Chloroplastic photoprotective strategies differ between bundle sheath and mesophyll cells in maize (Zea mays L.) Under drought
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ABSTRACT:
SUBMITTER: Liu W
PROVIDER: S-EPMC9330506 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The biotrophic fungus Ustilago maydis causes smut disease on maize (Zea mays L.), which is characterized by immense plant tumours. To establish disease and reprogram organ primordia to tumours, U. maydis deploys effector proteins in an organ-specific manner. However, the cellular contribution to leaf tumours remains unknown. We investigated leaf tumour formation on the tissue- and cell type-specific level. Cytology and metabolite analysis were deployed to understand the cellular basis for tumourigenesis. Laser-capture microdissection was performed to gain a cell-type specific transcriptome of U. maydis during tumour formation. In-vivo visualization of plant DNA synthesis identified bundle sheath cells as the origin of hyperplasic tumour cells, while mesophyll cells become hypertrophic tumour cells. Cell type specific transcriptome profiling of U. maydis revealed tailored expression of fungal effector genes. Moreover, U. maydis See1 was identified the first cell type specific fungal effector, being required for induction of cell cycle reactivation in bundle sheath cells. Identification of distinct cellular mechanisms in two different leave cell types, and See1 as an effector for induction of proliferation of bundle-sheath cells, are major steps in understanding U. maydis-induced tumor formation. Moreover, the cell-type specific U. maydis transcriptome data is a valuable resource to the scientific community.
2018-02-13 | GSE105770 | GEO
Project description:The contents of endogenous brassinosteroids (BRs) together with various aspects of plant morphology, water management, photosynthesis and protection against cell damage were assessed in two maize genotypes that differed in their drought sensitivity. The presence of 28-norbrassinolide in rather high quantities (1-2 pg mg-1 fresh mass) in the leaves of monocot plants is reported for the first time. The intraspecific variability in the presence/content of the individual BRs in drought-stressed plants is also described for the first time. The drought-resistant genotype was characterised by a significantly higher content of total endogenous BRs (particularly typhasterol and 28-norbrassinolide) compared with the drought-sensitive genotype. On the other hand, the drought-sensitive genotype showed higher levels of 28-norcastasterone. Both genotypes also differed in the drought-induced reduction/elevation of the levels of 28-norbrassinolide, 28-norcastasterone, 28-homocastasterone and 28-homodolichosterone. The differences observed between both genotypes in the endogenous BR content are probably correlated with their different degrees of drought sensitivity, which was demonstrated at various levels of plant morphology, physiology and biochemistry.
| S-EPMC5967837 | biostudies-literature
Project description:When intact maize (Zea mays) mesophyll chloroplasts were illuminated in the presence of [32P]orthophosphate and subsequently subjected to sodium dodecyl sulphate/polyacrylamide-gel electrophoresis, a major polypeptide species of Mr 100000 was found to be heavily labelled. This polypeptide was not found in maize mesophyll thylakoid or cytoplasmic fractions, but was localized solely in the chloroplast stroma. No phosphorylation of polypeptides in the 100000-Mr region was observed in the mesophyll chloroplasts from C3 species (where the primary product of CO2 fixation is a 3-carbon compound), suggesting that this polypeptide arises from a protein associated with C4 metabolism (where the first product of CO2 fixation is a 4-carbon compound). The 100kDa polypeptide was major component of the maize mesophyll chloroplast, comprising 10-15% of the total protein, which banded in an identical position to the apoprotein of the enzyme pyruvate, orthophosphate dikinase, which catalyses a reaction of the C4 cycle [Edwards & Walker (1983) C3, C4: Mechanisms, and Cellular and Environmental Regulation, of Photosynthesis, Blackwell Scientific Publications, Oxford and London]. Phosphorylation in the 100kDa species was prohibited by treatment of lysed chloroplasts with antibody to pyruvate, orthophosphate dikinase (EC 2.7.9.1). These data suggest that the phosphorylated polypeptide observed after sodium dodecyl sulphate/polyacrylamide-gel electrophoresis is the monomeric form of this enzyme. The 100kDa polypeptide was partially phosphorylated in darkness, but a significant increase in the degree of phosphorylation was found on illumination. This polypeptide was found to be dephosphorylated only slowly when the chloroplasts were returned to darkness. Maximum phosphorylation was observed in the presence of pyruvate or dihydroxyacetone phosphate, which also caused maximum activation of pyruvate, orthophosphate dikinase. Phosphorylation of the 100kDa polypeptide did not coincide with deactivation of pyruvate, orthophosphate dikinase, but maximum phosphorylation occurred under conditions that promoted maximum activity of the enzyme, at which time one phosphate group was associated with each enzyme molecule. Protein phosphorylation did not appear to arise from the reaction mechanism of the enzyme.
