The RNA Polymerase-Associated Factor 1 Complex Is Required for Plant Touch Responses

Jensen, Gregory C.; Fal, Kateryna; Hamant, Olivier; Haswell, Elizabeth S.

doi:10.1093/jxb/erw439

Cited by 20 publications

(30 citation statements)

References 101 publications

(150 reference statements)

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“…The genes in cluster 3 had a high response at all‐time points and the response consistently increased with repeated stimuli with cluster 4 genes. The touch response genes TCH3 (At2 g41100 – CALMODULIN‐LIKE 4 ) and TCH4 (At5 g57560 – XYLOGLUCAN ENDOTRANSGLUCOSYLASE/HYDROLASE 22 ) were present in this cluster, consistent with their definition as touch response markers (Jensen et al ., ). The genes in cluster 5 showed highest responses at the 0.5 h and 24.5 h time points, with a reduced expression at 12.5 h. As the plants were grown in a 14 h light/10 h dark cycle during the touch experiments this pattern suggested a possible overlapping touch and diurnal response.…”

Section: Resultsmentioning

confidence: 97%

“…Some genes that change in abundance in response to touch are referred to as TOUCH ( TCH ), and encode calmodulins or calmodulin‐like proteins and cell wall, wound and deference enzymes. A forward genetic screen identified RNA polymerase II‐associated factor 1 (Paf1/VIP3) that was required for some aspects of thigmomorphogenesis and also was defective in the rapid induction of TOUCH3 ( TCH3 ) and TOUCH4 ( TCH4 ), providing a link between rapid molecular responses to a single touch stimulus and growth alteration to repeated stimulus (Jensen et al ., ). Alteration of H3K36 methylation by Paf1/VIP3 is consistent with another report that revealed the importance of epigenetic regulation for mechanical stimulation responses (Cazzonelli et al ., ).…”

Section: Introductionmentioning

confidence: 97%

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Mitochondrial function modulates touch signalling in Arabidopsis thaliana

Berkowitz

Narsai

et al. 2019

The Plant Journal

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Plants respond to short-and long-term mechanical stimuli, via altered transcript abundance and growth respectively. Jasmonate, gibberellic acid and calcium have been implicated in mediating responses to mechanical stimuli. Previously it has been shown that the transcript abundance for the outer mitochondrial membrane protein of 66 kDa (OM66), is induced several fold after 30 min in response to touch. Therefore, the effect of mitochondrial function on the response to mechanical stimulation by touch at 30 min was investigated. Twenty-five mutants targeting mitochondrial function or regulators revealed that all affected the touch transcriptome. Double and triple mutants revealed synergistic or antagonistic effects following the observed responses in the single mutants. Changes in the touch-responsive transcriptome were localised, recurring with repeated rounds of stimulus. The gene expression kinetics after repeated touch were complex, displaying five distinct patterns. These transcriptomic responses were altered by some regulators of mitochondrial retrograde signalling, such as cyclic dependent protein kinase E1, a kinase protein in the mediator complex, and KIN10 (SnRK1 À sucrose non-fermenting related protein kinase 1), revealing an overlap between the touch response and mitochondrial stress signalling and alternative mitochondrial metabolic pathways. Regulatory network analyses revealed touch-induced stress responses and suppressed growth and biosynthetic processes. Interaction with the phytohormone signalling pathways indicated that ethylene and gibberellic acid had the greatest effect. Hormone measurements revealed that mutations of genes that encoded mitochondrial proteins altered hormone concentrations. Mitochondrial function modulates touch-induced changes in gene expression directly through altered regulatory networks, and indirectly via altering hormonal levels.

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Section: Resultsmentioning

confidence: 97%

Section: Introductionmentioning

confidence: 97%

Mitochondrial function modulates touch signalling in Arabidopsis thaliana

Berkowitz

Narsai

et al. 2019

The Plant Journal

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“…When Arabidopsis stems are mechanically stimulated stem elongation is restricted in response. Interestingly, the screening for Arabidopsis mutants resistant to touch resulted in very different candidate genes such as jasmonic acid biosynthesis enzymes (24), or transcription associated proteins (27), and these genes were also affected in eki highlighting the fact that plant mechanosensing is a complex phenomenon with multiple pathways being involved (35).…”

