads
唯一比对序列数
Total unique reads
Peak数
Total peaks
共有Peak数
Common peaks
相关性
Correlation coefficient
H3K18cr-CK 1 45,952,156 45,268,705 (98.51%) 30,248,490 (65.83%) 25,218 20,077 0.92
H3K18cr-CK 2 48,099,538 47,360,155 (98.46%) 32,023,294 (66.58%) 29,127
H3K18cr-Cold 1 47,721,602 46,868,242 (98.21%) 30,382,217 (63.67%) 23,544 17,944 0.92
H3K18cr-Cold 2 48,128,162 47,304,118 (98.29%) 30,250,892 (62.85%) 29,632

Fig. 2

Analysis of H3K18cr response genes under cold stress A: the number of genes marked by H3K18cr under normal and cold stress. Red line indicates normal growth seedlings, blue line indicates seedlings treated with cold stress for 10 h; B: the number of H3K18cr differentially modified genes under normal and cold stress; C: GO enrichment analysis of genes with increased H3K18cr modifications under cold stress. The scatterplot shows the cluster representatives in a two-dimensional space derived by applying multidimensional scaling to a matrix of significant GO terms with semantic similarities. Bubble color and size indicates the log10(FDR). X-axis and Y-axis have no real meaning; D: GO enrichment of genes with decreased H3K18cr modifications under cold stress. Y-axis indicates the enriched GO terms, X-axis is represented by -log10(FDR), and the numbers in the graph indicate the number of genes enriched in the GO terms; E: KEGG enrichment pathway of genes with increased H3K18cr modifications under cold stress."

Table 3

RNA-seq data alignment"

样品名
Sample
重复数
Replicate
总序列数
Total reads
比对序列数
Aligned reads
表达基因数
FPKM>0
相关性
Correlation coefficient
正常温度Control 1 51,702,548 49,740,100 (92.62%) 26,992 0.94
正常温度Control 2 54,410,846 50,622,035 (93.04%) 24,422
低温Cold 1 61,244,656 52,044,285 (84.98%) 25,474 0.95
低温Cold 2 72,466,862 67,205,195 (92.74%) 27,191

Fig. 3

Relative expression pattern of genes under cold stress A: previously reported RT-qPCR of abiotic stress-related genes. Red indicates up-regulated genes, blue indicates down-regulated genes; B: relationship between H3K18cr modifications and gene expression under normal and cold stress; C: the relative expression pattern of differential genes under normal and cold stress; D: GO and KEGG enrichment analysis of the up-regulated genes; E: GO and KEGG enrichment analysis of the down-regulated genes."

Fig. 4

Relationship between H3K18cr and gene expression under cold stress A: Venn diagram between ChIP-seq differentially modified genes and RNA-seq differentially expressed genes after cold treatment; B: Heatmap of 199 genes with increased modifications and up-regulated gene expression modifications; C: Boxplot of the expression levels of 199 genes with increased modification and up-regulated expression; D: GO enrichment analysis of 199 genes with increased modifications and up-regulated expression. The scatterplot shows the cluster representatives in a two-dimensional space derived by applying multidimensional scaling to a matrix of significant GO terms with semantic similarities. Bubble color and size indicates the log10(FDR). X-axis and Y-axis have no real meaning; E: KEGG enrichment of 199 genes with increased modifications and up-regulated expression."

Fig. 5

Analysis of H3K18cr-related transcription factors under cold stress A: Venn diagram of 199 genes with increased H3K18cr modification and up-regulated expression with all transcription factors in rice; B: IGV shows that genes in the ERF family are associated with H3K18cr at cold stress; C: IGV screenshot shows that genes in the NAC family are associated with H3K18cr at cold stress; D: IGV screenshot shows that genes in the GRAS family are associated with H3K18cr at cold; E: IGV screenshot shows that genes in the DBB family are associated with H3K18cr at cold stress."

