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, 32 (7), 1767-73

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

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

Jinpu Jin et al. Mol Biol Evol.

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.

Keywords: network structure; novel family; transcription factor; transcriptional regulation; wiring preference.

Figures

F<sc>ig</sc>. 1.
Fig. 1.
The transcriptional regulatory landscape in Arabidopsis. (A) The ATRM. This figure shows the largest connected component in the ATRM. The circle and triangle nodes represent TFs and non-TFs, respectively. (B) Biological process distribution of the genes in the ATRM. (C) The comparison of the proportion of regulations co-existing in the same biological processes indicates the high quality of the ATRM. The significance values from one-tailed binomial tests are indicated above the horizontal lines. (D) Comparison of the Arabidopsis floral meristem establishment and specification pathway summarized in a previously published review (Irish 2010) with the regulations among these genes established in the ATRM. The black line represents regulation present in both the summarized pathway and the ATRM; the red line represents regulation added to the ATRM after the comparison; and the cyan line represents novel regulation present in the ATRM but not observed in the summarized pathway. The blue, red, and cyan nodes represent the A, B, and C functional genes, respectively, in the classic “ABC” model of flower development (Weigel and Meyerowitz 1994).
F<sc>ig</sc>. 2.
Fig. 2.
The architecture of developmental and stress response subnetworks in Arabidopsis. (A) Global topological parameters of the developmental and stress response subnetworks. (B) Topological parameters of the developmental and stress response subnetworks under subsamplings. We randomly sampled 50%, 60%, 70%, 80%, and 90% regulations from the developmental and stress response subnetworks 1,000 times and observed the effects on the calculated topological parameters. Standard deviations are indicated in the figure. (C) All identified three-node network motifs in the ATRM. The number in parentheses, for example, Motif 5 (303), represents the number of that motif present in the ATRM. (D) The distribution of network motifs in the developmental and stress response subnetworks. In panels (C) and (D), the network motifs absent from the unicellular organisms Escherichia coli and Saccharomyces cerevisiae are highlighted in bold (e.g., Motif 10).
F<sc>ig</sc>. 3.
Fig. 3.
The wiring positions of ancient- and novel-family TFs in the Arabidopsis transcriptional regulatory system and their binding specificities. (A) The classification of ancient and novel TF families. Plant landing corresponds to ∼1 billion years ago to ∼450 Ma (cyan line). (B) The wiring preference of ancient and novel families in biological processes. Each point represents a family. A jitter function was used to finely modify the point positions to display overlapping points. (C) The distributions of ancient- and novel-family TFs in the developmental and stress response processes. (D) The wiring positions of ancient- and novel-family TFs in the ATRM. For each aspect, we summarized the numbers of novel- and ancient-family TFs that were fewer than or more than the average value. One-tailed Fisher’s exact tests were performed to compare the wiring preferences of novel- and ancient-family TFs. (E and F) The binding specificities of ancient- and novel-family TFs measured based on the information content of binding matrices in Arabidopsis thaliana (E) and Homo sapiens (F). In panels (E) and (F), the P values obtained from one-tailed Wilcoxon rank-sum tests are indicated above the horizontal line.

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