biologia plantarum

International journal on Plant Life established by Bohumil Němec in 1959

Biologia plantarum 62:711-720, 2018 | DOI: 10.1007/s10535-018-0816-1

Phylogenetic and transcriptional analysis of chrysanthemum GRAS transcription factors

T. W. Gao1, W. W. Zhang1, A. P. Song1, C. An1, J. J. Xin1, J. F. Jiang1, Z. Y. Guan1, F. D. Chen1, S. M. Chen1,*
1 College of Horticulture, Nanjing Agricultural University, Nanjing, P.R. China

The GRAS transcription factors encoding proteins ranging from 400 to 700 residues are recognized by their conserved C terminus. Here, a set of 23 CmGRAS genes was identified from a scan of the chrysanthemum (Chrysanthemum morifolium) transcriptome. A phylogenetic analysis implied that nine of these genes could be assigned orthologs to the GRAS gene family, and that four of them formed two pairs of paralogs. A phylogenetic analysis of the GRAS protein family based on the chrysanthemum and recent study of eight representative species of angiosperms showed that most of the CmGRAS genes belonged to a recognized sub-group. CmGRAS4 and CmGRAS10 were strongly transcribed in flowers and roots, respectively. The DELLA subfamily transcript abundance of the CmGRAS19 and CmGRAS20 was high in the reproductive tissues and they were responsive to phytohormones and stresses. Establishment of the orthology relationships between the known representative GRAS genes and CmGRAS, and transcriptional profiles of CmGRASs after phytohormone treatments or stresses will facilitate subsequent functional analyses in the GRAS gene family.

Keywords: abscisic acid; Chrysanthemum morifolium; cold; heat; methyl jasmonate; osmotic stress; salicylic acid; salinity; wounding.
Subjects: transcription factors; gene expression; abscisic acid; cold; heat; osmotic stress; methyl jasmonate; salicylic acid; salt stress

Received: September 13, 2017; Revised: April 28, 2018; Accepted: May 18, 2018; Published: August 1, 2018  Show citation

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Gao, T.W., Zhang, W.W., Song, A.P., An, C., Xin, J.J., Jiang, J.F., ... Chen, S.M. (2018). Phylogenetic and transcriptional analysis of chrysanthemum GRAS transcription factors. Biologia plantarum, 62(4), 711-720. doi: 10.1007/s10535-018-0816-1
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    References

