Isolation and Functional Characterization of an AGAMOUS-LIKE 18 (AGL18) MADS-box Gene from Cucumber (Cucumis sativus L.)
Keywords:abiotic stress; AGL15; dwarf; small leaves; transgenic Arabidopsis
MADS-box proteins play vital roles in plant growth and development. However, few studies have addressed the biological functions of MADS-box genes in cucumber. In this study, a MADS-box gene, CsMADS25, was cloned from cucumber (Cucumis sativus L.). The open reading frame (ORF) of CsMADS25 was 810 bp in length and encoded a deduced protein consisting of 269 amino acids with a calculated MW of 30.53 kDa and a theoretical pI of 5.38. Sequence alignment showed that CsMADS25 shared the highest amino acid identity with CmMADS09 from Cucumis melo. Phylogenetic tree analysis indicated that CsMADS25 was clustered with AGL18 proteins with high bootstrap values. qRT-PCR analysis showed that the expression of CsMADS25 was observably regulated by various abiotic stresses and GAtreatments. Overexpression of CsMADS25 resulted in dwarf and small-leaf phenotypes in transgenic Arabidopsis plants, and the leaf index value (leaf length/width ratio) of transgenic plants was dramatically increased compared with that of wild-type (WT) plants. These findings suggest that CsMADS25 might play important roles in various developmental processes and in response to abiotic stress of cucumber.
Adamczyk BJ, Lehti-Shiu MD, Fernandez DE (2007). The MADS domain factors AGL15 and AGL18 act redundantly as repressors of the floral transition in Arabidopsis. Plant Journal 50(6):1007-1019.
Burko Y, Shleizer-Burko S, Yanai O, Shwartz I, Zelnik ID, Jacob-Hirsch J, … Ori N (2013). A role for APETALA1/fruitfull transcription factors in tomato leaf development. Plant Cell 25(6):2070-2083.
Chen N, Veerappan V, Abdelmageed H, Kang M, Allen RD (2018). HSI2/VAL1 silences AGL15 to regulate the developmental transition from seed maturation to vegetative growth in Arabidopsis. Plant Cell 30(3):600-619.
Clough SJ, Bent AF (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant Journal 16(6):735-743.
Cosio C, Ranocha P, Francoz E, Burlat V, Zheng Y, Perry SE, … Dunand C (2017). The class III peroxidase PRX17 is a direct target of the MADS-box transcription factor AGAMOUS-LIKE15 (AGL15) and participates in lignified tissue formation. New Phytologist 213(1):250-263.
de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, … Angenent GC (2005). Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17(5):1424-1433.
Fang SC, Fernandez DE (2002). Effect of regulated overexpression of the MADS domain factor AGL15 on flower senescence and fruit maturation. Plant Physiology 130(1):78-89.
Fernandez DE, Heck GR, Perry SE, Patterson SE, Bleecker AB, Fang SC (2000). The embryo MADS domain factor AGL15 acts postembryonically. Inhibition of perianth senescence and abscission via constitutive expression. Plant Cell 12(2):183-198.
Fernandez DE, Wang CT, Zheng Y, Adamczyk BJ, Singhal R, Hall PK, Perry SE (2014). The MADS-domain factors AGAMOUS-LIKE15 and AGAMOUS-LIKE18, along with SHORT VEGETATIVE PHASE and AGAMOUS-LIKE24, are necessary to block floral gene expression during the vegetative phase. Plant Physiology 165(4):1591-1603.
Geourjon C, Deleage G (1995). SOPMA: significant improvements in protein secondary structure prediction by consensus prediction from multiple alignments. Bioinformatics 11(6):681-684.
Grimplet J, Martinez-Zapater JM, Carmona MJ (2016). Structural and functional annotation of the MADS-box transcription factor family in grapevine. BMC Genomics 17:80.
Gu X, Wang Y, He Y (2013). Photoperiodic regulation of flowering time through periodic histone deacetylation of the florigen gene FT. PLoS Biology 11(9):e1001649.
Guo X, Chen G, Cui B, Gao Q, Guo JE, Li A, … Hu Z (2016). Solanum lycopersicum agamous-like MADS-box protein AGL15-like gene, SlMBP11, confers salt stress tolerance. Molecular Breeding 36(9):125.
Guo X, Chen G, Naeem M, Yu X, Tang B, Li A, Hu Z (2017). The MADS-box gene SlMBP11 regulates plant architecture and affects reproductive development in tomato plants. Plant Science 258:90-101.
Heck GR, Perry SE, Nichols KW, Fernandez DE (1995). AGL15, a MADS domain protein expressed in developing embryos. Plant Cell 7(8):1271-1282.
Hu L, Liu S (2012). Genome-wide analysis of the MADS-box gene family in cucumber. Genome 55(3):245-256.
Hu YX, Tao YB, Xu ZF (2017). Overexpression of Jatropha Gibberellin 2-oxidase 6 (JcGA2ox6) induces dwarfism and smaller leaves, flowers and fruits in Arabidopsis and Jatropha. Frontiers in Plant Science 8:2103.
Huang S, Li R, Zhang Z, Li L, Gu X, Fan W, … Du Y (2009). The genome of the cucumber, Cucumis sativus L. Nature Genetics 41(12):1275-1281.
Immink RG, Pose D, Ferrario S, Ott F, Kaufmann K, Valentim FL, … Angenent GC (2012). Characterization of SOC1's central role in flowering by the identification of its upstream and downstream regulators. Plant Physiology 160(1):433-449.
Kaufmann K, Melzer R, Theissen G (2005). MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347(2):183-198.
