Scientia Agricultura Sinica ›› 2023, Vol. 56 ›› Issue (4): 711-728.doi: 10.3864/j.issn.0578-1752.2023.04.010

• HORTICULTURE • Previous Articles     Next Articles

Genome-Wide Identification and Expression Analysis of DIR Gene Family in Cucumber

ZHANG KaiJing1(), HE ShuaiShuai1, JIA Li2, HU YuChao1, YANG DeKun1, LU XiaoMin1, ZHANG QiAn2, YAN CongSheng2()   

  1. 1College of Agriculture, Anhui Science and Technology University, Fengyang 233100, Anhui
    2Institute of Horticulture, Anhui Academy of Agricultural Sciences/Key Laboratory of Horticultural Crop Germplasm Innovation and Utilization (Co-construction by Ministry and Province)/Key Laboratory of Genetic Improvement and Ecophysiology of Horticultural Crop, Anhui Province, Hefei 230031
  • Received:2022-04-13 Accepted:2022-06-07 Online:2023-02-16 Published:2023-02-24

RichHTML

129

PDF

331

Abstract:

【Objective】 Based on the cucumber (Cucumis sativus L.) genome information and transcriptome sequencing big-data, the DIR gene family in cucumber was identified with bioinformatics methods, and the expression pattern analysis of DIR family genes in different tissues and stresses response were analyzed. It would lay an important foundation for further study on the biological function of cucumber DIR genes. 【Method】 With the reported HMM model file of DIR gene, the probable DIR genes ID from the cucumber protein database was firstly identified using HMMSearch program in the HMMER software package. The cucumber DIR genes were ultimately verified using online tools Pfam and SMART. The tools of ExPASy, TBtools, GSDS, MEME, MEGA, MCScanX and Circos were used to analyze the physicochemical characteristics, chromosomal distributions, gene structure, phylogenetic tree and synteny of cucumber DIR genes. Based on cucumber transcriptome sequencing big-data of different tissues and under different stresses, transcriptome sequencing analysis was re-analyzed using cucumber V3 version genome information. The data of cucumber DIR genes in different transcriptome sequencing analysis were retrieved. The expression heatmaps of DIR gene family were drawn using TBtools software, and the expression patterns of cucumber DIR genes in different tissues and stresses response were analyzed. 【Result】 Total of 23 DIR genes were identified from cucumber genome, which distributed to 7 chromosomes. The number of amino acids of these DIR genes ranged from 78 to 684, and the molecular weight ranged from 8.70 to 73.82 kD. Phylogenetic analysis divided the cucumber DIR genes into 3 subgroups, the structure and motif of the genes in each subgroup were similar. Synteny analysis showed that the 12 cucumber DIR genes were collinearity with 19 Arabidopsis DIR genes and with 27 kinds of linear relationships, and 12 cucumber DIR genes were collinearity and with 11 rice DIR genes with 19 kinds of linear relationships. While only 8 cucumber DIR genes were conservative, which were not collinearity with any DIR gene in Arabidopsis and rice. Tissue-specific expression analysis revealed that some cucumber DIR genes had low or no expression levels in all tissues including root, stem, flower, fruit, leaf and so on, some cucumber DIR genes had high expression levels in all tissues, and some DIR genes had specific expression levels in some tissues, but no or low expression levels in other tissues. This suggested that different cucumber DIR genes had tissue specific expression patterns. The expression profiles analysis of cucumber DIR genes under biotic and abiotic stresses conditions revealed that cucumber DIR gene, CsaV3_4G023490, were up-regulated expression in response to all stresses, which meant this gene played an important role in the process of cucumber growth and development. 【Conclusion】 Total of 23 DIR genes were identified in cucumber, which were divided into 3 subgroups. The gene members in each subgroup were highly conserved, and the gene structure and protein conserved domain were different among 3 subgroups. The expression patterns of cucumber DIR genes in different tissues and stresses response were different, which coordinately regulated the growth and development of cucumber.

Key words: cucumber, DIR, gene family, bioinformatics, expression analysis

Table 1

The physiochemical characteristics of 23 members in the cucumber DIR gene family"

