PORCUPINE regulates development in response to temperature through alternative splicing

Capovilla, Giovanna; Delhomme, Nicolas; Collani, Silvio; Shutava, Iryna; Bezrukov, Ilja; Symeonidi, Efthymia; Amorim, Marcella de Francisco; Laubinger, Sascha; Schmid, Markus

doi:10.1038/s41477-018-0176-z

Cited by 43 publications

(59 citation statements)

References 35 publications

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“…Moreover, SME1 has a critical role in controlling Arabidopsis development and interaction with its environment by ensuring the adequate processing of specific pre-mRNAs. While preparing this manuscript, the characterization of an Arabidopsis putative splicing regulator, PORCUPINE (PCP), which resulted to be identical to SME1, was reported (Capovilla et al, 2018). Conforming to our results, Capovilla and colleagues found that PCP expression is regulated by ambient temperature and that PCP controls the splicing of a number of pre-mRNAs under control and low-temperature conditions, its role being more relevant in the cold (16°C in this case).…”

Section: Discussionsupporting

confidence: 73%

Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity

et al. 2019

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J.A.J.); 0000-0003-2020-0950 (J.S.)The control of precursor-messenger RNA (pre-mRNA) splicing is emerging as an important layer of regulation in plant responses to endogenous and external cues. In eukaryotes, pre-mRNA splicing is governed by the activity of a large ribonucleoprotein machinery, the spliceosome, whose protein core is composed of the Sm ring and the related Sm-like 2-8 complex. Recently, the Arabidopsis (Arabidopsis thaliana) Sm-like 2-8 complex has been characterized. However, the role of plant Sm proteins in pre-mRNA splicing remains largely unknown. Here, we present the functional characterization of Sm protein E1 (SME1), an Arabidopsis homolog of the SME subunit of the eukaryotic Sm ring. Our results demonstrate that SME1 regulates the spliceosome activity and that this regulation is controlled by the environmental conditions. Indeed, depending on the conditions, SME1 ensures the efficiency of constitutive and alternative splicing of selected pre-mRNAs. Moreover, missplicing of most targeted pre-mRNAs leads to the generation of nonsense-mediated decay signatures, indicating that SME1 also guarantees adequate levels of the corresponding functional transcripts. In addition, we show that the selective function of SME1 in ensuring appropriate gene expression patterns through the regulation of specific pre-mRNA splicing is essential for adequate plant development and adaptation to freezing temperatures. These findings reveal that SME1 plays a critical role in plant development and interaction with the environment by providing spliceosome activity specificity.

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Section: Discussionsupporting

confidence: 73%

Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity

et al. 2019

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“…Nascent RNAPII transcription slows down close to exon-intron boundaries in a splicing-dependent manner and is responsible for intragenic RNAPII stalling(15). Splicing regulation is essential for the cold-response in Arabidopsis (22,23) but how this is connected to molecular adjustments of nascent RNAPII transcription is largely unknown.…”

Section: Introductionmentioning

confidence: 99%

Native Elongation Transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis

Kindgren

Ivanov

Marquardt

2019

Preprint

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15Temperature profoundly affects the kinetics of biochemical reactions, yet how large molecular 16 complexes such as the transcription machinery accommodate changing temperatures to maintain 17 cellular function is poorly understood. Here, we developed plant native elongating transcripts 18 sequencing (plaNET-seq) to profile genome-wide nascent RNA polymerase II (RNAPII) transcription 19 during the cold-response of Arabidopsis thaliana with single-nucleotide resolution. Combined with 20 temporal resolution, these data revealed transient genome-wide reprogramming of nascent RNAPII 21 transcription during cold, including characteristics of RNAPII elongation and thousands of non-22 coding transcripts connected to gene expression. Our results suggest a role for promoter-proximal 23 RNAPII stalling in predisposing genes for transcriptional activation during plant-environment 24 interactions. At gene 3'-ends, cold initially facilitated transcriptional termination by limiting the 25 distance of read-through transcription. Within gene bodies, cold reduced the kinetics of co-26 transcriptional splicing leading to increased intragenic stalling. Our data resolved multiple distinct 27 mechanisms by which temperature transiently altered the dynamics of nascent RNAPII transcription 28 and associated RNA processing, illustrating potential biotechnological solutions and future focus 29 areas to promote food security in the context of a changing climate. 30 32Changes to ambient temperatures challenge the development and growth of living organisms. While 33 mammals retain a stable body temperature, sessile organisms such as plants continually sense their 34 environment and rely on molecular mechanisms that compensate for temperature changes(1). 35Alterations to the ambient temperature frequently lead to re-programming of the transcriptional 36 output by RNA polymerase II (RNAPII) that reflects steady-state levels of messenger RNAs and non-37coding RNAs in the cell(2,3). Sequence-specific transcription factors controlling the initiation of 38 transcription often shape these responses. However, the significance of mechanisms regulating 39 eukaryotic gene expression after initiation, for example through control of elongation of the nascent 40 RNA chain is increasingly appreciated(4). Genome-wide profiling of transcriptionally engaged 41 RNAPII complexes has identified low-velocity regions of RNAPII elongation at the beginning (i.e. 42promoter-proximal stalling) and the end (i.e. poly-(A) associated stalling) of genes(4,5). Organisms 43 appear to alter the activity of RNAPII at these regions to re-program their transcriptional output to 44 acclimate to temperature changes. The release from promoter-proximal stalling at heat-shock genes 45 facilitates rapid transcriptional induction in response to heat in Drosophila (6), and promoter-proximal 46 stalling is reduced genome-wide when temperatures increase in mammalian cell cultures (7). RNAPII 47 accumulation at gene ends is associated with the mechanism of transcriptional termination(8)...

