An Arabidopsis Transcriptional Regulatory Map Reveals Distinct Functional and Evolutionary Features of Novel Transcription Factors

Overview

Journal Mol Biol Evol

Publisher Oxford University Press

Specialty Biology

Date 2015 Mar 10

PMID 25750178

Citations 89

Authors

Jinpu Jin

Kun He

Xing Tang

Zhe Li

Le Lv

Yi Zhao

Jingchu Luo

Ge Gao

Affiliations

Soon will be listed here.

Abstract

Transcription factors (TFs) play key roles in both development and stress responses. By integrating into and rewiring original systems, novel TFs contribute significantly to the evolution of transcriptional regulatory networks. Here, we report a high-confidence transcriptional regulatory map covering 388 TFs from 47 families in Arabidopsis. Systematic analysis of this map revealed the architectural heterogeneity of developmental and stress response subnetworks and identified three types of novel network motifs that are absent from unicellular organisms and essential for multicellular development. Moreover, TFs of novel families that emerged during plant landing present higher binding specificities and are preferentially wired into developmental processes and these novel network motifs. Further unveiled connection between the binding specificity and wiring preference of TFs explains the wiring preferences of novel-family TFs. These results reveal distinct functional and evolutionary features of novel TFs, suggesting a plausible mechanism for their contribution to the evolution of multicellular organisms.

Citing Articles

Foxtail millet research in supporting climate change resilience efforts: Bibliometric analysis and focused literature review.

Ardie S, Nugroho R, Dirpan A, Anshori M Heliyon. 2025; 11(3):e42348.

PMID: 39968133 PMC: 11834093. DOI: 10.1016/j.heliyon.2025.e42348.

Comparison of the Effects of UV-C Light in the Form of Flash or Continuous Exposure: A Transcriptomic Analysis on L.

Jazayeri S, Aarrouf J, Urban L, Lopez-Lauri F Int J Mol Sci. 2025; 25(24.

PMID: 39769480 PMC: 11676349. DOI: 10.3390/ijms252413718.

Transcriptional regulatory network reveals key transcription factors for regulating agronomic traits in soybean.

Jiao W, Wang M, Guan Y, Guo W, Zhang C, Wei Y Genome Biol. 2024; 25(1):313.

PMID: 39695844 PMC: 11656900. DOI: 10.1186/s13059-024-03454-w.

A Model for the Gene Regulatory Network Along the Arabidopsis Fruit Medio-Lateral Axis: Rewiring the Pod Shatter Process.

Moya-Cuevas J, Ortiz-Gutierrez E, Lopez-Sanchez P, Simon-Moya M, Ballester P, Alvarez-Buylla E Plants (Basel). 2024; 13(20).

PMID: 39458874 PMC: 11511003. DOI: 10.3390/plants13202927.

mulea: An R package for enrichment analysis using multiple ontologies and empirical false discovery rate.

Turek C, Olbei M, Stirling T, Fekete G, Tasnadi E, Gul L BMC Bioinformatics. 2024; 25(1):334.

PMID: 39425047 PMC: 11490090. DOI: 10.1186/s12859-024-05948-7.

References

Riechmann J, Heard J, Martin G, Reuber L, Jiang C, Keddie J . Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science. 2000; 290(5499):2105-10. DOI: 10.1126/science.290.5499.2105. View

Alon U . Network motifs: theory and experimental approaches. Nat Rev Genet. 2007; 8(6):450-61. DOI: 10.1038/nrg2102. View

Borneman A, Gianoulis T, Zhang Z, Yu H, Rozowsky J, Seringhaus M . Divergence of transcription factor binding sites across related yeast species. Science. 2007; 317(5839):815-9. DOI: 10.1126/science.1140748. View

Aerts S, Haeussler M, Van Vooren S, Griffith O, Hulpiau P, Jones S . Text-mining assisted regulatory annotation. Genome Biol. 2008; 9(2):R31. PMC: 2374703. DOI: 10.1186/gb-2008-9-2-r31. View

Christian Perez J, Groisman E . Evolution of transcriptional regulatory circuits in bacteria. Cell. 2009; 138(2):233-44. PMC: 2726713. DOI: 10.1016/j.cell.2009.07.002. View