基因 ID
Gene ID		 CDS大小
CDS size (bp)		 氨基酸数目
Number of amino
acids (aa)		 分子量
Molecular weight (kD)		 等电点
pI		 不稳定性系数
Instability index		 脂肪系数
Aliphatic index		 亲水性平均值
Grand
average of hydropathicity		 亚细胞定位预测
Prediction of subcellular location
CsaV3_1G003340.1 552 183 19.94 6.06 32.24 90.00 0.255 质膜 Plasma membrane
CsaV3_1G003540.1 633 210 22.89 9.30 54.28 82.19 -0.111 线粒体 Mitochondrion
CsaV3_1G010290.1 774 257 27.81 5.69 46.08 75.53 -0.284 质膜Plasma membrane
CsaV3_2G015820.1 2055 684 73.82 9.13 33.65 92.27 -0.027 叶绿体 Chloroplast
CsaV3_2G015830.1 867 288 32.11 10.08 52.35 89.65 -0.136 质膜Plasma membrane
CsaV3_2G034820.1 639 212 22.68 9.69 21.78 78.73 -0.116 细胞外间隙 Extracellular space
CsaV3_3G011390.1 750 249 25.45 5.35 32.07 90.88 0.248 质膜Plasma membrane
CsaV3_3G015180.1 465 154 16.95 4.66 23.21 80.91 0.049 细胞外间隙 Extracellular space
CsaV3_4G006220.1 720 239 26.49 7.77 29.99 96.69 0.274 质膜Plasma membrane
CsaV3_4G006240.1 780 259 28.92 9.65 30.21 84.79 -0.055 质膜Plasma membrane
CsaV3_4G006250.1 576 191 21.26 8.63 28.03 86.81 0.163 质膜Plasma membrane
CsaV3_4G023480.1 237 78 8.70 9.85 36.49 70.00 -0.338 线粒体 Mitochondrion
CsaV3_4G023490.1 1284 427 48.16 9.48 35.62 88.85 -0.053 质膜Plasma membrane
CsaV3_4G023500.1 588 195 21.70 9.76 28.73 81.54 -0.030 质膜Plasma membrane
CsaV3_4G023510.1 528 175 19.53 9.58 23.03 95.20 -0.003 线粒体 Mitochondrion
CsaV3_5G006660.1 834 277 31.22 9.75 36.00 64.37 -0.420 线粒体 Mitochondrion
CsaV3_5G006670.1 1185 394 41.43 4.31 47.97 77.54 -0.177 细胞外间隙 Extracellular space
CsaV3_5G026130.1 990 329 34.01 5.08 33.90 79.12 -0.011 细胞外间隙 Extracellular space
CsaV3_6G006930.1 675 224 25.28 6.97 37.75 100.63 0.099 质膜Plasma membrane
CsaV3_7G003510.1 615 204 22.55 7.72 33.85 96.62 0.119 质膜Plasma membrane
CsaV3_7G005610.1 597 198 21.23 9.56 43.93 91.67 0.228 质膜Plasma membrane
CsaV3_7G005630.1 525 174 19.04 9.69 56.27 83.56 0.068 质膜Plasma membrane
CsaV3_7G022920.1 1770 589 66.23 8.49 49.45 89.63 -0.177 质膜Plasma membrane

Fig. 1

The distribution of DIR gene family on cucumber chromosomes The genes marked in red are tandem duplication gene pairs, and the genes marked in blue are segmental duplication gene pairs"

Fig. 2

Phylogenetic analysis of DIR genes from cucumber and Arabidopsis"

Fig. 3

Exon-intron structures of DIR genes and a schematic diagram of the amino acid motifs of DIR proteins in cucumber"

Table 2

The motifs information of cucumber DIR proteins"

基序
Motif		 序列
Sequence		 氨基酸数目
Number of amino acid		 Pfam注释
Pfam annotation
motif 1 FGTVVVIDBPLTEGPELGSKLIGRAQGFYASASQDGFGLLM 41 Dirigent
motif 2 JSFFGRNPILEKVREMPVVGGTGKFRFARG 30 Dirigent
motif 3 THLRFYFHDILSGKNPTAIAV 21 Dirigent
motif 4 AMNFAFTSGKYNGSS 15 Dirigent
motif 5 YAKAKTHYLDFTTGDAVVEYN 21 -
motif 6 EDENSFARTVNRKRLGLRKEK 21 -
motif 7 TITVLALFLFSSSSCSALPMVKKQKHKPC 29 -
motif 8 VPPVSNTSRTR 11 -
motif 9 MAGISPISPTHFLFLSFLL 19 -
motif 10 ENQHVTDGVDTJJHFSVYLSY 21 -

Fig. 4

Syntenic relationships of DIR gene family in cucumber, Arabidopsis and rice"

Fig. 5

Cis-elements analysis of the promoters of cucumber DIR family genes A: The number of various cis-elements in the promoters of each cucumber DIR gene. B: The relative proportions of different cis-elements in the promoters of cucumber DIR genes are displayed by the doughnut chart. Cis elements with the same or similar functions were represented in the same color"

Fig. 6

The expression heatmap of DIR gene family in different tissues of cucumber"

