Seedling Establishment: A Dimmer Switch-Regulated Process between Dark and Light Signaling

Gommers, Charlotte M.M.; Monte, Elena

doi:10.1104/pp.17.01460

Cited by 118 publications

(112 citation statements)

References 170 publications

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“…There is strong evidence that the UV-B-sensing photoreceptor UVR8, the blue-light receptors CRY1 and CRY2 and the red/far-red discriminating phytochromes all regulate COP1 activity (Hoecker, 2017;Podolec and Ulm, 2018). The regulation of COP1 by photoreceptors enables a broad range of photomorphogenic responses, including de-etiolation, cotyledon expansion and transition to flowering, as well as UV-B light acclimation (Lau and Deng, 2012;Jenkins, 2017;Yin and Ulm, 2017;Gommers and Monte, 2018). Here we have dissected at the structural, biochemical and genetic level how the activated UVR8 and cryptochrome photoreceptors impinge on COP1 activity, by interacting with its central WD40 domain, resulting in the stabilization of COP1 substrate transcription factors.…”

Section: Discussionmentioning

confidence: 99%

“…Flowering plants etiolate in darkness, manifested by the rapid elongation of the embryonic stem, the hypocotyl, and closed and underdeveloped embryonic leaves, the cotyledons. Under light and upon photoreceptor activation, seedlings de-etiolate and display a photomorphogenic phenotype, characterized by a short hypocotyl and open green cotyledons, enabling a photosynthetic lifestyle (Gommers and Monte, 2018). The constitutively photomorphogenic 1 (cop1) mutant displays a light-grown phenotype in the dark, including a short hypocotyl, and open and expanded cotyledons.…”

Section: Introductionmentioning

confidence: 99%

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Plant photoreceptors and their signaling components compete for binding to the ubiquitin ligase COP1 using their VP-peptide motifs

Lau

Podolec

Chappuis

et al. 2019

Preprint

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Plants sense different parts of the sun's light spectrum using specialized photoreceptors, many of which signal through the E3 ubiquitin ligase COP1. Photoreceptor binding modulates COP1's ubiquitin ligase activity towards transcription factors. Here we analyze why many COP1-interacting transcription factors and photoreceptors harbor sequence-divergent Val-Pro (VP) peptide motifs. We demonstrate that VP motifs enable different light signaling components to bind to the WD40 domain of COP1 with various binding affinities. Crystal structures of the VP motifs of the UV-B photoreceptor UVR8 and the transcription factor HY5 in complex with COP1, quantitative binding assays and reverse genetic experiments together suggest that UVR8 and HY5 compete for the COP1 WD40 domain. Photoactivation of UVR8 leads to high-affinity cooperative binding of its VP domain and its photosensing core to COP1, interfering with the binding of COP1 to its substrate HY5. Functional UVR8 -VP motif chimeras suggest that UV-B signaling specificity resides in the UVR8 photoreceptor core, not its VP motif. Crystal structures of different COP1 -VP peptide complexes highlight sequence fingerprints required for COP1 targeting. The functionally distinct blue light receptors CRY1 and CRY2 also compete with downstream transcription factors for COP1 binding using similar VP-peptide motifs. Together, our work reveals that photoreceptors and

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Plant photoreceptors and their signaling components compete for binding to the ubiquitin ligase COP1 using their VP-peptide motifs

Lau

Podolec

Chappuis

et al. 2019

Preprint

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“…When germination occurs in darkness, or dim light seedlings adopt a skotomorphogenic-type program where growth is largely confined to the seedling stem (hypocotyl), at the expense of seedling leaf (cotyledon) and root development. A large body of work has shown that members of the light regulated PHYTOCHROME INTERACTING FACTOR (PIF) gene family operate cooperatively to regulate skotomorphogenesis ( Gommers and Monte, 2018; Leivar and Monte, 2014; Chaiwanon et al, 2016 ). This growth strategy allows seedlings to forage for light when occluded by soil, debris or vegetation cover.…”

