Identification and Expression Analysis of HSP90 Gene Family Under High Temperature Stress in Apple

doi:10.16420/j.issn.0513-353x.2020-0895

Acta Horticulturae Sinica ›› 2021, Vol. 48 ›› Issue (5): 849-859.doi: 10.16420/j.issn.0513-353x.2020-0895

• Research Papers • Next Articles

Identification and Expression Analysis of HSP90 Gene Family Under High Temperature Stress in Apple

YAO Fuwen^1,*, WANG Meige^1,*, SONG Chunhui¹, SONG Shangwei¹, JIAO Jian¹, WANG Miaomiao¹, WANG Kun², BAI Tuanhui¹^,^**(), ZHENG Xianbo¹^,^**()

¹College of Horticulture,Henan Agricultural University,Zhengzhou 450002,China
²Institute of Pomology,Chinese Academy of Agricultural Sciences,Xingcheng,Liaoning 125100,China

Received:2020-12-29 Revised:2021-04-08 Online:2021-05-25 Published:2021-06-07
Contact: BAI Tuanhui,ZHENG Xianbo E-mail:tuanhuibai88@163.com;xianboz@163.com

Abstract

Abstract:

In order to explore the role of heat shock protein(HSP90)gene family members in heat tolerance of apple(Malus × domestica Borkh.),bioinformatics method was used to identify the apple HSP90 gene family members,and their physicochemical properties,gene structure,cis elements,phylogenetic relationship and expression characteristics of HSP90 gene family under high temperature stress as well as in different tissues were analyzed. The results showed that a total of 11 HSP90 family members were identified in apple genome,which were distributed on 10 chromosomes. The amino acid sequence size was ranged from 104 to 818 aa,and molecular weight of protein ranged from 11.81 to 93.58 kD. Transcriptome analysis showed that four genes(MdHSP90-1,MdHSP90-3,MdHSP90-5and MdHSP90-11)of the 11 members were significantly up-regulated under high temperature stress. Subcellular localization analysis showed that MdHSP90-1,MdHSP90-3 and MdHSP90-5 proteins were located in the cell cytoplasm and nucleus,whereas MdHSP90-11 was targeted to the nucleus. Subsequent qRT-PCR analysis showed that the expression trend of the four genes in the two kinds of apple rootstocks were similar,the expression level increased greatly in the early stage of high temperature stress,and decreased in the middle and late stage. Four genes were also detected in different apple tissues,and the expressions of fourHSP90 genes were induced by heat stress to varying degrees,which indicated that the above four HSP90 genes may play an important role in the heat tolerance of apple.

Key words: apple, HSP90, high temperature stress, gene, structure, gene expression

CLC Number:

S661.1

YAO Fuwen, WANG Meige, SONG Chunhui, SONG Shangwei, JIAO Jian, WANG Miaomiao, WANG Kun, BAI Tuanhui, ZHENG Xianbo. Identification and Expression Analysis of HSP90 Gene Family Under High Temperature Stress in Apple[J]. Acta Horticulturae Sinica, 2021, 48(5): 849-859.