Fig. 7

The expression heatmaps of cucumber DIR gene family under abiotic stress treatments A: The expression patterns of cucumber DIR family genes under high temperature stress; HT0h_1, HT0h_2 and HT0h_3 were three replicates of the control treatment, HT3h_1 and HT3h_3 were two repetitions of high temperature treatment for 3 h, HT6h_1 and HT6h_3 were two repetitions of high temperature treatment for 6 h. B: The expression patterns of cucumber DIR family genes under low temperature stress; CT: Control, CS_2h: Low temperature treatment for 2 h, CS_6h: Low temperature treatment for 6 h; CS_12h: Low temperature treatment for 12 h. C: The expression patterns of cucumber DIR family genes under salt and silicon stresses; CT_1, CT_2 and CT_3 were three replicates of the control treatment, Na_1, Na_2 and Na_3 were three repetitions of salt stress treatment, Si_1 and Si_2 were two repetitions of silicon stress treatment. The data in the boxes indicated original FPKM values"

Fig. 8

The expression heatmaps of cucumber DIR gene family under biotic stress treatments A: The expression patterns of cucumber DIR family genes under downy mildew stress; S: Susceptible plants, R: Resistant plants, 1dpi, 2dpi, 3dpi, 4dpi and 6dpi were 1, 2, 3, 4 and 6 days post inoculation, respectively. B: The expression patterns of cucumber DIR family genes under powdery mildew stress; S: susceptible plants, R: Resistant plants, CT: Control, 48hpi: 48 hours post inoculation. C: The expression patterns of cucumber DIR family genes under root-knot nematode stress; S: Susceptible plants, R: Resistant plants, CT: Control, 1dpi, 2dpi and 3dpi were 1, 2 and 3 days post inoculation, respectively. The data in the boxes indicated original FPKM values"

Fig. 9

The expression patterns heatmap of cucumber DIR gene family under the abiotic and biotic stresses HT: High temperature stress; CS: Low temperature stress; Si: Silicon stress; DM: Downy mildew stress; PM: Powdery mildew stress; RKN: Root knot nematode stress. Gray color represents no change in expression level, red color represents up-regulated expression, green color represents down-regulated expression, and brown color represents both up-regulated and down-regulated expression"

[1]
BURLAT V, KWON M, DAVIN L B, LEWIS N G. Dirigent proteins and dirigent sites in lignifying tissues. Phytochemistry, 2001, 57(6): 883-897.

doi: 10.1016/s0031-9422(01)00117-0 pmid: 11423139
[2]
EFFENBERGER I, HARPORT M, PFANNSTIEL J, KLAIBER I, SCHALLER A. Expression in Pichia pastoris and characterization of two novel dirigent proteins for atropselective formation of gossypol. Applied Microbiology and Biotechnology, 2017, 101(5): 2021-2032.

doi: 10.1007/s00253-016-7997-3
[3]
HUANG S W, LI R Q, ZHANG Z H, LI L, GU X F, FAN W, LUCAS W J, WANG X W, XIE B Y, NI P X, REN Y, ZHU H M, LI J, LIN K, JIN W W, FEI Z J, LI G C, STAUB J B, KILIAN A, VAN DER VOSSEN E A G, et al. The genome of the cucumber, Cucumis sativus L. Nature Genetics, 2009, 41(12): 1275-1281.
[4]
陈家璐, 张智俊, 刘笑雨, 朱丰晓. 毛竹Dirigent基因家族的全基因组鉴定与分析. 植物生理学报, 2019, 55(9): 1406-1417. doi: 10.13592/j.cnki.ppj.2019.0238.

doi: 10.13592/j.cnki.ppj.2019.0238.
CHEN J L, ZHANG Z J, LIU X Y, ZHU F X. Genome-wide identification and analysis of Dirigent gene family in moso bamboo (Phyllostachys edulis). Plant Physiology Journal, 2019, 55(9): 1406-1417. doi: 10.13592/j.cnki.ppj.2019.0238. (in Chinese)

doi: 10.13592/j.cnki.ppj.2019.0238.
[5]
RALPH S G, JANCSIK S, BOHLMANN J. Dirigent proteins in conifer defense II: Extended gene discovery, phylogeny, and constitutive and stress-induced gene expression in spruce (Picea spp.). Phytochemistry, 2007, 68(14): 1975-1991.

doi: 10.1016/j.phytochem.2007.04.042
[6]
DAVIN L B, LEWIS N G. Dirigent phenoxy radical coupling: advances and challenges. Current Opinion in Biotechnology, 2005, 16(4): 398-406.

pmid: 16023845
[7]
MA Q H, LIU Y C. TaDIR13, a dirigent protein from wheat, promotes lignan biosynthesis and enhances pathogen resistance. Plant Molecular Biology Reporter, 2014, 33: 143-152.

doi: 10.1007/s11105-014-0737-x
[8]
DAVIN L B, WANG H B, CROWELL A L, BEDGAR D L, MARTIN D M, SARKANEN S, LEWIS N G. Stereoselective bimolecular phenoxy radical coupling by an auxiliary (dirigent) protein without an active center. Science, 1997, 275(5298): 362-366.

