Allele specific expression of Dof genes responding to hormones and abiotic stresses in sugarcane

Autoři: Mingxing Cai aff001;  Jishan Lin aff001;  Zeyun Li aff001;  Zhicong Lin aff002;  Yaying Ma aff001;  Yibin Wang aff001;  Ray Ming aff001
Působiště autorů: College of Life Sciences, Center for Genomics and Biotechnology, Fujian Provincial Key Laboratory of Haixia Applied Plant Systems Biology, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China aff001;  College of Crop Sciences, Fujian Agriculture and Forestry University, Fuzhou, Fujian, China aff002;  Department of Plant Biology, University of Illinois at Urbana-Champaign, Urbana, IL, United States of America aff003
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227716


Dof transcription factors plant-specific and associates with growth and development in plants. We conducted comprehensive and systematic analyses of Dof transcription factors in sugarcane, and identified 29 SsDof transcription factors in sugarcane genome. Those SsDof genes were divided into five groups, with similar gene structures and conserved motifs within the same groups. Segmental duplications are predominant in the evolution of Dof in sugarcane. Cis-element analysis suggested that the functions of SsDofs were involved in growth and development, hormones and abiotic stresses responses in sugarcane. Expression patterns indicated that SsDof7, SsDof23 and SsDof24 had a comparatively high expression in all detected tissues, indicating these genes are crucial in sugarcane growth and development. Moreover, we examined the transcription levels of SsDofs under four plant hormone treatments, SsDof7-3 and SsDof7-4 were down-regulated after ABA treatment, while SsDof7-1 and SsDof7-2 were induced after the same treatment, indicating different alleles may play different roles in response to plant hormones. We also analyzed SsDofs’ expression profiling under four abiotic stresses, SsDof5 and SsDof28 significantly responded to these four stresses, indicating they are associate with abiotic stresses responses. Collectively, our results yielded allele specific expression of Dof genes responding to hormones and abiotic stresses in sugarcane, and their cis-elements could be crucial for sugarcane improvement.

Klíčová slova:

Arabidopsis thaliana – Gene expression – Plant genomics – Plant hormones – Seedlings – Sequence motif analysis – Sugarcane – Transcription factors


1. Yanagisawa S, Schmidt RJ (1999) Diversity and similarity among recognition sequences of Dof transcription factors. Plant J 17: 209–214. doi: 10.1046/j.1365-313x.1999.00363.x 10074718

2. Ma J, Li MY, Wang F, Tang J, Xiong AS (2015) Genome-wide analysis of Dof family transcription factors and their responses to abiotic stresses in Chinese cabbage. BMC Genomics 16: 33. doi: 10.1186/s12864-015-1242-9 25636232

3. Yanagisawa S (2000) Dof1 and Dof2 transcription factors are associated with expression of multiple genes involved in carbon metabolism in maize. Plant J 21: 281–288. doi: 10.1046/j.1365-313x.2000.00685.x 10758479

4. Kloosterman B, Abelenda JA, Gomez Mdel M, Oortwijn M, de Boer JM, Kowitwanich K, et al. (2013) Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495: 246–250. doi: 10.1038/nature11912 23467094

5. Iwamoto M, Higo K, Takano M (2009) Circadian clock- and phytochrome-regulated Dof-like gene, Rdd1, is associated with grain size in rice. Plant Cell Environ 32: 592–603. doi: 10.1111/j.1365-3040.2009.01954.x 19210638

6. Corrales AR, Nebauer SG, Carrillo L, Fernandez-Nohales P, Marques J, Renau-Morata B, et al. (2014) Characterization of tomato Cycling Dof Factors reveals conserved and new functions in the control of flowering time and abiotic stress responses. J Exp Bot 65: 995–1012. doi: 10.1093/jxb/ert451 24399177

7. Yang J, Yang MF, Zhang WP, Chen F, Shen SH (2011) A putative flowering-time-related Dof transcription factor gene, JcDof3, is controlled by the circadian clock in Jatropha curcas. Plant Sci 181: 667–674. doi: 10.1016/j.plantsci.2011.05.003 21958709

8. Moreno-Risueno MA, Diaz I, Carrillo L, Fuentes R, Carbonero P (2007) The HvDOF19 transcription factor mediates the abscisic aciddependent repression of hydrolase genes in germinating barley aleurone. Plant Journal 51: 352–365. doi: 10.1111/j.1365-313X.2007.03146.x 17565581

9. Washio K (2001) Identification of Dof proteins with implication in the gibberellin-regulated expression of a peptidase gene following the germination of rice grains. Biochim Biophys Acta 1520: 54–62. doi: 10.1016/s0167-4781(01)00251-2 11470159

10. Washio K (2003) Functional dissections between GAMYB and Dof transcription factors suggest a role for protein-protein associations in the gibberellin-mediated expression of the RAmy1A gene in the rice aleurone. Plant Physiol 133: 850–863. doi: 10.1104/pp.103.027334 14500792

