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Journal ArticleDOI

The control of developmental phase transitions in plants.

01 Oct 2011-Development (Development)-Vol. 138, Iss: 19, pp 4117-4129
TL;DR: Recent advances in the field of plant phase transitions are reviewed, highlighting the role of two microRNAs – miR156 and miR172 – and their respective targets during these transitions and the evolutionary conservation of the functions of these miRNAs in regulating the control of plant developmental phase transitions.
Abstract: Plant development progresses through distinct phases: vegetative growth, followed by a reproductive phase and eventually seed set and senescence. The transitions between these phases are controlled by distinct genetic circuits that integrate endogenous and environmental cues. In recent years, however, it has become evident that the genetic networks that underlie these phase transitions share some common factors. Here, we review recent advances in the field of plant phase transitions, highlighting the role of two microRNAs - miR156 and miR172 - and their respective targets during these transitions. In addition, we discuss the evolutionary conservation of the functions of these miRNAs in regulating the control of plant developmental phase transitions.
Citations
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01 Jan 1989
TL;DR: Control by Day Length, Genetics of Sensitivity to Environmental Factors, and Control by Day length.
Abstract: ENVIRONMENTAL CONTROL . . . . . . . . . . . . . . . . .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Genetics of Sensitivity to Environmental Factors . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Control by Day Length . . . . . . . . . . . . . . . . . . . . . . . ... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

553 citations

Journal ArticleDOI
TL;DR: The authors show that a well-conserved miRNA-transcription factor module implicated previously in developmental control regulates responses to repeated heat stress in Arabidopsis thaliana and provides a conceptual framework for the integration of environmental stress responses with development to optimize growth under natural conditions.
Abstract: Plants are sessile organisms that gauge stressful conditions to ensure survival and reproductive success. While plants in nature often encounter chronic or recurring stressful conditions, the strategies to cope with those are poorly understood. Here, we demonstrate the involvement of ARGONAUTE1 and the microRNA pathway in the adaptation to recurring heat stress (HS memory) at the physiological and molecular level. We show that miR156 isoforms are highly induced after HS and are functionally important for HS memory. miR156 promotes sustained expression of HS-responsive genes and is critical only after HS, demonstrating that the effects of modulating miR156 on HS memory do not reflect preexisting developmental alterations. miR156 targets SPL transcription factor genes that are master regulators of developmental transitions. SPL genes are posttranscriptionally downregulated by miR156 after HS, and this is critical for HS memory. Altogether, the miR156-SPL module mediates the response to recurring HS in Arabidopsis thaliana and thus may serve to integrate stress responses with development.

453 citations


Cites background or result from "The control of developmental phase ..."

  • ...As expected from previous reports on miR156a-f (reviewed in Huijser and Schmid, 2011), manipulating the levels of miR156h correlated with changes in growth and development....

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  • ...It plays important roles in the endogenous timing of leaf initiation and developmental transitions by targeting SQUAMOSA-PROMOTER BINDING-LIKE (SPL) transcription factors (Cardon et al., 1999; Rhoades et al., 2002; Wang et al., 2008, 2009; Wu et al., 2009; Huijser and Schmid, 2011)....

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Journal ArticleDOI
TL;DR: It is shown here that DELLA directly binds to microRNA156 (miR156)-targeted SQUAMOSA PROMOTER BINDING–LIKE (SPL) transcription factors, which promote flowering by activating miR172 and MADS box genes.
Abstract: Gibberellin (GA), a diterpene hormone, plays diverse roles in plant growth and development, including seed germination, stem elongation, and flowering time. Although it is known that GA accelerates flowering through degradation of transcription repressors, DELLAs, the underlying mechanism is poorly understood. We show here that DELLA directly binds to microRNA156 (miR156)-targeted SQUAMOSA PROMOTER BINDING–LIKE (SPL) transcription factors, which promote flowering by activating miR172 and MADS box genes. The interaction between DELLA and SPL interferes with SPL transcriptional activity and consequently delays floral transition through inactivating miR172 in leaves and MADS box genes at shoot apex under long-day conditions or through repressing MADS box genes at the shoot apex under short-day conditions. Our results elucidate the molecular mechanism by which GA controls flowering and provide the missing link between DELLA and MADS box genes.

354 citations


Cites background from "The control of developmental phase ..."

  • ...The miR156–SPL interaction constitutes an evolutionarily conserved, endogenous cue for both vegetative phase transition and flowering (Huijser and Schmid, 2011)....