doi: 10.1126/science.275.5298.362 pmid: 8994027
[9]
PANIAGUA C, BILKOVA A, JACKSON P, DABRAVOLSKI S, RIBER W, DIDI V, HOUSER J, GIGLI-BISCEGLIA N, WIMMEROVA M, BUDÍNSKÁ E, HAMANN T, HEJATKO J. Dirigent proteins in plants: Modulating cell wall metabolism during abiotic and biotic stress exposure. Journal of experimental botany, 2017, 68(13): 3287-3301. doi: 10.1093/jxb/erx141.

doi: 10.1093/jxb/erx141 pmid: 28472349
[10]
LIAO Y R, LIU S B, JIANG Y Y, HU C Q, ZHANG X W, CAO X F, XU Z J, GAO X L, LI L H, ZHU J Q, CHEN R J. Genome-wide analysis and environmental response profiling of dirigent family genes in rice (Oryza sativa). Genes & Genomics, 2017, 39: 47-62.
[11]
SINGH D K, MEHRA S, CHATTERJEE S, PURTY R S. In silico identification and validation of miRNA and their DIR specific targets in Oryza sativa Indica under abiotic stress. Non-coding RNA Research, 2020, 5(4): 167-177.

doi: 10.1016/j.ncrna.2020.09.002
[12]
CHENG X, SU X Q, MUHAMMAD A, LI M L, ZHANG J Y, SUN Y M, LI G H, JIN Q, CAI Y P, LIN Y. Molecular characterization, evolution, and expression profiling of the Dirigent (DIR) family genes in Chinese white pear (Pyrus bretschneideri). Frontiers in Genetics, 2018, 9: 136.

doi: 10.3389/fgene.2018.00136
[13]
LI L L, SUN W B, ZHOU P J, WEI H, WANG P, LI H Y, REHMAN S, LI D W, ZHUGE Q. Genome-wide characterization of dirigent proteins in Populus: Gene expression variation and expression pattern in response to Marssonina brunnea and phytohormones. Forests, 2021, 12(4): 507.

doi: 10.3390/f12040507
[14]
ARASAN S K T, PARK J I, AHMED N U, JUNG H J, HUR Y, KANG K K, LIM Y P, NOU I S. Characterization and expression analysis of dirigent family genes related to stresses in Brassica. Plant Physiology and Biochemistry, 2013, 67: 144-153.

doi: 10.1016/j.plaphy.2013.02.030
[15]
KHAN A, LI R J, SUN J T, MA F, ZHANG H X, JIN J H, ALI M, HAQ S U, WANG J E, GONG Z H. Genome-wide analysis of dirigent gene family in pepper (Capsicum annuum L.) and characterization of CaDIR7 in biotic and abiotic stresses. Scientific Reports, 2018, 8: 5500.

doi: 10.1038/s41598-018-23761-0
[16]
SHI Y Q, SHEN Y R, AHMAD B, YAO L P, HE T N, FAN J S, LIU Y H, CHEN Q X, WEN Z F. Genome-wide identification and expression analysis of dirigent gene family in strawberry (Fragaria vesca) and functional characterization of FvDIR13. Scientia Horticulturae, 2022, 297: 110913.

doi: 10.1016/j.scienta.2022.110913
[17]
郭宝生, 师恭曜, 王凯辉, 刘素恩, 赵存鹏, 王兆晓, 耿军义, 华金平. 黄萎病菌侵染下陆地棉Dirigent-like蛋白基因表达差异分析. 中国农业科学, 2014, 47(22): 4349-4359. doi: 10.3864/j.issn.0578-1752.2014.22.001.

doi: 10.3864/j.issn.0578-1752.2014.22.001.
GUO B S, SHI G Y, WANG K H, LIU S E, ZHAO C P, WANG Z X, GENG J Y, HUA J P. Expression differences of dirigent-like protein genes in upland cotton respond to infection by Verticillium dahliae. Scientia Agricultura Sinica, 2014, 47(22): 4349-4359. doi: 10.3864/j.issn.0578-1752.2014.22.001. (in Chinese)

doi: 10.3864/ j.issn.0578-1752.2014.22.001.
[18]
WU R H, WANG L L, WANG Z, SHANG H H, LIU X, ZHU Y, QI D D, DENG X. Cloning and expression analysis of a dirigent protein gene from the resurrection plant Boea hygrometrica. Progress in Natural Science, 2009, 19(3): 347-352.

doi: 10.1016/j.pnsc.2008.07.010
[19]
GUO J L, XU L P, FANG J P, SU Y C, FU H Y, QUE Y X, XU J S. A novel dirigent protein gene with highly stem-specificexpression from sugarcane, response to drought, salt and oxidative stresses. Plant Cell Reports, 2012, 31(10): 1801-1812.

