Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (21): 4500-4513.doi: 10.3864/j.issn.0578-1752.2021.21.002

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

Over-expression of ZmIBH1-1 to Improve Drought Resistance in Maize Seedlings

ZHU FangFang(),DONG YaHui(),REN ZhenZhen,WANG ZhiYong,SU HuiHui,KU LiXia,CHEN YanHui()   

  1. College of Agronomy, Henan Agricultural University/National Key Laboratory of Wheat and Maize Crop Science, Zhengzhou 450046
  • Received:2021-04-25 Accepted:2021-06-16 Online:2021-11-01 Published:2021-11-09
  • Contact: YanHui CHEN E-mail:1261546452@qq.com;1018661461@qq.com;chy9890@163.com

RichHTML

58

PDF

488

Abstract:

【Objective】Drought is an important factor that affects the growth and development of maize seriously. Through the mining of genes related to drought resistance in maize, transgene function verification and transcriptome analysis, analyzing the molecular regulation mechanism of key genes in response to drought stress, this paper provides the theoretical basis for drought resistance molecular breeding and genetic improvement. 【Method】In this study, the maize inbred line B104 (wild-type, WT) was used as the background to construct the ZmIBH1-1 overexpression (ZmIBH1-1-OE) transgenic line by Agrobacterium-mediated method. The transgenic plants and lines were identified via screening transgenic plants for glufosinate-ammonium resistance, PCR detection of marker gene and target gene and expression analysis of target gene by qRT-PCR. We used the ZmIBH1-1-OE and WT transgenic lines as materials. Through drought treatment (20% PEG6000), phenotype identification and drought tolerance physiological and biochemical index determination were carried out to verify the drought resistance function of ZmIBH1-1; RNA-Seq was used to identify differentially expressed genes (DEGs) under drought stress at the 4-leaf stage; Combined with DAP-seq (DNA affinity purification sequencing) analysis, it is preliminarily determined that ZmIBH1-1 protein directly regulates downstream target genes related to drought resistance, and IGV (Integrative Genomics Viewer) was used to analyze the position of the ZmIBH1-1 protein binding candidate target gene, and then the Dual-Luciferase assay was used to verify the regulatory relationship between ZmIBH1-1 protein and target genes. 【Result】12 transformation events were obtained by genetic transformation of maize. In the T3 generation, there were 458 plants in which the marker gene Bar and the target gene ZmIBH1-1 were simultaneously detected. The results of qRT-PCR showed that the expression level of ZmIBH1-1 in ZmIBH1-1-OE lines was significantly higher than that of WT and the expression levels of transformation events 3 and 8 were the highest, which were self-crossed to obtain T4 generation for subsequent experiments. Under drought stress, the survival rate, the relative water content, the chlorophyll content, soluble protein content and the physiological and biochemical indicators (superoxide dismutase, peroxidase, catalase activity) of ZmIBH1-1-OE were higher than those of WT significantly, which indicating that the overexpression of ZmIBH1-1 in maize confers higher drought tolerance. The RNA-Seq results showed that there were 1 214 DEGs between WT and ZmIBH1-1-OE lines. Gene Ontology (GO) analysis showed that DEGs were mainly involved in biological processes, cell components and molecular functions, such as photosynthesis, stress response, dehydration response, etc. in biological processes; KEGG enrichment analysis showed that DEGs were mainly involved in the signal transduction of plant hormones, the metabolism and other processes. Combining the significantly DEGs of RNA-Seq and the target genes of ZmIBH1-1 obtained from DAP-seq analysis, it is preliminarily identified 11 candidate target genes related to drought resistance that may be directly regulated by ZmIBH1-1, including 2 calcium signal related genes, 3 cysteine metabolism related genes, 1 bHLH transcription factor, 1 stress response protein, 1 glutathione transferase, 1 redox process protein and 2 ethylene response factor; Integrative genomics viewer showed that ZmIBH1-1 protein could bind to the promoters of the target genes; Subsequent Dual-Luciferase assay further showed that ZmIBH1-1 protein can directly act on 11 candidate target genes, of which, ZmIBH1-1 directly binds to the promoters of ZmCa-M, ZmSYCO, ZmbHLH54, ZmGlu-r1, ZmCLPB3 and ZmP450-99A2 to promote their expression, and directly binds to the promoters of ZmAGD12, ZmCYS, ZmCYSB, ZmERF-107 and ZmEIN3 to repress their expression. In addition, transcription factors such as NAC, WRKY and MYB also differentially expressed between WT and ZmIBH1-1-OE under drought stress. 【Conclusion】The overexpression of ZmIBH1-1 can enhance the drought tolerance of maize; ZmIBH1-1 improves the drought tolerance of maize by directly regulating the expression of genes ZmERF-107 and ZmEIN3 in the ethylene signaling pathway; ZmIBH1-1 enhances the drought tolerance of maize by directly regulating the calcium signal-related genes ZmCa-M and ZmAGD12; ZmIBH1-1 may indirectly regulate NAC, WRKY, MYB and other transcription factors in response to drought stress.