    1. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., Genschik, P.: The cold-inducibleCBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. - Plant Cell 20: 2117-2129, 2008a. Go to original source...
    2. Achard, P., Renou, J. P., Berthomé, R., Harberd, N. P., Genschik, P.: Plant dellas restrain growth and promote survival of adversity by reducing the levels of reactive oxygen species. - Curr Biol. 18: 656-660, 2008b. Go to original source...
    3. Alaey, M., Babalar, M., Naderi, R., Kafi, M.: Effect of pre- and post-harvest salicylic acid treatment on physio-chemical attributes in relation to vase-life of rose cut flowers. - Postharvest Biol. Technol. 61: 91-94, 2011. Go to original source...
    4. Bailey, T.L., Boden, M., Buske, F.A., Frith, M., Grant, C.E., Clementi, L., Noble, W.S.: MEME SUITE: tools for motif discovery and searching. - Nucl. Acids Res. 37: W202-208, 2009. Go to original source...
    5. Banno, H., Ikeda, Y., Niu, Q.W., Chua, N.H.: Overexpression of Arabidopsis ESR1 induces initiation of shoot regeneration. - Plant Cell 13: 2609-2618, 2001. Go to original source...
    6. Bolle, C.: The role of GRAS proteins in plant signal transduction and development. - Planta 218: 683-692, 2004. Go to original source...
    7. Bolle, C., Koncz, C., Chua, N.-H.: PAT1, a new member of the GRAS family, is involved in phytochrome A signal transduction. - Gene. Dev. 14: 1269-1278, 2000. Go to original source...
    8. Cenci, A., Rouard, M.: Evolutionary analyses of GRAS transcription factors in angiosperms. - Front. Plant Sci. 8: 273, 2017. Go to original source...
    9. Chandler, P.M., Marion-Poll, A., Ellis, M., Gubler, F.: Mutants at the Slender1 locus of barley cv. Himalaya. Molecular and physiological characterization. - Plant Physiol. 129: 181-190, 2002. Go to original source...
    10. Chen, K., Li, H., Chen, Y., Zheng, Q., Li, B., Li, Z.: TaSCL14, a Novel wheat (Triticum aestivum L.) GRAS gene, regulates plant growth, photosynthesis, tolerance to photooxidative stress, and senescence. - J. Genet. Genomics 42: 21-32, 2015. Go to original source...
    11. De Hoon, M.J.L., Imoto, S., Nolan, J., Miyano, S.: Open source clustering software. - Bioinformatics 20: 1453, 2004. Go to original source...
    12. Eisen, M.B., Spellman, P.T., Brown, P.O., Botstein, D.: Cluster analysis and display of genome-wide expression patterns. - Proc. nat. Acad. Sci. USA 95: 14863-14868, 1998. Go to original source...
    13. Engstrom, E. M., Andersen, C.M., Gumulak-Smith, J., Hu, J., Orlova, E., Sozzani, R.: Arabidopsis homologs of the petunia hairy meristem gene are required for maintenance of shoot and root indeterminacy. - Plant Physiol. 155: 735, 2011. Go to original source...
    14. Fode, B., Siemsen, T., Thurow, C., Weigel, R. Gatz, C.: The Arabidopsis GRAS protein SCL14 interacts with class II TGA transcription factors and is essential for the activation of stress-inducible promoters. - Plant Cell 20: 3122-3135, 2008. Go to original source...
    15. Gao, M.-J., Li, X., Huang, J., Gropp, G.M., Gjetvaj, B., Lindsay, D.L., Wan, X.-C.: SCARECROW-LIKE15 interacts with HISTONE DEACETYLASE19 and is essential for repressing the seed maturation programme. - Nat. Commun. 6: 7243, 2015. Go to original source...
    16. Gao, M.-J., Parkin, I., Lydiate, D., Hannoufa, A.: An auxinresponsive SCARECROW-like transcriptional activator interacts with histone deacetylase. - Plant mol. Biol. 55: 417-431, 2004. Go to original source...
    17. Greb, T., Clarenz, O., Schafer, E., Muller, D., Herrero, R., Schmitz, G., Theres, K.: Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. - Gene Dev. 17: 1175-1187, 2003. Go to original source...
    18. Hedden, P.: The genes of the green revolution. - Trends Genet. 19: 5-9, 2003. Go to original source...
    19. Heo, J.-O., Chang, K.S., Kim, I.A., Lee, M.-H., Lee, S.A., Song, S.-K., Lim, J.: Funneling of gibberellin signaling by the GRAS transcription regulator scarecrow-like 3 in the Arabidopsis root. - Proc. nat. Acad. Sci. USA 108: 2166-2171, 2011. Go to original source...
    20. Hirsch, S., Oldroyd, G.E.D.: GRAS-domain transcription factors that regulate plant development. - Plant Signal. Behav. 4: 698-700, 2009. Go to original source...
    21. Hossain, M.A., Munemasa, S., Uraji, M., Nakamura, Y., Mori, I.C., Murata, Y.: Involvement of endogenous abscisic acid in methyl jasmonate-induced stomatal closure in Arabidopsis. - Plant Physiol. 156: 430-438, 2011. Go to original source...
