Expression of E-type MADS-box Genes in Flower and Fruits and Protein Interaction Analysis in Chinese Jujube

doi:10.16420/j.issn.0513-353x.2021-0179

Acta Horticulturae Sinica ›› 2022, Vol. 49 ›› Issue (4): 739-748.doi: 10.16420/j.issn.0513-353x.2021-0179

• Research Papers • Previous Articles Next Articles

Expression of E-type MADS-box Genes in Flower and Fruits and Protein Interaction Analysis in Chinese Jujube

GAO Weilin¹, ZHANG Liman¹, XUE Chaoling¹, ZHANG Yao¹, LIU Mengjun², ZHAO Jin¹^,^*()

1. College of Life Science,Hebei Agricultural University,Baoding,Hebei 071000,China
2. College of Horticulture,Hebei Agricultural University,Baoding,Hebei 071000,China

Received:2021-11-18 Revised:2022-01-18 Online:2022-04-25 Published:2022-04-24
Contact: ZHAO Jin E-mail:zhaojinbd@126.com

Abstract

Abstract:

In order to study the function of E-type MADS-box genes in flower and fruit of Chinese jujube（Ziziphus jujuba Mill.）,their bioinformatics analysis,expression pattern,subcellular location and protein interaction in‘Jinsi Xiaozao’were studied systematically. A total of three E-type MADS-box genes were identified in the jujube genome,which are located in the three clades of SEP1/2,SEP3 and SEP4. Compared with homologous sequences of other species,they are very conservative in evolution. Three E-type genes expressed in jujube flowers and fruits. The expression of ZjSEP1/2 was relatively stable at different stages of flower development,ZjSEP3 and ZjSEP4 were highly expressed in the early stage of flower development. After phytoplasma infection,their expressions in phyllody,a typical diseased symptom, were inhibited dramatically. All three proteins were located in the nucleus. According to the results of yeast one-hybrid analysis,ZjSEP1/2 and ZjSEP3 proteins had transcriptional activation activity and could be used as transcription factors to regulate downstream genes,while ZjSEP4 didn’t have this activity. According to the yeast two-hybrid results,all three proteins could interact with A-type and C/D-type proteins. Both ZjSEP4 and ZjSEP1/2 could interact with itself,but ZjSEP3 couldn’t interact with itself. In summary,the three E-type genes play an important role in the development of jujube flowers,but they should have various regulatory modes. ZjSEP3 couldn’t form homodimers,while ZjSEP4 and ZjSEP1/2 could form homodimers. But all of three proteins could form heterodimers with A-type and C/D-type proteins.

Key words: Ziziphus jujuba, MADS-box gene, E-type, flower and fruit development, expression analysis, transcriptional activation, protein interaction

CLC Number:

S665.1

GAO Weilin, ZHANG Liman, XUE Chaoling, ZHANG Yao, LIU Mengjun, ZHAO Jin. Expression of E-type MADS-box Genes in Flower and Fruits and Protein Interaction Analysis in Chinese Jujube[J]. Acta Horticulturae Sinica, 2022, 49(4): 739-748.