doi: 10.1007/s00299-012-1293-1
[20]
ANDRADE L M, PEIXOTO-JUNIOR R F, RIBEIRO R V, NÓBILE P M, BRITO M S, MARCHIORI P E R, CARLIN S D, MARTINS A P B, GOLDMAN M H S, LLERENA J P P, FREGONESI C, PERECIN D, NEBÓ J F C D O, FIGUEIRA A, BENATTI T R, DA SILVA J, MAZZAFERA P, CRESTE S. Biomass accumulation and cell wall structure of rice plants overexpressing a dirigent-jacalin of sugarcane (ShDJ) under varying conditions of water availability. Frontiers in Plant Science, 2019, 10: 65.

doi: 10.3389/fpls.2019.00065
[21]
LIU C H, QIN Z W, ZHOU X Y, XIN M, WANG C H, LIU D, LI S N. Expression and functional analysis of the propamocarb-related gene CsDIR16 in cucumbers. BMC Plant Biology, 2018, 18: 16.

doi: 10.1186/s12870-018-1236-2
[22]
RALPH S, PARK J Y, BOHLMANN J, MANSFIELD S D. Dirigent proteins in conifer defense: Gene discovery, phylogeny, and differential wound- and insect-induced expression of a family of DIR and DIR-like genes in spruce (Picea spp.). Plant Molecular Biology, 2006, 60: 21-40.

doi: 10.1007/s11103-005-2226-y
[23]
LI N H, ZHAO M, LIU T F, DONG L D, CHENG Q, WU J J, WANG L, CHEN X, ZHANG C Z, LU W C, XU P F, ZHANG S Z. A novel soybean dirigent gene GmDIR22 contributes to promotion of lignan biosynthesis and enhances resistance to Phytophthora sojae. Frontiers in Plant Science, 2017, 8: 1185.

doi: 10.3389/fpls.2017.01185
[24]
SENEVIRATNE H K, DALISAY D S, KIM K W, MOINUDDIN S G A, YANG H, HARTSHORN C M, DAVIN L B, LEWIS N G. Non-host disease resistance response in pea (Pisum sativum) pods: Biochemical function of DRR206 and phytoalexin pathway localization. Phytochemistry, 2015, 13: 140-148.
[25]
REBOLEDO G, DEL CAMPO R, ALVAREZ A, MONTESANO M, MARA H, PONCE DE LEÓN I. Physcomitrella patens activates defense responses against the pathogen Colletotrichum gloeosporioides. International Journal of Molecular Sciences, 2015, 16(9): 22280-22298.

doi: 10.3390/ijms160922280
[26]
BORGES A F, FERREIRA R B, MONTEIRO S. Transcriptomic changes following the compatible interaction Vitis vinifera-Erysiphe necator. Paving the way towards an enantioselective role in plant defence modulation. Plant Physiology and Biochemistry, 2013, 68: 71-80.

doi: 10.1016/j.plaphy.2013.03.024
[27]
LING J, JIANG W J, ZHANG Y, YU H J, MAO Z C, GU X F, HUANG S W, XIE B Y. Genome-wide analysis of WRKY gene family in Cucumis sativus. BMC Genomics, 2011, 12: 471.

doi: 10.1186/1471-2164-12-471
[28]
HU L F, LIU S Q. Genome-wide analysis of the MADS-box gene family in cucumber. Genome, 2012, 55(3): 245-256.

doi: 10.1139/g2012-009 pmid: 22376137
[29]
WAN H, YUAN W, BO K, SHEN J, PANG X, CHEN J F. Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics, 2013, 14: 109.

doi: 10.1186/1471-2164-14-109 pmid: 23418910
[30]
BALOGLU M C, ELDEM V, HAJYZADEH M, UNVER T. Genome-wide analysis of the bZIP transcription factors in cucumber. PLoS ONE, 2014, 9(4): e96014.

doi: 10.1371/journal.pone.0096014
[31]
YADAV V, WANG Z Y, YANG X Z, WEI C H, CHANGQING X, ZHANG X. Comparative analysis, characterization and evolutionary study of dirigent gene family in cucurbitaceae and expression of novel dirigent peptide against powdery mildew stress. Genes, 2021, 12(3): 326.

doi: 10.3390/genes12030326
[32]
LI Q, LI H B, HUANG W, XU Y C, ZHOU Q, WANG S H, RUAN J, HUANG S W, ZHANG Z H. A chromosome-scale genome assembly of cucumber (Cucumis sativus L.). GigaScience, 2019, 8(6): giz072. doi: 10.1093/gigascience/giz072.

doi: 10.1093/gigascience/giz072.
[33]
MISTRY J, CHUGURANSKY S, WILLIAMS L, QURESHI M, SALAZAR G A, SONNHAMMER E L L, TOSATTO S C E, PALADIN L, RAJ S, RICHARDSON L J, FINN R D, BATEMAN A. Pfam: The protein families database in 2021. Nucleic Acids Research, 2021, 49(D1): D412-D419. doi: 10.1093/nar/gkaa913.