    22. Huang. S., Gao, Y., Liu, J., Peng, X., Niu, X., Fei, Z., Liu, Y.: Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. - Mol. Genet. Genomic 287: 495-513, 2012. Go to original source...
    23. Kaló, P., Gleason, C., Edwards, A., Marsh, J., Mitra, R.M, Hirsch, S., Rogers, J.: Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. - Science 308: 1786-1789, 2005. Go to original source...
    24. Koizumi, K., Hayashi, T., Wu, S., Gallagher, K.L.: The SHORTROOT protein acts as a mobile, dose-dependent signal in patterning the ground tissue. - Proc. nat. Acad. Sci. USA 109: 13010-13015, 2012. Go to original source...
    25. Kumar, S., Stecher, G., Tamura, K.: MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. - Mol. Biol. Evol. 33: 1870, 2016. Go to original source...
    26. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., Mcgettigan, P.A., Mcwilliam, H., Lopez, R., Valentin, F., Wallace, I.M., Thompson, J.D., Gibson, T.J., Higgins, D.G.: Clustal W and Clustal X version 2.0. - Bioinformatics 23: 2947-2948, 2007. Go to original source...
    27. Lee, M.-H., Kim, B., Song, S.-K., Heo, J.-O., Yu, N.-I., Lee, S.A., Lim, C.E.: Large-scale analysis of the GRAS gene family in Arabidopsis thaliana. - Plant mol. Biol. 67: 659-670, 2008. Go to original source...
    28. Letunic, I., Bork, P.: Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees. - Nucl. Acids Res. 44: W242-W245, 2016. Go to original source...
    29. Li, X., Qian, Q., Fu, Z., Wang, Y., Xiong, G., Zeng, D., Wang, X., Liu, X., Teng, S., Hiroshi, F., Yuan, M., Luo, D., Han. B., Li, J.: Control of tillering in rice. - Nature 422: 618-621, 2003. Go to original source...
    30. Liu, X., Widmer, A.: Genome-wide Ccmparative analysis of the GRAS gene family in Populus, Arabidopsis and rice. - Plant Mol. Biol. Rep. 32: 1129-1145, 2014. Go to original source...
    31. Livak, K.J., Schmittgen, T.D.: Analysis of relative gene expression data using real-time quantitative PCR and the 2(- Delta Delta C(T)) method. - Methods 25: 402-408, 2001. Go to original source...
    32. Long, Y., Goedhart, J., Schneijderberg, M., Terpstra, I., Shimotohno, A., Bouchet, B.P., Scheres, B.: SCARECROWLIKE23 and SCARECROW jointly specify endodermal cell fate but distinctly control SHORT-ROOT movement. - Plant J. 78: 319-327, 2015. Go to original source...
    33. Ma, H.-S., Liang, D., Shuai, P., Xia, X.-L. Yin, W.-L.: The saltand drought-inducible poplar GRAS protein SCL7 confers salt and drought tolerance in Arabidopsis thaliana. - J. exp. Bot. 61: 4011-4019, 2010. Go to original source...
    34. Miura, K., Okamoto, H., Okuma, E., Shiba, H., Kamada, H., Hasegawa, P.M., Murata, Y.: SIZ1 deficiency causes reduced stomatal aperture and enhanced drought tolerance via controlling salicylic acid-induced accumulation of reactive oxygen species in Arabidopsis. - Plant J. 73: 9-104, 2013. Go to original source...
    35. Moran, P.J., Thompson, G.A: Molecular responses to aphid feeding in Arabidopsis in relation to plant defense pathways. - Plant Physiol. 2: 1074-1085, 2001. Go to original source...
    36. Peng, J., Richards, D.E., Hartley, N.M., Murphy, G.P., Devos, K.M., Flintham, J.E., Pelica, F.: Green revolution' genes encode mutant gibberellin response modulators. - Nature 400: 256, 1999. Go to original source...
    37. Pysh, L.D., Wysocka-Diller, J.W., Camilleri, C., Bouchez, D., Benfey, P.N.: The GRAS gene family in Arabidopsis: sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. - Plant J. cell mol. Biol. 18: 111-119, 1999. Go to original source...
    38. Ricachenevsky, F.K., Sperotto, R.A., Menguer, P.K., Fett, J.P.: Identification of Fe-excess-induced genes in rice shoots reveals a WRKY transcription factor responsive to Fe, drought and senescence. - Mol. Biol. Rep. 37: 3735, 2010. Go to original source...
    39. Santino, A., Taurino, M., De, D.S., Bonsegna, S., Poltronieri, P.: Jasmonate signaling in plant development and defense response to multiple (a)biotic stresses. - Plant Cell Rep. 32: 1085, 2013. Go to original source...
    40. Smit, P., Raedts, J., Portyanko, V., Debellé, F., Gough, C., Bisseling, T., Geurts, R.: NSP1 of the GRAS protein family is essential for rhizobial Nod factor-induced transcription. - Science 308: 1789-1791, 2005. Go to original source...
