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MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis (miRNA-Seq)

ABSTRACT: MicroRNAs (miRNAs) play diverse roles in plant development, but whether and how miRNAs participate in thermomorphogenesis remains ambiguous. Here we show that HYPONASTIC LEAVES1 (HYL1) – a key component of microRNA biogenesis – acts downstream of the thermal regulator PHYTOCHROME INTERACTING FACTOR 4 in temperature-dependent plasticity of hypocotyl growth in Arabidopsis. A hyl1-2 suppressor screen identified a dominant dicer-like1 (dcl1) allele, dcl1-24, which rescues hyl1-2’s defects in miRNA biosynthesis and warm temperature-induced hypocotyl elongation. Genome-wide miRNA and transcriptome analysis reveal microRNA156 (miR156) and its target SQUAMOSA PROMOTER-BINDING-LIKE 9 (SPL9) as critical regulators of thermomorphogenesis. Surprisingly, perturbation of the miR156/SPL9 module disengages seedling responsiveness to warm temperatures by impeding auxin sensitivity. Moreover, the miR156-dependent auxin sensitivity also operates in the shade avoidance response at lower temperatures. Thus, these results unveil the miRNA156/SPL9 module as a previously-uncharacterized genetic circuitry that enables plant growth plasticity in response to environmental temperature and light changes.

ORGANISM(S): Arabidopsis thaliana

PROVIDER: GSE216361 | GEO | 2023/02/11

REPOSITORIES: GEO

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MicroRNA156 conditions auxin sensitivity to enable growth plasticity in response to environmental changes in Arabidopsis (RNA-Seq)

Project description:MicroRNAs (miRNAs) play diverse roles in plant development, but whether and how miRNAs participate in thermomorphogenesis remains ambiguous. Here we show that HYPONASTIC LEAVES1 (HYL1) – a key component of microRNA biogenesis – acts downstream of the thermal regulator PHYTOCHROME INTERACTING FACTOR 4 in temperature-dependent plasticity of hypocotyl growth in Arabidopsis. A hyl1-2 suppressor screen identified a dominant dicer-like1 (dcl1) allele, dcl1-24, that rescues hyl1-2’s defects in miRNA biosynthesis and warm temperature-induced hypocotyl elongation. Genome-wide miRNA and transcriptome analysis reveal microRNA156 (miR156) and its target SQUAMOSA PROMOTER-BINDING-LIKE 9 (SPL9) as critical regulators of thermomorphogenesis. Surprisingly, perturbation of the miR156/SPL9 module disengages seedling responsiveness to warm temperatures by impeding auxin sensitivity. Moreover, the miR156-dependent auxin sensitivity also operates in the shade avoidance response at lower temperatures. Thus, these results unveil the miRNA156/SPL9 module as a previously-uncharacterized genetic circuitry that enables plant growth plasticity in response to environmental temperature and light changes.

2023-02-11 | GSE216360 | GEO

PIF7 is the master regulator of thermomorphogenesis in shade [ChIP-seq]

Project description:The size and shape of plant organs are highly responsive to environmental conditions. The plant's embryonic stem, or hypocotyl, displays phenotypic plasticity, in response to light and temperature. The, hypocotyl of shade avoiding species elongate to outcompete neighbouring plants and secure access to sunlight. Similar elongation occurs in high temperature. PHYTOCHROME-INTERACTING FACTORS (PIFs) family transcription are known to be importenet players in these responses. However, it is poorly understood how environmental light and temperature interact to affect plants development. We found that low R/FR combined with warm temperature produces a synergistic hypocotyl growth response that dependent on PIF7 and the hormone auxin. We demonstrate that additional, unknown factor/s must be working downstream of the phyB-PIF-auxin module. As shade responses are known to affect yield, susceptibility to pathogens, and fruit quality in many species, our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density, a condition in which mutual shading occurs.

