Abstract
Nelumbo nucifera (Sacred Lotus) is a basal eudicot with exceptional physiological and metabolic properties including seed longevity, adaptations for an aquatic habit, and floral thermiogenesis. It also occupies a unique position in the phylogeny of land plants and can be a useful species for studies of conserved plant gene families. The basic-helix-loop-helix (bHLH) proteins represent one of the largest transcription factor families in plants and has undergone extensive duplication and expansion during plant evolution. One hundred and seventeen transcript models encoding canonical bHLHs were identified in the sacred lotus genome, as well as several “atypical” bHLH-encoding genes. The canonical bHLH proteins fall into 23 previously characterized subfamilies also present in other sequenced plant genomes, and are expressed as mRNA. Analysis of bHLHs from sacred lotus and other sequenced angiosperms indicates most of these families of bHLHs, along with secondary motifs associated with the bHLH domain, were likely present in the progenitor of flowering plants. The absence of a bHLH subfamily involved in root development in sacred lotus is consistent with the possibility that the development of specialized root structures may be mediated in part by changes in the bHLH families that regulate root development in dicots.
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References
Atchley WR, Fitch WM (1997) A natural classification of the basic helix-loop-helix class of transcription factors. Proc Natl Acad Sci U S A 94:5172–5176
Bruex A, Kainkaryam RM, Wieckowski Y, Kang YH, Bernhardt C, Xia Y, Zheng X, Wang JY, Lee MM, Benfey P, Woolf PJ, Schiefelbein J (2012) A gene regulatory network for root epidermis cell differentiation in Arabidopsis. PLoS Genet 8:e1002446
Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martinez-Garcia JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412
Drummond AJ, Ashton B, Buxton S, Cheung M, Cooper A, Duran C, Field M, Heled J, Kearse M, Markowitz S, Moir R, Stones-Havas S, Sturrock S, Thierer T, Wilson A (2012) Geneious, version 5.4. 2011. Geneious, Auckland, New Zealand. Geneious version 5.6.2 created by Biomatters. Available from http://www.geneious.com/
Eddy SR (2008) A probabilistic model of local sequence alignment that simplifies statistical significance estimation. PLoS Comput Biol 4:e1000069
Feller A, Hernandez JM, Grotewold E (2006) An ACT-like domain participates in the dimerization of several plant basic-helix-loop-helix transcription factors. J Biol Chem 281:28964–28974
Feller A, Machemer K, Braun EL, Grotewold E (2011) Evolutionary and comparative analysis of MYB and bHLH plant transcription factors. Plant J 66:94–116
Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix-loop-helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Biol Evol 20:735–747
Hudson ME, Quail PH (2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiol 133:1605–1616
Hyun Y, Lee I (2006) KIDARI, encoding a non-DNA Binding bHLH protein, represses light signal transduction in Arabidopsis thaliana. Plant Mol Biol 61:283–296
Jang G, Yi K, Pires ND, Menand B, Dolan L (2011) RSL genes are sufficient for rhizoid system development in early diverging land plants. Development 138:2273–2281
Katoh K, Toh H (2008) Recent developments in the MAFFT multiple sequence alignment program. Brief Bioinform 9:286–298
Khanna R, Huq E, Kikis EA, Al-Sady B, Lanzatella C, Quail PH (2004) A novel molecular recognition motif necessary for targeting photoactivated phytochrome signaling to specific basic helix-loop-helix transcription factors. Plant Cell 16:3033–3044
Kim M-J, Nelson W, Soderlund C, Gang D (2013) Next-generation sequencing-based transcriptional profiling of sacred lotus “China antique”. Trop Plant Biol 6:161–179
Landschulz WH, Johnson PF, McKnight SL (1988) The leucine zipper: a hypothetical structure common to a new class of DNA binding proteins. Science 240:1759–1764
Li X, Duan X, Jiang H, Sun Y, Tang Y, Yuan Z, Guo J, Liang W, Chen L, Yin J, Ma H, Wang J, Zhang D (2006) Genome-wide analysis of basic/helix-loop-helix transcription factor family in rice and Arabidopsis. Plant Physiol 141:1167–1184
Martinez-Garcia JF, Huq E, Quail PH (2000) Direct targeting of light signals to a promoter element-bound transcription factor. Science 288:859–863
Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20:429–440
Ming R et al (2013) Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 14:R41
Moon J, Zhu L, Shen H, Huq E (2008) PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci U S A 105:9433–9438
Ohashi-Ito K, Bergmann DC (2007) Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development 134:2959–2968
Pires N, Dolan L (2010) Origin and diversification of basic-helix-loop-helix proteins in plants. Mol Biol Evol 27:862–874
Pires ND, Yi K, Breuninger H, Catarino B, Menand B, Dolan L (2013) Recruitment and remodeling of an ancient gene regulatory network during land plant evolution. Proc Natl Acad Sci U S A 110:9571–9576
Stamatakis A (2006) RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688–2690
Toledo-Ortiz G, Huq E, Quail PH (2003) The Arabidopsis basic/helix-loop-helix transcription factor family. Plant Cell 15:1749–1770
Wang Y et al (2013) The sacred lotus genome provides insights into the evolution of flowering plants. Plant J 76(4):557–567
Yi K, Wu Z, Zhou J, Du L, Guo L, Wu Y, Wu P (2005) OsPTF1, a novel transcription factor involved in tolerance to phosphate starvation in rice. Plant Physiol 138:2087–2096
Yi K, Menand B, Bell E, Dolan L (2010) A basic helix-loop-helix transcription factor controls cell growth and size in root hairs. Nat Genet 42:264–267
Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J (2005) A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell 120:249–259
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Communicated by: Ray Ming
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Additional file 1
Table – Sacred lotus bHLH gene models (XLSX 66 kb)
Additional file 2
bHLH phylogeny. See Methods for details. (PDF 583 kb)
Additional file 3
Atypical bHLH alignments (PPTX 7258 kb)
Additional File 4
Intron position in sacred lotus bHLH transcripts (PDF 47 kb)
Additional File 5
Consensus sequences for additional motifs found in sacred lotus bHLH proteins (PPTX 431 kb)
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Hudson, K.A., Hudson, M.E. The Basic Helix-Loop-Helix Transcription Factor Family in the Sacred Lotus, Nelumbo Nucifera . Tropical Plant Biol. 7, 65–70 (2014). https://doi.org/10.1007/s12042-014-9138-4
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DOI: https://doi.org/10.1007/s12042-014-9138-4