| S-EPMC1144166 | biostudies-other
Project description:Chloroplasts of maize leaves differentiate into specific bundle sheath (BS) and mesophyll (M) types to accommodate C(4) photosynthesis. Chloroplasts contain thylakoid and envelope membranes that contain the photosynthetic machineries and transporters but also proteins involved in e.g. protein homeostasis. These chloroplast membranes must be specialized within each cell type to accommodate C(4) photosynthesis and regulate metabolic fluxes and activities. This quantitative study determined the differentiated state of BS and M chloroplast thylakoid and envelope membrane proteomes and their oligomeric states using innovative gel-based and mass spectrometry-based protein quantifications. This included native gels, iTRAQ, and label-free quantification using an LTQ-Orbitrap. Subunits of Photosystems I and II, the cytochrome b(6)f, and ATP synthase complexes showed average BS/M accumulation ratios of 1.6, 0.45, 1.0, and 1.33, respectively, whereas ratios for the light-harvesting complex I and II families were 1.72 and 0.68, respectively. A 1000-kDa BS-specific NAD(P)H dehydrogenase complex with associated proteins of unknown function containing more than 15 proteins was observed; we speculate that this novel complex possibly functions in inorganic carbon concentration when carboxylation rates by ribulose-bisphosphate carboxylase/oxygenase are lower than decarboxylation rates by malic enzyme. Differential accumulation of thylakoid proteases (Egy and DegP), state transition kinases (STN7,8), and Photosystem I and II assembly factors was observed, suggesting that cell-specific photosynthetic electron transport depends on post-translational regulatory mechanisms. BS/M ratios for inner envelope transporters phosphoenolpyruvate/P(i) translocator, Dit1, Dit2, and Mex1 were determined and reflect metabolic fluxes in carbon metabolism. A wide variety of hundreds of other proteins showed differential BS/M accumulation. Mass spectral information and functional annotations are available through the Plant Proteome Database. These data are integrated with previous data, resulting in a model for C(4) photosynthesis, thereby providing new rationales for metabolic engineering of C(4) pathways and targeted analysis of genetic networks that coordinate C(4) differentiation.