2022-07-26 | GSE205208 | GEO

B-box family proteins BBX18 and BBX23 control thermoresponsive hypocotyl growth in Arabidopsis

Project description:Plants coordinate their growth and developmental programs with various endogenous signals and environmental challenges such as seasonal and diurnal temperature fluctuations. The bHLH transcription factor PIF4 plays critical roles in thermoresponsive hypocotyl growth in Arabidopsis, and the evening complex component ELF3 negatively regulates PIF4's activity for downstream gene expression and hypocotyl elongation at elevated temperature. However, how warm temperature signal is transmitted to ELF3 is not known. Here, we report the identification of two B-Box protein BBX18/BBX23 as new regulators of thermomorphogenesis in Arabidopsis. Mutations of BBX18/BBX23 confer reduced thermoresponsive hypocotyl elongation. Overexpression of BBX18 enhances the sensitivity of hypocotyl growth to elevated temperature, which is dependent on the function of PIF4 and RING E3 ligase COP1, respectively. Both BBX18 and BBX23 interact with ELF3 or COP1, relegating the protein abundance of ELF3 at warm temperature. Further, the expression of multiple thermoresponsive genes is impaired in both the PIF4 single mutant and BBX18/BBX23 double mutant. In addition, both the transcription and protein levels of BBX18/BBX23 are up-regulated by elevated ambient temperature. Thus, our findings reveal the important roles of B-Box proteins in plant thermomorphogenesis, and build a new connection from warm temperature information to ELF3 and its downstream signaling components.

2018-12-21 | GSE108162 | GEO

The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis[ChIP-seq]

Project description:Global warming imposes a major threat to plant growth and crop production. In some plants including Arabidopsis thaliana, elevated temperatures induce a series of morphological and developmental adjustments, termed thermomorphogenesis to facilitate plant cooling under high-temperature conditions. Plant thermal response is suppressed by histone variant H2A.Z. At warm temperatures, H2A.Z is evicted from nucleosomes at thermo-responsive genes, resulting in their activation. However, the mechanisms that regulate H2A.Z eviction and subsequent transcription activation are largely unknown. Here, we show that the ino80 chromatin-remodeling complex (ino80-C) promotes thermomorphogenesis and activates the expression of thermo-responsive and auxin-related genes. ino80-C associates with PHYTOCHROME-INTERACTING FACTOR 4 (PIF4), a potent regulator in thermomorphogenesis, and mediates temperature-induced H2A.Z eviction at PIF4 targets. Moreover, ino80-C directly interacts with COMPASS-like and transcription elongation factors to promote active histone modification Histone H3 lysine 4 trimethylation (H3K4me3) and RNA Polymerase II (RNA Pol II) elongation, leading to the thermal induction of transcription. Notably, transcription elongation factors are required for the eviction of H2A.Z at PIF4 targets, suggesting the cooperation of ino80-C and transcription elongation in H2A.Z removal. Our results demonstrate that the (PIF4)-(ino80-C)-(COMPASS-like)-(transcription elongator) module controls plant thermal response, and establish a link between H2A.Z eviction and active transcription.

2021-11-27 | GSE168119 | GEO

The INO80 chromatin remodeling complex promotes thermomorphogenesis by connecting H2A.Z eviction and active transcription in Arabidopsis[RNA-seq]

2021-11-27 | GSE168118 | GEO

The epidermis coordinates thermoresponsive growth through the phyB-PIF4-auxin pathway

Project description:In plants, an elevation in ambient temperature induces morphological changes including elongation hypocotyls, considered to be adaptive responses to alleviate the heat-induced damages. The high temperature-induced morphological changes are called thermomorphogenesis, which is predominantly regulated by a bHLH transcription factor PIF4. Although PIF4 is expressed in all aerial tissues including the epidermis, mesophyll, and vascular bundle, its tissue-specific functions in thermomorphogenesis are not known. Here, we found that epidermis-specific expression of PIF4 induced constitutive long hypocotyls, while vasculature-specific expression of PIF4 had no effect on hypocotyl growth. Consistently, RNA-Seq and qRT-PCR analyses revealed that auxin responsive genes and growth-related genes were highly activated by epidermal, but not by vascular, PIF4. The epidermal, but not vascular, inactivation of PIF4 by a PIF4 artificial microRNA or a dominant negative form of PIF4 suppressed thermoresponsive gene expression and hypocotyl growth. Additionally, both the block of epidermal auxin signaling and the epidermal overexpression of a thermosensor phytochrome B (phyB) inhibited thermoresponsive growth, indicating that epidermal PIF4-auxin pathway are essential for the temperature responses. We further show that epidermal PIF4 is increased by high temperatures mainly through the transcriptional activation of PIF4. Taken together, our study demonstrates that the epidermis regulates thermoresponsive growth through the phyB-PIF4-auxin pathway.