Key words: maize, drought stress, ZmIBH1-1, RNA-Seq, transcription factor, gene expression

Fig. 1

Schematic diagram of the T-DNA region of the ZmIBH1-1 overexpression recombinant plasmid LB: Left border repeat of T-DNA; Tnos: Terminator; Bar: Herbicide screening gene; PMAS: MAS promoter; P35S: 35S promoter; ETMV: TMV enhancer; RB: Right border repeat of T-DNA"

Table 1

Primers used in the study"

引物名称
Primer name		 引物序列
Primer sequence (5′-3′)
Bar-F CATCGAGACAAGCACGGTC
Bar-R AAACCCACGTCATGCCAGTT
ZmIBH-F CAATTACATTTACAATTACCATGGTCATGGCCAGGAAGAGGAC
ZmIBH-R CTCTCTAGACTCACCTAGGATCCTCATTGGGCGGAGAAG
qIBH-F AGGAACCACCGCCAAACC
qIBH-R GCHTCTCCGCAGCAGGAC
Tublin-F CCGCTATCTCCGTCGC
Tublin-R GTTCTTGGATGGCGGTCG

Fig. 2

Identification of some T3 transgenic maize plants A: Phenotypic identification of herbicide glyphosate sprayed or applied; B: PCR detection of Bar; C: PCR detection of IBH1-1. WT: Wild-type plant; T: Transgenic ZmIBH1-1-OE plant; 1: Positive control (plasmid DNA); 2: Blank; M: DL5000 DNA Marker; The rest represent transgenic plants"

Fig. 3

Expression of ZmIBH1-1 in 12 transformation events lines WT: Wild-type plant; 1-12: 12 transformation events of ZmIBH1-1-OE lines (n=3, ±SD, **P<0.01)"

Fig. 4

Phenotype and physiological changes of ZmIBH1-1-OE and wild type B104 lines under drought stress A: The phenotype of B104 and ZmIBH1-1-OE lines under PEG6000 stress; B: Mean survival rate of B104 and ZmIBH1-1-OE lines under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant); C: Mean relative water contents (RWCs) of B104 and ZmIBH1-1-OE lines under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant); D: Determination of POD, SOD and CAT enzyme activities of B104 and ZmIBH1-1-OE strains under PEG6000 stress (n=3, ±SD, **P< 0.01, n.s not significant); E: Determination of the contents of Cht, Car and SP of B104 and ZmIBH1-1-OE strains under PEG6000 stress (n=3, ±SD, **P<0.01, n.s not significant)"

Table 2

The summary of reads analysis from RNA-Seq data"

样品
Sample		 正常条件Normal 干旱胁迫Drought stress
原始reads
Raw reads		 过滤后的reads
Clean reads		 过滤后的
reads所占比
Reads keep rate (%)		 比对上的
reads
Mapped reads		 比对上的
reads占比
Mapped reads rate (%)		 原始reads
Raw reads		 过滤后的
reads
Clean reads		 过滤后的
reads所占比
Reads keep rate (%)		 比对上的reads
Mapped reads		 比对上的
reads占比
Mapped reads rate (%)
WT-1 5407756 5032404 93.05 4492503 89.27 3870308 3532833 91.28 3128759 88.56
WT-2 7232533 6586333 91.06 5987305 90.90 4119004 3813323 92.57 3482561 91.32
OE-1 8523635 7780152 91.27 6893250 88.60 6322179 5776743 91.37 5367210 92.91
OE-2 7647821 6977539 91.23 6289035 90.13 6994016 6490634 92.80 5901352 90.92