Figures/Tables 7

References 34

[1]	Becker A, Theissen G. 2003. The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Molecular Phylogenetics and Evolution, 29 (3):464-489. doi: 10.1016/S1055-7903(03)00207-0 URL
[2]	Coen E S, Meyerowitz E M. 1991. The war of the whorls:genetic interactions controlling flower development. Nature, 353 (6339):31-37. doi: 10.1038/353031a0 URL
[3]	Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky M F. 2004. The SEP 4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Current Biology, 14 (21):1935-1940. pmid: 15530395
[4]	Günter Theißen. 2001. Development of floral organ identity:stories from the MADS house. Current Opinion in Plant Biology, 4 (1):75-85. doi: 10.1016/S1369-5266(00)00139-4 URL
[5]	Honma T, Goto K. 2001. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 409 (6819):525-529. doi: 10.1038/35054083 URL
[6]	Huang Fang. 2007. Cloning and functional analysis of flower development related genes in soybean(Glycine max L.)[Ph. D. Dissertation]. Nanjing: Nanjing Agricultural University. (in Chinese)
	黄方. 2007. 大豆花发育相关基因的克隆与功能研究[博士论文]. 南京: 南京农业大学.
[7]	Huang J, Zhang C, Zhao X, Fei Z, Wan K, Zhang Z, Pang X, Yin X, Bai Y, Sun X, Gao L, Li R, Zhang J, Li X. 2016. The jujube genome provides insights into genome evolution and the domestication of sweetness/acidity taste in fruit trees. PLoS Genetics, 12 (12):e1006433. doi: 10.1371/journal.pgen.1006433 URL
[8]	Immink R G, Tonaco I A, de Folter S, Shchennikova A, van Dijk A D, Busscher-Lange J, Borst J W, Angenent G C. 2009. SEPALLATA3:the‘glue’for MADS box transcription factor complex formation. Genome Biology, 10 (2):R24. doi: 10.1186/gb-2009-10-2-r24 URL
[9]	Ireland H S, Yao J L, Tomes S, Sutherland P W, Nieuwenhuizen N, Gunaseelan K, Winz R A, David K M, Schaffer R J. 2013. Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. Plant Journal, 73 (6):1044-1056. doi: 10.1111/tpj.12094 URL
[10]	Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, Kimizu M, Yoshida H, Nagamura Y, Kyozuka J. 2012. Inflorescence meristem identity in rice is specified by overlapping functions of three AP 1 /FUL-like MADS box genes and PAP2,a SEPALLATA MADS box gene. Plant Cell, 24 (5):1848-1859. doi: 10.1105/tpc.112.097105 URL
[11]	Krizek B A, Meyerowitz E M. 1996. The Arabidopsis homeotic genes APETALA3 and PISTILLATA are sufficient to provide the B class organ identity function. Development, 122 (1):11-22. pmid: 8565821
[12]	Li Chengru, Dong Na, Li Xiaoping, Wu Shasha, Liu Zhongjian, Zhai Junwen. 2020. A review of MADS-box genes,the molecular regulatory genes for floral organ development in Orchidaceae. Acta Horticulturae Sinica, 47 (10):2047-2062. (in Chinese)
	李成儒, 董钠, 李笑平, 吴沙沙, 刘仲健, 翟俊文. 2020. 兰科植物花发育调控MADS-box基因家族研究进展. 园艺学报, 47 (10):2047-2062.
[13]	Liao Y T, Lin S S, Lin S J, Shen B N, Cheng H P, Lin C P. 2019. Structural insights into the interaction between phytoplasmal effector causing phyllody 1(PHYL1)and MADS transcription factor. Plant Journal, 100 (4):706-719. doi: 10.1111/tpj.14463 URL
[14]	Lin X, Wu F, Du X, Shi X, Liu Y, Liu S, Hu Y, Theissen G, Meng Z. 2014. The pleiotropic SEPALLATA-like gene OsMADS34 reveals that the‘empty glumes’of rice(Oryza sativa)spikelets are in fact rudimentary lemmas. New Phytologist, 202 (2):689-702. doi: 10.1111/nph.12657 URL
[15]	Liu M J, Zhao J, Cai Q L, Liu G C, Wang J R, Zhao Z H, Liu P, Dai L, Yan G, Wang W J, Li X S, Chen Y, Sun Y D, Liu Z G, Lin M J, Xiao J, Chen Y Y, Li X F, Wu B, Ma Y, Jian J B, Yang W, Yuan Z, Sun X C, Wei Y L, Yu L L, Zhang C, Liao S G, He R J, Guang X M, Wang Z, Zhang Y Y, Luo L H. 2014. The complex jujube genome provides insights into fruit tree biology. Nature Communications, 28 (5):5315.
[16]	Liu Shinan, Qi Tiantian, Ma Jingjing, Ma Lyuyi, Lin Xinchun. 2016. Cloning and functional analysis of SEP-like gene from phyllostachys violascens. Journal of Nuclear Agricultural Sciences, 30 (8):1453-1459. (in Chinese)
	刘世男, 戚田田, 马晶晶, 马履一, 林新春. 2016. 雷竹SEP-like基因的克隆及功能分析. 核农学报, 30 (8):1453-1459.