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Journal ArticleDOI
TL;DR: It is found that miR156 integrates environmental signals to ensure timely flowering, thus enabling the completion of breeding and uncovering a molecular mechanism for plant adaptation to the environment through the miR 156-SPLs-DFR pathway, which coordinates development and abiotic stress tolerance.
Abstract: Young organisms have relatively strong resistance to diseases and adverse conditions. When confronted with adversity, the process of development is delayed in plants. This phenomenon is thought to result from the rebalancing of energy, which helps plants to coordinate the relationship between development and stress tolerance; however, the molecular mechanism underlying this phenomenon remains mysterious. In this study, we found that miR156 integrates environmental signals to ensure timely flowering, thus enabling the completion of breeding. Under stress conditions, miR156 is induced to maintain the plant in the juvenile state for a relatively long period of time, whereas under favorable conditions, miR156 is suppressed to accelerate the developmental transition. Blocking the miR156 signaling pathway in Arabidopsis thaliana with 35S::MIM156 (via target mimicry) increased the sensitivity of the plant to stress treatment, whereas overexpression of miR156 increased stress tolerance. In fact, this mechanism is also conserved in Oryza sativa (rice). We also identified downstream genes of miR156, i.e. SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9 (SPL9) and DIHYDROFLAVONOL-4-REDUCTASE (DFR), which take part in this process by influencing the metabolism of anthocyanin. Our results uncover a molecular mechanism for plant adaptation to the environment through the miR156-SPLs-DFR pathway, which coordinates development and abiotic stress tolerance.

337 citations

Journal ArticleDOI
TL;DR: The plethora of roles that FT-like genes have acquired during evolution are assessed and their implications in plant diversity, adaptation and domestication are assessed.
Abstract: One of the key developmental processes in flowering plants is the differentiation of the shoot apical meristem into a floral meristem. This transition is regulated through the integration of environmental and endogenous stimuli, involving a complex, hierarchical signalling network. In arabidopsis, the FLOWERING LOCUS T (FT) protein, a mobile signal recognized as a major component of florigen, has a central position in mediating the onset of flowering. FT-like genes seem to be involved in regulating the floral transition in all angiosperms examined to date. Evidence from molecular evolution studies suggests that the emergence of FT-like genes coincided with the evolution of the flowering plants. Hence, the role of FT in floral promotion is conserved, but appears to be restricted to the angiosperms. Besides flowering, FT-like proteins have also been identified as major regulatory factors in a wide range of developmental processes including fruit set, vegetative growth, stomatal control and tuberization. These multifaceted roles of FT-like proteins have resulted from extensive gene duplication events, which occurred independently in nearly all modern angiosperm lineages, followed by sub- or neo-functionalization. This review assesses the plethora of roles that FT-like genes have acquired during evolution and their implications in plant diversity, adaptation and domestication.

286 citations


Cites background from "The control of developmental phase ..."

  • ...…TOE2, SCHLAFMÜTZE (SMZ) and SCHNARCHZAPFEN (SNZ), which are subject to aging-dependent regulation through concomitant reductions in miR156 and increases in miR172 levels (Wu et al. 2009; Huijser & Schmid 2011), repress FT transcription in a concerted manner (Jung et al. 2007; Mathieu et al. 2009)....

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References
More filters
Journal ArticleDOI
TL;DR: This work has mapped reads from short RNA deep-sequencing experiments to microRNAs in miRBase and developed web interfaces to view these mappings, which can be used as a proxy for relative expression levels of microRNA sequences, provide detailed evidence for microRNA annotations and alternative isoforms of mature micro RNAs, and allow us to revisit previous annotations.
Abstract: miRBase is the primary online repository for all microRNA sequences and annotation. The current release (miRBase 16) contains over 15,000 microRNA gene loci in over 140 species, and over 17,000 distinct mature microRNA sequences. Deep-sequencing technologies have delivered a sharp rise in the rate of novel microRNA discovery. We have mapped reads from short RNA deep-sequencing experiments to microRNAs in miRBase and developed web interfaces to view these mappings. The user can view all read data associated with a given microRNA annotation, filter reads by experiment and count, and search for microRNAs by tissue- and stage-specific expression. These data can be used as a proxy for relative expression levels of microRNA sequences, provide detailed evidence for microRNA annotations and alternative isoforms of mature microRNAs, and allow us to revisit previous annotations. miRBase is available online at: http://www.mirbase.org/.

3,618 citations


"The control of developmental phase ..." refers background in this paper

  • ...In Arabidopsis, miR156 and some miR156 isoforms can potentially be encoded by many loci, e.g. MIR156a-f, MIR156g-h and MIR157a-d (Kozomara and Griffiths-Jones, 2011; Xie et al., 2005)....

