Genome-wide identification and characterization, phylogenetic comparison and expression profiles of SPL transcription factor family in B. juncea (Cruciferae)


Autoři: Jian Gao aff001;  Hua Peng aff003;  Fabo Chen aff001;  Yi Liu aff001;  Baowei Chen aff001;  Wenbo Li aff001
Působiště autorů: Department of Life Sciences and Technology, Yangtze Normal University, Fuling, Chongqing, China aff001;  Centre for Green Development and Collaborative Innovation in Wuling Mountain Region, Yangtze Normal University, Fuling, Chongqing, China aff002;  Sichuan Tourism College, Chengdu, Sichuan, China aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0224704

Souhrn

SQUAMOSA promoter-binding protein-like (SPL), as plant specific transcription factors, is involved in many plant growth and development processes. However, there is less systematical study for SPL transcription factor in B. juncea (Cruciferae). Here, a total of 59 SPL genes classified into eight phylogenetic groups were identified in B. juncea, highly conserved within each ortholog were also found based on gene structure, conserved motif, as well as clustering level. In addition, clustering of SPL domain showed that two zinc finger-like structures and NLS segments were identified in almost of BjuSPLs. Analyzed of putative cis-elements for BjuSPLs demonstrated that SPL transcription factors were involved in adverse environmental changes, such as light, plant stresses and phytohormones response. Expression analysis showed that differentially expressed SPL genes were identified in flower and stem development of Cruciferae; such as BjuSPL3a-B, BjuSPL2b_B and BjuSPL2c_A were significantly expressed in flower; BjuSPL 3b_B and BjuSPL10a_A were significantly expressed in stem node (VP: vegetative period). Moreover, 28 of the 59 BjuSPLs were found involved in their posttranscriptional regulation targeted by miR156. We demonstrated that miR156 negatively regulated BjuSPL10a_A and BjuSPL3b_B to act for stem development in B. juncea.

Klíčová slova:

Arabidopsis thaliana – Introns – Phylogenetic analysis – Protein domains – Protein structure comparison – Seedlings – Sequence motif analysis – Transcription factors


Zdroje

1. Liu N, Tu L, Wang L, Hu H, Xu J, Zhang X. MicroRNA 157-targeted SPL genes regulate floral organ size and ovule production in cotton. Bmc Plant Biology. 2017; 17(1): 7. doi: 10.1186/s12870-016-0969-z 28068913

2. Yang Z, Wang X, Gu S, Hu Z, Hua X, Xu C. Comparative study of SBP-box gene family in Arabidopsis and rice. Gene. 2008; 407(1): 1–11.

3. Wang H, Wang H. The miR156/SPL Module, a Regulatory Hub and Versatile Toolbox, Gears up Crops for Enhanced Agronomic Traits. Molecular Plant. 2015; 8(5): 677–688. doi: 10.1016/j.molp.2015.01.008 25617719

4. George C, A Mark C, Koy S, Sarah H. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nature Genetics. 2007; 39(4): 544–549. doi: 10.1038/ng2001 17369828

5. Wu G, Poethig RS. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development. 2006; 133(18): 3539–3547. doi: 10.1242/dev.02521 16914499

6. Tsubosa Y, Sato H, Tachimori Y, Hokamura N, Hosokawa M, Kinoshita Y, et al. Functional analysis of the Arabidopsis thaliana SBP-box gene SPL3: a novel gene involved in the floral transition. Plant Journal. 2010; 12(2): 367–377.

7. Shuping X, María S, Susanne HH, Rita B, Peter H. miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell. 2010; 22(12): 3935–3950. doi: 10.1105/tpc.110.079343 21177480

8. Zhang Y, Schwarz S, Saedler H, Huijser P. SPL8, a local regulator in a subset of gibberellin-mediated developmental processes in Arabidopsis. Plant Molecular Biology. 2007; 63(3): 429. doi: 10.1007/s11103-006-9099-6 17093870

9. Stone JM, Xinwen L, Nekl ER, Stiers JJ. Arabidopsis AtSPL14, a plant-specific SBP-domain transcription factor, participates in plant development and sensitivity to fumonisin B1. Plant Journal. 2010; 41(5): 744–754.

10. Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, et al. PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Research. 2017; 45(D1): D1040–D1045. doi: 10.1093/nar/gkw982 27924042

11. Finn RD, Alex B, Jody C, Penelope C, Eberhardt RY, Eddy SR, et al. Pfam: the protein families database. Nucleic Acids Research. 2014; 42(D1): 222–230.

12. Finn RD, Jody C, Eddy SR. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research. 2011; 39(Web Server): 29–37.

13. Ivica L, Tobias D, Peer B. SMART: recent updates, new developments and status in 2015. Nucleic Acids Research. 2015; 43(D1): 257–260.

14. Aron MB, Derbyshire MK, Gonzales NR, Shennan L, Farideh C, Geer LY, et al. CDD: NCBI's conserved domain database. Nucleic Acids Research. 2015; 43(D1): D222.

15. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Altschul S F. Basic local alignment search tool (BLAST)[J]. Journal of Molecular Biology, 1990, 215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2 2231712

16. Kong X, Lv W, Jiang S, Zhang D, Cai G, Pan J, et al. Genome-wide identification and expression analysis of calcium-dependent protein kinase in maize. Bmc Genomics. 2013; 14(1): 433–433.

17. Holub EB. The arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews Genetics. 2001; 2(7): 516–527. doi: 10.1038/35080508 11433358

18. Yi W, Colemanderr D, Chen G, Gu YQ. OrthoVenn: a web server for genome wide comparison and annotation of orthologous clusters across multiple species. Nucleic Acids Research. 2015; 43(1): 78–84.