[17]	Ma H, Yanofsky M F, Meyerowitz E M. 1991. AGL1AGL6,an Arabidopsis gene family with similarity to floral hometic and transcription factor genes. Genes and Development, 5 (3):484-495. pmid: 1672119
[18]	MacLean A M, Sugio A, Makarova O V, Findlay K C, Grieve V M. 2011. Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiology 157:831-841.
[19]	Maejima K, Iwai R, Himeno M, Komatsu K, Kitazawa Y, Fujita N, Ishikawa K, Fukuoka M, Minato N, Yamaji Y, Oshima K, Namba S. 2014. Recognition of floral homeotic MADS domain transcription factors by a phytoplasmal effector,phyllogen,induces phyllody. Plant Journal, 78 (4):541-554. doi: 10.1111/tpj.12495 URL
[20]	Maejima K, Kitazawa Y, Tomomitsu T, Yusa A, Neriya Y, Himeno M, Yamaji Y, Oshima K, Namba S. 2015. Degradation of class E MADs-domain transcription factors in Arabidopsis by a phytoplasmal effector,phyllogen. Plant Signaling and Behavior, 10 (8):e1042635. doi: 10.1080/15592324.2015.1042635 URL
[21]	Melzer R, Verelst W, Theissen G. 2009. The class E floral homeotic protein SEPALLATA 3 is sufficient to loop DNA in‘floral quartet’-like complexes in vitro. Nucleic Acids Research, 37 (1):144-157. doi: 10.1093/nar/gkn900 URL
[22]	Meng X W, Li Y, Yuan Y, Zhang Y, Li H T, Zhao J, Liu M J. 2020. The regulatory pathways of distinct flowering characteristics in Chinese jujube. Horticulture Research, 7 (1):13-19. doi: 10.1038/s41438-019-0236-1 URL
[23]	Ng M, Yanofsky M F. 2001. Function and evolution of the plant MADS box gene family. Nature Reviews Genetics, 2:186-195. pmid: 11256070
[24]	Pelaz S, Ditta G S, Baumann E, Wisman E, Yanofsky M F. 2000. B and C floral organ identity functions require SEPALLATA MADS box genes. Nature, 405 (6783):200-203. doi: 10.1038/35012103 URL
[25]	Pelaz S, Tapia-López R, Alvarez-Buylla E R, Yanofsky M F. 2001. Conversion of leaves into petals in Arabidopsis. Current Biology, 11 (3):182-184. pmid: 11231153
[26]	Seymour G B., Ryder C D, Cevik V, Hammond J P, Popovich A., King G J, Vrebalov J, Giovannoni J J, Manning K. 2011. A SEPALLATA gene is involved in the development and ripening of strawberry(Fragaria × ananassa Duch.)fruit,a non-climacteric tissue. Journal of Experimental Botany, 62 (3):1179-1188. doi: 10.1093/jxb/erq360 pmid: 21115665
[27]	Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6:molecular evolutionary genetics analysis Version 6.0. Molecular Biology & Evolution, 30 (12):2725-2729.
[28]	Teo Z W N, Zhou W, Shen L. 2019. Dissecting the function of MADS-box transcription factors in orchid reproductive development. Frontiers in Plant Science, 15 (10):1474.
[29]	Xu K, Huang X, Wu M, Wang Y, Chang Y, Liu K, Zhang J, Zhang Y, Zhang F, Yi L, Li T, Wang R, Tan G, Li C. 2014a. A rapid,highly efficient and economical method of Agrobacterium-mediated in planta transient transformation in living onion epidermis. PLoS ONE, 9 (1):e83556. doi: 10.1371/journal.pone.0083556 URL
[30]	Xu Y, Zhang L, Xie H, Zhang Y Q, Oliveira M M, Ma R C. 2008. Expression analysis and genetic mapping of three SEPALLATA -like genes from peach(Prunus persica(L.)Batsch). Tree Genetics & Genomes, 4 (4):693-703.
[31]	Xu Z, Zhang Q, Sun L, Du D, Cheng T, Pan H, Yang W, Wang J. 2014b. Genome-wide identification,characterisation and expression analysis of the MADS-box gene family in Prunus mume. Molecular Genetics and Genomics, 289 (5):903-920. doi: 10.1007/s00438-014-0863-z URL
[32]	Zhang L M, Zhao J, Feng C F, Liu M J, Wang J R, Hu Y F. 2017. Genome-wide identification,characterization of the MADS-box gene family in Chinese jujube and their involvement in flower development. Scientific Reports, 7 (1):1025. doi: 10.1038/s41598-017-01159-8 URL
[33]	Zhou Y, Xu Z, Yong X, Ahmad S, Yang W, Cheng T, Wang J, Zhang Q. 2017. SEP-class genes in Prunus mume and their likely role in floral organ development. BMC Plant Biology, 17 (1):10. doi: 10.1186/s12870-016-0954-6 URL
[34]	Zong Chengwen, Fang Jinggui, Tao Jianmin, Zhang Zhen, Qian Yaming. 2007. Cloning and sequence analysis of MADS-box family protein gene fragments from grape. Journal of Fruit Science, 25 (1):27-32. (in Chinese)
	宗成文, 房经贵, 陶建敏, 章镇, 钱亚明. 2007. 葡萄MADS-box家族基因保守片段的克隆与序列分析. 果树学报, 25 (1):27-32.

