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"Ott, Thomas"
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Optogenetic control of gene expression in plants in the presence of ambient white light
Optogenetics is the genetic approach for controlling cellular processes with light. It provides spatiotemporal, quantitative and reversible control over biological signaling and metabolic processes, overcoming limitations of chemically inducible systems. However, optogenetics lags in plant research because ambient light required for growth leads to undesired system activation. We solved this issue by developing plant usable light-switch elements (PULSE), an optogenetic tool for reversibly controlling gene expression in plants under ambient light. PULSE combines a blue-light-regulated repressor with a red-light-inducible switch. Gene expression is only activated under red light and remains inactive under white light or in darkness. Supported by a quantitative mathematical model, we characterized PULSE in protoplasts and achieved high induction rates, and we combined it with CRISPR–Cas9-based technologies to target synthetic signaling and developmental pathways. We applied PULSE to control immune responses in plant leaves and generated
Arabidopsis
transgenic plants. PULSE opens broad experimental avenues in plant research and biotechnology.
PULSE is an optogenetic tool that consists of two modules with different wavelength sensitivities. Their interplay enables optogenetic access to gene expression in plants independently of ambient light.
Journal Article
Symbiosome functionality in Medicago truncatula nodules requires continuous clearing of pectins from the symbiosome space
Central to the legume–rhizobium symbiosis is the formation of organelle-like symbiosomes where nitrogen-fixing bacteroids are enclosed by a host-derived symbiosome membrane. This creates the symbiosome space, which topologically resembles an apoplastic compartment within the cell. While the apoplast of plant cells is largely occupied by the cell wall, symbiosomes are devoid of cell wall polymers. Here, we describe a mechanism that functions to protect and maintain effective nitrogen fixation through the action of cell-wall-degrading enzymes that prevent accumulation of un-esterified pectin within symbiosomes. We identify two symbiotically-induced polygalacturonase (PG) genes in
Medicago truncatula
,
SyPG1
and
SyPG2
, that are secreted into the symbiosome space. Silencing the expression of
SyPG1/2
or editing
SyPG1/2
via CRISPR-Cas9 both lead to nodule senescence and trigger excessive accumulation of un-esterified pectin in symbiosome containing cells. Additionally, we show that un-esterified pectins inhibit rhizobial growth both in vivo and in vitro. Together, our results provide evidence for a host-controlled cell wall clearance mechanism that is essential for symbiosome maintenance.
Here a mechanism for nitrogen fixation maintenance is identified in
Medicago truncatula
where two polygalacturoneases are expressed in nodules and secreted into the symbiosome space for clearing of excessive un-esterified pectins.
Journal Article
A Multidataset Assessment of Climatic Drivers and Uncertainties of Recent Trends in Evaporative Demand across the Continental United States
Increased atmospheric evaporative demand has important implications for humans and ecosystems in water-scarce lands. While temperature plays a significant role in driving evaporative demand and its trend, other climate variables are also influential and their contributions to recent trends in evaporative demand are unknown. We address this gap with an assessment of recent (1980–2020) trends in annual reference evapotranspiration (ETo) and its drivers across the continental United States based on five gridded datasets. In doing so, we characterize the structural uncertainty of ETo trends and decompose the relative influences of temperature, wind speed, solar radiation, and humidity. Results highlight large and robust changes in ETo across much of the western United States, centered on the Rio Grande region where ETo increased 135–235 mm during 1980–2020. The largest uncertainties in ETo trends are in the central and eastern United States and surrounding the Upper Colorado River. Trend decomposition highlights the strong and widespread influence of temperature, which contributes to 57% of observed ETo trends, on average. ETo increases are mitigated by increases in specific humidity in non-water-limited regions, while small decreases in specific humidity and increases in wind speed and solar radiation magnify ETo increases across the West. Our results show increases in ETo across the West that are already emerging outside the range of variability observed 20–40 years ago. Our results suggest that twenty-first-century land and water managers need to plan for an already increasing influence of evaporative demand on water availability and wildfire risks.
Journal Article
The B-type response regulator GmRR11d mediates systemic inhibition of symbiotic nodulation
Key to the success of legumes is the ability to form and maintain optimal symbiotic nodules that enable them to balance the trade-off between symbiosis and plant growth. Cytokinin is essential for homeostatic regulation of nodulation, but the mechanism remains incompletely understood. Here, we show that a B-type response regulator GmRR11d mediates systemic inhibition of nodulation.
GmRR11d
is induced by rhizobia and low level cytokinin, and GmRR11d can suppress the transcriptional activity of GmNSP1 on
GmNIN1a
to inhibit soybean nodulation. GmRR11d positively regulates cytokinin response and its binding on the
GmNIN1a
promoter is enhanced by cytokinin. Intriguingly, rhizobial induction of
GmRR11d
and its function are dependent upon GmNARK that is a CLV1-like receptor kinase and inhibits nodule number in shoots. Thus, GmRR11d governs a transcriptional program associated with nodulation attenuation and cytokinin response activation essential for systemic regulation of nodulation.
