Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (4): 704-718.doi: 10.3864/j.issn.0578-1752.2025.04.007

• PLANT PROTECTION • Previous Articles     Next Articles

Genome-Wide Identification and Expression Analysis of HMG Family Genes in Botrytis cinerea

ZHANG TianYu(), LI Bai, ZANG JinPing, CAO HongZhe, DONG JinGao, XING JiHong(), ZHANG Kang()   

  1. College of Life Sciences, Hebei Agricultural University/Key Laboratory of Hebei Province for Plant Physiology and Molecular Pathology, Baoding 071000, Hebei
  • Received:2024-10-17 Accepted:2024-12-10 Online:2025-02-16 Published:2025-02-24
  • Contact: XING JiHong, ZHANG Kang

RichHTML

20

PDF

62

Abstract:

【Objective】High mobility group protein (HMG), as a widespread eukaryotic protein, plays an important role in the regulation of fungal growth and development. This study aims to identify the HMG family members of Botrytis cinerea through the genome-wide identification, and analyze their expression rules during the growth and development, infection and response to stress, so as to lay a foundation for further investigation of the function of this family gene in the growth and development and pathogenic mechanism of B. cinerea.【Method】HMMER software was used to screen out possible HMG gene IDs in B. cinerea protein database, and the online tools Pfam and SMART were used to verify the possible HMG family members. Using ProtParam, TBtools, MEME, MEGA, MCScanX and other tools, the physicochemical characteristics, chromosome localization, gene structure, phylogenetic tree and collinearity of B. cinerea HMG gene family members were analyzed. Based on transcriptome sequencing data of B. cinerea during conidial development and infection, the expression of HMG family genes in B. cinerea during conidial development and infection was analyzed by using TBtools software. In addition, the expression of HMG family genes in B. cinerea under NaCl, KCl, H2O2 and other stresses was observed by real-time quantitative PCR (qPCR).【Result】Nine HMG family members were identified in B. cinerea, the number of encoded amino acids ranged from 101 to 1076, and the molecular weight ranged from 11.48 to 120.64 kDa. They could be divided into HMGA and HMGB subfamilies, which had conserved HMG domain, distributed on six chromosomes, and had gene collinearity with Fusarium graminearum and Fusarium oxysporum. The expression pattern analysis showed that the expression levels of this family gene showed obvious changes during conidial development and B. cinerea infection. Among them, Bcin01g08840, Bcin07g04610, Bcin11g04340 and Bcin11g03320 continued to be highly expressed during conidial development. The expression levels of Bcin07g04610, Bcin11g04340, Bcin11g05790 and Bcin01g08840 were significantly down-regulated during B. cinerea infection. qPCR analysis showed that the gene expression of this family was significantly down-regulated after NaCl and KCl stress treatment.【Conclusion】B. cinerea contains nine HMG family members, which can be divided into HMGA and HMGB subfamilies, the members distribute on six chromosomes, and have different expression patterns in the process of conidial development, infection and stress response of the pathogen. It is speculated that the family genes play an important role in the growth and development, pathogenicity and stress response of B. cinerea.

Key words: Botrytis cinerea, HMG family gene, genome-wide, gene expression, bioinformatics, stress

Table 1

Primers used for qPCR"

基因名称 Gene name 引物序列 Primer sequence (5′→3′)
Bcin07g04610 F: GAATGGGAAGGCAAGCACAC R: CGCCTCTATTGACTCGCCAT
Bcin09g02870 F: GCGCGGTGATTGCTATTGAG R: TCCTGCATCTCAGAATCCGC
Bcin11g03320 F: AACAAGGCTGTCAATGCACG R: CGTTGCTCAGGCGACATAGA
Bcin05g01760 F: TCTACATGCAAACCGCTCGT R: CTACGAGTTGAGCATCGGCA
Bcin02g06030 F: CCGCATACCATCTACCCCAC R: GCTCCTGATACCTCTTCGCC
Bcin11g05790 F: CTGTGGTGATAGTTGGCCGT R: CTGCATGGGTCTCTGTTGGT
Bcin01g08840 F: ACAGGGCTACAGGGAAGGAT R: CGGCGATGCTGTTTTGAGTC
Bcin11g04340 F: TCCCCAGCAATCTTTCACCC R: TGGAAGGTGTTGATTGGGCT
Bcin11g05240 F: GCTCGCCATCCTCCAATACA R: GCAGAAAGTCCACGCTTTGG
β-tubulin F: ACATGCTCTGCCATTTTCCG R: TTGTTAGGGATCCACTCAACGAAG