| S-EPMC2556027 | biostudies-literature
Project description:During Zea mays (maize) C4 differentiation, mesophyll (M) and bundle sheath (BS) cells accumulate distinct sets of photosynthetic enzymes, with very low photosystem II (PSII) content in BS chloroplasts. Consequently, there is little linear electron transport in the BS and ATP is generated by cyclic electron flow. In contrast, M thylakoids are very similar to those of C3 plants and produce the ATP and NADPH that drive metabolic activities. Regulation of this differentiation process is poorly understood but involves expression and coordination of nuclear and plastid genomes. Here, we identify a recessive allele of the maize Hcf136 homologue that in Arabidopsis thaliana functions as a PSII stability or assembly factor located in the thylakoid lumen. Proteome analysis of the thylakoids and electron microscopy reveal that Zm hcf136 lacks PSII complexes and grana thylakoids in M chloroplasts, consistent with the previously defined Arabidopsis function. Interestingly, hcf136 is also defective in processing the full-length psbB-psbT-psbH-petB-petD polycistron specifically in M chloroplasts. To determine whether the loss of PSII in M cells affects C4 differentiation, we performed cell-type specific transcript analysis of hcf136 and wild-type seedlings. The results indicate that M and BS cells respond uniquely to the loss of PSII, with little overlap in gene expression changes between data sets. These results are discussed in the context of signals that may drive differential gene expression in C4 photosynthesis. Keywords: cell type comparison
2008-02-01 | GSE9698 | GEO
Project description:Zea mays is a C4 plant that utilizes two distinct cell types, mesophyll (M) and bundle sheath (BS), to cooperatively fix carbon. Regulation of M and BS cell differentiation is poorly understood. Here, we explore the transcriptional networks of M and BS cells by microarray analysis. The maize mutant bundle sheath defective2 lacks the accumulation of Rubisco small and large subunits (Roth et al 1996; Brutnell et al 1999) and cannot perform the Calvin Cycle (Smith et al 1998). Therefore, this mutant provides an opportunity to study M and BS cell differentiation in a perturbed BS background, potentially revealing regulons important to cell identity. M and BS cells were independently isolated from mutant and wild-type siblings. Transcriptional profiling was then performed in a cell specific manner between mutant and wild-type.
2018-04-30 | GSE13758 | GEO
Project description:During Zea mays (maize) C4 differentiation, mesophyll (M) and bundle sheath (BS) cells accumulate distinct sets of photosynthetic enzymes, with very low photosystem II (PSII) content in BS chloroplasts. Consequently, there is little linear electron transport in the BS and ATP is generated by cyclic electron flow. In contrast, M thylakoids are very similar to those of C3 plants and produce the ATP and NADPH that drive metabolic activities. Regulation of this differentiation process is poorly understood but involves expression and coordination of nuclear and plastid genomes. Here, we identify a recessive allele of the maize Hcf136 homologue that in Arabidopsis thaliana functions as a PSII stability or assembly factor located in the thylakoid lumen. Proteome analysis of the thylakoids and electron microscopy reveal that Zm hcf136 lacks PSII complexes and grana thylakoids in M chloroplasts, consistent with the previously defined Arabidopsis function. Interestingly, hcf136 is also defective in processing the full-length psbB-psbT-psbH-petB-petD polycistron specifically in M chloroplasts. To determine whether the loss of PSII in M cells affects C4 differentiation, we performed cell-type specific transcript analysis of hcf136 and wild-type seedlings. The results indicate that M and BS cells respond uniquely to the loss of PSII, with little overlap in gene expression changes between data sets. These results are discussed in the context of signals that may drive differential gene expression in C4 photosynthesis. To explore the disruption of PSII activity on gene expression, transcript profiles from separated M and BS cells were examined using two-label microarray analysis. Total RNA was isolated from the second leaves of mutant and wild-type silbings. Six biological replicates were used to compare wild-type and mutant transcript profiles in separate M and BS experiments. To maximize biological replication, different seedling pools were used for each of the 12 hybridizations. Microarray experiments and analyses were performed using the Genisphere MPX900 kit and the Maize Array Consortium oligonucleotide platform (GPL5439; GPL5440). Feature intensity values were log-transformed and corrected for local background signal, and a LOWESS procedure (Dudoit et al., 2002) was used to normalize between channels. Features with either low or saturating signal intensity were discarded from further analysis. High expression filtering was less stringent to avoid elimination of previously