Table 4

Transcription factor functional information"

TF 家族
TF family
基因 ID
Gene ID
基因名字
Gene name
功能
Function
参考文献References
Dof LOC_Os01g15900 RDD1; OsDof-2 产量相关 Yield-related [45]
LOC_Os10g26620 OsDof-26; OsDof27 非生物逆境抗性 Abiotic stress tolerance [46]
ERF LOC_Os09g35030 OsDREB1A 非生物逆境抗性 Abiotic stress tolerance [28]
LOC_Os09g28440 OsEATB 株高发育; 非生物逆境抗性
Plant growth; Abiotic stress tolerance
[37-38]
LOC_Os04g52090 OsAP2-39 非生物逆境抗性 Abiotic stress tolerance [39]
ARF LOC_Os04g36054 OsARF9 — —
NAC LOC_Os03g60080 SNAC1; OsNAC9 非生物逆境抗性 Abiotic stress tolerance [41]
LOC_Os07g12340 OsNAC3 非生物逆境抗性 Abiotic stress tolerance [40]
CO-like LOC_Os09g06464 OsCO3 调控光周期 Regulate photoperiodic [47]
LOC_Os02g39710 OsCOL4 调控抽穗期 Regulate heading date [48]
HD-ZIP LOC_Os04g45810 Oshox22 非生物逆境抗性 Abiotic stress tolerance [49]
bZIP LOC_Os02g16680 RITA-1; OsbZIP20 非生物逆境抗性; 重金属胁迫
Abiotic stress tolerance; High metal stress
[50-51]
HSF LOC_Os02g13800 OsHsfC2a 非生物逆境抗性 Abiotic stress tolerance [52]
DBB LOC_Os02g39360 OsBBX4; OsBBX25 非生物逆境抗性 Abiotic stress tolerance [44]
LOC_Os09g35880 OsBBX29 非生物逆境抗性 Abiotic stress tolerance [43]
LOC_Os04g41560 OsBBX11 非生物逆境抗性 Abiotic stress tolerance [43]
bHLH LOC_Os01g50940 OsMYL1 调控JA信号 Regulate JA signal [53]
LOC_Os04g41229 OsbHLH111 调控糖信号 Regulate sugar signal [54]
LOC_Os09g29930 OsbHLH032 调控BR信号 Regulate BR signal [55]
GRAS LOC_Os02g44360 SCL6-IIb; OsHAM1 非生物逆境抗性 Abiotic stress tolerance [42]
LOC_Os02g45760 OsGRAS-10 — —
LOC_Os01g62460 OsGRAS-2 — —
MYB_related LOC_Os04g49450 OsMYBR1 非生物逆境抗性 Abiotic stress tolerance [56]
LOC_Os02g46030 OsMYB1R 非生物逆境抗性 Abiotic stress tolerance [57]
LOC_Os02g45670 — — —
LOC_Os01g41900 OsDLN13 — —
[1] Zhou Y, Simpson S, Holloway A F, Charlesworth J, van der Mei I, Taylor B V. The potential role of epigenetic modifications in the heritability of multiple sclerosis. Mult Scler, 2014, 20: 135-140.
doi: 10.1177/1352458514520911
[2] Peach S E, Rudomin E L, Udeshi N D, Carr S A, Jaffe J D. Quantitative assessment of chromatin immunoprecipitation grade antibodies directed against histone modifications reveals patterns of co-occurring marks on histone protein molecules. Mol Cell Proteomics, 2012, 11: 128-137.
doi: 10.1074/mcp.M111.015941 pmid: 22442256
[3] Kouzarides T. Chromatin modifications and their function. Cell, 2007, 128: 693-705.
doi: 10.1016/j.cell.2007.02.005 pmid: 17320507
[4] 薛超. 水稻盐胁迫下组蛋白乙酰化修饰特征及HATs相关基因的功能研究. 扬州大学博士学位论文, 江苏扬州, 2018.
Xue C. Characteristic Analysis of Histone Acetylation Dynamics under Salt Stress and Functional Analysis of HATs in Rice. PhD Dissertation of Yangzhou University, Yangzhou, Jiangsu, China, 2018. (in Chinese with English abstract)
[5] Bao X C, Wang Y, Li X, Li X M, Liu Z, Yang T P, Wong C F, Zhang J W, Hao Q, Li X D. Identification of ‘erasers’ for lysine crotonylated histone marks using a chemical proteomics approach. eLife, 2014, 3: e02999.
doi: 10.7554/eLife.02999
[6] Tan M J, Luo H, Lee S, Jin F L, Yang J S, Montellier E, Buchou T, Cheng Z Y, Rousseaux S, Rajagopal N, Lu Z K, Ye Z, Zhu Q, Wysocka J, Ye Y, Khochbin S, Ren B, Zhao Y M. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell, 2011, 146: 1015-1027.
[7] Sabari B R, Tang Z Y, Huang H, Yong-Gonzalez V, Molina H, Kong H E, Dai L Z, Shimada M, Cross J R, Zhao Y M, Roeder R G, Allis C D. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell, 2015, 58: 203-215.
