The<i>NGATHA</i>Genes Direct Style Development in the<i>Arabidopsis</i>Gynoecium

Trigueros, Marina; Navarrete-Gómez, Marisa; Sato, Shusei; Christensen, S.; Pelaz, Soraya; Weigel, Detlef; Yanofsky, Martin F.; Ferrándiz, Cristina

doi:10.1105/tpc.109.065508

Cited by 129 publications

(229 citation statements)

References 45 publications

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“…This is consistent with additional, tissue-specific factors being required for RVE1 promotion of YUC8 expression. Similarly, precise expression of YUC4 in inflorescences is likely achieved via the combined action of the widely expressed NGATHA genes and unidentified tissue-specific factors (36).…”

Section: Rve1 Increases Auxin Levelsmentioning

confidence: 99%

REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways

Rawat

Schwartz

Jones

et al. 2009

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

233

203

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The circadian clock modulates expression of a large fraction of the Arabidopsis genome and affects many aspects of plant growth and development. We have discovered one way in which the circadian system regulates hormone signaling, identifying a node that links the clock and auxin networks. Auxin plays key roles in development and responses to environmental cues, in part through regulation of plant growth. We have characterized REVEILLE1 (RVE1), a Myb-like, clockregulated transcription factor that is homologous to the central clock genes CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) and LATE ELON-GATED HYPOCOTYL (LHY). Despite this homology, inactivation of RVE1 does not affect circadian rhythmicity but instead causes a growth phenotype, indicating this factor is a clock output affecting plant development. CCA1 regulates growth via the bHLH transcription factors PHYTOCHROME INTERACTING FACTOR4 (PIF4) and PIF5, but RVE1 acts independently of these genes. RVE1 instead controls auxin levels, promoting free auxin production during the day but having no effect during the night. RVE1 positively regulates the expression of the auxin biosynthetic gene YUCCA8 (YUC8), providing a mechanism for its growth-promoting effects. RVE1 is therefore a node that connects two important signaling networks that coordinate plant growth with rhythmic changes in the environment.growth control ͉ hypocotyl ͉ yucca C ircadian rhythms are approximately 24-h rhythms in physiology or behavior that are generated by an endogenous clock. Circadian rhythms persist in constant environmental conditions; however they can be entrained or set by environmental cues like light/dark or temperature cycles (1). In plants, these rhythms regulate myriad processes including leaf and cotyledon movement, growth, photosynthesis, and timing of the transition to flowering (2). A functional circadian clock provides an adaptive advantage, perhaps by predicting fluctuations in the external environment (3, 4). In all model systems studied, these self-sustained rhythms are generated by a cell-autonomous central oscillator which regulates the expression of many genes involved in metabolic and physiological functions (1). Microarray studies show that nearly one third of Arabidopsis genes are circadian regulated, with peak expression at different times of day (5, 6).In plants, the central oscillator is composed of interlocking feedback loops with both positive and negative transcriptional regulators (1). The central loop is thought to consist of three genes, CIRCADIAN CLOCK ASSOCIATED 1 (CCA1), LATE ELON-GATED HYPOCOTYL (LHY), and TIMING OF CAB EXPRES-SION (TOC1). CCA1 and LHY are morning-phased transcription factors with a single Myb-like domain containing a distinctive SHAQKYF motif (7,8). They bind a motif, termed the evening element (EE; AAAATATCT), in the TOC1 promoter to negatively regulate TOC1 expression. TOC1, an evening-phased gene, in turn positively regulates the expression of CCA1 and LHY through an unknown mechanism, thus forming the core clock negative feedback loop (7...

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Section: Rve1 Increases Auxin Levelsmentioning

confidence: 99%

REVEILLE1, a Myb-like transcription factor, integrates the circadian clock and auxin pathways

Rawat

Schwartz

Jones

et al. 2009

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

233

203

View full text Add to dashboard Cite

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“…This discovery originated from a yeast two hybrid screen, in which the BRX family protein, BRX-LIKE 4, was recovered as an interactor of NGATHA1 (NGA1) (Alvarez et al, 2006;Trigueros et al, 2009). Given the high level of conservation among BRX family genes (Briggs et al, 2006), it was not surprising that NGA1 could also interact with BRX (Fig.…”

Section: Brx Activity Is Required In the Nucleusmentioning

confidence: 99%

“…4F). Moreover, similar to BRX, NGA1 is expressed in the root vasculature (Birnbaum et al, 2003;Trigueros et al, 2009). Thus, BRX might regulate transcription in conjunction with NGA1.…”

Section: Brx Activity Is Required In the Nucleusmentioning

confidence: 99%

Dynamic, auxin-responsive plasma membrane-to-nucleus movement ofArabidopsisBRX

et al. 2009

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In Arabidopsis, interplay between nuclear auxin perception and trans-cellular polar auxin transport determines the transcriptional auxin response. In brevis radix (brx) mutants, this response is impaired, probably indirectly because of disturbed crosstalk between the auxin and brassinosteroid pathways. Here we provide evidence that BRX protein is plasma membrane-associated, but translocates to the nucleus upon auxin treatment to modulate cellular growth, possibly in conjunction with NGATHA class B3 domain-type transcription factors. Application of the polar auxin transport inhibitor naphthalene phthalamic acid (NPA) resulted in increased BRX abundance at the plasma membrane. Thus, nuclear translocation of BRX could depend on cellular auxin concentration or on auxin flux. Supporting this idea, NPA treatment of wild-type roots phenocopied the brx root meristem phenotype. Moreover, BRX is constitutively turned over by the proteasome pathway in the nucleus. However, a stabilized C-terminal BRX fragment significantly rescued the brx root growth phenotype and triggered a hypocotyl gain-of-function phenotype, similar to strong overexpressors of full length BRX. Therefore, although BRX activity is required in the nucleus, excess activity interferes with normal development. Finally, similar to the PIN-FORMED 1 (PIN1) auxin efflux carrier, BRX is polarly localized in vascular cells and subject to endocytic recycling. Expression of BRX under control of the PIN1 promoter fully rescued the brx short root phenotype, suggesting that the two genes act in the same tissues. Collectively, our results suggest that BRX might provide a contextual readout to synchronize cellular growth with the auxin concentration gradient across the root tip.

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“…1). Current models propose that auxin levels are manipulated through coordinated regulation of SHORT INTERNODE (SHI)/STYLISH (STY) transcription factor family-induced local auxin biosynthesis and the relative efficiency of auxin transport away from sites of synthesis (Sohlberg et al 2006;Alvarez et al 2009;Trigueros et al 2009). The balance of production and transport determines the timing and location of style and stigmatic tissue development.…”

Section: The Developmental Programmentioning

confidence: 99%

“…An inducible STY1 causes rapid induction of the gene encoding the auxin biosynthetic enzyme YUCCA4 and a concomitant increase in free auxin levels (Sohlberg et al 2006). This auxin maximum in the ring of cells near the apex of gynoecium primordia triggers activation of the NGATHA (NGA) genes (Alvarez et al 2009;Trigueros et al 2009). These in turn alter the suite of transcription factors expressed in these cells, promoting apical cell identity.…”

Section: The Developmental Programmentioning

confidence: 99%