用途 Usage	基因名称 Gene name	正向序列（5′-3′） Forward primer sequence	反向序列（5′-3′） Reverse primer sequence
q-RT-PCR Quantitative real-time PCR	ZjSEP1/2	GGGGAGAGGTAAGGTGGAG	GGTTGGAGAAGATGATAAGAGC
	ZjSEP3	GGGGAAGACCTTGGACCTTT	AGCAAGTGTTCCTTGCGTTG
	ZjSEP4	GGGGTTCTTCCAGGCCTTAG	ACTTGCTGGGCATGACTTGT
内参 Primers for internal control	ZjACT	AGCCTTCCTGCCAACGAGT	TTGCTTCTCACCCTTGATGC
酵母双杂交 Yeast two- Hybrid（Y2H）	ZjBDZjSEP1/2	ATGGCCATGGAGGCCGATGGGGAGAGGTAAGGTGGA	GGATCCCCGGGAATTTCAAAGCATCCACCCAGGG
	ZjBDZjSEP3	GGATCCCCGGGAATTTCAAAGCATCCACCCAGGG	GGATCCCCGGGAATTTCATGGTAACCATCCTGGCA
	ZjBDZjSEP4	ATGGCCATGGAGGCCGATGGGGAGGGGTAGAGTTGA	GGATCCCCGGGAATTTCAAAGCATCCATCCAGGAA
	ZjADZjSEP1/2	CCATGGAGGCCAGTGATGGGGAGAGGTAAGGTGGA	CACCCGGGTGGAATTTCAAAGCATCCACCCAGGG
	ZjADZjSEP3	CCATGGAGGCCAGTGATGGGAAGAGGTAGAGTGGA	CACCCGGGTGGAATTTCATGGTAACCATCCTGGCA
	ZjADZjSEP4	CCATGGAGGCCAGTGATGGGGAGGGGTAGAGTTGA	CACCCGGGTGGAATTTCAAAGCATCCATCCAGGAA
	ZjADZjMADS46	CCATGGAGGCCAGTGATGGAGTTCCCAAATCAAGCA	CACCCGGGTGGAATTTCAAACAAGTTGGAGAGCTG
	ZjADMADS24	CCATGGAGGCCAGTGATGGGGAGGGGAAGGGTTC	CACCCGGGTGGAATTGCATCCAAGCGGGCAGGAG
亚细胞定位 Subcellular localization	ZjSEP1/2	AGCTCGGGTACCCGGGATGGGGAGAGGTAAGGTGGA	TCTAGAGGATCAAGCATCCACCCAGGG
	ZjSEP3	AGCTCGGGTACCCGGGATGCTCAAAACACTTGAGA	TCTAGAGGATCTGGTAACCATCCTGGCAT
	ZjSEP4	AGCTCGGGTACCCGGGATGGGGAGGGGTAGAGTTGA	TCTAGAGGATCAAGCATCCATCCAGGAA