doi: 10.1016/j.molcel.2015.02.029 pmid: 25818647
[8] Sun H J, Liu X W, Li F F, Li W, Zhang J, Xiao Z X, Shen L L, Li Y, Wang F L, Yang J G. First comprehensive proteome analysis of lysine crotonylation in seedling leaves of Nicotiana tabacum. Sci Rep, 2017, 7: 3013.
doi: 10.1038/s41598-017-03369-6
[9] Liu K D, Yuan C C, Li H L, Chen K Y, Lu L S, Shen C J, Zheng X L. A qualitative proteome-wide lysine crotonylation profiling of papaya (Carica papaya L.). Sci Rep, 2018, 8: 8230.
doi: 10.1038/s41598-018-26676-y
[10] Sun J H, Qiu C, Qian W J, Wang Y, Sun L T, Li Y S, Ding Z T. Ammonium triggered the response mechanism of lysine crotonylome in tea plants. BMC Genomics, 2019, 20: 340.
doi: 10.1186/s12864-019-5716-z pmid: 31060518
[11] Dong Y B, Chen C. Comprehensive profiling of paper mulberry (Broussonetia papyrifera) crotonylome reveals the significance of lysine crotonylation in young leaves. Int J Mol Sci, 2022, 23: 1173.
doi: 10.3390/ijms23031173
[12] Xu M L, Luo J D, Li Y, Shen L L, Zhang X, Yu J, Guo Z Q, Wu J X, Chi Y C, Yang J G. First comprehensive proteomics analysis of lysine crotonylation in leaves of peanut (Arachis hypogaea L.). Proteomics, 2021, 21: e2000156.
[13] Liu S, Xue C, Fang Y, Chen G, Peng X J, Zhou Y, Chen C, Liu G Q, Gu M H, Wang K, Zhang W L, Wu Y F, Gong Z Y. Global involvement of lysine crotonylation in protein modification and transcription regulation in rice. Mol Cell Proteomics, 2018, 17: 1922-1936.
doi: 10.1074/mcp.RA118.000640 pmid: 30021883
[14] Yuan L Y, Liu X C, Luo M, Yang S G, Wu K Q. Involvement of histone modifications in plant abiotic stress responses. J Integr Plant Biol, 2013, 55: 892-901.
doi: 10.1111/jipb.12060
[15] Li H, Yan S H, Zhao L, Tan J J, Zhang Q, Gao F, Wang P, Hou H L, Li L J. Histone acetylation associated up-regulation of the cell wall related genes is involved in salt stress induced maize root swelling. BMC Plant Biol, 2014, 14: 105.
doi: 10.1186/1471-2229-14-105 pmid: 24758373
[16] Kim J M, To T K, Ishida J, Morosawa T, Kawashima M, Matsui A, Toyoda T, Kimura H, Shinozaki K, Seki M. Alterations of lysine modifications on the histone H3 N-tail under drought stress conditions in Arabidopsis thaliana. Plant Cell Physiol, 2008, 49: 1580-1588.
doi: 10.1093/pcp/pcn133
[17] Van D K, Ding Y, Malkaram S, Riethoven J J M, Liu R, Yang J Y, Laczko P, Chen H, Xia Y N, Ladunga I, Avramova Z, Fromm M. Dynamic changes in genome-wide histone H3 lysine 4 methylation patterns in response to dehydration stress in Arabidopsis thaliana. BMC Plant Biol, 2010, 10: 238.
doi: 10.1186/1471-2229-10-238
[18] Vlachonasios K E, Thomashow M F, Triezenberg S J. Disruption mutations of ADA2b and GCN5 transcriptional adaptor genes dramatically affect Arabidopsis growth, development, and gene expression. Plant Cell, 2003, 15: 626-638.
doi: 10.1105/tpc.007922
[19] Kwon C S, Lee D, Choi G, Chung W I. Histone occupancy- dependent and -independent removal of H3K27 trimethylation at cold-responsive genes in Arabidopsis. Plant J, 2009, 60: 112-121.
doi: 10.1111/tpj.2009.60.issue-1
[20] Roy D, Paul A, Roy A, Ghosh R, Ganguly P, Chaudhuri S. Differential acetylation of histone H3 at the regulatory region of OsDREB1b promoter facilitates chromatin remodelling and transcription activation during cold stress. PLoS One, 2014, 9: e100343.
