苹果MdTOPP13/28在腋芽萌发中的表达分析

doi:10.16420/j.issn.0513-353x.2022-0011

摘要/Abstract

摘要：

利用苹果全基因组数据，对苹果TOPP基因家族进行鉴定和生物学分析。结果表明：苹果TOPP基因家族共44个成员，分布于15条染色体上；系统进化树分析表明，苹果、桃和拟南芥TOPP高度同源；苹果TOPP基因结构中含1 ~ 2个外显子和0 ~ 20个内含子，以及10个保守基序；启动子顺式作用元件分析表明，苹果TOPP基因家族成员不仅受到光、热等环境影响，还受多种激素综合调控；基因芯片表达谱分析结果表明该基因家族在不同组织中均有表达。分析外源细胞分裂素（6-BA和TDZ）诱导苹果腋芽萌发的转录组数据，锁定了与其相关的候选基因MdTOPP13和MdTOPP28；克隆其序列并进行比对，两者表现出高同源性。以苹果砧木品种‘SH40’腋芽为材料，实时定量PCR分析表明，外源6-BA和TDZ处理后上调了MdTOPP13和MdTOPP28在腋芽中的表达量。综上可知，MdTOPP13和MdTOPP28在介导细胞分裂素调控腋芽萌发过程中可能发挥着重要作用。

关键词: 苹果, TOPP, 腋芽, 萌发, 细胞分裂素

Abstract:

In this study，apple whole-genome data were used to identify and conduct a biological analysis of the MdTOPP gene family. A total of 44 TOPP genes were systematically identified from apple genome，and they distributed on 15 chromosomes. The phylogenetic tree analysis showed that MdTOPP，PpTOPP and AtTOPP were highly homologous；the gene structure and conserved domain analysis showed that 1-2 exons，0-20 introns and 10 conserved motifs were in MdTOPP genes. The promoter cis-acting element analysis showed that the MdTOPP genes were not only affected by the external environment such as light and heat，but also comprehensively regulated by multiple hormones. All the MdTOPP genes have distinctive expression patterns in different apple tissues. MdTOPP13 and MdTOPP28 were identified from the transcriptome data of exogenous cytokinin（6-BA and TDZ）induced apple axillary bud outgrowth，and cloning sequence alignment showed high homology. Using quantitative real-time PCR，the expressions of MdTOPP13 and MdTOPP28 were upregulated after exogenous 6-BA or TDZ applied on the axillary buds of apple rootstock‘SH40’. In summary，MdTOPP13 and MdTOPP28 may play an important role in mediating cytokinin regulation of axillary bud outgrowth.

Key words: apple, TOPP, axillary bud, outgrowth, cytokinin

中图分类号:

S666.1

刘柚藓, 李国防, 檀鸣, 杨志昌, 周世伟, 霍文静, 张鹤, 孙建设, 邵建柱. 苹果MdTOPP13/28在腋芽萌发中的表达分析[J]. 园艺学报, 2023, 50(4): 697-712.

LIU Youxian, LI Guofang, TAN Ming, YANG Zhichang, ZHOU Shiwei, HUO Wenjing, ZHANG He, SUN Jianshe, SHAO Jianzhu. Expression Analysis of MdTOPP13/28 During Axillary Bud Outgrowth in Malus[J]. Acta Horticulturae Sinica, 2023, 50(4): 697-712.