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Section: Validation Against Public Datasetsmentioning

confidence: 99%

“…We used images from three published studies [20][21][22], which were generated on the RAPA platform [23], and re-analyzed them using araDEEPopsis. Correlation analysis of published rosette area and our own measurements resulted in R 2 values of 0.996 [21] and 0.979 [20], respectively ( Fig 5). Despite this overall very strong correlation, we noticed individual images in which our segmentation disagreed with the published one.…”

Section: Validation Against Public Datasetsmentioning

confidence: 99%

“…Second, we wanted to test whether our pipeline would remain robust when using data generated on different phenotyping platforms, with different image recording systems, pot sizes and shapes, and background composition. We used images from three published studies [20][21][22], generated on either the RAPA platform [23] at the Max Planck Institute for Developmental Biology in Tübingen, Germany [20,21], or the WIWAM platform (https://www.psb.ugent.be/phenotyping/pippa) at the VIB in Ghent, Belgium [22,24], and re-analyzed them using ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs. Correlation analysis of the published rosette area derived from the RAPA system and our own measurements resulted in R 2 values of 0.996 [21] and 0.979 [20], respectively (Fig 5A,B).…”

Section: Validation Against Public Datasetsmentioning

confidence: 99%

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aradeepopsis: From images to phenotypic traits using deep transfer learning

Huether

Schandry

Jandrasits

et al. 2020

Preprint

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Linking plant phenotype to genotype, i.e., identifying genetic determinants of phenotypic traits, is a common goal of both plant breeders and geneticists. While the ever-growing genomic resources and rapid decrease of sequencing costs have led to enormous amounts of genomic data, collecting phenotypic data for large numbers of plants remains a bottleneck. Many phenotyping strategies rely on imaging plants, which makes it necessary to extract phenotypic measurements from these images rapidly and robustly. Common image segmentation tools for plant phenotyping mostly rely on color information, which is error-prone when either background or plant color deviate from the underlying expectations. We have developed a versatile, fully open-source pipeline to extract phenotypic measurements from plant images in an unsupervised manner. ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs was built around the deep-learning model DeepLabV3+ that was re-trained for segmentation of Arabidopsis thaliana rosettes. It uses semantic segmentation to classify leaf tissue into up to three categories: healthy, anthocyaninrich, and senescent. This makes ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs particularly powerful at quantitative phenotyping from early to late developmental stages, of mutants with aberrant leaf color and/or phenotype, and of plants growing in stressful conditions where leaf color may deviate from green. Using our tool on a panel of 210 natural Arabidopsis accessions, we were able to not only accurately segment images of phenotypically diverse genotypes but also to map known loci related to anthocyanin production and early necrosis using the ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs output in genome-wide association analyses. Our pipeline is able to handle images of diverse origins, image quality, and background composition, and could even accurately segment images of a distantly related Brassicaceae. Because it can be deployed on virtually any common operating system and is compatible with several high-performance computing environments, ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs can be used independently of bioinformatics expertise and computing resources. ᴀʀᴀᴅᴇᴇᴘᴏᴘsɪs is available at https://github.com/Gregor-Mendel-Institute/aradeepopsis.

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PORCUPINE regulates development in response to temperature through alternative splicing

Cited by 43 publications

References 35 publications

Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity

Arabidopsis SME1 Regulates Plant Development and Response to Abiotic Stress by Determining Spliceosome Activity Specificity

Native Elongation Transcript sequencing reveals temperature dependent dynamics of nascent RNAPII transcription in Arabidopsis

aradeepopsis: From images to phenotypic traits using deep transfer learning

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