High Light and High Temperature Reduce Photosynthetic Efficiency via Different Mechanisms in the C4 Model Setaria viridis
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ABSTRACT:
ORGANISM(S): Setaria viridis
PROVIDER: GSE178320 | GEO | 2021/08/01
REPOSITORIES: GEO
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Project description:Plasmodesmata (PD) are nanochannels that facilitate cell-to-cell transport in plants. More productive and photosynthetically efficient C4 plants form more PD at the mesophyll (M)-bundle sheath (BS) interface in their leaves than their less efficient C3 relatives. In C4 leaves, PD play an essential role in facilitating the rapid metabolite exchange between the M and BS cells to operate a biochemical CO2 concentrating mechanism, which increases the CO2 partial pressure at the site of Rubisco in the BS cells and hence photosynthetic efficiency. The genetic mechanism controlling PD formation in C3 and C4 leaves is largely unknown, especially in monocot crops, due to the technical challenge of quantifying these nanostructures with electron microscopy. To address this issue, we have generated stably transformed lines of Oryza sativa (rice, C3) and Setaria viridis (setaria, C4) with fluorescent protein-tagged PD to build the first spatiotemporal atlas of leaf pit field (cluster of PD) density in monocots without the need for electron microscopy. Across leaf development, setaria had consistently more PD connections at the M-BS wall interface than rice while the difference in M-M pit field density varied. While light was a critical trigger of PD formation, cell type and function determined leaf pit field density. Complementary temporal mRNA sequencing and gene co-expression network analysis revealed that the pattern of pit field density correlated with differentially expressed PD-associated genes and photosynthesis-related genes. PD-associated genes identified from our co-expression network analysis are related to cell wall expansion, translation and chloroplast signalling.
2024-11-21 | GSE260855 | GEO
Project description:The C4 photosynthetic pathway provided a major advantage to plants growing in hot, dry environments, including the ancestors of our most productive crops. Two traits were essential for the evolution of this pathway: increased vein density and the functionalization of bundle sheath cells for photosynthesis. Although GRAS transcriptional regulators, including SHORT ROOT (SHR), have been implicated in mediating leaf patterning in both C3 and C4 species1-4, little is known about what controls the specialized features of the cells that mediate C4 metabolism and physiology. We show in the model monocot, Setaria viridis, that SHR regulates components of multiple cell identities, including chloroplast biogenesis and photosynthetic gene expression in bundle sheath cells, a central feature of C4 plants. Furthermore, we found that it also contributes to the two-cell compartmentalization of the characteristic four-carbon shuttle pathway. Disruption of SHR function clearly reduced photosynthetic capacity and seed yield in mutant plants under heat stress. Together, these results show how cell identities are remodeled by SHR to host the suite of traits characteristic of C4 regulation, which are a main engineering target in non-C4 crops to improve climate resilience.
2024-02-09 | GSE249836 | GEO
Project description:These data are associated with the following peer-reviewed scientific paper:
Peng Zhang, Robert Sharwood, Adam Carroll, Gonzalo M Estavillo, Susanne von Caemmerer and Robert T Furbank (2024) Systems analysis of long-term heat stress responses in the C4 grass Setaria viridis, The Plant Cell
Corresponding Author: Robert Sharwood (R.Sharwood@westernsydney.edu.au)
Abstract
A substantial number of C4 plants are utilized as food and fodder crops and often display improved resource use efficiency compared to C3 plants. However, the response of C4 plants to future extreme conditions such as heatwaves is less understood. Here, Setaria viridis, an emerging C4 model grass closely related to important C4 crops, was grown under long-term high temperature stress for two weeks (42C, compared to 28C). High temperature resulted in stunted growth, but surprisingly had little impact on leaf thickness, leaf area-based photosynthetic rates and bundle sheath leakiness. Dark respiration rates increased significantly (p<0.05 two-tailed Student's t-test assuming equal variance) and there were major alterations in carbon and nitrogen metabolism in the heat-stressed plants, including reduced starch levels, accumulation of soluble sugars and increased leaf nitrogen content. Quantification of major phytohormones revealed a dramatic increase in abscisic acid and accumulation of IAA-amino acid conjugates in the heat-stressed plants, consistent with transcriptional changes of genes in these pathways. Leaf transcriptomics, proteomics and metabolomics analyses were carried out and mapped onto the metabolic pathways of photosynthesis, respiration, carbon/nitrogen metabolism and phytohormone biosynthesis and signaling. While poor correlations were observed between transcript and protein log2(FoldChange) values for some photosynthetic genes, we provide an in-depth analysis of 37 hierarchical functional groups. Overall, many stress signaling pathways were upregulated, consistent with multiple potent signals leading to reduced plant growth. A systems-based model of the plant response to long-term heat stress is presented based on the oxidative stress, phytohormone and sugar signaling pathways.