图/表 12

参考文献 38

[1]	Aggen J B, Nairn A C, Chamberlin R. 2000. Regulation of protein phosphatase-1. Chemistry & Biology, 7 (1):R13-R23. doi: 10.1016/S1074-5521(00)00069-7 URL
[2]	Bennett T, Hines G, van Rongen M, Waldie T, Sawchuk M G, Scarpella E, Ljung K, Leyser O. 2016. Connective auxin transport in the shoot facilitates communication between shoot apices. PLoS Biol, 14 (4):e1002446.
[3]	Böhm S, Buchberger A. 2013. The budding yeast Cdc48(Shp1)complex promotes cell cycle progression by positive regulation of protein phosphatase 1(Glc7). PLoS ONE, 8 (2):276-276.
[4]	Chatfield S P, Stirnberg P, Forde B G, Leyser O. 2000. The hormonal regulation of axillary bud growth in Arabidopsis. Plant Journal, 24 (2):159-169. doi: 10.1046/j.1365-313x.2000.00862.x pmid: 11069691
[5]	Cline M G. 1991. Apical dominance. The Botanical Review, 57 (4):318-358. doi: 10.1007/BF02858771 URL
[6]	Cohen P T. 2002. Protein phosphatase 1-targeted in many directions. J Cell Sci, 115:241-256. doi: 10.1242/jcs.115.2.241 URL
[7]	Chen Hong-fei, Shao Hong-xia, Fan Sheng, Ma Juan-juan, Zhang Dong, Han Ming-yu. 2016. Identification and phylogenetic analysis of the polygalacturonase gene family in apple. Acta Horticulturae Sinica, 43 (10):1863-1877. (in Chinese) doi: 10.16420/j.issn.0513-353x.2016-0224 URL
	陈鸿飞, 邵红霞, 樊胜, 马娟娟, 张东, 韩明玉. 2016. 苹果全基因组多聚半乳糖醛酸酶基因家族的鉴定及进化分析. 园艺学报, 43 (10):1863-1877. doi: 10.16420/j.issn.0513-353x.2016-0224 URL
[8]	Daccord N, Celton J M, Linsmith G, Becker C, Choisne N, Schijlen E, Geest H, Bianco L, Micheletti D, Velasco R, Di Pierro E A, Gouzy J, Rees D J G, Guérif P, Muranty H, Durel C E, Laurens F, Lespinasse Y, Gaillard S, Aubourg S, Quesneville H, Weigel D, Weg E, Troggio M, Bucher E. 2017. High-quality de novo assembly of the apple genome and methylome dynamics of early fruit development. Nature Genetics, 49:1099-1106. doi: 10.1038/ng.3886
[9]	Fan S, Zhang D, Xing L, Qi S, Du L, Wu H, Shao H, Li Y, Ma J, Han M. 2017. Phylogenetic analysis of IDD gene family and characterization of its expression in response to flower induction in Malus. Molecular Genetics and Genomics, 292 (4):755. doi: 10.1007/s00438-017-1306-4
[10]	Fan Sheng, Zhang Lan-qing, Liu Ke, Lei Chao, Chen Xin, Yao Dian-cheng, Zhang Dong, Han Ming-yu. 2016. Cloning and expression of the flowering regulation transcription factor gene MdSPL6 in Malus × domestica. Acta Horticulturae Sinica, 43 (11):2089-2098. (in Chinese)
	樊胜, 张岚清, 刘柯, 雷超, 陈欣, 姚殿城, 张东, 韩明玉. 2016. 苹果‘长富2号’开花调控转录因子MdSPL6基因的克隆和表达分析. 园艺学报, 43 (11):2089-2098.
[11]	Farkas I, Dombrádi V, Miskei M, Szabados L, Koncz C. 2007. Arabidopsis PPP family of serine/threonine phosphatases. Trends in Plant Science, 12:169-181. doi: 10.1016/j.tplants.2007.03.003 pmid: 17368080
[12]	Foster T M, Ledger S E, Janssen B J, Luo Z W, Drummond Revel S M, Tomes S, Karunairetnam S, Waite C N, Funnell K A, van Hooijdonk B M, Saei A, Seleznyova A N, Snowden K C. 2018. Expression of MdCCD7 in the scion determines the extent of sylleptic branching and the primary shoot growth rate of apple trees. Journal of Experimental Botany, 69 (9):2379-2390. doi: 10.1093/jxb/erx404 pmid: 29190381