[21] Zheng D Y, Wang L, Chen L F, Pan X C, Lin K D, Fang Y, Wang X E, Zhang W L. Salt-responsive genes are differentially regulated at the chromatin levels between seedlings and roots in rice. Plant Cell Physiol, 2019, 60: 1790-1803.
doi: 10.1093/pcp/pcz095 pmid: 31111914
[22] Lu Y, Xu Q T, Liu Y, Yu Y, Cheng Z Y, Zhao Y, Zhou D X. Dynamics and functional interplay of histone lysine butyrylation, crotonylation, and acetylation in rice under starvation and submergence. Genome Biol, 2018, 19: 144.
doi: 10.1186/s13059-018-1533-y pmid: 30253806
[23] 徐青山, 黄晶, 孙爱军, 洪小智, 朱练峰, 曹小闯, 孔亚丽, 金千瑜, 朱春权, 张均华. 低温影响水稻发育机理及调控途径研究进展. 中国水稻科学, 2022, 36: 118-130.
doi: 10.16819/j.1001-7216.2022.210602
Xu Q S, Huang J, Sun A J, Hong X Z, Zhu L F, Cao X C, Kong Y L, Jin Q Y, Quan C, Zhang J H. Effects of low temperature on the growth and development of rice plants and the advance of regulation pathways: a review. Chin J Rice Sci, 2022, 36: 118-130. (in Chinese with English abstract)
doi: 10.16819/j.1001-7216.2022.210602
[24] Hu Y F, Zhu N, Wang X M, Yi Q P, Zhu D Y, Lai Y, Zhao Y. Analysis of rice Snf2 family proteins and their potential roles in epigenetic regulation. Plant Physiol Biochem, 2013, 70: 33-42.
doi: 10.1016/j.plaphy.2013.05.001
[25] Sharma R, Singh R K M, Malik G, Deveshwar P, Tyagi A K, Kapoor S, Kapoor M. Rice cytosine DNA methyltransferases: gene expression profiling during reproductive development and abiotic stress. FEBS J, 2009, 276: 6301-6311.
doi: 10.1111/j.1742-4658.2009.07338.x pmid: 19788421
[26] Xue C, Liu S, Chen C, Zhu J, Yang X B, Zhou Y, Guo R, Liu X Y, Gong Z Y. Global proteome analysis links lysine acetylation to diverse functions in Oryza sativa. Proteomics, 2018, 18: 1700036.
doi: 10.1002/pmic.v18.1
[27] Nagaki K, Talbert P B, Zhong C X, Dawe R K, Henikoff S, Jiang J M. Chromatin immunoprecipitation reveals that the 180-bp satellite repeat is the key functional DNA element of Arabidopsis thaliana centromeres. Genetics, 2003, 163: 1221-1225.
doi: 10.1093/genetics/163.3.1221
[28] Ito Y, Katsura K, Maruyama K, Taji T, Kobayashi M, Seki M, Shinozaki K, Yamaguchi-Shinozaki K. Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol, 2006, 47: 141-153.
doi: 10.1093/pcp/pci230 pmid: 16284406
[29] Mao D H, Chen C Y. Colinearity and similar expression pattern of rice DREB1s reveal their functional conservation in the cold-responsive pathway. PLoS One, 2012, 7: e47275.
doi: 10.1371/journal.pone.0047275
[30] Huang L, Hong Y B, Zhang H J, Li D Y, Song F M. Rice NAC transcription factor ONAC095 plays opposite roles in drought and cold stress tolerance. BMC Plant Biol, 2016, 16: 203.
doi: 10.1186/s12870-016-0897-y pmid: 27646344
[31] Liu H J, Li Q Z, Yang F, Zhu F Y, Sun Y, Tao Y Z, Lo C. Differential regulation of protochlorophyllide oxidoreductase abundances by VIRESCENT 5A (OsV5A) and VIRESCENT 5B (OsV5B) in rice seedlings. Plant Cell Physiol, 2016, 57: 2392-2402.
pmid: 27565208
[32] He S, Tan L L, Hu Z L, Chen G P, Wang G X, Hu T Z. Molecular characterization and functional analysis by heterologous expression in E. coli under diverse abiotic stresses for OsLEA5, the atypical hydrophobic LEA protein from Oryza sativa L. Mol Genet Genomics, 2012, 287: 39-54.