    41. Song, A., Gao T, Li P, Chen S, Guan Z, Wu D, Chen F.: Transcriptome-wide identification and expression profiling of the DOF transcription factor gene family in Chrysanthemum morifolium. - Front. Plant Sci. 7: 199, 2016a. Go to original source...
    42. Song, A., Gao, T., Wu, D., Xin, J., Chen, S., Guan, Z., Chen, F.: Transcriptome-wide identification and expression analysis of chrysanthemum SBP-like transcription factors. - Plant Physiol. Biochem. 102: 10-16, 2016b. Go to original source...
    43. Song, A., Li, P., Jiang, J., Chen, S., Li, H., Zeng, J., Chen, F.: Phylogenetic and transcription analysis of Chrysanthemum WRKY transcription factors. - Int. J. mol. Sci. 15: 14442-14455, 2014. Go to original source...
    44. Song, A., Lu, J., Jiang, J., Chen, S., Guan, Z., Fang, W., Chen, F.: Isolation and characterisation of Chrysanthemum crassum SOS1, encoding a putative plasma membrane Na(+) /H(+) antiporter. - Plant Biol. 14: 706-713, 2012. Go to original source...
    45. Stuurman, J., Jäggi, F., Kuhlemeier, C.: Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. - Genes Dev. 16: 2213-2218, 2002. Go to original source...
    46. Torres-Galea, P., Hirtreiter, B., Bolle, C.: Two GRAS proteins, SCARECROW-LIKE21 and PHYTOCHROME A SIGNAL TRANSDUCTION1, function cooperatively in phytochrome A signal transduction. - Plant Physiol. 161: 291-304, 2013. Go to original source...
    47. Torres-Galea, P., Huang, L.-F., Chua, N.-H., Bolle, C.: The GRAS protein SCL13 is a positive regulator of phytochrome-dependent red light signaling, but can also modulate phytochrome A responses. - Mol. Genet. Genomics 276: 13-30, 2006. Go to original source...
    48. Traw, M.B., Bergelson, J.: Interactive effects of jasmonic acid, salicylic acid, and gibberellin on induction of trichomes in Arabidopsis. - Plant Physiol. 133: 1367-1375, 2003. Go to original source...
    49. Ubeda-Tomás, S., Swarup, R., Coates, J., Swarup, K., Laplaze, L., Beemster, G.T., Hedden, P., Bhalerao, R., Bennett, M.J.: Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. - Nat. cell. Biol. 10: 625-628, 2008. Go to original source...
    50. Wang, J., Andersson-Gunneras, S., Gaboreanu, I., Hertzberg, M., Tucker, M.R., Zheng, B.: Reduced expression of the SHORT-ROOT gene increases the rates of growth and development in hybrid poplar and Arabidopsis. - PLoS ONE 6: e28878, 2011. Go to original source...
    51. War, A.R., Hussain, B., Sharma, H.C. Induced resistance in groundnut by jasmonic acid and salicylic acid through alteration of trichome density and oviposition by Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). - AoB Plants 5: 38-51, 2013. Go to original source...
    52. Willige, B.C., Ghosh, S., Nill, C., Zourelidou, M., Dohmann, EMN., Maier, A., Schwechheimer, C.: The DELLA domain of GA INSENSITIVE mediates the interaction with the GA INSENSITIVE DWARF1A gibberellin receptor of Arabidopsis. - Plant Cell 19: 1209-1220, 2007. Go to original source...
    53. Xia, X., Shao, Y., Jiang, J., Ren, L., Chen, F., Fang, W., Chen, S.: Gene expression profiles responses to aphid feeding in chrysanthemum (Chrysanthemum morifolium). - BMC Genomics 15: 1050, 2014. Go to original source...
    54. Yoon, E.K., Dhar, S., Lee, M.H., Song, J.H., Lee, S.A., Kim, G., Kim, J.H.: Conservation and diversification of the SHRSCR- SCL23 Rrgulatory network in the development of the functional endodermis in Arabidopsis shoots. - Mol. Plant 9: 1197-1209, 2016. Go to original source...
    55. Zhang, D., Iyer, L.M., Aravind, L.:Bacterial GRAS domain proteins throw new light on gibberellic acid response mechanisms. - Bioinformatics 28: 2407-2411, 2012. Go to original source...
    56. Zhang, F., Wang, Z., Dong, W., Sun, C., Wang, H., Song, A., Teng, N.: Transcriptomic and proteomic analysis reveals mechanisms of embryo abortion during chrysanthemum cross breeding. - Sci. Rep. 4: 6536, 2014. Go to original source...
    57. Zhang, J., Jia, W., Yang, J., Ismail, A.M.: Role of ABA in integrating plant responses to drought and salt stresses. - Field Crop Res. 97: 111-119, 2006. Go to original source...
    58. Zhang, Z.L., Ogawa, M., Fleet, C.M., Zentella, R., Hu, J.H., Heo, J.O., Lim, J., Kamiya, Y.,Yamaguchi, S., Sun, T.P.: SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing master growth repressor DELLA in Arabidopsis. - Proc. nat. Acad. Sci. USA 108: 2160, 2011. Go to original source...

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