[13]	Gill S S, Tajrishi M, Madan M, Tuteja N. 2013. A DESD-box helicase functions in salinity stress tolerance by improving photosynthesis and antioxidant machinery in rice(Oryza sativa). Plant Molecular Biology, 82:1-22. doi: 10.1007/s11103-013-0031-6 URL
[14]	Heisler M G, Ohno C, Das P, Sieber P, Reddy G V, Long J A, Meyerowitz E M. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Current Biology, 15 (21):1899-1911. doi: 10.1016/j.cub.2005.09.052 pmid: 16271866
[15]	Hou Y J, Zhu Y, Wang P, Zhao Y, Xie S, Giorgia B, Wang B, Duan C G, Wang X, Xing L. 2016. Type one protein phosphatase 1 and its regulatory protein inhibitor 2 negatively regulate ABA signaling. PLoS Genetics, 12:583-595.
[16]	Lesage B, Qian J, Bollen M. 2011. Spindle checkpoint silencing:PP1 tips the balance. Current Biology, 21:898-903. doi: 10.1016/j.cub.2011.08.063 pmid: 22075433
[17]	Li Guo-fang. 2018. Functional study of MAX2 gene on the regulation of axillary bud outgrowth by mediating strigolactone signaling in Malus[Ph. D. Dissertation]. Yangling: Northwest A & F University. (in Chinese)
	李国防. 2018. 苹果MAX2基因介导独脚金内酯信号调控腋芽萌发的功能研究[博士论文]. 杨凌: 西北农林科技大学.
[18]	Li G F, Tan M, Cheng F, Liu X J, Qi S Y, Chen H F, Zhang D, Zhao C P, Han M Y, Ma J J. 2018. Molecular role of cytokinin in bud activation and outgrowth in apple branching based on transcriptomic analysis. Plant Molecular Biology, 98:261-274. doi: 10.1007/s11103-018-0781-2 pmid: 30311175
[19]	Li G F, Tan M, Ma J J, Cheng F, Li K, Liu X J, Zhao C P, Zhang D, Xing L B, Ren X L, Han M Y, An N. 2021. Molecular mechanism of MdWUS2-MdTCP12 interaction in mediating cytokinin signaling to control axillary bud outgrowth. Journal of Experimental Botany, 72:4822-4838. doi: 10.1093/jxb/erab163 pmid: 34113976
[20]	Liao Bao-peng, Wang Song-man, Du Ming-wei, Li Fang-jun, Tian Xiao-li, Li Zhao-hu. 2020. Responses and underlying mechanisms of different mainstem leaves on cotton to defoliant thidiazuron. Cotton Science, 32 (5):418-424. (in Chinese)
	廖宝鹏, 王崧嫚, 杜明伟, 李芳军, 田晓莉, 李召虎. 2020. 棉花不同部位主茎叶对脱叶剂噻苯隆的响应及机理. 棉花学报, 32 (5):418-424.
[21]	Lin Q, Li J, Smith1 R D, Walker J C. 1998. Molecular cloning and chromosomal mapping of type one serine/threonine protein phosphatases in Arabidopsis thaliana. Plant Molecular Biology, 37:471-481. pmid: 9617814
[22]	Liu Xiao-jie, Fan Sheng, Li Guo-fang, Tan Ming, Mo Ning, Ma Juan-juan, Zhang Dong, Han Ming-yu. 2017. Genome-wide identification of PIN gene family,cloning and expression analysis of MdPIN15 during axillary bud burst in Malus. Acta Horticulturae Sinica, 44 (11):2041-2054. (in Chinese)
	刘小杰, 樊胜, 李国防, 檀鸣, 默宁, 马娟娟, 张东, 韩明玉. 2017. 苹果全基因组PIN成员鉴定及MdPIN15的克隆和在腋芽萌发中的表达分析. 园艺学报, 44 (11):2041-2054. doi: 10.16420/j.issn.0513-353x.2017-0219
[23]	Lo S F, Yang S Y, Chen K T, Hsing Y L, Zeevaart J A D, Chen L J, Yu S M. 2008. A novel class of gibberellin 2-oxidases control semidwarfism,tillering,and root development in rice. The Plant Cell, 20 (10):2603-2618. doi: 10.1105/tpc.108.060913 URL
[24]	Luan S. 2003. Protein phosphatase in plans. Annu Rev Plant Biol, 54:63-92. doi: 10.1146/arplant.2003.54.issue-1 URL
[25]	Meng Yun, Ma Shao-feng, Shao Jian-zhu, Sun Jian-she, Ma Bao-kun, Wang Hong-ning. 2012. Effects of spraying 6-BA on axillary bud growth and the dynamic changes of endogenous hormones in‘Tianhong 2’Fuji nursery apple trees. Acta Horticulturae Sinica, 39 (5):837-844. (in Chinese)