2024-12-09 | MSV000096617 | MassIVE
Project description:A number of taxa utilize C4 photosynthesis, to limit the impact of photorespiration upon photosynthetic performance. In order to achieve a local elevation of CO2 concentration, maize plants possess two photosynthetic cell types. Rubisco accumulation is restricted to bundle sheath (BS) cells that surround the leaf veins. Carbon fixation occurs initially in adjacent mesophyll (ME) cells. C4 compounds are transported into the BS cells where they are subsequently decarboxylated, releasing CO2. Although the major components of the C4 pathway have been well characterized, less is known about further metabolic partitioning in the maize leaf. Microarray hybridizations have been performed in order to further investigate metabolic differences between BS and ME cell types. BS strands and ME protoplasts were isolated from the leaves of 10 day old maize seedlings by mechanical disruption and enzymatic digestion respectively. To control for differences arising from these different protocols, total leaf (TO) and total leaf stress (ST) samples were also isolated. The ST sample was subjected to the same treatments as the ME sample, with the omission of cell-wall degrading enzymes. Leaves for the TO sample were harvested as for the BS strand sample. An interwoven loop design was used to compare the four treatment groups. A biological group consisted of a growth of plants from which pooled individuals were taken for the four treatments. Six biological replicates (groups) were used. Labeling was performed using the Genisphere Array 900-MPX kit according to the manufacturer's protocol. Post hybridization washes were performed according to the recommendations of the Maize Oligo Array Project. Scan settings were used for detection of moderate to high expression signals (gain ~ 60%. power 90%). Following hybridization with TO cDNA, ~1/3 of features provided signal above twice background and below saturation. A number of taxa utilize C4 photosynthesis, to limit the impact of photorespiration upon photosynthetic performance. In order to achieve a local elevation of CO2 concentration, maize plants possess two photosynthetic cell types. Rubisco accumulation is restricted to bundle sheath (BS) cells that surround the leaf veins. Carbon fixation occurs initially in adjacent mesophyll (ME) cells. C4 compounds are transported into the BS cells where they are subsequently decarboxylated, releasing CO2. Although the major components of the C4 pathway have been well characterized, less is known about further metabolic partitioning in the maize leaf. Microarray hybridizations have been performed in order to further investigate metabolic differences between BS and ME cell types. BS strands and ME protoplasts were isolated from the leaves of 10 day old maize seedlings by mechanical disruption and enzymatic digestion respectively. To control for differences arising from these different protocols, total leaf (TO) and total leaf stress (ST) samples were also isolated. The ST sample was subjected to the same treatments as the ME sample, with the omission of cell-wall degrading enzymes. Leaves for the TO sample were harvested as for the BS strand sample. An interwoven loop design was used to compare the four treatment groups. A biological group consisted of a growth of plants from which pooled individuals were taken for the four treatments. Six biological replicates (groups) were used. Labeling was performed using the Genisphere Array 900-MPX kit according to the manufacturer's protocol. Post hybridization washes were performed according to the recommendations of the Maize Oligo Array Project. Scan settings were used for detection of moderate to high expression signals (gain ~ 60%. power 90%). Following hybridization with TO cDNA, ~1/3 of features provided signal above twice background and below saturation. Keywords: Gene expression profiling of bundle sheath and mesophyll cell types
2005-12-24 | GSE3890 | GEO
Project description:Understanding how microorganisms adjust their metabolism to maintain their ability to survive to short-term environmental variations constitutes one of the major current challenges in microbial ecology. Here WH7803, the best physiologically characterized marine Synechococcus strain was submitted to modulated light/dark cycles or acclimated to continuous high-light (HL) or low-light (LL), then shifted to various stress conditions, including low (LT) or high temperature (HT), HL and ultraviolet (UV) radiations. Physiological responses were analyzed by measuring time courses of photosystem II (PSII) quantum yield, PSII repair rate, pigment and lipid content as well as whole transcriptomes. This notably revealed that cells previously acclimated to HL seem to be better prepared than LL-acclimated cells to sustain an additional light or UV stress, but not a LT stress. Indeed, LT seems to induce a synergic effect with the HL treatment, as previously observed with oxidative stress. While all tested shift conditions induced the downregulation of many photosynthetic genes, notably those encoding PSI, cytochrome b6/f and phycobilisomes, UV stress proved to be more deleterious for PSII than the other treatments, and full recovery of damaged PSII from UV stress seemed to involve the neo-synthesis of a fairly large number of PSII subunits and not just the reassembly of pre-existing subunits after D1 replacement. In contrast, genes involved in glycogen degradation and carotenoid biosynthesis pathways were more particularly upregulated in response to LT. Altogether, these experiments allowed us to identify responses common to all stresses and those more specific to a given stress, thus highlighting genes potentially involved in niche acclimation of this key component of marine ecosystems. Our data also highlighted important specificities of the stress responses compared to model freshwater cyanobacteria.