Section: Discussionmentioning

confidence: 99%

“…The jasmonic acid biosynthesis gene AOS is required for touch induced developmental responses in Arabidopsis(24), this gene was also significantly downregulated in eki IN5-bark and wood. Another gene required for thigmomorphogenesis is VIP3(27), this gene was significantly upregulated in eki bark. The birch orthologous genes of Arabidopsis TOUCH3 and TOUCH4 had barely detectable expression in our samples.…”

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confidence: 99%

ELIMÄKI locus is required for mechanosensing and proprioception in birch trees

Alonso‐Serra¹,

Shi²,

Peaucelle³

et al. 2019

Preprint

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The remarkable vertical and radial growth observed in tree species, encompasses a major physical challenge for wood forming tissues. To compensate with increasing size and weight, cambiumderived radial growth increases the stem width, thereby supporting the aerial body of trees. This feedback appears to be part of a so-called "proprioception" (1, 2) mechanism that controls plant size and biomass allocation. Yet, how trees experience or respond to mechanical stress derived from their own vertical loading, remains unknown. Here, we combined two strategies to dissect the proprioceptive response in birch. First, we show that in response to physical loading, trees promote radial growth with different magnitudes along the stem. Next, we identified a mutant cultivar (B. pubescens cv. Elimäki) in which the main stem shows normal vertical development, but collapses after three months. By inducing precocious flowering, we generated a backcrossed population (BC1) by producing two generations in 4 years. In his scheme, we uncovered a recessive trait (eki) that segregates and genetically maps with a Mendelian monogenic pattern. Unlike WT, eki is resistant to vertical mechanical stimulation. However, eki responds normally to the gravitropic stimulus by making tension wood. Before the collapse, cell size in eki is compromised resulting in radial growth defects, depending on stem height. Cell walls of developing xylem and phloem tissues have delayed differentiation in eki, and its tissues are softer compared to WT as indicated by atomic force microscopy (AFM). The transcriptomic profile of eki highlighted the overlap with that of the Arabidopsis response to touch. Taken together, our results suggest that the mechanical environment and cell wall properties of developing woody tissues, can significantly affect the growth responses to vertical loading thereby compromising their proprioceptive capacity. Additionally, we introduce a fast forward genetics strategy to dissect complex phenotypes in trees.

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“…The chromatin modifying enzyme SDG8 is required for the control of gene expression in response to touch (Cazzonelli et al 2014 ). More recently, in a screen for touch-insensitive mutants, the transcriptional regulator VIP3, a member of the Paf1 complex, was identified (Jensen et al 2017 ), suggesting that nuclear factors might have a stronger role in mechanotransduction than anticipated. Here, we propose to investigate the possible contribution of the nuclear envelope in that framework.…”

Section: Introductionmentioning

confidence: 99%

Nuclear envelope: a new frontier in plant mechanosensing?

et al. 2017

Self Cite

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In animals, it is now well established that forces applied at the cell surface are propagated through the cytoskeleton to the nucleus, leading to deformations of the nuclear structure and, potentially, to modification of gene expression. Consistently, altered nuclear mechanics has been related to many genetic disorders, such as muscular dystrophy, cardiomyopathy and progeria. In plants, the integration of mechanical signals in cell and developmental biology has also made great progress. Yet, while the link between cell wall stresses and cytoskeleton is consolidated, such cortical mechanical cues have not been integrated with the nucleoskeleton. Here, we propose to take inspiration from studies on animal nuclei to identify relevant methods amenable to probing nucleus mechanics and deformation in plant cells, with a focus on microrheology. To identify potential molecular targets, we also compare the players at the nuclear envelope, namely lamina and LINC complex, in both plant and animal nuclei. Understanding how mechanical signals are transduced to the nucleus across kingdoms will likely have essential implications in development (e.g. how mechanical cues add robustness to gene expression patterns), in the nucleoskeleton–cytoskeleton nexus (e.g. how stress is propagated in turgid/walled cells), as well as in transcriptional control, chromatin biology and epigenetics.

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The RNA Polymerase-Associated Factor 1 Complex Is Required for Plant Touch Responses

Abstract: HIGHLIGHTThe chromatin-modifying complex Paf1 is required for shoot and root thigmomorphogenesis and touch-inducible gene expression.

Cited by 20 publications

References 101 publications

Mitochondrial function modulates touch signalling in Arabidopsis thaliana

Mitochondrial function modulates touch signalling in Arabidopsis thaliana

ELIMÄKI locus is required for mechanosensing and proprioception in birch trees

Nuclear envelope: a new frontier in plant mechanosensing?

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