Adjustment of the PIF7‐HFR1 transcriptional module activity controls plant shade adaptation

Paulišić, Sandi; Qin, Wenting; Verasztó, Harshul Arora; Then, Christiane; Alary, Benjamin; Nogué, Fabien; Tsiantis, Miltos; Hothorn, Michael; Martínez‐Garcia, Jaime F.

doi:10.15252/embj.2019104273

Cited by 42 publications

(43 citation statements)

References 58 publications

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“…Consistent with the RNA-seq data, the transcript level of these genes was upregulated in response to high ambient temperature and correlated with thermomorphogensis as previously shown [ 15 , 29 , 30 ]. Interestingly, the transcript level of LONG HYPOCOTYL IN FAR-RED 1 ( HFR1 ) and PIF3-LIKE 1 ( PIL1 ), which are known inhibitors of PIFs in photomorphogenesis, thermomorphogenesis and shade avoidance responses [ 41 – 46 ], were up-regulated in the absence of HECs ( Fig 3F ). These data suggest that similar to HEC1 and HEC2 , genes encoding the inhibitors of PIFs are also induced under high ambient temperature responses and perhaps participate in the negative feedback loop to regulate PIF level and activity at high ambient temperature.…”

Section: Resultsmentioning

confidence: 99%

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

Lee

Zhu

2021

PLoS Genet

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Plant growth and development are acutely sensitive to high ambient temperature caused in part due to climate change. However, the mechanism of high ambient temperature signaling is not well defined. Here, we show that HECATEs (HEC1 and HEC2), two helix-loop-helix transcription factors, inhibit thermomorphogenesis. While the expression of HEC1 and HEC2 is increased and HEC2 protein is stabilized at high ambient temperature, hec1hec2 double mutant showed exaggerated thermomorphogenesis. Analyses of the four PHYTOCHROME INTERACTING FACTOR (PIF1, PIF3, PIF4 and PIF5) mutants and overexpression lines showed that they all contribute to promote thermomorphogenesis. Furthermore, genetic analysis showed that pifQ is epistatic to hec1hec2. HECs and PIFs oppositely control the expression of many genes in response to high ambient temperature. PIFs activate the expression of HECs in response to high ambient temperature. HEC2 in turn interacts with PIF4 both in yeast and in vivo. In the absence of HECs, PIF4 binding to its own promoter as well as the target gene promoters was enhanced, indicating that HECs control PIF4 activity via heterodimerization. Overall, these data suggest that PIF4-HEC forms an autoregulatory composite negative feedback loop that controls growth genes to modulate thermomorphogenesis.

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Section: Resultsmentioning

confidence: 99%

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

Lee

Zhu

2021

PLoS Genet

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“…Consistent with the RNA-seq data, the transcript level of these genes was upregulated in response to high ambient temperature and correlated with thermomorphogensis as previously shown (Hayes et al , 2017; Ma et al , 2016; Sun et al , 2012). Interestingly, the transcript level of LONG HYPOCOTYL IN FAR-RED 1 ( HFR1 ) and PIF3-LIKE 1 ( PIL1 ), which are known inhibitors of PIFs in photomorphogenesis, thermomorphogenesis and shade avoidance responses (Foreman et al , 2011; Hornitschek et al , 2009; Luo et al , 2014; Paulišić et al , 2020; Tavridou et al , 2020; Xu et al , 2017), were up-regulated in the absence of HECs (Fig. 5F).…”

Section: Resultsmentioning

confidence: 99%

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

Lee

Zhu

2021

Preprint

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Plant growth and development are acutely sensitive to high ambient temperature ascribable in part to climate change. However, the mechanism of high ambient temperature signaling is not well defined. Here, we show that HECATEs (HEC1 and HEC2), two helix-loop-helix transcription factors, inhibit thermomorphogenesis. While the expression of HEC1 and HEC2 is increased and HEC2 protein is stabilized at high ambient temperature, hec1hec2 double mutant showed exaggerated thermomorphogenesis. Analyses of the four major PIF (PIF1, PIF3, PIF4 and PIF5) mutants and overexpression lines showed that they all contribute to promote thermomorphogenesis. Furthermore, genetic analysis showed that pifQ is epistatic to hec1hec2. HECs and PIFs oppositely control the expression of many genes in response to high ambient temperature. HEC2 interacts with PIF4 both in yeast and in vivo. In the absence of HECs, PIF4 binding to its own promoter as well as the target gene promoters was enhanced, indicating that HECs control PIF4 activity via heterodimerization. Overall, these data suggest that PIF4-HEC forms an autoregulatory composite negative feedback loop that controls growth genes to modulate thermomorphogenesis.

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“…AtPIF7 has been shown to bind to PHYB (Leivar et al, 2008) and to have a role in promoting Arabidopsis hypocotyls as a result of shade and warm temperature treatments (Li et al, 2012; Fiorucci et al, 2020). Considering that in A. thaliana a functional AtPAR1 binds in vivo to PIFs and other bHLH proteins in the nucleus (Hao et al, 2012; Cifuentes-Esquivel et al, 2013; Paulišić et al, 2021), we aimed to determine whether the DcPAR1 protein is nuclear and capable of heterodimerizing with other bHLH proteins. First, we observed that DcPAR1-GFP presents nuclear localization in cells of Nicotiana benthamiana leaves (Supplemental Figure 3).…”

Section: Resultsmentioning

confidence: 99%

DcPAR1 is Required for Development and Carotenoid Synthesis in the Dark-Grown Carrot Taproot

Arias

Ortega

González

et al. 2021

Preprint

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Light stimulates carotenoid synthesis in plants during photomorphogenesis through the expression of PHYTOENE SYNTHASE (PSY), a key gene in carotenoid biosynthesis. The orange Daucus carota (carrot) synthesizes and accumulates high amounts of carotenoids in the taproot that grows underground. Contrary to other organs, light impairs carrot taproot development and represses the expression of carotenogenic genes such as DcPSY1 and DcPSY2 reducing carotenoid accumulation. By means of an RNA-seq, in previous analysis we observed that carrot PHYTOCHROME RAPIDLY REGULATED 1 (DcPAR1) is more expressed in the underground grown taproot respect to those grown in light. PAR1 is a transcriptional cofactor with a negative role in the shade avoidance syndrome regulation in Arabidopsis thaliana through the dimerization with PHYTOCHROME INTERACTING FACTORs (PIFs), allowing a moderate synthesis of carotenoids. Here we show that overexpressing AtPAR1 in carrot produces an increment of carotenoids in taproots grown underground as well as higher DcPSY1 expression. The high identity of AtPAR1 and DcPAR1 let us to suggest a functional role of DcPAR1 that was verified through the in vivo binding to AtPIF7 and the overexpression in Arabidopsis, where it increments AtPSY expression and carotenoid accumulation together with a photomorphogenic phenotype. Finally, DcPAR1 antisense carrot lines presented a dramatic decrease in carotenoids levels and in the relative expression of key carotenogenic genes as well as impairment in taproot development. These results let us to propose that DcPAR1 is a key factor for secondary root development, plastid differentiation and carotenoid synthesis in carrot taproot grown underground.

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Adjustment of the PIF7‐HFR1 transcriptional module activity controls plant shade adaptation

Cited by 42 publications

References 58 publications

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

An autoregulatory negative feedback loop controls thermomorphogenesis in Arabidopsis

DcPAR1 is Required for Development and Carotenoid Synthesis in the Dark-Grown Carrot Taproot

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