	孟云, 马少锋, 邵建柱, 孙建设, 马宝焜, 王红宁. 2012. 喷施6-BA对‘天红2号’苹果苗腋芽萌发及其内源激素的影响. 园艺学报, 39 (5):837-844.
[26]	Qin Qianqian. 2014. Molecular mechanism on protein phosphatase TOPP 4 regulating gibberellin signaling in Arabidopsis[Ph. D. Dissertation]. Lanzhou: Lanzhou University. (in Chinese)
	秦倩倩. 2014. 拟南芥磷酸酶TOPP4调控赤霉素信号通路的分子机理[博士论文]. 兰州: 兰州大学.
[27]	Qin Q Q, Wang W, Guo X L, Yue J, Huang Y, Xu X F, Li J, Hou S W. 2014. Arabidopsis DELLA protein degradation is controlled by a type-one protein phosphatase,TOPP4. PLoS Genetics, 10 (7):e1004464.
[28]	Shen Y, Khanna R, Carle C M, Quail P H. 2007. Phytochrome induces rapid PIF5 phosphorylation and degradation in response to red-light activation. Plant Physiology, 145:1043-1051. doi: 10.1104/pp.107.105601 pmid: 17827270
[29]	Silverstone A L, Ciampaglio C N, Sun T. 1998. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. The Plant Cell, 10 (2):155-169. doi: 10.1105/tpc.10.2.155 URL
[30]	Stubbs M D, Tran H T, Atwell A J, Smith C S, Olson D, Moorhead G B. 2001. Purification and properties of Arabidopsis thaliana type one protein phosphatase(PP1). Biochimica Et Biophysica Acta, 1550:52-63. pmid: 11738087
[31]	Tan M, Li G, Liu X, Cheng F, Ma J, Zhao C, Zhang D, Han M. 2018. Exogenous application of GA₃ inactively regulates axillary bud outgrowth by influencing of branching-inhibitors and bud-regulating hormones in apple(Malus domestica Borkh.). Mol Genet Genomics, 293 (6):1547-1563. doi: 10.1007/s00438-018-1481-y
[32]	Tanaka M, Takei K, Ojima M, Akakibara H, Mori H. 2006. Auxin controls local cytokinin biosynthesis in the nodal stem in apical dominance. The Plant Journal, 45:1028-1036. doi: 10.1111/tpj.2006.45.issue-6 URL
[33]	Viaene T, Delwiche C F, Rensing S A, Friml J. 2013. Origin and evolution of PIN auxin transporters in the green lineage. Trends in Plant Science, 18 (1):5-10. doi: 10.1016/j.tplants.2012.08.009 pmid: 22981345
[34]	Wickson M, Thimann K V. 2010. The antagonism of auxin and kinetin in apical dominance. Physiologia Plantarum, 11 (1):62-74. doi: 10.1111/ppl.1958.11.issue-1 URL
[35]	Xiong Ting-ting. 2019. Identification and preliminary function prediction of PpTOPP4 gene family members[Ph. D. Dissertation]. Zhengzhou: Agricultural University of Henan. (in Chinese)
	熊婷婷. 2019. PpTOPP4基因家族成员鉴定及功能初探[博士论文]. 郑州: 河南农业大学.
[36]	Yan Jia, Bai Yu-e. 2020. Review on the phosphorylation of PIN protein in auxin transport. Molecular Plant Breeding, 18 (24):8138-8146. (in Chinese)
	闫佳, 白玉娥. 2020. 生长素极性运输中PIN蛋白磷酸化修饰研究进展. 分子植物育种, 18 (24):8138-8146.
[37]	Zhao Y. 2010. Auxin biosynthesis and its role in plant development. Annual Review of Plant Biology, 61:49-64. doi: 10.1146/annurev-arplant-042809-112308 pmid: 20192736
[38]	Zhang Xiao-hong, Zhang Hong-yan, Wu Jun, Min Dong-hong, Kang Bing, Li Jun-chao. 2002. Effect of TDZ on the induction of callus and bud proliferation and growth of Chinese toon. Journal of Northwest Sci-Tech University of Agriculture and Forestry(Natural Science Edition), 30 (5):35-39. (in Chinese)
	张小红, 张红燕, 武军, 闵东红, 康冰, 李军超. 2002. TDZ对香椿愈伤组织诱导及芽增殖生长等的影响. 西北农林科技大学学报(自然科学版), 30 (5):35-39.