doi: 10.1007/s00438-011-0660-x
[33] Li H W, Zang B S, Deng X W, Wang X P. Overexpression of the trehalose-6-phosphate synthase gene OsTPS1 enhances abiotic stress tolerance in rice. Planta, 2011, 234: 1007-1018.
doi: 10.1007/s00425-011-1458-0
[34] Yu C Y, Su S, Xu Y C, Zhao Y Q, Yan A, Huang L L, Ali I, Gan Y B. The effects of fluctuations in the nutrient supply on the expression of five members of the AGL17 clade of MADS-Box genes in rice. PLoS One, 2014, 9: e105597.
doi: 10.1371/journal.pone.0105597
[35] Su C F, Wang Y C, Hsieh T H, Lu C A, Tseng T H, Yu S M. A novel MYBS3-dependent pathway confers cold tolerance in rice. Plant Physiol, 2010, 153: 145-158.
doi: 10.1104/pp.110.153015
[36] Jin J P, Tian F, Yang D C, Meng Y Q, Kong L, Luo J C, Gao G. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res, 2017, 45: D1040-D1045.
doi: 10.1093/nar/gkw982
[37] Tripathi A K, Pareek A, Sopory S K, Singla-Pareek S L. Narrowing down the targets for yield improvement in rice under normal and abiotic stress conditions via expression profiling of yield- related genes. Rice, 2012, 5: 37.
doi: 10.1186/1939-8433-5-37 pmid: 24280046
[38] Qi W W, Sun F, Wang Q J, Chen M L, Huang Y Q, Feng Y Q, Luo X J, Yang J S. Rice ethylene-response AP2/ERF factor OsEATB restricts internode elongation by down-regulating a gibberellin biosynthetic gene. Plant Physiol, 2011, 157: 216-228.
doi: 10.1104/pp.111.179945
[39] Wan L Y, Zhang J F, Zhang H W, Zhang Z J, Quan R D, Zhou S R, Huang R F. Transcriptional activation of OsDERF1 in OsERF3 and OsAP2-39 negatively modulates ethylene synthesis and drought tolerance in rice. PLoS One, 2011, 6: e25216.
doi: 10.1371/journal.pone.0025216
[40] Zhang X, Long Y, Chen X X, Zhang B L, Xin Y F, Li L Y, Cao S L, Liu F H, Wang Z G, Huang H, Zhou D G, Xia J X. A NAC transcription factor OsNAC3 positively regulates ABA response and salt tolerance in rice. BMC Plant Biol, 2021, 21: 546.
doi: 10.1186/s12870-021-03333-7 pmid: 34800972
[41] Redillas M C F R, Jeong J S, Kim Y S, Jung H, Bang S W, Choi Y D, Ha S H, Reuzeau C, Kim J K. The overexpression of OsNAC9 alters the root architecture of rice plants enhancing drought resistance and grain yield under field conditions. Plant Biotechnol J, 2012, 10: 792-805.
doi: 10.1111/j.1467-7652.2012.00697.x pmid: 22551450
[42] Um T, Choi J, Park T, Chung P J, Jung S E, Shim J S, Kim Y S, Choi I Y, Park S C, Oh S J, Seo J S, Kim J K. Rice microRNA171f/SCL6 module enhances drought tolerance by regulation of flavonoid biosynthesis genes. Plant Direct, 2022, 6: e374.
[43] 刘兰兰. 水稻OsBBX基因响应热胁迫的初步研究. 湖南农业大学硕士学位论文, 湖南长沙, 2015.
Liu L L. Preliminary Study on OsBBX Genes under Heat Stress in Rice. MS Thesis of Hunan Agricultural University, Changsha, Hunan, China, 2015. (in Chinese with English abstract)
[44] 刘焱, 邢立静, 李俊华, 戴绍军. 水稻含有B-box锌指结构域的OsBBX25蛋白参与植物对非生物胁迫的响应. 植物学报, 2012, 47: 366-378.
doi: 10.3724/SP.J.1259.2012.00366
Liu Y, Xing L J, Li J H, Dai S J. Rice B-box zinc finger protein OsBBX25 is involved in the abiotic response. Chin Bull Bot, 2012, 47: 366-378. (in Chinese with English abstract)
[45] Iwamoto M, Higo K, Takano M. Circadian clock- and phytochrome-regulated Dof-like gene, Rdd1, is associated with grain size in rice. Plant Cell Environ, 2009, 32: 592-603.
doi: 10.1111/pce.2009.32.issue-5