11. Chen W, Chao G, Singh KB (1996) The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J 10: 955–966. doi: 10.1046/j.1365-313x.1996.10060955.x 9011080

12. Papi M, Sabatini S, Bouchez D, Camilleri C, Costantino P, Vittorioso P (2000) Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev 14: 28–33. 10640273

13. Wen CL, Cheng Q, Zhao L, Mao A, Yang J, Yu S, et al. (2016) Identification and characterisation of Dof transcription factors in the cucumber genome. Sci Rep 6: 23072. doi: 10.1038/srep23072 26979661

14. Guo Y, Qiu LJ (2013) Genome-Wide Analysis of the Dof Transcription Factor Gene Family Reveals Soybean-Specific Duplicable and Functional Characteristics (Retracted article. See vol. 11, e0167019, 2016). Plos One 8.

15. Zhang J, Zhou M, Walsh J, Lin Z, Ming R (2013) Sugarcane Genetics and Genomics: John Wiley & Sons Ltd. doi: 10.1186/1471-2164-14-314

16. Zhang J, Zhang X, Tang H, Zhang Q, Hua X, Ma X, et al. (2018) Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L. Nat Genet 50: 1565–1573. doi: 10.1038/s41588-018-0237-2 30297971

17. Chen Y, Zhang Q, Hu W, Zhang X, Wang L, Hua X, et al. (2017) Evolution and expression of the fructokinase gene family in Saccharum. BMC Genomics 18: 197. doi: 10.1186/s12864-017-3535-7 28222695

18. Hu W, Hua X, Zhang Q, Wang J, Shen Q, Zhang X, et al. (2018) New insights into the evolution and functional divergence of the SWEET family in Saccharum based on comparative genomics. BMC Plant Biol 18: 270. doi: 10.1186/s12870-018-1495-y 30404601

19. Zhang Q, Hu W, Zhu F, Wang L, Yu Q, Ming R, et al. (2016) Structure, phylogeny, allelic haplotypes and expression of sucrose transporter gene families in Saccharum. BMC Genomics 17: 88. doi: 10.1186/s12864-016-2419-6 26830680

20. Stormo GD (2000) Gene-finding approaches for eukaryotes. Genome Res 10: 394–397. doi: 10.1101/gr.10.4.394 10779479

21. Guo AY, Zhu QH, Chen X, Luo JC (2007) [GSDS: a gene structure display server]. Yi Chuan 29: 1023–1026.

22. Bailey TL, Boden M, Buske FA, Frith M, Grant CE, Clementi L, et al. (2009) MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res 37: W202–208. doi: 10.1093/nar/gkp335 19458158

23. Wu Z, Cheng J, Cui J, Xu X, Liang G, Luo X, et al. (2016) Genome-Wide Identification and Expression Profile of Dof Transcription Factor Gene Family in Pepper (Capsicum annuum L.). Front Plant Sci 7: 574. doi: 10.3389/fpls.2016.00574 27200047

24. Wang D, Zhang Y, Zhang Z, Zhu J, Yu J (2010) KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8: 77–80. doi: 10.1016/S1672-0229(10)60008-3 20451164

25. Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Curr Protoc Bioinformatics Chapter 6: Unit 6 5.

26. Lynch M, Conery JS (2000) The evolutionary fate and consequences of duplicate genes. Science 290: 1151–1155. doi: 10.1126/science.290.5494.1151 11073452

27. Chow CN, Lee TY, Hung YC, Li GZ, Tseng KC, Liu YH, et al. (2019) PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants. Nucleic Acids Res 47: D1155–D1163. doi: 10.1093/nar/gky1081 30395277

28. Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, et al. (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30: 325–327. doi: 10.1093/nar/30.1.325 11752327

29. Chen C, Chen H, He Y, Xia R (2018) TBtools, a <span class = "underline">Toolkit for <span class = "underline">Biologists integrating various biological data handling <span class = "underline">tools with a user-friendly interface. bioRxiv.

30. Ma J, He Y, Wu C, Liu H, Hu Z, Sun G Cloning and Molecular Characterization of a SERK Gene Transcriptionally Induced During Somatic Embryogenesis inAnanas comosus cv. Shenwan. Plant Molecular Biology Reporter 30: 195–203.

31. Ling H, Wu Q, Guo J, Xu L, Que Y (2014) Comprehensive selection of reference genes for gene expression normalization in sugarcane by real time quantitative rt-PCR. PLoS One 9: e97469. doi: 10.1371/journal.pone.0097469 24823940

32. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45. doi: 10.1093/nar/29.9.e45 11328886

33. Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7: 555–560. doi: 10.1016/s1360-1385(02)02362-2 12475498

34. Kushwaha H, Gupta S, Singh VK, Rastogi S, Yadav D (2011) Genome wide identification of Dof transcription factor gene family in sorghum and its comparative phylogenetic analysis with rice and Arabidopsis. Mol Biol Rep 38: 5037–5053. doi: 10.1007/s11033-010-0650-9 21161392