Table 2

Physicochemical characteristics of the HMG family genes in B. cinerea"

基因名称
Gene name		 起始位点
Initiation site		 终止位点
Termination site		 CDS (bp) 氨基酸数目
Number of amino acids (aa)		 分子量
Molecular weight (Da)		 pI
Bcin01g08840 3070697 3074891 1629 542 59264 8.46
Bcin02g06030 2131709 2133995 2100 699 78297 8.98
Bcin05g01760 667383 669885 1026 341 36349 8.39
Bcin07g04610 1655881 1659887 3231 1076 120642 6.18
Bcin09g02870 1026663 1029821 2403 800 89042 9.39
Bcin11g03320 1138331 1139915 1008 335 37277 10.16
Bcin11g05240 1867672 1869358 306 101 11476 9.22
Bcin11g05790 2042942 2046139 1617 538 61800 6.49
Bcin11g04340 1606589 1608013 675 224 24949 7.76

Fig. 1

Phylogenetic tree of HMG gene family proteins"

Fig. 2

Phylogenetic analysis of HMG family proteins"

Fig. 3

Chromosomal localization of HMG family genes in B. cinerea"

Fig. 4

Collinearity relationships of HMG family genes in B. cinerea, F. oxysporum and F. graminearum"

Fig. 5

Gene structure analysis of HMG family genes in B. cinerea"

Fig. 6

Structural analysis of HMG family proteins in B. cinerea"

Fig. 7

Analysis of the conserved motifs of HMG family proteins in B. cinerea"

Fig. 8

Interaction protein prediction of B. cinerea HMG family proteins"

Fig. 9

Expression of HMG family genes during conidial development of B. cinerea"

Fig. 10

Expression of HMG family genes during B. cinerea infecting A. thaliana"

Fig. 11

Effects of stress treatment on the expression of HMG family genes in B. cinerea"

[1]
SOULLIER S, JAY P, POULAT F, VANACKER J M, BERTA P, LAUDET V. Diversification pattern of the HMG and SOX family members during evolution. Journal of Molecular Evolution, 1999, 48(5): 517-527.

pmid: 10198118
[2]
STROS M, LAUNHOLT D, GRASSER K D. The HMG-box: A versatile protein domain occurring in a wide variety of DNA-binding proteins. Cellular and Molecular Life Sciences, 2007, 64(19/20): 2590-2606.
[3]
骆辑, 潘润桑, 聂瑛洁, 陈辉, 罗振华, 何志旭. 高迁移率族核小体结合蛋白及其应用潜能. 山地农业生物学报, 2017, 36(3): 68-74.
LUO J, PAN R S, NIE Y J, CHEN H, LUO Z H, HE Z X. High-mobility group nucleosome-binding protein and its potential clinical uses. Journal of Mountain Agriculture and Biology, 2017, 36(3): 68-74. (in Chinese)
[4]
赵红霞, 苟萍. 灰葡萄孢菌致病机理研究进展. 生物技术, 2014, 24(1): 100-103.
ZHAO H X, GOU P. Advances in pathogenesis mechanism of Botrytis cinerea. Biotechnology, 2014, 24(1): 100-103. (in Chinese)
[5]
SI H L, ZHANG K, LI B, YUAN X M, ZANG J P, CAO H Z, XING J H, DONG J G. BcSDR1 is involved in regulation of glucose transport and cAMP and MAPK signaling pathways in Botrytis cinerea. Journal of Integrative Agriculture, 2022, 21(9): 2628-2640.
[6]
李白, 张子妍, 张强, 曹宏哲, 藏金萍, 张康, 邢继红, 董金皋. 灰葡萄孢bZIP家族基因的全基因组鉴定与表达规律分析. 农业生物技术学报, 2022, 30(4): 762-771.
LI B, ZHANG Z Y, ZHANG Q, CAO H Z, ZANG J P, ZHANG K, XING J H, DONG J G. Genome-wide identification and expression analysis of bZIP family genes in Botrytis cinerea. Journal of Agricultural Biotechnology, 2022, 30(4): 762-771. (in Chinese)
[7]
ZHANG K, YUAN X M, ZANG J P, WANG M, ZHAO F X, LI P F, CAO H Z, HAN J M, XING J H, DONG J G. The kynurenine 3-monooxygenase encoding gene, BcKMO, is involved in the growth, development, and pathogenicity of Botrytis cinerea. Frontiers in Microbiology, 2018, 9: 1039.
[8]
DUMITRIU I E, BARUAH P, VALENTINIS B, VOLL R E, HERRMANN M, NAWROTH P P, ARNOLD B, BIANCHI M E, MANFREDI A A, ROVERE-QUERINI P. Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. Journal of Immunology, 2005, 174(12): 7506-7515.

