Arabidopsis NIN-like transcription factors have a central role in nitrate signalling

Konishi, Mineko; Yanagisawa, Shuichi

doi:10.1038/ncomms2621

Cited by 342 publications

(378 citation statements)

References 51 publications

(75 reference statements)

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“…Consistent with the characteristics of NLP6, repression of NLP function using a chimeric repressor form of NLP6, which was produced by fusing the transcriptional repression domain of SUPERMAN to NLP6, was found to result in the inhibition of growth in A. thaliana (Konishi and Yanagisawa 2013). We have also observed decreases in nitrate-inducible expression of many genes related to N assimilation, and several genes that are possibly associated with cellular regulatory processes.…”

Section: Introductionsupporting

confidence: 58%

“…The results of detailed analyses using NLP6, which probably plays a dominant role among the NLP family, indicated that the DNA-binding domain in the C-terminal region of this protein can interact with an NRE independently of nitrate, but that it is post-translationally activated through its amino-terminal region in a nitrate-dependent manner and then promotes NRE-dependent transcription (Konishi and Yanagisawa 2013). Consistent with the characteristics of NLP6, repression of NLP function using a chimeric repressor form of NLP6, which was produced by fusing the transcriptional repression domain of SUPERMAN to NLP6, was found to result in the inhibition of growth in A. thaliana (Konishi and Yanagisawa 2013).…”

Section: Introductionmentioning

confidence: 99%

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An NLP-binding site in the 3' flanking region of the nitrate reductase gene confers nitrate-inducible expression inArabidopsis thaliana(L.) Heynh.

Konishi

Yanagisawa

2013

Soil Science and Plant Nutrition

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As a signaling molecule, nitrate induces the expression of multiple genes involved in nitrate assimilation in plants. We previously showed that the expression of the Arabidopsis thaliana (L.) Heynh. nitrite reductase gene (NIR1) was activated by nitrate signaling through an interaction between NODULE INCEPETIONlike protein (NLP) transcription factors (NLP1-9) and a nitrate-responsive cis-element (NRE) in the NIR1 promoter. By in vitro binding assays, we have also demonstrated the binding of NLP6 to an NRE-like sequence, designated NIA1-NRE1, in the 3' flanking region of an A. thaliana nitrate reductase gene, NIA1.In our current study, we characterize the role of NIA1-NRE1 in NIA1 expression. Deletion analysis of the 3' flanking region of NIA1 revealed that a 345-bp sequence containing NIA1-NRE1 has a dominant role in nitrate-inducible NIA1 expression. We also found that the 35S minimal promoter fused to the 345-bp sequence, or to NIA1-NRE1, can confer nitrate-inducible expression. Furthermore, the NIA1-NRE1-fused 35S minimal promoter is transactivated by NLP6 in vivo. These results suggest that NIA1-NRE1 alone is sufficient to direct nitrate-responsive gene expression and that nitrate-inducible NIA1 expression is regulated through the interaction between NLPs and NIA1-NRE1. Additionally, we show that the distance between the NRE and the gene under the control of the NRE is not critical for this process.

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Section: Introductionsupporting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

An NLP-binding site in the 3' flanking region of the nitrate reductase gene confers nitrate-inducible expression inArabidopsis thaliana(L.) Heynh.

Konishi

Yanagisawa

2013

Soil Science and Plant Nutrition

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“…Thus, factors regulated by cytokinin signaling may be targeted by CLE peptide-mediated AON. NIN is evolved from a member of NIN-like proteins (NLPs), which regulate the expression of primary nitrate-responsive genes (35,36), suggesting integration of a part of nitrateresponsive pathway in the nodule symbiosis. Indeed, CLE-RS2 and GmNIC1 are activated by nitrate, which also has an inhibitory effect on nodulation (11,37,38).…”