19. Hu B, Jin J, Guo AY, Zhang H, Luo J, Gao G. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics. 2014; 31(8): 1296. doi: 10.1093/bioinformatics/btu817 25504850

20. Bailey TL, Nadya W, Chris M, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Research. 2006; 34(Web Server): 369–373.

21. Magali L, Patrice D, Gert T, Kathleen M, Yves M, Yves VDP, et al. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research. 2002; 30(1): 325–327. doi: 10.1093/nar/30.1.325 11752327

22. Dai X, Zhao PX. psRNATarget: a plant small RNA target analysis server. Nucleic Acids Research. 2011; 39(suppl): W155–W159.

23. Jian G, Mao L, Zhang C, Hua P, Lin H, Shen Y, et al. A putative pathogen-resistant regulatory pathway between MicroRNAs and candidate target genes in maize. Journal of Plant Biology. 2015; 58(4): 211–219.

24. Schefe JH, Lehmann KE, Buschmann IR, Unger T, Funke-Kaiser H. Quantitative real-time RT-PCR data analysis: current concepts and the novel “gene expression’sCTdifference” formula. Journal of Molecular Medicine. 2006; 84(11): 901–910. doi: 10.1007/s00109-006-0097-6 16972087

25. Kavas M, Kızıldoğan AK, Abanoz B. Comparative genome-wide phylogenetic and expression analysis of SBP genes from potato (Solanum tuberosum). Computational Biology & Chemistry. 2017; 67: 131–140.

26. Geraldo Felipe FES, Eder Marques S, Azevedo MDS, Guivin MAC, Daniel Alves R, Cassia Regina F, et al. microRNA156-targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. Plant Journal. 2014; 78(4): 604–618. doi: 10.1111/tpj.12493 24580734

27. Xu M, Hu T, Zhao J, Park MY, Earley KW, Wu G, et al. Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. Plos Genetics. 2016; 12(8): e1006263. doi: 10.1371/journal.pgen.1006263 27541584

28. Hua-Wei T, Xiao-Ming S, Wei-Ke D, Yan W, Xi-Lin H. Genome-wide analysis of the SBP-box gene family in Chinese cabbage (Brassica rapa subsp. pekinensis). Genome / National Research Council Canada = Ge?nome / Conseil national de recherches Canada. 2015; 58(11): 463–477.

29. Hongmin H, Jun L, Min G, Singer SD, Hao W, Linyong M, et al. Genomic organization, phylogenetic comparison and differential expression of the SBP-box family genes in grape. Plos One. 2013; 8(3): e59358. doi: 10.1371/journal.pone.0059358 23527172

30. Li C, Lu S. Molecular characterization of the SPL gene family in Populus trichocarpa. Bmc Plant Biology. 2014; 14(1): 131.

31. Yang J, Liu X, Yang X, Zhang M. Mitochondrially-targeted expression of a cytoplasmic male sterility-associated orf220 gene causes male sterility in Brassica juncea. Bmc Plant Biology. 2010; 10(1): 231.

32. Jia-Wei W, Benjamin C, Detlef W. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell. 2009; 138(4): 738–749. doi: 10.1016/j.cell.2009.06.014 19703399

33. Kabin X, Jianqiang S, Xin H, Jialing Y, Xianghua L, Jinghua X, et al. Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiology. 2012; 158(3): 1382–1394. doi: 10.1104/pp.111.190488 22271747

34. Stief A, Altmann S, Hoffmann K, Pant BD, Scheible WR, Bäurle I. Arabidopsis miR156 Regulates Tolerance to Recurring Environmental Stress through SPL Transcription Factors. Plant Cell. 2014; 26(4): 1792. doi: 10.1105/tpc.114.123851 24769482

35. Tripathi RK, Goel R, Kumari S, Dahuja A. Genomic organization, phylogenetic comparison, and expression profiles of the SPL family genes and their regulation in soybean. Development Genes & Evolution. 2017; 227(2): 1–19.

36. Kabin X, Congqing W, Lizhong X. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiology. 2006; 142(1): 280–293. doi: 10.1104/pp.106.084475 16861571

37. Xu M, Hu T, Zhao J, Park MY, Earley KW, Wu G, et al. Developmental Functions of miR156-Regulated SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) Genes in Arabidopsis thaliana. Plos Genetics. 2016; 12(8): e1006263–. doi: 10.1371/journal.pgen.1006263 27541584

38. Jae-Hoon J, Yun J, Pil Joon S, Jae-Hyung L, Chung-Mo P. The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. Plant Journal. 2012; 69(4): 577–588. doi: 10.1111/j.1365-313X.2011.04813.x 21988498

39. Yu N, Niu QW, Ng KH, Chua NH. The role of miR156/SPLs modules in Arabidopsis lateral root development. Plant Journal. 2015; 83(4): 673–685. doi: 10.1111/tpj.12919 26096676

40. Chao LM, Liu YQ, Chen DY, Xue XY, Mao YB. Arabidopsis Transcription Factors SPL1 and SPL12 Confer Plant Thermotolerance at Reproductive Stage. Molecular Plant. 2017; 10(5): 735–748. doi: 10.1016/j.molp.2017.03.010 28400323

41. Garcia-Molina A, Xing S, Huijser P. Functional characterisation of Arabidopsis SPL7 conserved protein domains suggests novel regulatory mechanisms in the Cu deficiency response. Bmc Plant Biology. 2014; 14(1): 231.

42. Shuping X, María S, Antoni GM, Susanne HH, Rita B, Peter H. SPL8 and miR156-targeted SPL genes redundantly regulate Arabidopsis gynoecium differential patterning. Plant Journal. 2013; 75(4): 566–577. doi: 10.1111/tpj.12221 23621152


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2019 Číslo 11