doi: 10.4049/jimmunol.174.12.7506 pmid: 15944249
[9]
CZAJA W, MILLER K Y, MILLER B L. Complex mechanisms regulate developmental expression of the matA (HMG) mating type gene in homothallic Aspergillus nidulans. Genetics, 2011, 189(3): 795-808.
[10]
BUSTIN M. Revised nomenclature for high mobility group (HMG) chromosomal proteins. Trends in Biochemical Sciences, 2001, 26(3): 152-153.

pmid: 11246012
[11]
BUSTIN M. Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Molecular and Cellular Biology, 1999, 19(8): 5237-5246.

doi: 10.1128/MCB.19.8.5237 pmid: 10409715
[12]
MONZEN K, ITO Y, NAITO A T, KASAI H, HIROI Y, HAYASHI D, SHIOJIMA I, YAMAZAKI T, MIYAZONO K, ASASHIMA M, NAGAI R, KOMURO I. A crucial role of a high mobility group protein HMGA2 in cardiogenesis. Nature Cell Biology, 2008, 10(5): 567-574.

doi: 10.1038/ncb1719 pmid: 18425117
[13]
BENKHALI J A, COPPIN E, BRUN S, PERAZA-REYES L, MARTIN T, DIXELIUS C, LAZAR N, VAN TILBEURGH H, DEBUCHY R. A network of HMG-box transcription factors regulates sexual cycle in the fungus Podospora anserina. PLoS Genetics, 2013, 9(7): e1003642.
[14]
BAKKAIOVA J, MARINI V, WILLCOX S, NOSEK J, GRIFFITH J D, KREJCI L, TOMASKA L. Yeast mitochondrial HMG proteins: DNA-binding properties of the most evolutionarily divergent component of mitochondrial nucleoids. Bioscience Reports, 2016, 36(1): e00288.
[15]
胡悦, 蔡英丽, 喻晶晶, 周雁, 李军平, 边银丙, 龚钰华. 香菇HMG-box转录因子lelcrp1基因的功能. 微生物学报, 2018, 58(12): 2100-2109.
HU Y, CAI Y L, YU J J, ZHOU Y, LI J P, BIAN Y B, GONG Y H. Function analysis of HMG-box transcription factor lelcrp1 in Lentinula edodes. Acta Microbiologica Sinica, 2018, 58(12): 2100-2109. (in Chinese)
[16]
HORTSCHANSKY P, ANDO E, TUPPATSCH K, ARIKAWA H, KOBAYASHI T, KATO M, HAAS H, BRAKHAGE A A. Deciphering the combinatorial DNA-binding code of the CCAAT- binding complex and the iron-regulatory basic region leucine zipper (bZIP) transcription factor HapX. Journal of Biological Chemistry, 2015, 290(10): 6058-6070.
[17]
贾晓曼, 王怡霖, 孙庚午, 何邦令, 葛顺峰, 王玉涛, 刘会香. 苹果腐烂病菌VmHMG基因敲除突变体获得及表型分析. 核农学报, 2018, 32(3): 448-454.