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  • ...MIR156a-f, MIR156g-h and MIR157a-d (Kozomara and Griffiths-Jones, 2011; Xie et al., 2005)....

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Journal ArticleDOI
TL;DR: Examining the expression patterns of large gene families, it is found that they are often more similar than would be expected by chance, indicating that many gene families have been co-opted for specific developmental processes.
Abstract: Regulatory regions of plant genes tend to be more compact than those of animal genes, but the complement of transcription factors encoded in plant genomes is as large or larger than that found in those of animals. Plants therefore provide an opportunity to study how transcriptional programs control multicellular development. We analyzed global gene expression during development of the reference plant Arabidopsis thaliana in samples covering many stages, from embryogenesis to senescence, and diverse organs. Here, we provide a first analysis of this data set, which is part of the AtGenExpress expression atlas. We observed that the expression levels of transcription factor genes and signal transduction components are similar to those of metabolic genes. Examining the expression patterns of large gene families, we found that they are often more similar than would be expected by chance, indicating that many gene families have been co-opted for specific developmental processes.

2,510 citations


"The control of developmental phase ..." refers background in this paper

  • ...Accordingly, and concomitantly with decreasing miR156 activity, their transcript levels gradually increase during aging (Cardon et al., 1999; Schmid et al., 2005; Wu and Poethig, 2006)....

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Journal ArticleDOI
23 Aug 2002-Cell
TL;DR: This work predicts regulatory targets for 14 Arabidopsis microRNAs (miRNAs) by identifying mRNAs with near complementarity and identifies members of transcription factor gene families involved in developmental patterning or cell differentiation.

2,221 citations


"The control of developmental phase ..." refers background in this paper

  • ...However, when the first miRNAs were identified in plants, it was soon recognized that many of the predicted targets encode transcription factors, some of which were known to affect flowering (Rhoades et al., 2002)....

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Journal ArticleDOI
Milo Aukerman1, Hajime Sakai1
TL;DR: It is demonstrated that miRNA 172 (miR172) causes early flowering and disrupts the specification of floral organ identity when overexpressed in Arabidopsis through an activation-tagging approach, supporting the notion that miR172 regulates flowering time by downregulating AP2-like target genes.
Abstract: MicroRNAs (miRNAs) are ∼21-nucleotide noncoding RNAs that have been identified in both animals and plants. Although in animals there is direct evidence implicating particular miRNAs in the control of developmental timing, to date it is not known whether plant miRNAs also play a role in regulating temporal transitions. Through an activation-tagging approach, we demonstrate that miRNA 172 (miR172) causes early flowering and disrupts the specification of floral organ identity when overexpressed in Arabidopsis. miR172 normally is expressed in a temporal manner, consistent with its proposed role in flowering time control. The regulatory target of miR172 is a subfamily of APETALA2 (AP2) transcription factor genes. We present evidence that miR172 downregulates these target genes by a translational mechanism rather than by RNA cleavage. Gain-of-function and loss-of-function analyses indicate that two of the AP2-like target genes normally act as floral repressors, supporting the notion that miR172 regulates flowering time by downregulating AP2-like target genes.

1,848 citations


"The control of developmental phase ..." refers background in this paper

  • ...Aukerman, M. J. and Sakai, H. (2003)....

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  • ...Abbreviations: AP2, APETALA2; Gl 15, Glossy15; Ids1, Indeterminate spikelet1; RAP, RELATED TO APETALA2; SMZ, SCHLAFMÜTZE; SNZ, SCHNARCHZAPFEN; TOE, TARGET OF EAT; Ts, Tasselseed....

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  • ...…of flowering Jung et al., 2007 Mathieu et al., 2009 Schmid et al., 2003 Yant et al., 2010 TOE1 A. thaliana At2g28550 Repressor of flowering Aukerman and Sakai, 2003 Jung et al., 2007 Mathieu et al., 2009 Wu et al., 2009 Yant et al., 2010 TOE2 A. thaliana At5g60120 Repressor of flowering…...

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  • ...Chuck, G., Meeley, R., Irish, E., Sakai, H. and Hake, S. (2007b)....