Figures/Tables 8

References 36

[1]	Al-Whaibi M H. 2011. Plant heat-shock proteins:a mini review. Journal of King Saud University science, 23:139-150. doi: 10.1016/j.jksus.2010.06.022 URL
[2]	Asea A A A, Kaur P, Calderwood S K. 2016. Heat shock proteins and plants//Heat shock proteins. Switzerland: Springer International Publishing.
[3]	Banilas G, Korkas E, Englezos V, Nisiotou A A, Hatzopoulos P. 2012. Genome wide analysis of the heat shock protein 90 gene family in grapevine (Vitis vinifera L.). Australian Journal of Grape and Wine Research, 18:29-38. doi: 10.1111/ajgw.2012.18.issue-1 URL
[4]	Botton A, Eccher G, Forcato C, Ferrarini A, Begheldo M, Zermiani M, Ramina A. 2011. Signalling pathways mediating the induction of apple fruitlet abscission. Plant Physiology, 155(1):185-208. doi: 10.1104/pp.110.165779 URL
[5]	Chen C, Chen H, Zhang Y, Thomas H R, Xia R. 2020. TBtools:an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13:8. doi: 10.1016/j.molp.2019.12.009 URL
[6]	El-Gebali J, Mistry A, Bateman S R, Eddy A, Luciani S C, Potter M, Quresh L J, Richardson G A, Salazar A, Smart E L L, Sonnhammer L, Hirsh L, Paladin D, Piovesan S C E, Tosatto R D. 2019. The Pfam protein families database in 2019. Nucleic Acids Research, 47:427-432.
[7]	Felsheim R F, Das A. 1992. Structure and expression of a heat-shock protein 83 gene of Pharbitis nil. Plant Physiology, 100:1764-1771. doi: 10.1104/pp.100.4.1764 URL
[8]	Gupta S C, Sharma A, Mishra M, Mishra R K, Chowdhuri D K. 2010. Heat shock proteins in toxicology:how close and how far? Life Science, 86(11-12):377-384.
[9]	Hsu A L, Murphy C T, Kenyon C. 2003. Regulation of aging and age-related disease by DAF-16 and heat-shock factor. Science, 300(5622):1142. doi: 10.1126/science.1083701 URL
[10]	Hu W, Hu G, Han B. 2009. Genome-wide survey and expression profiling of heat shock proteins and heat shock factors revealed overlapped and stress specific response under abiotic stresses in rice. Plant Science, 176(4):583-590. doi: 10.1016/j.plantsci.2009.01.016 URL
[11]	Ji X R, Yu Y H, Ni P Y, Zhang G H, Guo D L. 2019. Genome-wide identification of small heats hock protein(HSP20)gene family in grape and expression profile during berry development. BMC Plant Biology, 19:433. doi: 10.1186/s12870-019-2031-4 URL
[12]	Jin Z, Chandrasekaran U, Liu A. 2014. Genome-wide analysis of the Dof transcription factors in castor bean(Ricinus communis L.). Genes and Genomics, 36(4):527-537. doi: 10.1007/s13258-014-0189-6 URL
[13]	Krishna P, Gloor G. 2001. The HSP90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones, 6(3):238-246. doi: 10.1379/1466-1268(2001)006<0238:THFOPI>2.0.CO;2 URL
[14]	Liu Da-li. 2006. Cloning and characterization of rHsp90 gene in rice(Oryza sativa L.)under stress[Ph. D. Dissertation]. Habin:Northeast Forestry University. (in Chinese)
	刘大丽. 2006. 逆境胁迫下水稻(Oryza sativa L.) rHsp90基因的克隆及功能分析[硕士论文]. 哈尔滨:东北林业大学.
[15]	Liu Ling-ling. 2012. Sequence characterization and functional analysis of drought-tolerant genes ZmHSP90-1 and ZmMYB-R1 in maize[Ph. D. Dissertation]. Harbin:Northeast Agricultural University. (in Chinese)
	刘玲玲. 2012. 玉米耐旱相关基因ZmHSP90-1和ZmMYB-R1的序列特征分析与功能验证[硕士论文]. 哈尔滨:东北农业大学.
[16]	Liu Yun-fei, Wan Jian-hong, Yang Yue-jian, Wei Yan-ping, Li Zhi-miao, Ye Qing-jing, Wang Rong-qing, Ruan Mei-ying, Yao Zhu-ping, Zhou Guo-zhi. 2014. Genome-wide identification and analysis of heat shock protein 90 in tomato. Hereditas, 36(10):1043-1052. (in Chinese)
	刘云飞, 万红建, 杨悦俭, 韦艳萍, 李志邈, 叶青静, 王荣青, 阮美颖, 姚祝平, 周国治. 2014. 番茄热激蛋白90的全基因组鉴定及分析. 遗传, 36(10):1043-1052.
[17]	Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2^-∆∆CT method. Methods, 25(4):402-408. pmid: 11846609
[18]	Lescot M, Dhais P, Thijs G, Marchal K, Moreau Y, Van P, Rouz P, Rombauts S. 2002. PlantCARE,a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30(1):325-327. doi: 10.1093/nar/30.1.325 URL
[19]	Mukhopadhyay I, Nazir A, Saxena D K, Chowdhuri D K. 2003. Heat shock response:HSP70 in environmental monitoring. Journal of Biochemical and Molecular Toxicology, 17(5):249-54. doi: 10.1002/(ISSN)1099-0461 URL