用途 Usage	基因名称 Gene name	正向序列（5′-3′） Forward primer sequence	反向序列（5′-3′） Reverse primer sequence
q-RT-PCR Quantitative real-time PCR	ZjSEP1/2	GGGGAGAGGTAAGGTGGAG	GGTTGGAGAAGATGATAAGAGC
	ZjSEP3	GGGGAAGACCTTGGACCTTT	AGCAAGTGTTCCTTGCGTTG
	ZjSEP4	GGGGTTCTTCCAGGCCTTAG	ACTTGCTGGGCATGACTTGT
内参 Primers for internal control	ZjACT	AGCCTTCCTGCCAACGAGT	TTGCTTCTCACCCTTGATGC
酵母双杂交 Yeast two- Hybrid（Y2H）	ZjBDZjSEP1/2	ATGGCCATGGAGGCCGATGGGGAGAGGTAAGGTGGA	GGATCCCCGGGAATTTCAAAGCATCCACCCAGGG
	ZjBDZjSEP3	GGATCCCCGGGAATTTCAAAGCATCCACCCAGGG	GGATCCCCGGGAATTTCATGGTAACCATCCTGGCA
	ZjBDZjSEP4	ATGGCCATGGAGGCCGATGGGGAGGGGTAGAGTTGA	GGATCCCCGGGAATTTCAAAGCATCCATCCAGGAA
	ZjADZjSEP1/2	CCATGGAGGCCAGTGATGGGGAGAGGTAAGGTGGA	CACCCGGGTGGAATTTCAAAGCATCCACCCAGGG
	ZjADZjSEP3	CCATGGAGGCCAGTGATGGGAAGAGGTAGAGTGGA	CACCCGGGTGGAATTTCATGGTAACCATCCTGGCA
	ZjADZjSEP4	CCATGGAGGCCAGTGATGGGGAGGGGTAGAGTTGA	CACCCGGGTGGAATTTCAAAGCATCCATCCAGGAA
	ZjADZjMADS46	CCATGGAGGCCAGTGATGGAGTTCCCAAATCAAGCA	CACCCGGGTGGAATTTCAAACAAGTTGGAGAGCTG
	ZjADMADS24	CCATGGAGGCCAGTGATGGGGAGGGGAAGGGTTC	CACCCGGGTGGAATTGCATCCAAGCGGGCAGGAG
亚细胞定位 Subcellular localization	ZjSEP1/2	AGCTCGGGTACCCGGGATGGGGAGAGGTAAGGTGGA	TCTAGAGGATCAAGCATCCACCCAGGG
	ZjSEP3	AGCTCGGGTACCCGGGATGCTCAAAACACTTGAGA	TCTAGAGGATCTGGTAACCATCCTGGCAT
	ZjSEP4	AGCTCGGGTACCCGGGATGGGGAGGGGTAGAGTTGA	TCTAGAGGATCAAGCATCCATCCAGGAA

Expression of E-type MADS-box Genes in Flower and Fruits and Protein Interaction Analysis in Chinese Jujube

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