2020-01-26 | GSE133564 | GEO

PIF7 is the master regulator of thermomorphogenesis in shade [RNA-seq]

Project description:The size and shape of plant organs are highly responsive to the local environmental conditions. The embryonic stem, or hypocotyl, of the plant is one such organ that displays impressive phenotypic plasticity, and its length is affected by both light and temperature. After sensing surrounding vegetation, hypocotyls of shade avoiding species elongate to outcompete neighbouring plants and secure access to sunlight. A similar elongation response occurs when the plants are grown in high ambient temperatures. Previous studies have shown that this response is mediated by a family of transcription factors called PHYTOCHROME-INTERACTING FACTORS (PIFs). However, it is poorly understood how environmental light and temperature interact to affect plants at the morphological and molecular levels. Here, we examine the genetic and molecular basis of the response to low R/FR under warm ambient temperatures. We found that low R/FR combined with warm temperature dominantly regulate by PIF7 and exhibit a synergistic effect on hypocotyl growth, greater than either stimulus alone. While the synergistic response was dependent on PIF7 and the plant hormone auxin, we demonstrate that additional, yet unknown key factor/s must be involved, likely working downstream of the phyB-PIF-auxin module. As shade responses are known to affect crop yield and fruit quality in many species, our findings will improve the predictions of how plants will respond to increased ambient temperatures when grown at high density, a condition in which mutual shading occurs. In addition, we point out key factors in this response that can potentially be modulated to minimize the negative effect on yield.

2022-07-26 | GSE196725 | GEO

The histone H3K27 demethylase REF6/JMJ12 Promotes thermomorphogenesis in Arabidopsis

Project description:Dynamic trimethylation of histone H3 at Lys27 (H3K27me3) affects gene expression and controls plant development and environmental responses. In Arabidopsis thaliana, RELATIVE OF EARLY FLOWERING 6/JUMONJI DOMAIN-CONTAINING PROTEIN 12 (REF6/JMJ12) demethylates H3K27me3 by recognizing a specific DNA motif; however, little is known about how REF6 activates target gene expression after recognition, especially in environmental responses. In response to warm ambient temperature, plants undergo thermomorphogenesis, which involves accelerated growth, early flowering, and changes in morphology. Here we show that REF6 regulates thermomorphogenesis and cooperates with the transcription factor PHYTOCHROME INTERACTING FACTOR 4 (PIF4) to synergistically activate thermo-responsive genes under warm ambient temperature. The ref6 loss-of-function mutants exhibited attenuated hypocotyl elongation at warm temperature, partially due to down-regulation of GIBBERELLIN 20-OXIDASE2 (GA20ox2) and BASIC HELIX-LOOP-HELIX 87 (bHLH87). REF6 enzymatic activity is necessary for warm ambient temperature responses. Together, our results provide direct evidence of an epigenetic modifier and a transcription factor working together to respond to the environment.

2021-12-31 | GSE181292 | GEO

Control of root thermomorphogenesis by systemic and local regulatory signals (4h RNA-seq)

Project description:Temperature is one of the most impactful environmental factors in response to which plants adjust their growth and development. While the regulation of temperature signaling has been extensively investigated for the aerial part of plants, much less is known and understood about how roots sense and modulate their growth in response to fluctuating temperatures. Here we found that shoot and root growth responses to high ambient temperature are negatively correlated during early seedling development. A shoot signaling module that includes HY5, the phytochromes and the PIFs exerts a central function in coupling these responses and triggers long-distance signaling to control root growth and auxin levels in the root. In addition to the HY5/PIF dependent shoot module, a local regulatory axis composed of auxin biosynthesis and auxin perception factors mediates root responses to high ambient temperature. Together, our findings uncover that roots integrate long-distance signals with local hormonal inputs during thermomorphogenesis.

2020-11-04 | GSE138131 | GEO

Control of root thermomorphogenesis by systemic and local regulatory signals (18h RNA-seq)

2020-11-04 | GSE138132 | GEO

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