[20]	Pearl L H, Prodromou C. 2006. Structure and mechanism of the Hsp90 molecular chaperone machinery. Annual Review of Biochemistry, 75(75):271. doi: 10.1146/annurev.biochem.75.103004.142738 URL
[21]	Prasinos C, Krampis K, Samakovli D, Hatzopoulos P. 2005. Tight regulation of expression of two Arabidopsis cytosolic HSP90 genes during embryo development. Journal of Experimental Biology, 56:633-644.
[22]	Prodromou C. 1997. Identification and structural characterization of the ATP/ADP binding site in the Hsp90 molecular chaperone. Cell, 90(1):65-75. pmid: 9230303
[23]	Queitsch C, Sangster T A, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature, 417(6889):618. doi: 10.1038/nature749 URL
[24]	Song H, Zhao R, Fan P, Wang X, Chen X, Li Y. 2009. Overexpression of AtHsp90.2,AtHsp90.5 and AtHsp90.7 in Arabidopsis thaliana enhances plant sensitivity to salt and drought stresses. Planta, 229(4):955-964. doi: 10.1007/s00425-008-0886-y URL
[25]	Song Z P, Pan F L, Yang C, Jia H F, Jiang H L, He F, Li N J, Lu X C, Zhang H Y. 2019. Genome-wide identification and expression analysis of HSP90 gene family in Nicotiana tabacum. BMC Genetics, 20:35. doi: 10.1186/s12863-019-0738-8 URL
[26]	Subramanian B, Gao S H, Lercher M J, Hu S N, Chen W H. 2019. Evolview v3:a webserver for visualization,annotation,and management of phylogenetic trees. Nucleic Acids Research, 47:270-275.
[27]	Terasawa K, Minami M, Minami Y. 2005. Constantly updated knowledge of hsp90. Journal of Biochemistry and Molecular Biology, 137(4):443.
[28]	Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, Fontana P, Bhatnagar S K, Troggio M, Pruss D. 2010. The genome of the domesticated apple(Malus domesticaBorkh.). Nature Genetics, 42:833-839. doi: 10.1038/ng.654 URL
[29]	Wang Jing, Tan Fangjun, Liang Chengliang, Zhang Xilu, Ou Lijun, Niran Juntawong, Wang Fei, Jiao Chunyan, Zou Xuexiao, Chen Wenchao. 2020. Genome-wide identification and analysis of HSP90 gene family in pepper. Acta Horticulturae Sinica, 47(4):665-674. (in Chinese)
	王静, 谭放军, 梁成亮, 张西露, 欧立军, Niran Juntawong, 王飞, 焦春海, 邹学校, 陈文超. 2020. 辣椒热激蛋白HSP90家族基因鉴定及分析. 园艺学报, 47(4):665-674.
[30]	Wang W, Vinocur B, Shoseyov O, Altman A. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Science, 9(5):244-252. doi: 10.1016/j.tplants.2004.03.006 URL
[31]	Xu J Y, Xue C C, Xue D, Zhao J M, Gai J Y, Guo N, Xing H, Swati P D. 2013. Overexpression of GmHsp90s,a heat shock protein 90(HSP90)gene family cloning from soybean,decrease damage of abiotic stresses inArabidopsis thaliana. PLoS ONE, 8(7):e69810. doi: 10.1371/journal.pone.0069810 URL
[32]	Yan Shuangshuang, Qiu Zhengkun, Yu Bingwei, Ming Fangyan, Chen Changming, Lei Jianjun, Cao Bihao. 2020. Advances in phytohormone auxin response to high temperature. Acta Horticulturae Sinica, 47(11):2238-2246. (in Chinese)
	颜爽爽, 邱正坤, 余炳伟, 明方艳, 陈长明, 雷建军, 曹必好. 2020. 植物生长素响应高温胁迫研究进展. 园艺学报, 47(11):2238-2246.
[33]	Yang Z, Zhou Y, Wang X, Gu S, Yu J, Liang G, Yan C, Xu C. 2008. Genome wide comparative phylogenetic and molecular evolutionary analysis of tubby-like protein family in Arabidopsis,rice,and poplar. Genomics, 92(4):246-53. doi: 10.1016/j.ygeno.2008.06.001 URL
[34]	Wang Yi, Li Wei, Xu Xuefeng, Qiu Changpeng, Wu Ting, Wei Qinping, Ma Fengwang, Han Zhenhai. 2019. Progress of apple rootstock breeding and its use. Horticultural Plant Journal, 5(5):183-191. doi: 10.1016/j.hpj.2019.06.001
[35]	Zai W S, Miao L X, Xiong Z L, Zhang H L, Ma Y R, Li Y L, Chen Y B, Ye S G. 2015. Comprehensive identification and expression analysis of Hsp90s gene family in Solanum lycopersicum. Genetics and Molecular Research, 14(3):7811-7820. doi: 10.4238/2015.July.14.7 pmid: 26214462
[36]	Zhang J, Li J, Liu B, Zhang L, Chen J, Liu M Z. 2013. Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns,localization,and heat stress responses. BMC Genomics, 14(1):532. doi: 10.1186/1471-2164-14-532 URL