doi: 10.1093/nar/gkaa913 pmid: 33125078
[34]
FINN R D, CLEMENTS J, EDDY S R. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 2011, 39: W29-W37. doi: 10.1093/nar/gkr367.

doi: 10.1093/nar/gkr367.
[35]
LETUNIC I, KHEDKAR S, BORK P. SMART: Recent updates, new developments and status in 2020. Nucleic Acids Research, 2021, 49(D1): D458-D460. doi: 10.1093/nar/gkaa937.

doi: 10.1093/nar/gkaa937 pmid: 33104802
[36]
YU C S, LIN C J, HWANG J K. Predicting subcellular localization of proteins for Gram-negative bacteria by support vector machines based on n-peptide compositions. Protein Science, 2004, 13(5): 1402-1406.

doi: 10.1110/ps.03479604
[37]
CHEN C J, CHEN H, ZHANG Y, THOMAS H R, FRANK M H, HE Y H, XIA R. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 2020, 13(8): 1194-1202.

doi: S1674-2052(20)30187-8 pmid: 32585190
[38]
HU B, JIN J P, GUO A Y, ZHANG H, LUO J C, GAO G. GSDS 2.0: An upgraded gene feature visualization server. Bioinformatics, 2015, 31(8): 1296-1297. doi: 10.1093/bioinformatics/btu817.

doi: 10.1093/bioinformatics/btu817 pmid: 25504850
[39]
BAILEY T L, WILLIAMS N, MISLEH C, LI W W. MEME: Discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research, 2006, 34: W369-W373. doi: 10.1093/nar/gkl198.

doi: 10.1093/nar/gkl198 pmid: 16845028
[40]
TAMURA K, STECHER G, KUMAR S. MEGA11: Molecular evolutionary genetics analysis version 11. Molecular Biology and Evolution, 2021, 38(7): 3022-3027. doi: 10.1093/molbev/msab120.

doi: 10.1093/molbev/msab120 pmid: 33892491
[41]
LESCOT M, DÉHAIS P, THIJS G, MARCHAL K, MOREAU Y, VAN DE PEER Y, ROUZÉ P, ROMBAUTS S. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 2002, 30(1): 325-327. doi: 10.1093/nar/30.1.325.

doi: 10.1093/nar/30.1.325 pmid: 11752327
[42]
WANG Y P, TANG H B, DEBARRY J D, TAN X, LI J P, WANG X Y, LEE T H, JIN H Z, MARLER B, GUO H, KISSINGER J C, PATERSON A H. MCScanX: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 2012, 40(7): e49. doi: 10.1093/nar/gkr1293.

doi: 10.1093/nar/gkr1293.
[43]
KRZYWINSKI M, SCHEIN J, BIROL I, CONNORS J, GASCOYNE R, HORSMAN D, JONES S J, MARRA M A. Circos: An information aesthetic for comparative genomics. Genome Research, 2009, 19(9): 1639-1645.

doi: 10.1101/gr.092759.109 pmid: 19541911
[44]
LI Z, ZHANG Z H, YAN P C, HUANG S W, FEI Z J, LIN K. RNA-Seq improves annotation of protein-coding genes in the cucumber genome. BMC Genomics, 2011, 12: 540.

doi: 10.1186/1471-2164-12-540 pmid: 22047402
[45]
CHEN C H, CHEN X Q, HAN J, LU W L, REN Z H. Genome-wide analysis of the WRKY gene family in the cucumber genome and transcriptome-wide identification of WRKY transcription factors that respond to biotic and abiotic stresses. BMC Plant Biology, 2020, 20: 443.

doi: 10.1186/s12870-020-02625-8
[46]
ZHU Y X, YIN J L, LIANG Y F, LIU J Q, JIA J H, HUO H Q, WU Z F, YANG R L, GONG H J. Transcriptomic dynamics provide an insight into the mechanism for silicon-mediated alleviation of salt stress in cucumber plants. Ecotoxicology and Environmental Safety, 2019, 174: 245-254.

doi: S0147-6513(19)30234-9 pmid: 30831473
[47]
BURKHARDT A, DAY B. Transcriptome and small RNAome dynamics during a resistant and susceptible interaction between cucumber and downy mildew. Plant Genome, 2016, 9(1): 1-19.
[48]
XU Q, XU X X, SHI Y, QI X H, CHEN X H. Elucidation of the molecular responses of a cucumber segment substitution line carrying Pm5.1 and its recurrent parent triggered by powdery mildew by comparative transcriptome profiling. BMC Genomics, 2017, 18: 21.

doi: 10.1186/s12864-016-3438-z
[49]
WANG X, CHENG C Y, ZHANG K J, TIAN Z, XU J, YANG S Q, LOU Q F, LI J, CHEN J F. Comparative transcriptomics reveals suppressed expression of genes related to auxin and the cell cycle contributes to the resistance of cucumber against Meloidogyne incognita. BMC Genomics, 2018, 19: 583.