[46] Gandass N, Kajal, Salvi P. Intrinsically disordered protein, DNA binding with one finger transcription factor (OsDOF27) implicates thermotolerance in yeast and rice. Front Plant Sci, 2022, 13: 956299.
doi: 10.3389/fpls.2022.956299
[47] Kim S K, Yun C H, Lee J H, Jang Y H, Park H Y, Kim J K. OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta, 2008, 228: 355-365.
doi: 10.1007/s00425-008-0742-0
[48] Lee Y S, Jeong D H, Lee D Y, Yi J, Ryu C H, Kim S L, Jeong H J, Choi S C, Jin P, Yang J, Cho L H, Choi H, An G. OsCOL4 is a constitutive flowering repressor upstream of Ehd1 and downstream of OsphyB. Plant J, 2010, 63: 18-30.
[49] Zhang S X, Haider I, Kohlen W, Jiang L, Bouwmeester H, Meijer A H, Schluepmann H, Liu C M, Ouwerkerk P B F. Function of the HD-Zip I gene Oshox22 in ABA-mediated drought and salt tolerances in rice. Plant Mol Biol, 2012, 80: 571-585.
doi: 10.1007/s11103-012-9967-1
[50] Sun L, Di D W, Li G, Kronzucker H J, Wu X, Shi W. Endogenous ABA alleviates rice ammonium toxicity by reducing ROS and free ammonium via regulation of the SAPK9-bZIP20 pathway. J Exp Bot, 2020, 71: 4562-4577.
doi: 10.1093/jxb/eraa076 pmid: 32064504
[51] Wang B X, Xu B, Liu Y, Li J F, Sun Z G, Chi M, Xing Y G, Yang B, Li J, Liu J B, Chen T M, Fang Z W, Lu B G, Xu D Y, Bello B K. A novel mechanisms of the signaling cascade associated with the SAPK10-bZIP20-NHX1 synergistic interaction to enhance tolerance of plant to abiotic stress in rice (Oryza sativa L.). Plant Sci, 2022, 323: 111393.
doi: 10.1016/j.plantsci.2022.111393
[52] Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A. Heat shock factor gene family in rice: Genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem, 2009, 47: 785-795.
doi: 10.1016/j.plaphy.2009.05.003
[53] Ogawa S, Miyamoto K, Nemoto K, Sawasaki T, Yamane H, Nojiri H, Okada K. OsMYC2, an essential factor for JA-inductive sakuranetin production in rice, interacts with MYC2-like proteins that enhance its transactivation ability. Sci Rep, 2017, 7: 40175.
doi: 10.1038/srep40175 pmid: 28067270
[54] 李梦琪. 转录因子OsbHLH111抑制水稻幼苗生长机理的初步研究. 河南农业大学硕士学位论文, 河南郑州, 2018.
Li M Q. Preminary Study on the Mechanism for Rice Seedling Growth-inhibition of bHLH111. MS Thesis of Henan Agricultural University, Zhengzhou, Henan, China, 2018. (in Chinese with English abstract)
[55] Tian Q X, Luan J X, Guo C X, Shi X Y, Deng P, Zhou Z Z, Zhang W H, Shen L K. A bHLH protein, OsBIM1, positively regulates rice leaf angle by promoting brassinosteroid signaling. Biochem Biophys Res Commun, 2021, 578: 129-135.
doi: 10.1016/j.bbrc.2021.09.035
[56] Yin X, Cui Y, Wang M, Xia X. Overexpression of a novel MYB-related transcription factor, OsMYBR1, confers improved drought tolerance and decreased ABA sensitivity in rice. Biochem Biophys Res Commun, 2017, 490: 1355-1361.
doi: 10.1016/j.bbrc.2017.07.029
[57] Rongjun C. Isolation of a novel MYB transcription factor OsMyb1R from rice and analysis of the response of this gene to abiotic stresses. Afr J Biotechnol, 2012, 11: 3731-3737.
[58] Jha U C, Bohra A, Jha R, Parida S K. Salinity stress response and ‘omics’ approaches for improving salinity stress tolerance in major grain legumes. Plant Cell Rep, 2019, 38: 255-277.
doi: 10.1007/s00299-019-02374-5