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  • ...This raises the issue of whether the roles of miR156 and miR172 in regulating Gene Species Locus identifier* Function/comments References MIR172 A. thaliana a) At2g28056 b) At5g04275 c) At3g11435 d) At3g55512 e) At5g59505 Promotes adult vegetative phase and flowering; involved in floral patterning; targets six AP2like transcripts in A. thaliana; MIR172b=EARLY ACTIVATION TAGGED (EAT) Aukerman and Sakai, 2003 Axtell and Bowman, 2008 Cuperus et al., 2011 Jung et al., 2007 Park et al., 2002 Schwab et al., 2005 Wu et al., 2009 AP2 A. thaliana At4g36920 Repressor of flowering and floral homeotic gene; a founding member of the AP2-domain transcription factor family Chen, 2004 Jofuku et al., 1994 Wollmann et al., 2010 Yant et al., 2010 AP2a S. lycopersicum SGN-U579591 Regulates fruit ripening as part of a negative feedback loop with CNR; a likely AP2 orthologue Karlova et al., 2011 Gl15 Z. mays Promotes adult phase; AP2-like gene Lauter et al., 2005 Moose and Sisco, 1996 Ids1/Ts6 Z. mays Specifies determinate spikelet meristem fate; AP2-like gene Chuck et al., 2007b Q locus T. aestivum AP2-like gene; dominant mutations in Q contributed to the domestication of wheat Simons et al., 2006 RAP1 S. tuberosum FM246879 Possible repressor of tuberization and/or flowering; AP2 homolog Martin et al., 2009 SMZ A. thaliana At3g54990 Repressor of flowering Jung et al., 2007 Mathieu et al., 2009 Schmid et al., 2003 Yant et al., 2010 SNZ A. thaliana At2g39250 Repressor of flowering Jung et al., 2007 Mathieu et al., 2009 Schmid et al., 2003 Yant et al., 2010 TOE1 A. thaliana At2g28550 Repressor of flowering Aukerman and Sakai, 2003 Jung et al., 2007 Mathieu et al., 2009 Wu et al., 2009 Yant et al., 2010 TOE2 A. thaliana At5g60120 Repressor of flowering Aukerman and Sakai, 2003 Jung et al., 2007 Mathieu et al., 2009 Wu et al., 2009 Yant et al., 2010 TOE3 A. thaliana At5g67180 Repressor of flowering Yant et al., 2010 Ts4 Z. mays MIR172e gene; controls sex determination and meristem cell fate Chuck et al., 2007b *Gene identifier under which it can be found in public databases....

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Journal ArticleDOI
TL;DR: Target mimicry can be generalized beyond the control of Pi homeostasis, as demonstrated using artificial target mimics and coined to define this mechanism of inhibition of miRNA activity.
Abstract: MicroRNAs (miRNA) regulate key aspects of development and physiology in animals and plants. These regulatory RNAs act as guides of effector complexes to recognize specific mRNA sequences based on sequence complementarity, resulting in translational repression or site-specific cleavage. In plants, most miRNA targets are cleaved and show almost perfect complementarity with the miRNAs around the cleavage site. Here, we examined the non-protein coding gene IPS1 (INDUCED BY PHOSPHATE STARVATION 1) from Arabidopsis thaliana. IPS1 contains a motif with sequence complementarity to the phosphate (Pi) starvation-induced miRNA miR-399, but the pairing is interrupted by a mismatched loop at the expected miRNA cleavage site. We show that IPS1 RNA is not cleaved but instead sequesters miR-399. Thus, IPS1 overexpression results in increased accumulation of the miR-399 target PHO2 mRNA and, concomitantly, in reduced shoot Pi content. Engineering of IPS1 to be cleavable abolishes its inhibitory activity on miR-399. We coin the term 'target mimicry' to define this mechanism of inhibition of miRNA activity. Target mimicry can be generalized beyond the control of Pi homeostasis, as demonstrated using artificial target mimics.

1,767 citations


"The control of developmental phase ..." refers background in this paper

  • ...Transgenics that constitutively overexpress SPL3 flower only slightly earlier than do wild-type plants, reflecting the repressing strength of endogenous miR156 (Gandikota et al., 2007; Wu and Poethig, 2006)....

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  • ...…a rSPL3 transgene may result in a complete consumption of the IM in creating floral organs and thereby in determinate growth of the inflorescence (Gandikota et al., 2007). miR156-targeted SPL genes promote fertility The first few flowers formed in Arabidopsis often produce significantly fewer…...

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  • ...The closely related genes SPL3, SPL4 and SPL5 The three smallest of all SPL genes in Arabidopsis, SPL3, SPL4 and SPL5 are exceptional in that they carry a miR156 MRE in their 3 UTRs (Gandikota et al., 2007)....

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  • ...Moreover, such transgenics show a precocious appearance of adult leaf traits, providing clear support that these SPL genes promote the expression of the adult phase (Gandikota et al., 2007; Wang et al., 2009; Wu et al., 2009; Wu and Poethig, 2006)....

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