用途Useage	基因 Gene	引物(5′-3′)Primer
实时荧光定量qRT-PCR	MdHSP90-1	F:CGTCGATTCGGATGATTTGC;R:TGGCTCTGTTCTGGCTGTCC
	MdHSP90-3	F:GGAAATCAGCGACGACGAAG;R:CAAGGTGCTCCTCCCAGTCA
	MdHSP90-5	F:ATGTTGCTTCTGACAGCGTGAC;R:CCATATTCCTGCTTAATCTCCTTTT
	MdHSP90-11	F:CGTATTGCTCCGTTGCTTAG;R:AGTTTCTCCAGGAATGGTGTATT
	Actin	F:GGATTTGCTGGTGATGATGCT;R:AGTTGCTCACTATGCCGTGC
亚细胞定位 Subcellular location	GFPHSP90-1	F:GTGGATCCAAAGAATTCATGGCCGACGTTCAGATGCAC
		R:CTCCTTTACCCATGAATTCTCAAAATTATATTAACATTATCGAG
	GFPHSP90-3	F:GTGGATCCAAAGAATTCCCGATGTCAGCATGATTGG
		R:CTCCTTTACCCATGAATTCAAAAACCCGAAACATCCACAAACTC
	GFPHSP90-9	F:GTGGATCCAAAGAATTCATGCACAGGCTCCCAC
		R:CTCCTTTACCCATGAATTCTTTCTGGCTGCC
	GFPHSP90-11	F:GTGGATCCAAAGAATTCATGCACAGGCTCCCACGACGCTCCG
		R:CTCCTTTACCCATGAATTCTTTCTGACTGCCG

用途Useage	基因 Gene	引物(5′-3′)Primer
实时荧光定量qRT-PCR	MdHSP90-1	F:CGTCGATTCGGATGATTTGC;R:TGGCTCTGTTCTGGCTGTCC
	MdHSP90-3	F:GGAAATCAGCGACGACGAAG;R:CAAGGTGCTCCTCCCAGTCA
	MdHSP90-5	F:ATGTTGCTTCTGACAGCGTGAC;R:CCATATTCCTGCTTAATCTCCTTTT
	MdHSP90-11	F:CGTATTGCTCCGTTGCTTAG;R:AGTTTCTCCAGGAATGGTGTATT
	Actin	F:GGATTTGCTGGTGATGATGCT;R:AGTTGCTCACTATGCCGTGC
亚细胞定位 Subcellular location	GFPHSP90-1	F:GTGGATCCAAAGAATTCATGGCCGACGTTCAGATGCAC
		R:CTCCTTTACCCATGAATTCTCAAAATTATATTAACATTATCGAG
	GFPHSP90-3	F:GTGGATCCAAAGAATTCCCGATGTCAGCATGATTGG
		R:CTCCTTTACCCATGAATTCAAAAACCCGAAACATCCACAAACTC
	GFPHSP90-9	F:GTGGATCCAAAGAATTCATGCACAGGCTCCCAC
		R:CTCCTTTACCCATGAATTCTTTCTGGCTGCC
	GFPHSP90-11	F:GTGGATCCAAAGAATTCATGCACAGGCTCCCACGACGCTCCG
		R:CTCCTTTACCCATGAATTCTTTCTGACTGCCG

