The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes

Corrêa, Luiz Gustavo Guedes; Riaño-Pachón, Diego Mauricio; Schrago, Carlos G.; Vicentini, Renato; Mueller‐Roeber, Bernd; Vincentz, Michel

doi:10.1371/journal.pone.0002944

Cited by 275 publications

(318 citation statements)

References 119 publications

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“…Instead it looks like plants have evolved their own zinc responsive regulation system controlling sufficient uptake of zinc in case of deficiency, depending on bZIP19-or bZIP23-like genes. Putative orthologs have been found in monocots and dicots, but also in gymnosperms and lower plants like Physcomitrella patens (20). These genes can be distinguished from putative paralogues resembling the bZIP24 gene of Arabidopsis (Fig.…”

Section: Discussionmentioning

confidence: 99%

“…bZIP genes that are closely related to Arabidopsis bZIP19 and bZIP23 are found in several species, including rice, poplar, and soybean (respectively OsbZIP48, PtrbZIP38/PtrbZIP39, and GmbZIP121/GmbZIP122), but also in gymnosperms like Picea glauca and Pinus taeda (PgbZIP4 and PtbZIP12, respectively) and lower plants like the Bryophyte Physcomitrella patens (PpbZIP18 and PpbZIP19) (20) (Fig. S1 B and C).…”

Section: Zdre Is Present In the Promoter Of Arabidopsis Zinc-deficiency-mentioning

confidence: 99%

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Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency

Assunção

Herrero

Lin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

327

381

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Zinc is an essential micronutrient for all living organisms. When facing a shortage in zinc supply, plants adapt by enhancing the zinc uptake capacity. The molecular regulators controlling this adaptation are not known. We present the identification of two closely related members of the Arabidopsis thaliana basic-region leucinezipper (bZIP) transcription factor gene family, bZIP19 and bZIP23, that regulate the adaptation to low zinc supply. They were identified, in a yeast-one-hybrid screening, to associate to promoter regions of the zinc deficiency-induced ZIP4 gene of the Zrt-and Irtrelated protein (ZIP) family of metal transporters. Although mutation of only one of the bZIP genes hardly affects plants, we show that the bzip19 bzip23 double mutant is hypersensitive to zinc deficiency. Unlike the wild type, the bzip19 bzip23 mutant is unable to induce the expression of a small set of genes that constitutes the primary response to zinc deficiency, comprising additional ZIP metal transporter genes. This set of target genes is characterized by the presence of one or more copies of a 10-bp imperfect palindrome in their promoter region, to which both bZIP proteins can bind. The bZIP19 and bZIP23 transcription factors, their target genes, and the characteristic cis zinc deficiency response elements they can bind to are conserved in higher plants. These findings are a significant step forward to unravel the molecular mechanism of zinc homeostasis in plants, allowing the improvement of zinc bio-fortification to alleviate human nutrition problems and phytoremediation strategies to clean contaminated soils.biofortification | zinc homeostasis regulation | plant nutrition | abiotic stress | adaptation Z inc is an essential cofactor for many transcription factors, protein interaction domains, and enzymes in plants (1). Plants are thought to control zinc homeostasis by using a tightly regulated network of zinc status sensors and signal transducers controlling the coordinated expression of proteins involved in zinc acquisition from soil, mobilization between organs and tissues, and sequestration within cellular compartments (2). Although candidate genes for the required proteins such as zinc transporters and chelator biosynthesizing enzymes are found, no regulator of such network was ever identified in plants.Zinc influx facilitators, members of the ZIP family of metal transporters, are thought to play a major role in zinc uptake in plants (3). In Arabidopsis there are 15 ZIP genes (4), with ZIP1, ZIP2, ZIP3, and IRT3 functionally characterized as zinc uptake transporters (3, 5). Gene expression analysis has shown that approximately half of the ZIP genes are induced in response to zinc deficiency (3,(5)(6)(7)(8). The ZIP4 gene in particular is strongly induced upon shortage in zinc supply (3,(6)(7)(8).We focused on the promoter of this zinc-deficiency-responsive gene as the starting point for unraveling the regulation of the zinc homeostasis network in plants. By using DNA fragments of the zincdeficiency-responsive Arabidopsi...