用途 Use	基因名称 Gene name	上游引物（5′-3′） Forward primer	下游引物（5′-3′） Reverse primer
克隆Clone	MdTOPP13	ATGGACCAATCGGTTCTGGAC	CCTGTGCATCAGAGACTTGATTC
	MdTOPP28	ATGGACCAATCGGTTCTGGAC	CCTGTGCATCATGGACCTGAT
qRT-PCR	MdTOPP13	GACTGCCTCCTAATGCCAATT	ACTCTGTGAATGTCTTCCATAGC
	MdTOPP28	GAGGCTATGGAAGACATTCACA	ACCAGAGAAGGTCACAGAGTAA

用途 Use	基因名称 Gene name	上游引物（5′-3′） Forward primer	下游引物（5′-3′） Reverse primer
克隆Clone	MdTOPP13	ATGGACCAATCGGTTCTGGAC	CCTGTGCATCAGAGACTTGATTC
	MdTOPP28	ATGGACCAATCGGTTCTGGAC	CCTGTGCATCATGGACCTGAT
qRT-PCR	MdTOPP13	GACTGCCTCCTAATGCCAATT	ACTCTGTGAATGTCTTCCATAGC
	MdTOPP28	GAGGCTATGGAAGACATTCACA	ACCAGAGAAGGTCACAGAGTAA