Fig. 5

RNA-Seq analysis of B104 and ZmIBH1-1-OE lines under normal and drought conditions A: PCA analysis of RNA-Seq. p represents PEG treatment, 0 h represents normal conditions, 1 and 2 represents two biological replicates respectively; B: Correlation analysis of RNA-Seq; C: The expression of ZmIBH1-1 in B104 and ZmIBH1-1-OE lines under normal/drought stress (n=2, ±SD, **P<0.01)"

Fig. 6

IGV showed that ZmIBH1-1 had peaks enrichment in the promoter region of some target genes A-D represents that ZmIBH1-1 can bind to the promoter region of target genes ZmEIN3, ZmERF-107, ZmCLPB3, and ZmAGD12, respectively. The red box represents the location of ZmIBH1-1 binding peaks"

Fig. 7

Regulation of target genes by ZmIBH1-1 A: The 35S: REN-Pro gene LUC reporter constructs were transiently expressed in N.benthamiana leaves together with control vector or 35S:ZmIBH1-1 effector, respectively. The expression level of REN was used an internal control; B-C: The LUC/REN ratio represents the relative activity of promoters. Data are values of three independent experiments. Significant differences from the corresponding control values (n=3, ±SD, **P<0.01). NC: Negative control"

[1] QU D Y. Food and Agriculture Organization of the United Nations. Viale delle Terme di Caracalla, Rome, Italy. 2016 [June 2021], http://www.fao.org/statistics/databases/en/ .
[2] 代宇佳, 罗晓峰, 周文冠, 陈锋, 帅海威, 杨文钰, 舒凯. 生物和非生物逆境胁迫下的植物系统信号. 植物学报, 2019, 54(2):102-111.
DAI Y J, LUO X F, ZHOU W G, CHEN F, SHUAI H W, YANG W Y, SHU K. Plant systemic signaling under biotic and abiotic stresses conditions. Chinese Bulletin of Botany, 2019, 54(2):102-111. (in Chinese)
[3] BARTELS D, SUNKAR R. Drought and salt tolerance in plants. Critical Reviews in Plant Sciences, 2005, 24(1):23-58.
doi: 10.1080/07352680590910410
[4] MAO H, WANG H, LIU S, LI Z, YANG X, YAN J, LI J, TRAN L, 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
[5] MAO H, YU L, HAN R, LI Z, LIU H. ZmNAC55, a maize stress-responsive NAC transcription factor, confers drought resistance in transgenic Arabidopsis. Plant Physiology & Biochemistry, 2016, 105:55-66.
[6] WANG C T, RU J N, LIU Y W, LI M, ZHAO D, YANG J F, FU J D, XU Z S. Maize WRKY transcription factor ZmWRKY106 confers drought and heat tolerance in transgenic plants. International Journal of Molecular Sciences, 2018, 19(10):3046.
doi: 10.3390/ijms19103046
[7] WANG C T, RU J N, LIU Y W, YANG J F, MENG L, XU Z S, FU J D. The maize WRKY transcription factor ZmWRKY40 confers drought resistance in transgenic Arabidopsis. International Journal of Molecular Sciences, 2018, 19(9):2580.
doi: 10.3390/ijms19092580
[8] YING S, ZHANG D F, JING F, SHI Y S, SONG Y C, WANG T Y, YU L. Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis. Planta, 2012, 235(2):253-266.
doi: 10.1007/s00425-011-1496-7
[9] 刘彦丹, 英生, 张登峰, 石云素, 宋燕春, 白志川, 王天宇, 黎裕. 玉米逆境胁迫响应基因ZmbZIP71的克隆与表达分析. 植物遗传资源学报, 2011, 12(5):775-781.
LIU Y D, YING S, ZHANG D F, SHI Y S, SONG Y C, BAI Z C, WANG T Y, LI Y. Isolation and expression analysis of a stress-responsive gene ZmbZIP71 in maize (Zea mays L.). Journal of Plant Genetic Resources, 2011, 12(5):775-781. (in Chinese)
[10] WU J, JIANG Y, LIANG Y, CHEN L, CHEN W, CHENG B. Expression of the maize MYB transcription factor ZmMYB3R enhances drought and salt stress tolerance in transgenic plants. Plant Physiology and Biochemistry, 2019, 137:179-188.