doi: 10.1186/s12864-018-4979-0
[50]
谢玲娟, 叶楚玉, 沈恩惠. 植物基因组测序研究进展. 植物科学学报, 2021, 39(6): 681-691. doi: 10.11913/PSJ.2095-0837.2021.60681.

doi: 10.11913/PSJ.2095-0837.2021.60681.
XIE L J, YE C Y, SHEN E H. Advances in plant genome construction. Plant Science Journal, 2021, 39(6): 681-691. doi: 10.11913/PSJ.2095-0837.2021.60681. (in Chinese)

doi: 10.11913/PSJ.2095-0837.2021.60681.
[51]
UN Food and Agriculture Organization,Corporate Statistical Database (FAOSTAT). Production of cucumbers and gherkins in 2016[OL], 2017.
[52]
JAIN M, TYAGI A K, KHURANA J P. Genome-wide analysis, evolutionary expansion, and expression of early auxin-responsive SAUR gene family in rice (Oryza sativa). Genomics, 2006, 88(3): 360-371.

doi: 10.1016/j.ygeno.2006.04.008 pmid: 16707243
[53]
ZHANG S B, CHEN C, LI L, MENG L, SINGH J, JIANG N, DENG X W, HE Z H, LEMAUX P G. Evolutionary expansion, gene structure, and expression of the rice wall-associated kinase gene family. Plant Physiology, 2005, 139(3): 1107-1124. doi: 10.1104/pp.105.069005.

doi: 10.1104/pp.105.069005. pmid: 16286450
[54]
崔凯, 吴伟伟, 刁其玉. 转录组测序技术的研究和应用进展. 生物技术通报, 2019, 35(7): 1-9. doi: 10.13560/j.cnki.biotech.bull.1985.2019-0374.

doi: 10.13560/j.cnki.biotech.bull.1985.2019-0374
CUI K, WU W W, DIAO Q Y. Application and research progress on transcriptomics. Biotechnology Bulletin, 2019, 35(7): 1-9. doi: 10.13560/j.cnki.biotech.bull.1985.2019-0374. (in Chinese)

doi: 10.13560/j.cnki.biotech.bull.1985.2019-0374
[55]
LIU Q Q, LUO L, ZHENG L Q. Lignins: Biosynthesis and biological functions in plants. International Journal of Molecular Sciences, 2018, 19(2): 335.

doi: 10.3390/ijms19020335
[56]
ALVAREZ A, MONTESANO M, SCHMELZ E, PONCE DE LEÓN I. Activation of shikimate, phenylpropanoid, oxylipins, and auxin pathways in Pectobacterium carotovorum elicitors-treated moss. Frontiers in Plant Science, 2016, 7: 328.
[57]
PONCE DE LEÓN I, SCHMELZ E A, GAGGERO C, CASTRO A, ÁLVAREZ A, MONTESANO M. Physcomitrella patens activates reinforcement of the cell wall, programmed cell death and accumulation of evolutionary conserved defence signals, such as salicylic acid and 12-oxo-phytodienoic acid, but not jasmonic acid, upon Botrytis cinerea infection. Molecular Plant Pathology, 2012, 13(8): 960-974.

doi: 10.1111/j.1364-3703.2012.00806.x
[58]
WEIDENBACH D, ESCH L, MÖLLER C, HENSEL G, KUMLEHN J, HÖFLE C, HÜCKELHOVEN R, SCHAFFRATH U. Polarized defense against fungal pathogens is mediated by the jacalin-related lectin domain of modular poaceae-specific proteins. Molecular Plant, 2016, 9(4): 514-527.

doi: 10.1016/j.molp.2015.12.009
[59]
CORBIN C, DROUET S, MARKULIN L, AUGUIN D, LAINÉ É, DAVIN L B, CORT J R, LEWIS N G, HANO C. A genome-wide analysis of the flax (Linum usitatissimum L.) dirigent protein family: From gene identification and evolution to differential regulation. Plant Molecular Biology, 2018, 97: 73-101.