基因名称 Gene name	基因登录号 Gene locus	染色体位置 Location	基因链 Strand	编码区长/bp CDS	氨基酸数/aa Protein	蛋白分子量 KDMW	亲水指数 GRA	等电点 pI	不稳定系数 Ⅱ
MdTOPP1	MD01G1140800	Chr01:24992947..24997431	-	726	241	26.83	-0.182	4.88	35.20
MdTOPP2	MD01G1140900	Chr01:24999027..25001036	-	1059	352	39.40	-0.131	7.96	46.55
MdTOPP3	MD01G1141200	Chr01:25025190..25027819	-	258	85	9.86	-0.192	4.99	41.56
MdTOPP4	MD02G1108000	Chr02:8722439..8725518	-	1377	458	50.62	-0.340	5.16	44.73
MdTOPP5	MD03G1007300	Chr03:580509..585577	-	936	311	35.62	-0.393	5.21	36.25
MdTOPP6	MD03G1156600	Chr03:18384616..18392711	-	2229	742	80.25	-0.129	5.78	37.73
MdTOPP7	MD03G1192600	Chr03:26421006..26425412	+	918	305	34.73	-0.202	5.24	41.77
MdTOPP8	MD03G1274100	Chr03:35710860..35716942	+	2655	884	96.77	-0.295	6.08	37.83
MdTOPP9	MD04G1083500	Chr04:11955473..11956621	-	336	111	12.33	-0.047	6.10	43.08
MdTOPP10	MD04G1083600	Chr04:11956624..11958010	-	591	196	22.49	-0.156	9.07	46.88
MdTOPP11	MD04G1179900	Chr04:27091697..27093197	-	906	301	34.34	-0.136	5.04	36.91
MdTOPP12	MD04G1198300	Chr04:28585017..28587856	-	969	322	36.48	-0.237	5.54	42.12
MdTOPP13	MD04G1229100	Chr04:30925518..30929906	+	1029	342	38.38	-0.184	5.67	41.09
MdTOPP14	MD05G1232900	Chr05:36572845..36576146	+	432	143	16.01	-0.133	4.82	31.79
MdTOPP15	MD06G1183800	Chr06:32220590..32223741	-	921	306	35.01	-0.320	4.96	34.94
MdTOPP16	MD06G1202700	Chr06:33587486..33592104	-	2115	704	78.87	-0.347	5.59	47.92
MdTOPP17	MD07G1205100	Chr07:28233219..28237816	-	951	316	35.76	-0.176	5.25	43.02
MdTOPP18	MD09G1156000	Chr09:12430531..12438867	+	1449	482	54.22	-0.316	5.86	35.61
MdTOPP19	MD09G1191500	Chr09:17014278..17019396	+	2487	828	91.16	-0.385	4.98	45.41
MdTOPP20	MD11G1010600	Chr11:795712..801172	-	936	311	35.62	-0.393	5.21	36.25
MdTOPP21	MD11G1174100	Chr11:20340736..20354133	-	3009	1002	106.68	-0.199	5.72	40.47
MdTOPP22	MD11G1209100	Chr11:30467821..30476248	+	918	305	34.76	-0.204	5.24	41.36
MdTOPP23	MD11G1296400	Chr11:41407336..41413456	+	2661	886	96.76	-0.310	6.13	39.57
MdTOPP24	MD12G1049700	Chr12:5646206..5647318	-	1113	370	41.01	-0.099	5.24	32.51
MdTOPP25	MD12G1052900	Chr12:5923211..5929636	-	942	313	35.76	-0.369	5.13	35.32
MdTOPP26	MD12G1195100	Chr12:27647081..27649008	-	906	301	34.40	-0.111	5.17	36.04
MdTOPP27	MD12G1210900	Chr12:28940837..28943702	-	975	324	36.67	-0.239	5.69	41.20
MdTOPP28	MD12G1246200	Chr12:31638713..31643111	+	1029	342	38.56	-0.228	5.85	41.23
MdTOPP29	MD13G1001400	Chr13:102885..107604	+	768	255	29.15	-0.195	4.85	39.20
MdTOPP30	MD13G1054400	Chr13:3810784..3816831	-	2583	860	97.00	-0.281	5.88	47.84
MdTOPP31	MD13G1083600	Chr13:5864560..5867786	+	921	306	35.05	-0.304	4.85	38.94
MdTOPP32	MD13G1213200	Chr13:20015224..20016220	+	666	221	25.16	-0.219	5.08	41.16
MdTOPP33	MD13G1216200	Chr13:20567021..20567531	-	399	132	14.93	-0.561	5.88	33.32
MdTOPP34	MD14G1051300	Chr14:4891465..4897083	-	942	313	35.77	-0.378	5.13	34.84
MdTOPP35	MD14G1112500	Chr14:18172736..18176908	-	960	319	36.09	-0.273	5.72	34.33
MdTOPP36	MD14G1112700	Chr14:18199211..18201364	-	231	76	8.61	-0.092	5.52	8.40
MdTOPP37	MD14G1112800	Chr14:18201367..18205580	-	906	301	34.34	-0.281	5.67	36.20
MdTOPP38	MD14G1112900	Chr14:18226998..18231411	-	960	319	36.09	-0.273	5.60	34.93
MdTOPP39	MD14G1189900	Chr14:28117305..28120399	-	921	306	35.02	-0.286	4.90	33.44
MdTOPP40	MD15G1227500	Chr15:18487996..18491614	-	1383	460	50.58	-0.336	5.17	46.63
MdTOPP41	MD16G1004700	Chr16:353770..361929	-	912	303	34.87	-0.271	4.88	38.04
MdTOPP42	MD16G1083000	Chr16:5813202..5816273	+	921	306	35.05	-0.308	4.86	39.57
MdTOPP43	MD16G1217200	Chr16:21423719..21427410	+	975	324	36.70	-0.183	6.88	41.38
MdTOPP44	MD17G1142100	Chr17:12801908..12811146	+	1449	482	54.25	-0.306	5.74	35.79