doi: 10.1016/j.plaphy.2019.02.010
[11] ZHANG H, XIANG Y, HE N, LIU X, DAI M. Enhanced vitamin C production mediated by an ABA-induced PTP-like nucleotidase improves drought tolerance of Arabidopsis and maize. Molecular Plant, 2020, 13(5):760-776.
doi: 10.1016/j.molp.2020.02.005
[12] ZHANG X, MI Y, MAO H, LIU S, QIN F. Genetic variation in ZmTIP1 contributes to root hair elongation and drought tolerance in maize. Plant Biotechnology Journal, 2020, 18(5):1271-1283.
doi: 10.1111/pbi.v18.5
[13] DING S, HE F, TANG W, DU H, WANG H. Identification of maize CC-type glutaredoxins that are associated with response to drought stress. Genes, 2019, 10(8):610.
doi: 10.3390/genes10080610
[14] LI L, DU Y, HE C, DIETRICH C R, ZHENG J. Maize glossy6 is involved in cuticular wax deposition and drought tolerance. Journal of Experimental Botany, 2019, 70(12):3089-3099.
doi: 10.1093/jxb/erz131
[15] ZHOU L, ZHOU J, XIONG Y, LIU C, WANG J, WANG G, CAI Y, WU K. Overexpression of a maize plasma membrane intrinsic protein ZmPIP1;1 confers drought and salt tolerance in Arabidopsis. PLoS ONE, 2018, 13(6):e198639.
[16] WANG H, WANG M, XIA Z. The maize class-I SUMO conjugating enzyme ZmSCE1d is involved in drought stress response. International Journal of Molecular Sciences, 2019, 21(1):29.
doi: 10.3390/ijms21010029
[17] LIANG Y, JIANG Y, DU M, LI B, WU J. ZmASR3 from the maize ASR gene family positively regulates drought tolerance in transgenic Arabidopsis. International Journal of Molecular Sciences, 2019, 20(9):2278.
doi: 10.3390/ijms20092278
[18] FELLER A, MACHEMER K, BRAUN E L, GROTEWOLD E. Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant Journal for Cell & Molecular Biology, 2011, 66(1):94-116.
[19] WANG F, ZHU H, KONG W, PENG R, LIU Q, YAO Q. The antirrhinum AmDEL gene enhances flavonoids accumulation and salt and drought tolerance in transgenic Arabidopsis. Planta, 2016, 244(1):59-73.
doi: 10.1007/s00425-016-2489-3
[20] WANG F, ZHU H, CHEN D, LI Z, PENG R, YAO Q. A grape bHLH transcription factor gene, VvbHLH1, increases the accumulation of flavonoids and enhances salt and drought tolerance in transgenic Arabidopsis thaliana. Plant Cell Tissue & Organ Culture, 2016, 125(2):387-398.
[21] DONG Y, WANG C, HAN X, TANG S, LIU S, XIA X, YIN W. A novel bHLH transcription factor PebHLH35 from Populus euphratica confers drought tolerance through regulating stomatal development, photosynthesis and growth in Arabidopsis. Biochemical and Biophysical Research Communications, 2014, 450(1):453-458.
doi: 10.1016/j.bbrc.2014.05.139
[22] CUI X, WANG Y X, LIU Z W, WANG W L, LI H, ZHUANG J. Transcriptome-wide identification and expression profile analysis of the bHLH family genes in Camellia sinensis. Functional and Integrative Genomics, 2018, 18(5):489-503.
doi: 10.1007/s10142-018-0608-x
[23] LIU W, TAI H, LI S, GAO W, ZHAO M, XIE C, LI W X. bHLH122is important for drought and osmotic stress resistance in Arabidopsis and in the repression of ABA catabolism. New Phytologist, 2014, 201(4):1192-1204.
doi: 10.1111/nph.2014.201.issue-4