35. Lijavetzky D, Carbonero P, Vicente-Carbajosa J (2003) Genome-wide comparative phylogenetic analysis of the rice and Arabidopsis Dof gene families. BMC Evol Biol 3: 17. doi: 10.1186/1471-2148-3-17 12877745

36. Cai X, Zhang Y, Zhang C, Zhang T, Hu T, Ye J, et al. (2013) Genome-wide analysis of plant-specific Dof transcription factor family in tomato. J Integr Plant Biol 55: 552–566. doi: 10.1111/jipb.12043 23462305

37. Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4: 10. doi: 10.1186/1471-2229-4-10 15171794

38. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2: 516–527. doi: 10.1038/35080508 11433358

39. Liu Y, Jiang H, Chen W, Qian Y, Ma Q, Cheng B, et al. Genome-wide analysis of the auxin response factor (ARF) gene family in maize (Zea mays). Plant Growth Regulation 63: 225–234.

40. Konishi M, Yanagisawa S (2007) Sequential activation of two Dof transcription factor gene promoters during vascular development in Arabidopsis thaliana. Plant Physiol Biochem 45: 623–629. doi: 10.1016/j.plaphy.2007.05.001 17583520

41. Gardiner J, Sherr I, Scarpella E (2010) Expression of DOF genes identifies early stages of vascular development in Arabidopsis leaves. Int J Dev Biol 54: 1389–1396. doi: 10.1387/ijdb.093006jg 20563990

42. Negi J, Moriwaki K, Konishi M, Yokoyama R, Nakano T, Kusumi K, et al. (2013) A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr Biol 23: 479–484. doi: 10.1016/j.cub.2013.02.001 23453954

43. Venkatesh J, Park SW (2015) Genome-wide analysis and expression profiling of DNA-binding with one zinc finger (Dof) transcription factor family in potato. Plant Physiol Biochem 94: 73–85. doi: 10.1016/j.plaphy.2015.05.010 26046625

44. Baumann K, De Paolis A, Costantino P, Gualberti G (1999) The DNA binding site of the Dof protein NtBBF1 is essential for tissue-specific and auxin-regulated expression of the rolB oncogene in plants. Plant Cell 11: 323–334. doi: 10.1105/tpc.11.3.323 10072394

45. Le DT, Nishiyama R, Watanabe Y, Vankova R, Tanaka M, Seki M, et al. (2012) Identification and expression analysis of cytokinin metabolic genes in soybean under normal and drought conditions in relation to cytokinin levels. PLoS One 7: e42411. doi: 10.1371/journal.pone.0042411 22900018

46. Walther D, Brunnemann R, Selbig J (2007) The regulatory code for transcriptional response diversity and its relation to genome structural properties in A. thaliana. PLoS Genet 3: e11. doi: 10.1371/journal.pgen.0030011 17291162

47. Skirycz A, Reichelt M, Burow M, Birkemeyer C, Rolcik J, Kopka J, et al. (2006) DOF transcription factor AtDof1.1 (OBP2) is part of a regulatory network controlling glucosinolate biosynthesis in Arabidopsis. Plant J 47: 10–24. doi: 10.1111/j.1365-313X.2006.02767.x 16740150

48. Taylor JS, Raes J (2004) Duplication and divergence: the evolution of new genes and old ideas. Annu Rev Genet 38: 615–643. doi: 10.1146/annurev.genet.38.072902.092831 15568988

49. Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8: 122–128. doi: 10.1016/j.pbi.2004.12.001 15752990

50. Semon M, Wolfe KH (2007) Consequences of genome duplication. Curr Opin Genet Dev 17: 505–512. doi: 10.1016/j.gde.2007.09.007 18006297

51. Wang J, Li Y, Zhu F, Ming R, Chen L-Q Genome-Wide Analysis of Nitrate Transporter (NRT/NPF) Family in Sugarcane Saccharum spontaneum L. Tropical Plant Biology.

52. Nelson DR (2019) Cytochrome P450s in the sugarcane Saccharum spontaneum. Tropical Plant Biology 12: 150–157.

53. Ma PP, Yuan Y, Shen QC, Jiang Q, Hua XT, Zhang Q, et al. (2019) Evolution and Expression Analysis of Starch Synthase Gene Families in Saccharum spontaneum. Tropical Plant Biology 12: 158–173.

54. Shi Y, Xu H, Shen Q, Lin J, Zhang J (2019) Comparative Analysis of SUS Gene Family between Saccharum officinarum and Saccharum spontaneum. Tropical Plant Biology.

55. Lin JS, Zhu MT, Cai MX, Zhang WP, Fatima M, Jia HF, et al. (2019) Identification and Expression Analysis of TCP Genes in Saccharum spontaneum L. Tropical Plant Biology 12: 206–218.

56. Zhang WP, Lin JS, Dong F, Ma Q, Wu SL, Ma XY, et al. (2019) Genomic and Allelic Analyses of Laccase Genes in Sugarcane (Saccharum spontaneum L.). Tropical Plant Biology 12: 219–229.

Článek vyšel v časopise


2020 Číslo 1