doi: 10.11869/j.issn.100-8551.2018.03.0448
JIA X M, WANG Y L, SUN G W, HE B L, GE S F, WANG Y T, LIU H X. Production and phenotypic analysis of mutants with knockout of VmHMG gene in Valsa mali var. mali causing apple canker. Journal of Nuclear Agricultural Sciences, 2018, 32(3): 448-454. (in Chinese)
[18]
YOSHIHARA R, LI Z H, ISHIMORI K, KUWABARA K, HATAKEYAMA S, TANAKA S. Phenotypic analysis of newly isolated short-lifespan Neurospora crassa mutant deficient in a high mobility group box protein. Fungal Genetics and Biology, 2017, 105: 28-36.
[19]
DING H, TANG L, GAO D, YAN X. The involvement of an HMG-box gene in germ cell genesis in Pyropia haitanensis. Algal Research, 2023, 70: 102978.
[20]
MURATA Y, FUJII M, ZOLAN M E, KAMADA T. Molecular analysis of pcc1, a gene that leads to A-regulated sexual morphogenesis in Coprinus cinereus. Genetics, 1998, 149(4): 1753-1761.
[21]
BROWN A J, CASSELTON L A. Mating in mushrooms: Increasing the chances but prolonging the affair. Trends in Genetics, 2001, 17(7): 393-400.

doi: 10.1016/s0168-9525(01)02343-5 pmid: 11418220
[22]
HARTMANN H A, KAHMANN R, BOLKER M. The pheromone response factor coordinates filamentous growth and pathogenicity in Ustilago maydis. EMBO Journal, 1996, 15(7): 1632-1641.
[23]
MURAGUCHI H, FUJITA T, KISHIBE Y, KONNO K, UEDA N, NAKAHORI K, YANAGI S O, KAMADA T. The exp1 gene essential for pileus expansion and autolysis of the inky cap mushroom Coprinopsis cinerea (Coprinus cinereus) encodes an HMG protein. Fungal Genetics and Biology, 2008, 45(6): 890-896.
[24]
卢园萍, 连玲丹, 郭丽, 严俊杰, 谢斌, 王威, 谢宝贵. 与草菇子实体形成和开伞相关的vv-exp基因的克隆及表达分析. 菌物学报, 2015, 34(4): 717-723.

doi: 10.13346/j.mycosystema.150088
LU Y P, LIAN L D, GUO L, YAN J J, XIE B, WANG W, XIE B G. Cloning and expression analysis of a vv-exp gene related to the formation and expansion of fruiting body in Volvariella volvacea. Mycosystema, 2015, 34(4): 717-723. (in Chinese)
[25]
SAKAMOTO Y, NAKADE K, SATO S, YOSHIDA K, MIYAZAKI K, NATSUME S, KONNO N. Lentinula edodes genome survey and postharvest transcriptome analysis. Applied and Environmental Microbiology, 2017, 83(10): e02990-16.
[26]
AMANZADEH E, MOHABATKAR H, BIRIA D. Classification of DNA minor and major grooves binding proteins according to the NLSs by data analysis methods. Applied Biochemistry and Biotechnology, 2014, 174(1): 437-451.

doi: 10.1007/s12010-014-0926-y pmid: 24869743
[27]
JIN M, WANG Y, ZHOU D, LIU W, HAN R, CHI Y. Downregulation of circ-YES1 suppresses NSCLC migration and proliferation through the miR-142-3p-HMGB1 axis. Respiratory Research, 2023, 24(1): 100.
[28]
ALBERT B, COLLERAN C, LÉGER-SILVESTRE I, BERGER A B, DEZ C, NORMAND C, PEREZ-FERNANDEZ J, MCSTAY B, GADAL O. Structure-function analysis of Hmo1 unveils an ancestral organization of HMG-Box factors involved in ribosomal DNA transcription from yeast to human. Nucleic Acids Research, 2013, 41(22): 10135-10149.