基因名称 Gene name	基因登录号 Gene locus	染色体位置 Location	基因链 Strand	编码区长/bp CDS	氨基酸数/aa Protein	蛋白分子量 KDMW	亲水指数 GRA	等电点 pI	不稳定系数 Ⅱ
MdTOPP1	MD01G1140800	Chr01:24992947..24997431	-	726	241	26.83	-0.182	4.88	35.20
MdTOPP2	MD01G1140900	Chr01:24999027..25001036	-	1059	352	39.40	-0.131	7.96	46.55
MdTOPP3	MD01G1141200	Chr01:25025190..25027819	-	258	85	9.86	-0.192	4.99	41.56
MdTOPP4	MD02G1108000	Chr02:8722439..8725518	-	1377	458	50.62	-0.340	5.16	44.73
MdTOPP5	MD03G1007300	Chr03:580509..585577	-	936	311	35.62	-0.393	5.21	36.25
MdTOPP6	MD03G1156600	Chr03:18384616..18392711	-	2229	742	80.25	-0.129	5.78	37.73
MdTOPP7	MD03G1192600	Chr03:26421006..26425412	+	918	305	34.73	-0.202	5.24	41.77
MdTOPP8	MD03G1274100	Chr03:35710860..35716942	+	2655	884	96.77	-0.295	6.08	37.83
MdTOPP9	MD04G1083500	Chr04:11955473..11956621	-	336	111	12.33	-0.047	6.10	43.08
MdTOPP10	MD04G1083600	Chr04:11956624..11958010	-	591	196	22.49	-0.156	9.07	46.88
MdTOPP11	MD04G1179900	Chr04:27091697..27093197	-	906	301	34.34	-0.136	5.04	36.91
MdTOPP12	MD04G1198300	Chr04:28585017..28587856	-	969	322	36.48	-0.237	5.54	42.12
MdTOPP13	MD04G1229100	Chr04:30925518..30929906	+	1029	342	38.38	-0.184	5.67	41.09
MdTOPP14	MD05G1232900	Chr05:36572845..36576146	+	432	143	16.01	-0.133	4.82	31.79
MdTOPP15	MD06G1183800	Chr06:32220590..32223741	-	921	306	35.01	-0.320	4.96	34.94
MdTOPP16	MD06G1202700	Chr06:33587486..33592104	-	2115	704	78.87	-0.347	5.59	47.92
MdTOPP17	MD07G1205100	Chr07:28233219..28237816	-	951	316	35.76	-0.176	5.25	43.02
MdTOPP18	MD09G1156000	Chr09:12430531..12438867	+	1449	482	54.22	-0.316	5.86	35.61
MdTOPP19	MD09G1191500	Chr09:17014278..17019396	+	2487	828	91.16	-0.385	4.98	45.41
MdTOPP20	MD11G1010600	Chr11:795712..801172	-	936	311	35.62	-0.393	5.21	36.25
MdTOPP21	MD11G1174100	Chr11:20340736..20354133	-	3009	1002	106.68	-0.199	5.72	40.47
MdTOPP22	MD11G1209100	Chr11:30467821..30476248	+	918	305	34.76	-0.204	5.24	41.36
MdTOPP23	MD11G1296400	Chr11:41407336..41413456	+	2661	886	96.76	-0.310	6.13	39.57
MdTOPP24	MD12G1049700	Chr12:5646206..5647318	-	1113	370	41.01	-0.099	5.24	32.51
MdTOPP25	MD12G1052900	Chr12:5923211..5929636	-	942	313	35.76	-0.369	5.13	35.32
MdTOPP26	MD12G1195100	Chr12:27647081..27649008	-	906	301	34.40	-0.111	5.17	36.04
MdTOPP27	MD12G1210900	Chr12:28940837..28943702	-	975	324	36.67	-0.239	5.69	41.20
MdTOPP28	MD12G1246200	Chr12:31638713..31643111	+	1029	342	38.56	-0.228	5.85	41.23
MdTOPP29	MD13G1001400	Chr13:102885..107604	+	768	255	29.15	-0.195	4.85	39.20
MdTOPP30	MD13G1054400	Chr13:3810784..3816831	-	2583	860	97.00	-0.281	5.88	47.84
MdTOPP31	MD13G1083600	Chr13:5864560..5867786	+	921	306	35.05	-0.304	4.85	38.94
MdTOPP32	MD13G1213200	Chr13:20015224..20016220	+	666	221	25.16	-0.219	5.08	41.16
MdTOPP33	MD13G1216200	Chr13:20567021..20567531	-	399	132	14.93	-0.561	5.88	33.32
MdTOPP34	MD14G1051300	Chr14:4891465..4897083	-	942	313	35.77	-0.378	5.13	34.84
MdTOPP35	MD14G1112500	Chr14:18172736..18176908	-	960	319	36.09	-0.273	5.72	34.33
MdTOPP36	MD14G1112700	Chr14:18199211..18201364	-	231	76	8.61	-0.092	5.52	8.40
MdTOPP37	MD14G1112800	Chr14:18201367..18205580	-	906	301	34.34	-0.281	5.67	36.20
MdTOPP38	MD14G1112900	Chr14:18226998..18231411	-	960	319	36.09	-0.273	5.60	34.93
MdTOPP39	MD14G1189900	Chr14:28117305..28120399	-	921	306	35.02	-0.286	4.90	33.44
MdTOPP40	MD15G1227500	Chr15:18487996..18491614	-	1383	460	50.58	-0.336	5.17	46.63
MdTOPP41	MD16G1004700	Chr16:353770..361929	-	912	303	34.87	-0.271	4.88	38.04
MdTOPP42	MD16G1083000	Chr16:5813202..5816273	+	921	306	35.05	-0.308	4.86	39.57
MdTOPP43	MD16G1217200	Chr16:21423719..21427410	+	975	324	36.70	-0.183	6.88	41.38
MdTOPP44	MD17G1142100	Chr17:12801908..12811146	+	1449	482	54.25	-0.306	5.74	35.79