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Section: Discussionmentioning

confidence: 99%

Section: Zdre Is Present In the Promoter Of Arabidopsis Zinc-deficiency-mentioning

confidence: 99%

Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency

Assunção

Herrero

Lin

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

327

381

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“…Applying a dynamic tree cut (Langfelder et al, 2008) to the clustering dendrogram, we identified 85 motif types ( Figure S2A). At the family level, motif clusters from the large and functionally diverse bZIP ( Figure 3A) and NAC families ( Figure S2B) closely reflected TF phylogeny (Corrêa et al, 2008;Olsen et al, 2005), indicating target sequences are conserved for close paralogs. Binding peaks of these TFs showed a range of enrichment in conserved non-coding regions (Haudry et al, 2013) (Figure S2C).…”

Section: The Arabidopsis Cistromementioning

confidence: 96%

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

O’Malley¹,

Huang²,

Song³

et al. 2016

Cell

373

482

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SUMMARYThe cistrome is the complete set of transcription factor (TF) binding sites (cis-elements) in an organism, while an epicistrome incorporates tissue-specific DNA chemical modifications and TFspecific chemical sensitivities into these binding profiles. Robust methods to construct comprehensive cistrome and epicistrome maps are critical for elucidating complex transcriptional networks that underlie growth, behavior, and disease. Here, we describe DNA affinity purification sequencing (DAP-seq), a high-throughput TF binding site discovery method that interrogates genomic DNA with in-vitro-expressed TFs. Using DAP-seq, we defined the Arabidopsis cistrome by resolving motifs and peaks for 529 TFs. Because genomic DNA used in DAP-seq retains 5-methylcytosines, we determined that >75% (248/327) of Arabidopsis TFs surveyed were methylation sensitive, a property that strongly impacts the epicistrome landscape. DAP-seq datasets also yielded insight into the biology and binding site architecture of numerous TFs, demonstrating the value of DAP-seq for cost-effective cistromic and epicistromic annotation in any organism.

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“…They showed a total P value >10% from T000 to T048, perhaps reflecting the requirement for ethylene action in germination. bZIP proteins control seed and leaf development, nitrogen/carbon balance, and photomorphogenesis (33)(34)(35), whereas C3H proteins are implicated in embryogenesis (36) and stress response (37). The NAC gene family maintained high expression (P > 5%) until T030.…”

Section: Expression Dynamics Of Tf Gene Families During Germination Andmentioning

confidence: 99%

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

Chen²,

Chang³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Maize is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, a genomewide regulatory network of leaf development is not yet available. This knowledge is useful for developing C3 crops to perform C4 photosynthesis for enhanced yields. Here, using 22 transcriptomes of developing maize leaves from dry seeds to 192 h post imbibition, we studied gene up-and down-regulation and functional transition during leaf development and inferred sets of strongly coexpressed genes. More significantly, we developed a method to predict transcription factor binding sites (TFBSs) and their cognate transcription factors (TFs) using genomic sequence and transcriptomic data. The method requires not only evolutionary conservation of candidate TFBSs and sets of strongly coexpressed genes but also that the genes in a gene set share the same Gene Ontology term so that they are involved in the same biological function. In addition, we developed another method to predict maize TF-TFBS pairs using known TF-TFBS pairs in Arabidopsis or rice. From these efforts, we predicted 1,340 novel TFBSs and 253 new TF-TFBS pairs in the maize genome, far exceeding the 30 TF-TFBS pairs currently known in maize. In most cases studied by both methods, the two methods gave similar predictions. In vitro tests of 12 predicted TF-TFBS interactions showed that our methods perform well. Our study has significantly expanded our knowledge on the regulatory network involved in maize leaf development. maize transcriptomes | coexpressed genes | cis binding site M aize (Zea mays) is a major crop and a model plant for studying C4 photosynthesis and leaf development. However, the regulatory network that controls maize leaf development is still not well understood. In fact, the number of known maize transcription factor (TF)-binding sites (TFBSs) is far smaller than that for Arabidopsis thaliana (1-3).To understand better the regulation of maize leaf development, several recent studies used next-generation sequencing (NGS) technologies to survey transcriptomic differences among maize leaf cell types and developmental stages. The first large-scale study was by Li et al. (7) investigated the transcriptomes of Kranz (i.e., the foliar leaf blade) and non-Kranz (the husk leaf sheath) maize leaves to identify cohorts of genes associated with procambium initiation and vascular patterning. Recently, Wang et al. (8) conducted comparative transcriptomic and metabolomic analyses of developing leaves in maize and rice and identified putative structural and regulatory components important for C4 and C3 photosynthesis. These studies provided insights into the regulatory mechanisms underlying the development of Kranz leaf anatomy in maize.In the present study, we obtained nine transcriptomes of the second leaf from 84-192 h post imbibition at 12-h (6:00 AM and 6:00 PM) or 24-h (6:00 PM only) intervals. Together with the 13 SignificanceMaize is a major crop and a model plant for studying C4 leaf development. However, its regulatory network of leaf ...

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The Role of bZIP Transcription Factors in Green Plant Evolution: Adaptive Features Emerging from Four Founder Genes

Cited by 275 publications

References 119 publications

Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency

Arabidopsis thaliana transcription factors bZIP19 and bZIP23 regulate the adaptation to zinc deficiency

Cistrome and Epicistrome Features Shape the Regulatory DNA Landscape

Transcriptome dynamics of developing maize leaves and genomewide prediction ofciselements and their cognate transcription factors

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