Section: Discussionmentioning

confidence: 99%

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Soyano

Hirakawa

Sato

et al. 2014

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

174

200

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Autoregulatory negative-feedback loops play important roles in finebalancing tissue and organ development. Such loops are composed of short-range intercellular signaling pathways via cell-cell communications. On the other hand, leguminous plants use a long-distance negative-feedback system involving root-shoot communication to control the number of root nodules, root lateral organs that harbor symbiotic nitrogen-fixing bacteria known as rhizobia. This feedback system, known as autoregulation of nodulation (AON), consists of two long-distance mobile signals: root-derived and shoot-derived signals. Two Lotus japonicus CLAVATA3/ENDOSPERM SURROUNDING REGION (CLE)-related small peptides, CLE ROOT SIGNAL1 (CLE-RS1) and CLE-RS2, function as root-derived signals and are perceived by a shoot-acting AON factor, the HYPERNODULATION ABERRANT ROOT FORMATION1 (HAR1) receptor protein, an ortholog of Arabidopsis CLAVATA1, which is responsible for shoot apical meristem homeostasis. This peptide-receptor interaction is necessary for systemic suppression of nodulation. How the onset of nodulation activates AON and how optimal nodule numbers are maintained remain unknown, however. Here we show that an RWP-RK-containing transcription factor, NODULE INCEPTION (NIN), which induces nodule-like structures without rhizobial infection when expressed ectopically, directly targets CLE-RS1 and CLE-RS2. Roots constitutively expressing NIN systemically repress activation of endogenous NIN expression in untransformed roots of the same plant in a HAR1-dependent manner, leading to systemic suppression of nodulation and down-regulation of CLE expression. Our findings provide, to our knowledge, the first molecular evidence of a long-distance autoregulatory negative-feedback loop that homeostatically regulates nodule organ formation.L ong-distance organ-to-organ communications are generally critical for coordinating development and environmental adaptation in multicellular organisms, particularly plants that continuously produce postembryonic organs in various environmental conditions (1, 2). Autoregulatory negative-feedback loops play important roles in fine-balancing tissue and organ development. Such feedback loops include short-range intercellular signaling via cell-cell communication. In Arabidopsis, shoot apical meristem (SAM) regulation involves a well-characterized short-range negative-feedback loop that maintains the homeostasis of plant organ development (3-6). The molecular substance of long-distance negative-feedback loops that homeostatically regulate organ production and development remains largely unknown, however.Leguminous plants use long-distance autoregulatory negativefeedback systems involving root-shoot communications to control the number of root nodules, symbiotic root lateral organs formed as consequence of successful interaction with nitrogenfixing bacteria, collectively known as rhizobia. This nodule symbiosis is beneficial to host plants, because rhizobia accommodated in nodules convert atmospheric nitrogen to ammonium, a ...

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“…Within minutes, primary nitrate response genes, including members of the nitrate transporter families NRT1 and NRT2 and the nitrate and nitrite reductase genes NIA1, NIA2, and NiR, are induced. These responses are mediated by signaling pathways that include the nitrate transceptor NRT1.1 (13,14), two kinases (CIPK8 and CIPK23) (13,15), and the transcription factors NLP6/7 (16)(17)(18), LBD37/38/39 (19), and SPL9 (12).…”

mentioning

confidence: 99%

“…Another key nitrate regulator is NLP7, a member of the RWP-PK TF family (14,(16)(17)(18). NLP7, like TCP20, is not nitrateresponsive at the mRNA level, but NLP7 accumulates inside the nucleus to mediate early nitrate responses (18).…”

mentioning

confidence: 99%

Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway

Guan

Wang

Nacry

et al. 2014

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

190

188

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To compete for nutrients in diverse soil microenvironments, plants proliferate lateral roots preferentially in nutrient-rich zones. For nitrate, root foraging involves local and systemic signaling; however, little is known about the genes that function in the systemic signaling pathway. By using nitrate enhancer DNA to screen a library of Arabidopsis transcription factors in the yeast one-hybrid system, the transcription factor gene TEOSINTE BRANCHED1/CYCLO-IDEA/PROLIFERATING CELL FACTOR1-20 (TCP20) was identified. TCP20, which belongs to an ancient, plant-specific gene family that regulates shoot, flower, and embryo development, was implicated in nitrate signaling by its ability to bind DNA in more than 100 nitrate-regulated genes. Analysis of insertion mutants of TCP20 showed that they had normal primary and lateral root growth on homogenous nitrate media but were impaired in preferential lateral root growth (root foraging) on heterogeneous media in split-root plates. Inhibition of preferential lateral root growth was still evident in the mutants even when ammonium was uniformly present in the media, indicating that the TCP20 response was to nitrate. Comparison of tcp20 mutants with those of nlp7 mutants, which are defective in local control of root growth but not in the root-foraging response, indicated that TCP20 function is independent of and distinct from NLP7 function. Further analysis showed that tcp20 mutants lack systemic control of root growth regardless of the local nitrate concentrations. These results indicate that TCP20 plays a key role in the systemic signaling pathway that directs nitrate foraging by Arabidopsis roots. TCP20 | nitrate | root foraging | systemic signaling | Arabidopsis

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Arabidopsis NIN-like transcription factors have a central role in nitrate signalling

Cited by 342 publications

References 51 publications

An NLP-binding site in the 3' flanking region of the nitrate reductase gene confers nitrate-inducible expression inArabidopsis thaliana(L.) Heynh.

An NLP-binding site in the 3' flanking region of the nitrate reductase gene confers nitrate-inducible expression inArabidopsis thaliana(L.) Heynh.

NODULE INCEPTION creates a long-distance negative feedback loop involved in homeostatic regulation of nodule organ production

Nitrate foraging by Arabidopsis roots is mediated by the transcription factor TCP20 through the systemic signaling pathway

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