基因名称 Gene name	序列ID Sequence ID	染色体 Chr	基因组位置 Genomic location	开放阅读框/bp ORF	氨基酸/aa Amino acid	蛋白质分子质量/kD mw	等电点 pI
MdHSP90-1	MD01G1208700	1	30 315 406 ~ 30 318 680	2 112	703	80.77	5.00
MdHSP90-2	MD03G1036600	3	2 907 372 ~ 2 910 570	2 100	699	80.21	4.95
MdHSP90-3	MD07G1279200	7	34 367 607 ~ 34 369 506	1 749	582	67.39	5.06
MdHSP90-4	MD08G1011200	8	864 457 ~ 869 106	2 547	818	93.59	4.85
MdHSP90-5	MD09G1122200	9	9 421 880 ~ 9 427 733	2 430	809	91.89	5.29
MdHSP90-6	MD11G1037400	11	3 204 284 ~ 3 207 461	2 100	699	80.04	4.95
MdHSP90-7	MD11G1152300	11	14 614 376 ~ 14 614 690	315	104	11.81	4.16
MdHSP90-8	MD13G1055300	13	3 867 643 ~ 3 871 210	1 143	380	43.56	4.89
MdHSP90-9	MD14G1110600	14	17 566 378 ~ 17 567 467	930	309	36.35	9.40
MdHSP90-10	MD16G1054100	16	3 825 148 ~ 3 830 828	2 385	794	89.67	5.02
MdHSP90-11	MD17G1113200	17	9 690 370 ~ 9 696 630	2 421	806	91.69	5.34

基因名称 Gene name	序列ID Sequence ID	染色体 Chr	基因组位置 Genomic location	开放阅读框/bp ORF	氨基酸/aa Amino acid	蛋白质分子质量/kD mw	等电点 pI
MdHSP90-1	MD01G1208700	1	30 315 406 ~ 30 318 680	2 112	703	80.77	5.00
MdHSP90-2	MD03G1036600	3	2 907 372 ~ 2 910 570	2 100	699	80.21	4.95
MdHSP90-3	MD07G1279200	7	34 367 607 ~ 34 369 506	1 749	582	67.39	5.06
MdHSP90-4	MD08G1011200	8	864 457 ~ 869 106	2 547	818	93.59	4.85
MdHSP90-5	MD09G1122200	9	9 421 880 ~ 9 427 733	2 430	809	91.89	5.29
MdHSP90-6	MD11G1037400	11	3 204 284 ~ 3 207 461	2 100	699	80.04	4.95
MdHSP90-7	MD11G1152300	11	14 614 376 ~ 14 614 690	315	104	11.81	4.16
MdHSP90-8	MD13G1055300	13	3 867 643 ~ 3 871 210	1 143	380	43.56	4.89
MdHSP90-9	MD14G1110600	14	17 566 378 ~ 17 567 467	930	309	36.35	9.40
MdHSP90-10	MD16G1054100	16	3 825 148 ~ 3 830 828	2 385	794	89.67	5.02
MdHSP90-11	MD17G1113200	17	9 690 370 ~ 9 696 630	2 421	806	91.69	5.34

Identification and Expression Analysis of HSP90 Gene Family Under High Temperature Stress in Apple