Jothi R, Balaji S, Wuster A, Grochow J, Gsponer J, Przytycka T . Genomic analysis reveals a tight link between transcription factor dynamics and regulatory network architecture. Mol Syst Biol. 2009; 5:294. PMC: 2736650. DOI: 10.1038/msb.2009.52. View

Price M, Dehal P, Arkin A . Horizontal gene transfer and the evolution of transcriptional regulation in Escherichia coli. Genome Biol. 2008; 9(1):R4. PMC: 2395238. DOI: 10.1186/gb-2008-9-1-r4. View

Irish V . The flowering of Arabidopsis flower development. Plant J. 2010; 61(6):1014-28. DOI: 10.1111/j.1365-313X.2009.04065.x. View

Schmidt D, Wilson M, Ballester B, Schwalie P, Brown G, Marshall A . Five-vertebrate ChIP-seq reveals the evolutionary dynamics of transcription factor binding. Science. 2010; 328(5981):1036-40. PMC: 3008766. DOI: 10.1126/science.1186176. View

10.

Lang D, Weiche B, Timmerhaus G, Richardt S, Riano-Pachon D, Correa L . Genome-wide phylogenetic comparative analysis of plant transcriptional regulation: a timeline of loss, gain, expansion, and correlation with complexity. Genome Biol Evol. 2010; 2:488-503. PMC: 2997552. DOI: 10.1093/gbe/evq032. View

11.

Chen S, Zhang Y, Long M . New genes in Drosophila quickly become essential. Science. 2010; 330(6011):1682-5. PMC: 7211344. DOI: 10.1126/science.1196380. View

12.

Yilmaz A, Mejia-Guerra M, Kurz K, Liang X, Welch L, Grotewold E . AGRIS: the Arabidopsis Gene Regulatory Information Server, an update. Nucleic Acids Res. 2010; 39(Database issue):D1118-22. PMC: 3013708. DOI: 10.1093/nar/gkq1120. View

13.

Zhang H, Jin J, Tang L, Zhao Y, Gu X, Gao G . PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res. 2010; 39(Database issue):D1114-7. PMC: 3013715. DOI: 10.1093/nar/gkq1141. View

14.

Shou C, Bhardwaj N, Lam H, Yan K, Kim P, Snyder M . Measuring the evolutionary rewiring of biological networks. PLoS Comput Biol. 2011; 7(1):e1001050. PMC: 3017101. DOI: 10.1371/journal.pcbi.1001050. View

15.

Zhang Y, Landback P, Vibranovski M, Long M . Accelerated recruitment of new brain development genes into the human genome. PLoS Biol. 2011; 9(10):e1001179. PMC: 3196496. DOI: 10.1371/journal.pbio.1001179. View

16.

Wang X, Wei X, Thijssen B, Das J, Lipkin S, Yu H . Three-dimensional reconstruction of protein networks provides insight into human genetic disease. Nat Biotechnol. 2012; 30(2):159-64. PMC: 3708476. DOI: 10.1038/nbt.2106. View

17.

Gerstein M, Kundaje A, Hariharan M, Landt S, Yan K, Cheng C . Architecture of the human regulatory network derived from ENCODE data. Nature. 2012; 489(7414):91-100. PMC: 4154057. DOI: 10.1038/nature11245. View

18.

Neph S, Stergachis A, Reynolds A, Sandstrom R, Borenstein E, Stamatoyannopoulos J . Circuitry and dynamics of human transcription factor regulatory networks. Cell. 2012; 150(6):1274-86. PMC: 3679407. DOI: 10.1016/j.cell.2012.04.040. View

19.

Jolma A, Yan J, Whitington T, Toivonen J, Nitta K, Rastas P . DNA-binding specificities of human transcription factors. Cell. 2013; 152(1-2):327-39. DOI: 10.1016/j.cell.2012.12.009. View

20.

Chen S, Krinsky B, Long M . New genes as drivers of phenotypic evolution. Nat Rev Genet. 2013; 14(9):645-60. PMC: 4236023. DOI: 10.1038/nrg3521. View