[24] SEO J S, JOO J, KIM M J, KIM Y K, NAHM B H, SANG I S, CHEONG J J, LEE J S, KIM J K, YANG D C. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant Journal for Cell & Molecular Biology, 2011, 65(6):907-921.
[25] LI Z, LIU C, ZHANG Y, WANG B, RAN Q, ZHANG J. The bHLH family member ZmPTF1 regulates drought tolerance in maize by promoting root development and ABA synthesis. Journal of Experimental Botany, 2019, 70(19):5471-5486.
doi: 10.1093/jxb/erz307
[26] CAO Y, ZENG H, KU L X, REN Z, HAN Y, SU H, DOU D, LIU H, DONG Y, ZHU F. ZmIBH1-1 regulates plant architecture in maize. Journal of Experimental Botany, 2020, 71(10):2943-2955.
doi: 10.1093/jxb/eraa052
[27] KENNETH J L, THOMAS D S. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods, 2002, 25:402-408.
doi: 10.1006/meth.2001.1262
[28] 韩赞平. 玉米种子活力相关性状QTL定位及相关基因的克隆[D]. 郑州: 河南农业大学, 2014.
HAN Z P. QTL mapping of seed vigor related traits and related gene cloning in maize[D]. Zhengzhou: Henan Agricultural University, 2014. (in Chinese)
[29] 姚晓云, 蓝海军, 邓伟, 陈红萍, 罗晨曦, 况震, 罗宗铭, 王记林, 陈大洲. 水稻淡白叶突变体的叶绿素含量测定及农艺性状比较分析. 江西农业学报, 2020, 32(12):12-15.
YAO X Y, LAN H J, DENG W, CHEN H P, LUO C X, KUANG Z, LUO Z M, WANG L J, CHEN D Z. Determination of chlorophyll content and comparative analysis of agronomic traits of pale-white- leaf mutant in rice. Acta Agriculturae Jiangxi, 2020, 32(12):12-15. (in Chinese)
[30] 焦洁. 考马斯亮蓝G-250染色法测定苜蓿中可溶性蛋白含量. 农业工程技术, 2016, 36(17):33-34.
JIAO J. Determination of soluble protein content in Alfalfa by Coomassie brilliant blue G-250 staining. Agricultural Engineering Technology, 2016, 36(17):33-34. (in Chinese)
[31] YE J. WEGO: A web tool for plotting GO annotations. Nucleic Acids Research, 2006, 34(Web Server issue):W293-W297.
doi: 10.1093/nar/gkl031
[32] PIERIK R, SASIDHARAN R, VOESENEK L. Growth control by ethylene: Adjusting phenotypes to the environment. Journal of Plant Growth Regulation, 2007, 26(2):188-200.
doi: 10.1007/s00344-006-0124-4
[33] LANAHAN M B. The never ripe mutation blocks ethylene perception in tomato. The Plant Cell, 1994, 6(4):521-530.
[34] GRBI V, Bleecker A B. Ethylene regulates the timing of leaf senescence in Arabidopsis. The Plant Journal, 1995, 8(4):595-602.
doi: 10.1046/j.1365-313X.1995.8040595.x
[35] LUO J, MA N, PEI H, CHEN J, LI J, GAO J. A DELLA gene, RhGAI1, is a direct target of EIN3 and mediates ethylene-regulated rose petal cell expansion via repressing the expression of RhCesA2. Journal of Experimental Botany, 2013, 64(16):5075-5084.
doi: 10.1093/jxb/ert296
[36] HUA J, MEYEROWITZ E M. Ethylene responses are negatively regulated by a receptor gene family in Arabidopsis thaliana. Cell (Cambridge), 1998, 94(2):261-271.
doi: 10.1016/S0092-8674(00)81425-7
[37] GUO H W. Paradigms and paradox in the ethylene signaling pathway and interaction network. Molecular Plant, 2011, 4(4):626-634.
doi: 10.1093/mp/ssr042
[38] OHME-TAKAGI M, SHINSHI H. Ethylene-inducible DNA binding proteins that interact with an ethylene-responsive element. The Plant Cell, 1995, 7(2):173-182.
[39] HATTORI Y, NAGAI K, FURUKAWA S, SONG XJ, KAWANO R, SAKAKIBARA H, WU J, MATSUMOTO T, YOSHIMURA A, KITANO H, MATSUOKA M, MORI H, ASHIKARI M. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature, 2009, 460(7258):1026-1030.
doi: 10.1038/nature08258
[40] KNIGHT H. Calcium signaling during abiotic stress in plants. International Review of Cytology-a Survey of Cell Biology, 1999, 195:269-324.