[59] Zeng Z X, Zhang W L, Marand A P, Zhu B, Buell C R, Jiang J M. Cold stress induces enhanced chromatin accessibility and bivalent histone modifications H3K4me3 and H3K27me3 of active genes in potato. Genome Biol, 2019, 20: 123.
doi: 10.1186/s13059-019-1731-2 pmid: 31208436
[60] Sun L, Song G S, Guo W J, Wang W X, Zhao H K, Gao T T, Lyu Q X, Yang X, Xu F, Dong Y S, Pu L. Dynamic changes in genome-wide histone3 lysine27 trimethylation and gene expression of soybean roots in response to salt stress. Front Plant Sci, 2019, 10: 1031.
doi: 10.3389/fpls.2019.01031 pmid: 31552061
[61] Lee H G, Seo P J. MYB96 recruits the HDA15 protein to suppress negative regulators of ABA signaling in Arabidopsis. Nat Commun, 2019, 10: 1713.
doi: 10.1038/s41467-019-09417-1
[62] Ding Y, Avramova Z, Fromm M. The Arabidopsis trithorax-like factor ATX1 functions in dehydration stress responses via ABA-dependent and ABA-independent pathways. Plant J, 2011, 66: 735-744.
doi: 10.1111/j.1365-313X.2011.04534.x
[63] Pien S, Fleury D, Mylne J S, Crevillen P, Inze D, Avramova Z, Dean C, Grossniklaus U. ARABIDOPSIS TRITHORAX1 dynamically regulates FLOWERING LOCUS C activation via histone 3 lysine 4 trimethylation. Plant Cell, 2008, 20: 580-588.
doi: 10.1105/tpc.108.058172
[64] Ullah F, Xu Q, Zhao Y, Zhou D X. Histone deacetylase HDA710 controls salt tolerance by regulating ABA signaling in rice. J Integr Plant Biol, 2021, 63: 451-467.
doi: 10.1111/jipb.13042
[65] Nakashima K, Ito Y, Yamaguchi-Shinozaki K. Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol, 2009, 149: 88-95.
doi: 10.1104/pp.108.129791 pmid: 19126699
[66] 陈悦, 孙明哲, 贾博为, 冷月, 孙晓丽. 水稻AP2/ERF转录因子参与逆境胁迫应答的分子机制研究进展. 作物学报, 2022, 48: 781-790.
doi: 10.3724/SP.J.1006.2022.12026
Chen Y, Sun M Z, Jia B W, Leng Y, Sun X L. Research progress regarding the function and mechanism of rice AP2/ERF transcription factor in stress response. Acta Agron Sin, 2022, 48: 781-790. (in Chinese with English abstract)
doi: 10.3724/SP.J.1006.2022.12026
[67] Zheng Y, Ge J, Bao C, Chang W, Liu J, Shao J, Liu X, Su L, Pan L, Zhou D X. Histone deacetylase HDA9 and WRKY53 transcription factor are mutual antagonists in regulation of plant stress response. Mol Plant, 2020, 13: 598-611.
doi: S1674-2052(19)30408-3 pmid: 31891777
[68] Lamke J, Brzezinka K, Altmann S, Baurle I. A hit-and-run heat shock factor governs sustained histone methylation and transcriptional stress memory. EMBO J, 2016, 35: 162-175.
doi: 10.15252/embj.201592593 pmid: 26657708
[69] Mao Y, Pavangadkar K A, Thomashow M F, Triezenberg S J. Physical and functional interactions of Arabidopsis ADA 2 transcriptional coactivator proteins with the acetyltransferase GCN5 and with the cold-induced transcription factor CBF1. Biochim Biophys Acta, 2006, 1759: 69-79.
[70] Zong W, Yang J, Fu J, Xiong L. Synergistic regulation of drought-responsive genes by transcription factor OsbZIP23 and histone modification in rice. J Integr Plant Biol, 2020, 62: 723-729.
doi: 10.1111/jipb.12850
[71] Huang Q X, Liao X Q, Yang X H, Luo Y C, Lin P, Zeng Q H, Bai H R, Jiang B B, Pan Y Z, Zhang F, Zhang L, Jia Y, Liu Q L. Lysine crotonylation of DgTIL1 at K72 modulates cold tolerance by enhancing DgnsLTP stability in chrysanthemum. Plant Biotechnol J, 2021, 19: 1125-1140.
doi: 10.1111/pbi.13533 pmid: 33368971
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