doi: 10.1007/s11103-018-0725-x
[1] XIE Jun, YIN XueWei, WEI Ling, WANG ZiFang, LI QingHu, ZHANG XiaoChun, LU YuanYuan, WANG QiuYue, GAO Ming. Effects of Control Irrigation on Grain Yield and Greenhouse Gas Emissions in Ridge Cultivation Direct-Seeding Paddy Field [J]. Scientia Agricultura Sinica, 2023, 56(4): 697-710.
[2] WANG ZhuangZhuang, DONG ShaoYun, ZHOU Qi, MIAO Han, LIU XiaoPing, XU KuiPeng, GU XingFang, ZHANG ShengPing. Cloning and Analysis of Key Genes for Vitamin C Synthesis in Cucumber Fruit [J]. Scientia Agricultura Sinica, 2023, 56(3): 508-518.
[3] ZHANG XiaoLi, TAO Wei, GAO GuoQing, CHEN Lei, GUO Hui, ZHANG Hua, TANG MaoYan, LIANG TianFeng. Effects of Direct Seeding Cultivation Method on Growth Stage, Lodging Resistance and Yield Benefit of Double-Cropping Early Rice [J]. Scientia Agricultura Sinica, 2023, 56(2): 249-263.
[4] LIU RUI, ZHAO YuHan, FU ZhongJu, GU XinYi, WANG YanXia, JIN XueHui, YANG Ying, WU WeiHuai, ZHANG YaLing. Distribution and Variation of PWL Gene Family in Rice Magnaporthe oryzae from Heilongjiang Province and Hainan Province [J]. Scientia Agricultura Sinica, 2023, 56(2): 264-274.
[5] LI QingLin,ZHANG WenTao,XU Hui,SUN JingJing. Metabolites Changes of Cucumber Xylem and Phloem Sap Under Low Phosphorus Stress [J]. Scientia Agricultura Sinica, 2022, 55(8): 1617-1629.
[6] LI ShiJia,LÜ ZiJing,ZHAO Jin. Identification of R2R3-MYB Subfamily in Chinese Jujube and Their Expression Pattern During the Fruit Development [J]. Scientia Agricultura Sinica, 2022, 55(6): 1199-1212.
[7] LAI ChunWang, ZHOU XiaoJuan, CHEN Yan, LIU MengYu, XUE XiaoDong, XIAO XueChen, LIN WenZhong, LAI ZhongXiong, LIN YuLing. Identification of Ethylene Synthesis Pathway Genes in Longan and Its Response to ACC Treatment [J]. Scientia Agricultura Sinica, 2022, 55(3): 558-574.
[8] GUO ShaoLei,XU JianLan,WANG XiaoJun,SU ZiWen,ZHANG BinBin,MA RuiJuan,YU MingLiang. Genome-Wide Identification and Expression Analysis of XTH Gene Family in Peach Fruit During Storage [J]. Scientia Agricultura Sinica, 2022, 55(23): 4702-4716.
[9] ZHANG HongCheng,HU YaJie,DAI QiGen,XING ZhiPeng,WEI HaiYan,SUN ChengMing,GAO Hui,HU Qun. Discussions on Frontiers and Directions of Scientific and Technological Innovation in China’s Field Crop Cultivation [J]. Scientia Agricultura Sinica, 2022, 55(22): 4373-4382.
[10] GUO BaoWei,TANG Chuang,WANG Yan,CAI JiaXin,TANG Jian,ZHOU Miao,JING Xiu,ZHANG HongCheng,XU Ke,HU YaJie,XING ZhiPeng,LI GuoHui,CHEN Heng. Effects of Two Mechanical Planting Methods on the Yield and Quality of High-Quality Late Indica Rice [J]. Scientia Agricultura Sinica, 2022, 55(20): 3910-3925.
[11] KANG Chen,ZHAO XueFang,LI YaDong,TIAN ZheJuan,WANG Peng,WU ZhiMing. Genome-Wide Identification and Analysis of CC-NBS-LRR Family in Response to Downy Mildew and Powdery Mildew in Cucumis sativus [J]. Scientia Agricultura Sinica, 2022, 55(19): 3751-3766.
[12] CHEN FengQiong, CHEN QiuSen, LIN JiaXin, WANG YaTing, LIU HanLin, LIANG BingRuoShi, DENG YiRu, REN ChunYuan, ZHANG YuXian, YANG FengJun, YU GaoBo, WEI JinPeng, WANG MengXue. Genome-Wide Identification of DIR Family Genes in Tomato and Response to Abiotic Stress [J]. Scientia Agricultura Sinica, 2022, 55(19): 3807-3821.
[13] GUO Jun,WANG KeHua,HAN Wei,DOU TaoCun,WANG XingGuo,HU YuPing,MA Meng,QU Liang. Analysis of Indirect Genetic Effects on Body Weight of 42 Day-Old Rugao Yellow Chickens [J]. Scientia Agricultura Sinica, 2022, 55(19): 3854-3861.
[14] Chao MA,YuBao WANG,Gang WU,Hong WANG,JianFei WANG,Lin ZHU,JiaJia LI,XiaoJing MA,RuShan CHAI. Research Progress of Direct Straw Return in Anhui Province over the Last Decade [J]. Scientia Agricultura Sinica, 2022, 55(18): 3584-3599.
[15] CHEN Xi,LIU YingJie,DONG YongHao,LIU JinYan,LI Wei,XU PengJun,ZANG Yun,REN GuangWei. Effects of CMV-Infected Tobacco on the Performance, Feeding and Host Selection Behavior of Myzus persicae [J]. Scientia Agricultura Sinica, 2021, 54(8): 1673-1683.
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