2020-06-17 | GSE146246 | GEO
Project description:Setaria viridis (A10.1) circadian expression after light or temperature entrainment
2017-07-01 | GSE97739 | GEO
Project description:Maize, as a C4 plant, possesses two distinct types of photosynthetic cells, the mesophyll (M) and the bundle sheath (BS) cells. To elucidate their functional and regulatory differentiation we isolated large quantities of highly homogeneous M and BS cells from new mature leaves for transcriptome profiling by Illumina sequencing. More than 100,000,000 reads for each cell type were mapped to the maize genome, revealing 44,964 expressed genes. Among these, 37,105 genes were expressed in M cells, including 423 M-enriched genes and 20 M-enriched transcription factor (TF) genes, whereas 42,782 genes were expressed in BS cells, including 771 BS-enriched genes and 75 BS-enriched TF genes. Pathway analyses revealed cell differentiation in various cellular activities, with M cells playing more important roles in light reaction, protein synthesis, abiotic stress, tetrapyrrole synthesis and RNA-RNA binding, while BS cells specializing in transport, signaling, protein degradation, major C metabolism, and the Calvin cycle. Genes coding for enzymes and transporters involved in photosynthesis exhibit a strong cellular preference in expression. To a lesser extent, cell differentiation also occurs in genes involved in the metabolism of starch, sucrose, nitrogen, sulfur, amino acid, and secondary metabolites. This comprehensive dataset will be useful for studying the regulation and evolution of C4-specific and related genes.
2012-09-18 | E-MTAB-4320 | biostudies-arrayexpress
Project description:Transcriptome analysis of Dunaliella viridis in response to changes in light duration and temperature
2015-04-27 | GSE40997 | GEO
Project description:Abiotic stress is a major limitation on agricultural crop productivity and the steady rising of ambient air temperatures due to global climate change are predicted to have a negative impact on plant growth and crop yield. Plants using equipped with the C4 pathway of photosynthesis are thought to have evolved under warm and dry conditions and it is hypothesized that this biochemical and anatomical specialization serves to alleviate the cost of photorespiration at higher temperatures by saturating Rubisco with CO2. In this study Setaria viridis, an emerging C4 model grass, was grown under high temperature for two weeks (42°C as compared to 28°C). High temperature resulted in stunted growth, but surprisingly had little impact on leaf area based photosynthetic rates. Rates of dark respiration significantly increased and there were major alterations in carbon and nitrogen metabolism in the heat-stressed plants, including reduced starch levels, accumulation of soluble sugars and an increase in leaf nitrogen content. The levelsMeasurements of major phytohormones showed revealed a dramatic increase in abscisic acid in the heat-stressed plants. Leaf transcriptomics, proteomics and metabolomics analyses were carried out and mapped onto metabolic pathways of photosynthesis, respiration, carbon/nitrogen metabolism and hormone synthesis and signaling. Overall, an upregulation of a number of stress signaling pathways was observed, consistent with multiple potent signals leading to reduced plant growth. A systems model of plant response is presented based on oxidative stress, hormone and sugar signaling pathways.
2024-10-31 | GSE216993 | GEO
Project description:The photosynthetic capacity of mature leaves increases upon exposing plants to continuous or intermittent high light (HL). This is termed dynamic acclimation, which is an important determinant of plant productivity. We hypothesized that genes coding for transcription regulators (TRs), which respond rapidly (≤1h) and transiently to HL, initiate dynamic acclimation. To find such genes, a highly replicated time series transcriptomic dataset was generated from leaf 7 of low light (LL)-grown Arabidopsis thaliana plants subjected to HL for up to 6h. This revealed 3844 HL-responsive differentially expressed genes (DEGs). 49 transiently HL-induced TR DEGs were selected for Bayesian modeling, which revealed that B-BOX TRANSCRIPTION (CO) FACTOR32 (BBX32) was the most connected gene in an inferred network. Dynamic acclimation was elicited in Arabidopsis Col-0 by exposure to daily 4h HL over 5 days. Using this procedure on over-expressing (OE) and null mutant plants, it was shown that BBX32 is a negative regulator of dynamic acclimation. The same modeling connected BBX32 to the TR gene LONG HYPOCOTYL5 (HY5), but unlike BBX32, HY5 was shown to positively regulate dynamic acclimation. The severely diminished response to daily HL of BBX32–OE/hy5 plants suggest that in wild type plants, BBX32 and HY5 exert a balanced, flexible and complete regulation of dynamic acclimation.
2018-08-03 | GSE78251 | GEO