Section: Introductionmentioning

confidence: 99%

HEXOKINASE 1 Control of Post-Germinative Seedling Growth

Ganpudi¹,

Romanowski²,

Halliday³

2019

Preprint

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1 5 HEXOKINASE 1 (HXK1) is an evolutionarily conserved glycolytic enzyme that has a 1 6 separate nuclear glucose-sensor signalling function. In Arabidopsis, HXK1 mutant seedlings 1 7 have a stunted growth defect, yet how this relates to HXK1 function remains inconclusive. 1 8We show that the HXK1-glycolytic pathway performs a fundamental role in catabolising seed 1 9 reserves to fuel post-germinative cell division and expansion. This function is particularly 2 0 important in dim light which delays the switch to photoautotrophic growth. RNAseq analysis 2 1 reveals that HXK1 imposes strong repressive control on plastome gene expression, and 2 2 regulates nuclear-encoded genes that drive energy-consuming processes. Earlier studies 2 3 have implicated HXK1 sensor-signalling in the repression of CAB2 and CAA gene 2 4 expression by exogenous glucose. We show that over a wide range of irradiances this 2 5 pathway is not operative in seedlings. Our study therefore defines a new operational model 2 6for HXK1 action in catabolising carbon resources and tuning gene expression to optimize 2 7 seedling growth. 2 8 2 9

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“…Seed reserves are limited, hence a proper skotomorphogenic growth must be achieved in order to ensure survival of seedlings until they reach the light. A complex network of transcription factors and phytohormones such as ethylene, auxins and gibberellins tightly regulates skotomorphogenic growth once seeds germinate and during the transition to light [2, 3]. The bHLH PHYTOCHROME INTERACTING FACTORS (PIFs) exert their promoting role in darkness and, at the same time, repress photomorphogenesis [4].…”

Section: Introductionmentioning

confidence: 99%

Dual function of HYPONASTIC LEAVES 1 during early skotomorphogenic growth in Arabidopsis

Sacnun

Crespo

Palatnik

et al. 2019

Preprint

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23MicroRNAs are small RNA molecules with big impact in many eukaryotic biological 24 processes. In plants, their role as regulators of important developmental programs such as 25 leaf size and shape, flower organs or phase transitions, among others, have been evidenced 26 by mutants in specific miRNAs and by mutants in components of their biogenesis. However, 27 we are still far from understanding the scope of this regulatory system so other crucial 28 developmental phases might be influenced by the microRNA pathway. 29 Skotomorphogenesis is an essential developmental program that takes place after seeds 30 germinate underground in order to display a proper response when seedlings reach the light. 31 In this work, we found that the core components of microRNA pathway, DCL1, HYL1 and 32 SERRATE, promote hypocotyl elongation during skotomorphogenesis. Hook unfolding, 33 another characteristic phenotype displayed by dark-grown seedlings is also regulated by 34 these proteins but, surprisingly, they act in different ways. Thus, HYL1 represses hook 35 unfolding while DCL1 and SE promote it since the hooks of mutants on each component are 36 more or less open than those of wild-type during skotomorphogenesis, respectively. Genetic 37 and physiological analyses on HYL1 mutants provide evidence that repression of hook 38 unfolding is carried out through the HYL1 protein-protein interaction domain. Furthermore, 39 the data indicates that phosphorylated HYL1 is necessary for this function. Molecular and 40 genetic analyses also suggest that HYL1 regulates the activity of the master 3 41 photomorphogenic regulator HY5 in darkness to ensure a proper early skotomorphogenic 42 growth. In summary, while our data show a role for miRNAs in darkness, it also suggests a 43 microprocessor-independent role of HYL1 as a repressor of hook unfolding assigning a 44 biological function to phosphorylated HYL1. This work uncovers a previously unnoticed link 45 between components of the miRNA biogenesis machinery, the skotomorphogenic growth 46 and hook development in Arabidopsis. 48Author summary 49 Seeds germinating underground display a specific developmental program, termed 50 skotomorphogenesis, to ensure survival of the emerging seedlings until they reach the light. 51They rapidly elongate the hypocotyl and maintain the cotyledons closed, forming a hook with 52 the hypocotyl in order to protect apical meristematic cells from mechanical damage. Such 53 crucial events for the fate of the seedling are tightly regulated and although some 54 transcriptional regulators and phytohormones are known to be implicated in this regulation, 55 we are still far from a complete understanding of these biological processes. Our work 56 provides new information on the diverse roles in skotomorphogenesis of the core components 57 of microRNA biogenesis in Arabidopsis, HYL1, SE, and DCL1. We show that hypocotyl 58 elongation is promoted by all these components, probably through the action of specific 59 miRNAs. Hook development is also...

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Seedling Establishment: A Dimmer Switch-Regulated Process between Dark and Light Signaling

Cited by 118 publications

References 170 publications

Plant photoreceptors and their signaling components compete for binding to the ubiquitin ligase COP1 using their VP-peptide motifs

Plant photoreceptors and their signaling components compete for binding to the ubiquitin ligase COP1 using their VP-peptide motifs

HEXOKINASE 1 Control of Post-Germinative Seedling Growth

Dual function of HYPONASTIC LEAVES 1 during early skotomorphogenic growth in Arabidopsis

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