Khong GN, Pati PK, Richaud F, Parizot B, Bidzinski P, Mai CD, … Gantet P (2015). OsMADS26 negatively regulates resistance to pathogens and drought tolerance in rice. Plant Physiology 169(4):2935-2949.
Li C, Ma G, Xie T, Chen J, Wang Z, Song M, Tang Q (2018). SOC1 and AGL24 interact with AGL18-1, not the other family members AGL18-2 and AGL18-3 in Brassica juncea. Acta Physiologiae Plantarum 40(1):3.
Olszewski N, Sun TP, Gubler F (2002). Gibberellin signaling: biosynthesis, catabolism, and response pathways. Plant Cell 14 Suppl:S61-80.
Pabon-Mora N, Sharma B, Holappa LD, Kramer EM, Litt A (2013). The Aquilegia FRUITFULL-like genes play key roles in leaf morphogenesis and inflorescence development. Plant Journal 74(2):197-212.
Serivichyaswat P, Ryu HS, Kim W, Kim S, Chung KS, Kim JJ, Ahn JH (2015). Expression of the floral repressor miRNA156 is positively regulated by the AGAMOUS-like proteins AGL15 and AGL18. Molecules and Cells 38(3):259-266.
Smaczniak C, Immink RG, Angenent GC, Kaufmann K (2012). Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139(17):3081-3098.
Tan PH, Zhang L, Yin SX, Teng K (2018). Heterologous expression of a novel Poa pratensis gibberellin 2-oxidase gene, PpGA2ox, caused dwarfism, late flowering, and increased chlorophyll accumulation in Arabidopsis. Biologia Plantarum 62(3):462-470.
Thakare D, Tang W, Hill K, Perry SE (2008). The MADS-domain transcriptional regulator AGAMOUS-LIKE15 promotes somatic embryo development in Arabidopsis and soybean. Plant Physiology 146(4):1663-1672.
Wan H, Zhao Z, Qian C, Sui Y, Malik AA, Chen J (2010). Selection of appropriate reference genes for gene expression studies by quantitative real-time polymerase chain reaction in cucumber. Analytical Biochemistry 399(2):257-261.
Wang H, Caruso LV, Downie AB, Perry SE (2004). The embryo MADS domain protein AGAMOUS-Like 15 directly regulates expression of a gene encoding an enzyme involved in gibberellin metabolism. Plant Cell 16(5):1206-1219.
Wang L, Zeng XQ, Zhuang H, Shen YL, Chen H, Wang ZW, . . . Li YF (2017). Ectopic expression of OsMADS1 caused dwarfism and spikelet alteration in rice. Plant Growth Regulation 81(3):433-442.
Xiao Z, Fu R, Li J, Fan Z, Yin H (2016). Overexpression of the gibberellin 2-oxidase gene from Camellia lipoensis induces dwarfism and smaller flowers in Nicotiana tabacum. Plant Molecular Biology Reporter 34(1):182-191.
Xu K, Liu K, Wu J, Wang W, Zhu Y, Li C, … Zhao L (2018). A MADS-box gene associated with protocorm-like body formation in Rosa canina alters floral organ development in Arabidopsis. Canadian Journal of Plant Science 98(2):309-317.
Yang Z, Li C, Wang Y, Zhang C, Wu Z, Zhang X, … Li F (2014). GhAGL15s, preferentially expressed during somatic embryogenesis, promote embryogenic callus formation in cotton (Gossypium hirsutum L.). Molecular Genetics and Genomics 289(5):873-883.
Yin W, Hu Z, Hu J, Zhu Z, Yu X, Cui B, Chen G (2017). Tomato (Solanum lycopersicum) MADS-box transcription factor SlMBP8 regulates drought, salt tolerance and stress-related genes. Plant Growth Regulation 83(1):55-68.
Yin W, Yu X, Chen G, Tang B, Wang Y, Liao C, … Hu Z (2018). Suppression of SlMBP15 inhibits plant vegetative growth and delays fruit ripening in tomato. Frontiers in Plant Science 9:938.
Zhang Y, Zhao G, Li Y, Mo N, Zhang J, Liang Y (2017). Transcriptomic analysis implies that GA regulates sex expression via ethylene-dependent and ethylene-independent pathways in cucumber (Cucumis sativus L.). Frontiers in Plant Science 8:10.
Zheng Q, Perry SE (2014). Alterations in the transcriptome of soybean in response to enhanced somatic embryogenesis promoted by orthologs of AGAMOUS-Like15 and AGAMOUS-Like18. Plant Physiology 164(3):1365-1377.
Zheng Q, Zheng Y, Ji H, Burnie W, Perry SE (2016). Gene regulation by the AGL15 transcription factor reveals hormone interactions in somatic embryogenesis. Plant Physiology 172(4):2374-2387.
Zheng Q, Zheng Y, Perry SE (2013). AGAMOUS-Like15 promotes somatic embryogenesis in Arabidopsis and soybean in part by the control of ethylene biosynthesis and response. Plant Physiology 161(4):2113-2127.
Zheng Y, Ren N, Wang H, Stromberg AJ, Perry SE (2009). Global identification of targets of the Arabidopsis MADS domain protein AGAMOUS-Like15. Plant Cell 21(9):2563-2577.
Zhou Y, Hu L, Jiang L, Liu S (2018). Genome-wide identification, characterization, and transcriptional analysis of the metacaspase gene family in cucumber (Cucumis sativus). Genome 61(3):187-194.
How to Cite
Open Access Journal:
The journal allows the author(s) to retain publishing rights without restriction. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author.