Cytokinin is essential for regulation of nodulation. Here, the authors identified a B-type response regulator GmRR11d that governs a transcriptional program associated with nodulation and cytokinin activation essential for systemic regulation of nodulation.
Journal Article
Mutant analysis in the nonlegume Parasponia andersonii identifies NIN and NF-YA1 transcription factors as a core genetic network in nitrogen-fixing nodule symbioses
Nitrogen-fixing nodulation occurs in 10 taxonomic lineages, with either rhizobia or Frankia bacteria. To establish such an endosymbiosis, two processes are essential: nodule organogenesis and intracellular bacterial infection. In the legume–rhizobium endosymbiosis, both processes are guarded by the transcription factor NODULE INCEPTION (NIN) and its downstream target genes of the NUCLEAR FACTOR Y (NF-Y) complex.
It is hypothesized that nodulation has a single evolutionary origin c. 110 Ma, followed by many independent losses. Despite a significant body of knowledge of the legume–rhizobium symbiosis, it remains elusive which signalling modules are shared between nodulating species in different taxonomic clades. We used Parasponia andersonii to investigate the role of NIN and NF-YA genes in rhizobium nodulation in a nonlegume system.
Consistent with legumes, P. andersonii PanNIN and PanNF-YA1 are coexpressed in nodules. By analyzing single, double and higher-order CRISPR-Cas9 knockout mutants, we show that nodule organogenesis and early symbiotic expression of PanNF-YA1 are PanNIN-dependent and that PanNF-YA1 is specifically required for intracellular rhizobium infection.
This demonstrates that NIN and NF-YA1 have conserved symbiotic functions. As Parasponia and legumes diverged soon after the birth of the nodulation trait, we argue that NIN and NF-YA1 represent core transcriptional regulators in this symbiosis.
Journal Article
Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains
Cell surface receptors govern a multitude of signalling pathways in multicellular organisms. In plants, prominent examples are the receptor kinases FLS2 and BRI1, which activate immunity and steroid-mediated growth, respectively. Intriguingly, despite inducing distinct signalling outputs, both receptors employ common downstream signalling components, which exist in plasma membrane (PM)-localised protein complexes. An important question is thus how these receptor complexes maintain signalling specificity. Live-cell imaging revealed that FLS2 and BRI1 form PM nanoclusters. Using single-particle tracking we could discriminate both cluster populations and we observed spatiotemporal separation between immune and growth signalling platforms. This finding was confirmed by visualising FLS2 and BRI1 within distinct PM nanodomains marked by specific remorin proteins and differential co-localisation with the cytoskeleton. Our results thus suggest that signalling specificity between these pathways may be explained by the spatial separation of FLS2 and BRI1 with their associated signalling components within dedicated PM nanodomains.
Journal Article
Stabilization of membrane topologies by proteinaceous remorin scaffolds
In plants, the topological organization of membranes has mainly been attributed to the cell wall and the cytoskeleton. Additionally, few proteins, such as plant-specific remorins have been shown to function as protein and lipid organizers. Root nodule symbiosis requires continuous membrane re-arrangements, with bacteria being finally released from infection threads into membrane-confined symbiosomes. We found that mutations in the symbiosis-specific
SYMREM1
gene result in highly disorganized perimicrobial membranes. AlphaFold modelling and biochemical analyses reveal that SYMREM1 oligomerizes into antiparallel dimers and may form a higher-order membrane scaffolding structure. This was experimentally confirmed when expressing this and other remorins in wall-less protoplasts is sufficient where they significantly alter and stabilize
de novo
membrane topologies ranging from membrane blebs to long membrane tubes with a central actin filament. Reciprocally, mechanically induced membrane indentations were equally stabilized by SYMREM1. Taken together we describe a plant-specific mechanism that allows the stabilization of large-scale membrane conformations independent of the cell wall.
In plants, plasma membrane topologies are predominantly driven by the cell wall. In this study, the authors demonstrate that remorin proteins can take over these functions at specialized, unwalled plasma membranes such as infection droplets associated with symbiotic infection threads.
Journal Article
Competence for transcellular infection in the root cortex involves a post-replicative, cell-cycle exit decision in Medicago truncatula
During root nodule symbiosis (RNS), cell-division activity is reinitiated and sustained in the root cortex to create a hospitable cellular niche. Such a temporary and spatially confined site is required to render host cells compatible with the intracellular progression of rhizobia. Although it has been suggested that early infection events might involve a pre-mitotic cell-cycle arrest, this process has not been dissected with cellular resolution. Here, we show that a dual-color Medicago histone reporter robustly identifies cells with different mitotic or endoreduplication activities in the root cortex. By imaging deep root tissues, we found that a confined trajectory of cortical cells that are transcellularly passed by infection threads is in a stage of the cell cycle that is distinct from directly adjacent cells. Distinctive features of infected cells include nuclear widening and large-scale chromatin rearrangements consistent with a cell-cycle exit prior to differentiation. Using a combination of fluorescent reporters demarcating cell-cycle phase progression, we confirmed that a reduced proliferation potential and modulating the G2/M transition, a process possibly controlled by the NF-YA1 transcription factor, mark the success of rhizobial delivery to nodule cells.
Journal Article