RichHTML

PDF

Knowledge

Abstract

Cite this article

share this article

Figures/Tables 8

References 36

Related Articles 15

Recommended Articles

Metrics

Comments

[1]	WANG Xiaochen, NIE Ziye, LIU Xianju, DUAN Wei, FAN Peige, and LIANG Zhenchang, . Effects of Abscisic Acid on Monoterpene Synthesis in‘Jingxiangyu’Grape Berries [J]. Acta Horticulturae Sinica, 2023, 50(2): 237-249.
[2]	WANG Rui, HONG Wenjuan, LUO Hua, ZHAO Lina, CHEN Ying, and WANG Jun, . Construction of SSR Fingerprints of Pomegranate Cultivars and Male Parent Identification of Hybrids [J]. Acta Horticulturae Sinica, 2023, 50(2): 265-278.
[3]	ZHANG Xin, QI Yanxiang, ZENG Fanyun, WANG Yanwei, XIE Peilan, XIE Yixian, and PENG Jun. Functional Analysis of Dicer-like Genes in Fusarium oxysporum f. sp. cubense Race 4 [J]. Acta Horticulturae Sinica, 2023, 50(2): 279-294.
[4]	YU Tingting, LI Huan, NING Yuansheng, SONG Jianfei, PENG Lulin, JIA Junqi, ZHANG Weiwei, and YANG Hongqiang. Genome-wide Identification of GRAS Gene Family in Apple and Expression Analysis of Its Response to Auxin [J]. Acta Horticulturae Sinica, 2023, 50(2): 397-409.
[5]	WANG Mengmeng, SUN Deling, CHEN Rui, YANG Yingxia, ZHANG Guan, LÜ Mingjie, WANG Qian, XIE Tianyu, NIU Guobao, SHAN Xiaozheng, TAN Jin, and YAO Xingwei, . Construction and Evaluation of Cauliflower Core Collection [J]. Acta Horticulturae Sinica, 2023, 50(2): 421-431.
[6]	ZHAI Hanhan, ZHAI Yujie, TIAN Yi, ZHANG Ye, YANG Li, WEN Zhiliang, CHEN Haijiang. Genome-wide Identification of Peach SAUR Gene Family and Characterization of PpSAUR5 Gene [J]. Acta Horticulturae Sinica, 2023, 50(1): 1-14.
[7]	YANG Zhi, ZHANG Chuanjiang, YANG Xinfang, DONG Mengyi, WANG Zhenlei, YAN Fenfen, WU Cuiyun, WANG Jiurui, LIU Mengjun, LIN Minjuan. Analysis of Fruit Genetic Tendency and Mixed Inheritance in Hybrid Progeny of Jujube and Wild Jujube [J]. Acta Horticulturae Sinica, 2023, 50(1): 36-52.
[8]	HU Jingyu, QUE Kaijuan, MIAO Tianli, WU Shaozheng, WANG Tiantian, ZHANG Lei, DONG Xian, JI Pengzhang, DONG Jiahong. Identification of Tomato Spotted Wilt Orthotospovirus Infecting Iris tectorum [J]. Acta Horticulturae Sinica, 2023, 50(1): 170-176.
[9]	SHAO Fengqing, LUO Xiurong, WANG Qi, ZHANG Xianzhi, WANG Wencai. Advances in Research of DNA Methylation Regulation During Fruit Ripening [J]. Acta Horticulturae Sinica, 2023, 50(1): 197-208.
[10]	HAN Xiaolei, ZHANG Caixia, LIU Kai, YANG An, YAN Jiadi, LI Wuxing, KANG Liqun, and CONG Peihua. A New Mid-ripening Apple Cultivar‘Zhongping Youlei’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 1-2.
[11]	OU Kefang, SUN Hongbing, ZHAO Lekang, and DUAN Qingming. A New Waterlily Cultivar‘Yunjin Niangniang’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 217-218.
[12]	SUN Simiao, WANG Kun, GAO Yuan, WANG Dajiang, and LI Lianwen. A New Ornamental Crabapple Cultivar‘Zichen’ [J]. Acta Horticulturae Sinica, 2022, 49(S2): 267-268.
[13]	HAN Xiaolei, ZHANG Caixia, LIU Kai, YAN Jiadi, LI Wuxing, KANG Liqun, and CONG Peihua. A New Mid-ripening Apple Cultivar‘Pingyou 2’ [J]. Acta Horticulturae Sinica, 2022, 49(S1): 1-2.
[14]	WANG Qiang, CONG Peihua, and LIU Xiaofeng. A New Late Ripening Apple Cultivar‘Huayou Tianwa’ [J]. Acta Horticulturae Sinica, 2022, 49(S1): 3-4.
[15]	WANG Qiang, CONG Peihua, and LIU Xiaofeng. A New Mid-ripening Apple Cultivar‘Huayou Baomi’ [J]. Acta Horticulturae Sinica, 2022, 49(S1): 5-6.