[41] REDDY A, ALI G S, CELESNIK H, DAY I S. Coping with stresses: Roles of calcium- and calcium/calmodulin-regulated gene expression. The Plant Cell, 2011, 23(6):2010-2032.
doi: 10.1105/tpc.111.084988
[42] DUBROVINA A S, KISELEV K V, KHRISTENKO V S, ALEYNOVA O A. VaCPK20, a calcium-dependent protein kinase gene of wild grapevine Vitis amurensis Rupr., mediates cold and drought stress tolerance. Journal of Plant Physiology, 2015, 185:1-12.
doi: 10.1016/j.jplph.2015.05.020
[43] ZOU J J, LI X D, RATNASEKERA D, WANG C, LIU W X, SONG L F, ZHANG W Z, WU W H. Arabidopsis CALCIUM-DEPENDENT PROTEIN KINASE8 and CATALASE3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. The Plant Cell, 2015, 27(5):1445-1460.
doi: 10.1105/tpc.15.00144
[44] REN Z, ZHANG D, CAO L, ZHANG W, KU L. Functions and regulatory framework of ZmNST3 in maize under lodging and drought stress. Plant Cell and Environment, 2020, 43(9):2272-2286.
doi: 10.1111/pce.v43.9
[45] OH JE, KWON Y, KIM JH, NOH H, HONG SW, LEE H. A dual role for MYB60 in stomatal regulation and root growth of Arabidopsis thaliana under drought stress. Plant Molecular Biology, 2011, 77(1/2):91-103.
doi: 10.1007/s11103-011-9796-7
[46] NAKABAYASHI R, YONEKURA-SAKAKIBARA K, URANO K, SUZUKI M, YAMADA Y, NISHIZAWA T, MATSUDA F, KOJIMA M, SAKAKIBARA H, SHINOZAKI K. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. The Plant Journal, 2014, 77(3):367-379.
doi: 10.1111/tpj.2014.77.issue-3
[47] DAI X Y, XU Y Y, MA Q B, XU W Y, WANG T, XUE Y B, CHONG K. Overexpression of an R1R2R3 MYB gene, OsMYB3R-2, increases tolerance to freezing, drought, and salt stress in transgenic Arabidopsis. Plant Physiology, 2007, 143(4):1739-1751.
doi: 10.1104/pp.106.094532
[48] HONG S, CHEN S, JIANG J, CHEN F, CHEN Y, GU C, LI P, SONG A, ZHU X, GAO H. Heterologous expression of the chrysanthemum R2R3-MYB Transcription Factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Molecular Biotechnology, 2012, 51(2):160-173.
doi: 10.1007/s12033-011-9451-1
[49] QIN Y, WANG M, TIAN Y, HE W, LU H, XIA G. Over-expression of TaMYB33 encoding a novel wheat MYB transcription factor increases salt and drought tolerance in Arabidopsis. Molecular Biology Reports, 2012, 39(6):7183-7192.
doi: 10.1007/s11033-012-1550-y
[50] FINATTO T, VIANA V E, WOYANN L G, BUSANELLO C, OLIVEIRA A. Can WRKY transcription factors help plants to overcome environmental challenges? Genetics & Molecular Biology, 2018, 41(3):533-544.
[1] CHAI HaiYan,JIA Jiao,BAI Xue,MENG LingMin,ZHANG Wei,JIN Rong,WU HongBin,SU QianFu. Identification of Pathogenic Fusarium spp. Causing Maize Ear Rot and Susceptibility of Some Strains to Fungicides in Jilin Province [J]. Scientia Agricultura Sinica, 2023, 56(1): 64-78.
[2] GU LiDan,LIU Yang,LI FangXiang,CHENG WeiNing. Cloning of Small Heat Shock Protein Gene Hsp21.9 in Sitodiplosis mosellana and Its Expression Characteristics During Diapause and Under Temperature Stresses [J]. Scientia Agricultura Sinica, 2023, 56(1): 79-89.
[3] ZHAO ZhengXin,WANG XiaoYun,TIAN YaJie,WANG Rui,PENG Qing,CAI HuanJie. Effects of Straw Returning and Nitrogen Fertilizer Types on Summer Maize Yield and Soil Ammonia Volatilization Under Future Climate Change [J]. Scientia Agricultura Sinica, 2023, 56(1): 104-117.