基因 Gene	脱落酸 Abscisic acid	光信号Circadian	分生组织Meristem	茉莉酸甲酯MeJA	赤霉素 Gibberellin	胁迫 Stress	生长素 Auxin	水杨酸 Salicylic acid	栅栏状叶肉细胞分化Differentiation of the palisade mesophyll cells
MdTOPP1	1	11	1	6	—	1	1	1	—
MdTOPP2	3	9	—	10	2	—	—	1	—
MdTOPP3	—	14	2	—	1	—	1	1	—
MdTOPP4	3	14	—	4	2	1	1	1	—
MdTOPP5	3	13	1	2	1	2	3	2	—
MdTOPP6	1	5	—	—	—	—	1	1	1
MdTOPP7	3	8	—	—	—	1	6	1	—
MdTOPP8	1	5	1	2	—	3	—	—	—
MdTOPP9	3	10	—	4	2	2	1	1	—
MdTOPP10	7	10	—	—	1	—	—	1	—
MdTOPP11	2	12	1	2	—	1	—	1	—
MdTOPP12	9	7	1	—	1	—	1	—	—
MdTOPP13	3	17	—	4	1	4	—	3	—
MdTOPP14	1	14	3	8	1	1	2	1	—
MdTOPP15	1	12	1	10	—	—	1	—	—
MdTOPP16	3	14	1	—	1	1	2	1	—
MdTOPP17	4	7	—	6	—	3	—	1	—
MdTOPP18	3	16	—	2	—	—	—	—	—
MdTOPP19	2	16	1	8	2	—	3	—	—
MdTOPP20	—	11	—	2	1	—	2	1	1
MdTOPP21	5	14	1	2	1	—	—	—	—
MdTOPP22	—	10	—	4	—	3	2	1	—
MdTOPP23	2	10	1	10	—	5	—	—	—
MdTOPP24	—	10	—	4	1	16	2	1	—
MdTOPP25	3	13	—	—	—	1	—	—	—
MdTOPP26	4	11	2	4	—	6	3	1	—
MdTOPP27	4	5	2	6	—	1	2	—	2
MdTOPP28	2	9	—	—	3	5	3	1	—
MdTOPP29	—	8	—	—	—	1	1	—	—
MdTOPP30	—	17	—	—	1	2	2	—	—
MdTOPP31	7	18	—	4	3	—	2	1	—
MdTOPP32	1	5	—	2	—	—	1	2	—
MdTOPP33	1	17	1	4	2	—	—	1	—
MdTOPP34	—	13	—	2	2	1	1	—	—
MdTOPP35	4	11	2	4	1	—	—	1	1
MdTOPP36	2	9	1	4	1	1	—	1	—
MdTOPP37	6	9	—	2	2	2	—	—	—
MdTOPP38	2	13	1	4	2	—	—	1	1
MdTOPP39	6	17	1	4	—	3	—	1	—
MdTOPP40	1	12	—	18	—	2	1	—	—
MdTOPP41	5	16	1	6	—	—	—	1	—
MdTOPP42	4	10	—	2	—	—	3	—	—
MdTOPP43	—	16	—	2	1	1	—	—	—
MdTOPP44	3	13	—	—	2	2	—	—	—