doi: 10.1093/nar/gkt770 pmid: 24021628
[29]
ALMASAN A, MISHRA N C. Molecular characterization of the mitochondrial DNA of a new stopper mutant ER-3 of Neurospora crassa. Genetics, 1988, 120(4): 935-945.
[1] DIAO DengChao, LI YunLi, MENG XiangYu, JI SongHan, SUN YuChen, MA XueHong, LI Jie, FENG YongJia, LI ChunLian, WU JianHui, ZENG QingDong, HAN DeJun, $\boxed{\hbox{WANG ChangFa}}$, ZHENG WeiJun. Cloning and Heat Tolerance Function of Wheat TaGRAS34-5A Gene [J]. Scientia Agricultura Sinica, 2025, 58(4): 617-634.
[2] WANG WenJuan, SHI ShangLi, KANG WenJuan, DU YuanYuan, YIN Chen. The Physiological Response of Longzhong Alfalfa to Exogenous Spermine Under Drought Stress [J]. Scientia Agricultura Sinica, 2025, 58(4): 676-691.
[3] ZHANG LinLin, GONG Rui, CUI YanLing, ZHONG XiongHui, LI Ye, LI RanHong, QIAN ZongWei. Effect Analysis of SmWRKY30 in Eggplant Resistance to Ralstonia solanacearum by Virus Induced Gene Silencing (VIGS) [J]. Scientia Agricultura Sinica, 2025, 58(3): 548-563.
[4] ZHOU GuangFei, MA Liang, MA Lu, ZHANG ShuYu, ZHANG HuiMin, SONG XuDong, ZHANG ZhenLiang, LU HuHua, HAO DeRong, MAO YuXiang, XUE Lin, CHEN GuoQing. Genome-Wide Association Study of Husk Traits in Maize [J]. Scientia Agricultura Sinica, 2025, 58(3): 431-442.
[5] GE Yi, ZHENG QiuLing, CHEN MengXia, XIA JiaXin, FANG Xiang, TANG MeiLing, FANG JingGui, SHANGGUAN LingFei. Cloning and Functional Analysis of the Autophagy Gene ATG8f in the Grapevine [J]. Scientia Agricultura Sinica, 2025, 58(1): 156-169.
[6] WANG Wei, WU ChuanLei, HU XiaoYu, LI JiaJia, BAI PengYu, WANG GuoJi, MIAO Long, WANG XiaoBo. Genome-Wide Identification of Soybean LOX Gene Family and the Effect of GmLOX15A1 Gene Allele on 100-Seed Weight [J]. Scientia Agricultura Sinica, 2025, 58(1): 10-29.
[7] ZHANG Ying, SHI TingRui, CAO Rui, PAN WenQiu, SONG WeiNing, WANG Li, NIE XiaoJun. Genome-Wide Association Study of Drought Tolerance at Seedling Stage in ICARDA-Introduced Wheat [J]. Scientia Agricultura Sinica, 2024, 57(9): 1658-1673.
[8] LI YongFei, LI ZhanKui, ZHANG ZhanSheng, CHEN YongWei, KANG JianHong, WU HongLiang. Effects of Postponing Nitrogen Fertilizer Application on Flag Leaf Physiological Characteristics and Yield of Spring Wheat Under High Temperature Stress [J]. Scientia Agricultura Sinica, 2024, 57(8): 1455-1468.
[9] LIN Wei, WU ShuiJin, LI YueSen. Transcriptome and Proteome Association Analysis to Revealthe Molecular Mechanism of Baxi Banana Seedlings in Response to Low Temperature [J]. Scientia Agricultura Sinica, 2024, 57(8): 1575-1591.
[10] CHEN BingXian, ZHANG Qi, DAI ZhangYan, ZHOU Xu, LIU Jun. Physiological and Molecular Effects of Salicylic Acid on Rice Seed Germination at Low Temperature [J]. Scientia Agricultura Sinica, 2024, 57(7): 1220-1236.
[11] WANG ChengZe, ZHANG Yan, FU Wei, JIA JingZhe, DONG JinGao, SHEN Shen, HAO ZhiMin. Bioinformatics and Expression Pattern Analysis of Maize ACO Gene Family [J]. Scientia Agricultura Sinica, 2024, 57(7): 1308-1318.
[12] 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.
[13] LUO LiDan, CHEN JiaMing, AN Qi, LIU Lei, SUN QinZhe, LIU Huan, WANG SenShan, SONG LiWen. Effects of Extreme High Temperature on Trehalose Content and Trehalose Transporter Gene in Tetranychus truncatus [J]. Scientia Agricultura Sinica, 2024, 57(6): 1091-1101.
[14] LIU ZhuoLin, LIU HongYun. The Potential and Mechanisms of Apigenin to Relieve Heat Stress and Hypoxia in Dairy Cows Based on Network Pharmacology and Molecular Docking [J]. Scientia Agricultura Sinica, 2024, 57(5): 1010-1022.
[15] WANG Yu, ZHANG YuPeng, ZHU GuanYa, LIAO HangXi, HOU WenFeng, GAO Qiang, WANG Yin. Effects of Localized Nitrogen Supply on Plant Growth and Water and Nitrogen Use Efficiencies of Maize Seedling Under Drought Stress [J]. Scientia Agricultura Sinica, 2024, 57(5): 919-934.
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