[4] ZHANG KeKun,CHEN KeQin,LI WanPing,QIAO HaoRong,ZHANG JunXia,LIU FengZhi,FANG YuLin,WANG HaiBo. Effects of Irrigation Amount on Berry Development and Aroma Components Accumulation of Shine Muscat Grape in Root-Restricted Cultivation [J]. Scientia Agricultura Sinica, 2023, 56(1): 129-143.
[5] HU Sheng,LI YangYang,TANG ZhangLin,LI JiaNa,QU CunMin,LIU LieZhao. Genome-Wide Association Analysis of the Changes in Oil Content and Protein Content Under Drought Stress in Brassica napus L. [J]. Scientia Agricultura Sinica, 2023, 56(1): 17-30.
[6] LI ZhouShuai,DONG Yuan,LI Ting,FENG ZhiQian,DUAN YingXin,YANG MingXian,XU ShuTu,ZHANG XingHua,XUE JiQuan. Genome-Wide Association Analysis of Yield and Combining Ability Based on Maize Hybrid Population [J]. Scientia Agricultura Sinica, 2022, 55(9): 1695-1709.
[7] XIONG WeiYi,XU KaiWei,LIU MingPeng,XIAO Hua,PEI LiZhen,PENG DanDan,CHEN YuanXue. Effects of Different Nitrogen Application Levels on Photosynthetic Characteristics, Nitrogen Use Efficiency and Yield of Spring Maize in Sichuan Province [J]. Scientia Agricultura Sinica, 2022, 55(9): 1735-1748.
[8] LI YiLing,PENG XiHong,CHEN Ping,DU Qing,REN JunBo,YANG XueLi,LEI Lu,YONG TaiWen,YANG WenYu. Effects of Reducing Nitrogen Application on Leaf Stay-Green, Photosynthetic Characteristics and System Yield in Maize-Soybean Relay Strip Intercropping [J]. Scientia Agricultura Sinica, 2022, 55(9): 1749-1762.
[9] QIU YiLei,WU Fan,ZHANG Li,LI HongLiang. Effects of Sublethal Doses of Imidacloprid on the Expression of Neurometabolic Genes in Apis cerana cerana [J]. Scientia Agricultura Sinica, 2022, 55(8): 1685-1694.
[10] MA XiaoYan,YANG Yu,HUANG DongLin,WANG ZhaoHui,GAO YaJun,LI YongGang,LÜ Hui. Annual Nutrients Balance and Economic Return Analysis of Wheat with Fertilizers Reduction and Different Rotations [J]. Scientia Agricultura Sinica, 2022, 55(8): 1589-1603.
[11] LI Qian,QIN YuBo,YIN CaiXia,KONG LiLi,WANG Meng,HOU YunPeng,SUN Bo,ZHAO YinKai,XU Chen,LIU ZhiQuan. Effect of Drip Fertigation Mode on Maize Yield, Nutrient Uptake and Economic Benefit [J]. Scientia Agricultura Sinica, 2022, 55(8): 1604-1616.
[12] ZHANG JiaHua,YANG HengShan,ZHANG YuQin,LI CongFeng,ZHANG RuiFu,TAI JiCheng,ZHOU YangChen. Effects of Different Drip Irrigation Modes on Starch Accumulation and Activities of Starch Synthesis-Related Enzyme of Spring Maize Grain in Northeast China [J]. Scientia Agricultura Sinica, 2022, 55(7): 1332-1345.
[13] TAN XianMing,ZHANG JiaWei,WANG ZhongLin,CHEN JunXu,YANG Feng,YANG WenYu. Prediction of Maize Yield in Relay Strip Intercropping Under Different Water and Nitrogen Conditions Based on PLS [J]. Scientia Agricultura Sinica, 2022, 55(6): 1127-1138.
[14] DONG SangJie,JIANG XiaoChun,WANG LingYu,LIN Rui,QI ZhenYu,YU JingQuan,ZHOU YanHong. Effects of Supplemental Far-Red Light on Growth and Abiotic Stress Tolerance of Pepper Seedlings [J]. Scientia Agricultura Sinica, 2022, 55(6): 1189-1198.
[15] LIU Miao,LIU PengZhao,SHI ZuJiao,WANG XiaoLi,WANG Rui,LI Jun. Critical Nitrogen Dilution Curve and Nitrogen Nutrition Diagnosis of Summer Maize Under Different Nitrogen and Phosphorus Application Rates [J]. Scientia Agricultura Sinica, 2022, 55(5): 932-947.
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