characterized, high abundance, C4 cell-specific transcripts. After filtering, features that were not assigned an MZ number by the Maize Array Consortium were discarded from further analysis. The moderated t-test (Smyth, 2004) using the R package limma was applied to identify differentially expressed genes. The p-values for each test (gene) were converted to q-values for false discovery rate analysis as described by Storey et al. (2004). To avoid confounding treatment effects associated with direct comparisons of M and BS transcriptomes (Sawers et al., 2007), comparisons were only made using the same cell type across the hcf136 and wild-type sibling genotypes. Bundle sheath (BS) Samples: GSM245063-GSM245164 Mesophyll (M) Samples: GSM245165 - GSM245206
2008-01-31 | E-GEOD-9698 | biostudies-arrayexpress
Project description:Invertases (INVs) play essential roles in plant growth in response to environmental cues. Previous work showed that plant invertases can be post-translationally regulated by small protein inhibitors (INVINHs). Here, this study characterizes a proteinaceous inhibitor of INVs in maize (Zm-INVINH4). A functional analysis of the recombinant Zm-INVINH4 protein revealed that it inhibited both cell wall and vacuolar invertase activities from maize leaves. A Zm-INVINH4::green fluorescent protein fusion experiment indicated that this protein localized in the apoplast. Transcript analysis showed that Zm-INVINH4 is specifically expressed in maize sink tissues, such as the base part of the leaves and young kernels. Moreover, drought stress perturbation significantly induced Zm-INVINH4 expression, which was accompanied with a decrease of cell wall invertase (CWI) activities and an increase of sucrose accumulation in both base parts of the leaves 2 to 7 days after pollinated kernels. In summary, the results support the hypothesis that INV-related sink growth in response to drought treatment is (partially) caused by a silencing of INV activity via drought-induced induction of Zm-INVINH4 protein.
| S-EPMC6747265 | biostudies-literature
Project description:Drought severity and duration are expected to increase as a result of ongoing global climate change. Therefore, finding solutions to help plants to deal with drought stress and to improve growth in the face of limited water resources is critical. In this study, a drought tolerant- plant growth promoting endophytic bacterium was isolated from Aloe vera roots. It was identified as Sphingobacterium changzhouense based on 16S rRNA gene sequencing and was deposited into NCBI database with accession number (ON944028). The effect of S. changzhouense inoculation on maize growth under drought stress was investigated. The results revealed that inoculation significantly (p ≤ 0.05) enhanced root and shoot elongation by 205 and 176.19% respectively. Photosynthesis rate, stomatal conductance and water use efficiency were improved in inoculated plants. interestingly, inoculation resulted in significant increase in total chlorophyll, total carbohydrates, proline, total proteins, total phenolics and total flavonoids by 64, 31.5, 25.1, 75.07, 83.7 and 65.4% respectively. Total antioxidant capacity of inoculated plants (51.2 mg/g FW) was higher than that of non-inoculated plants (11.87 mg/g FW), which was found to be positively correlated to the levels of phenolics and flavonoids. Our finding suggests that S. changzhouense could be used to improve crop growth and assist plants to resist drought stress in arid agricultural lands.
| S-EPMC9616765 | biostudies-literature
Project description:The high efficiency of C4 photosynthesis relies on spatial division of labor, classically with initial carbon fixation in the mesophyll and carbon reduction in the bundle sheath. By employing grinding and serial filtration over liquid nitrogen, we enriched C4 tissues along a developing leaf gradient. This method treats both C4 tissues in an integrity-preserving and consistent manner, while allowing complementary measurements of metabolite abundance and enzyme activity, thus providing a comprehensive data set. Meta-analysis of this and the previous studies highlights the strengths and weaknesses of different C4 tissue separation techniques. While the method reported here achieves the least enrichment, it is the only one that shows neither strong 3' (degradation) bias, nor different severity of 3' bias between samples. The meta-analysis highlighted previously unappreciated observations, such as an accumulation of evidence that aspartate aminotransferase is more mesophyll specific than expected from the current NADP-ME C4 cycle model, and a shift in enrichment of protein synthesis genes from bundle sheath to mesophyll during development. The full comparative dataset is available for download, and a web visualization tool (available at http://www.plant-biochemistry.hhu.de/resources.html) facilitates comparison of the the Z. mays bundle sheath and mesophyll studies, their consistencies and their conflicts.
| S-EPMC5853576 | biostudies-literature