Developmental dynamics of Kranz cell transcriptional specificity in maize leaf reveals early onset of C4-related processes.
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ABSTRACT:
SUBMITTER: Tausta SL
PROVIDER: S-EPMC4085964 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:The comparison of the cell-specific transcriptomes of bundle sheath (BS) and mesophyll (M) cells from successive developmental stages of maize leafs reveals that the number of genes preferentially transcribed in one cell type or the other varies considerably from the sink-source transition to mature photosynthetic stages. The number of differentially expressed (DE) genes is maximal at a stage well prior to full maturity, including those that encode key functions for C4 photosynthesis. The developmental dynamics of BS/M differential expression can be used to identify candidates for other C4-related functions and to simplify the identification of specific pathways members from otherwise complex gene families. The candidates for C4-related transcription factors identified with this developmental DE strategy overlap with those identified in studies using alternative strategies.
2014-05-18 | GSE54272 | GEO
Project description:The comparison of the cell-specific transcriptomes of bundle sheath (BS) and mesophyll (M) cells from successive developmental stages of maize leafs reveals that the number of genes preferentially transcribed in one cell type or the other varies considerably from the sink-source transition to mature photosynthetic stages. The number of differentially expressed (DE) genes is maximal at a stage well prior to full maturity, including those that encode key functions for C4 photosynthesis. The developmental dynamics of BS/M differential expression can be used to identify candidates for other C4-related functions and to simplify the identification of specific pathways members from otherwise complex gene families. The candidates for C4-related transcription factors identified with this developmental DE strategy overlap with those identified in studies using alternative strategies. Nine day old third leaves of maize sections, located at -1 cm, +4 cm and +9 cm (leaf tip), relative to the sink-source transition, were collected. BS and M cells were captured from each section. There are two duplications for each section and each cell types. A total of 12 libraries were constructed for RNA-seq.
2014-05-18 | E-GEOD-54272 | biostudies-arrayexpress
Project description:In family Cleomaceae there are NAD-malic enzyme-type C4 species having different forms of leaf anatomy. Leaves of Cleome angustifolia have Glossocardioid-type anatomy with a single complex Kranz unit which surrounds all the veins, while C. gynandra has Atriplicoid anatomy with multiple Kranz units, each surrounding an individual vein. Biochemical and ultrastructural differentiation of mesophyll (M) and bundle sheath (BS) cells were studied along a developmental gradient, from the leaf base (youngest) to the tip (mature). Initially, there is cell-specific expression of certain photosynthetic enzymes, which subsequently increase along with structural differentiation. At the base of the leaf, following division of ground tissue to form M and BS cells which are structurally similar, there is selective localization of Rubisco and glycine decarboxylase to BS cells. Thus, a biochemical C3 default stage, with Rubisco expression in both cell types, does not occur. Additionally, phosphoenolpyruvate carboxylase (PEPC) is selectively expressed in M cells near the base. Surprisingly, in both species, an additional layer of spongy M cells on the abaxial side of the leaf has the same differentiation with PEPC, even though it is not in contact with BS cells. During development along the longitudinal gradient there is structural differentiation of the cells, chloroplasts, and mitochondria, resulting in complete formation of Kranz anatomy. In both species, development of the C4 system occurs similarly, irrespective of having very different types of Kranz anatomy, different ontogenetic origins of BS and M, and independent evolutionary origins of C4 photosynthesis.
| S-EPMC4085953 | biostudies-literature
Project description:In subfamily Suaedoideae, four independent gains of C4 photosynthesis are proposed, which includes two parallel origins of Kranz anatomy (sections Salsina and Schoberia) and two independent origins of single-cell C4 anatomy (Bienertia and Suaeda aralocaspica). Additional phylogenetic support for this hypothesis was generated from sequence data of the C-terminal portion of the phosphoenolpyruvate carboxylase (PEPC) gene used in C4 photosynthesis (ppc-1) in combination with previous sequence data. ppc-1 sequence was generated for 20 species in Suaedoideae and two outgroup Salsola species that included all types of C4 anatomies as well as two types of C3 anatomies. A branch-site test for positively selected codons was performed using the software package PAML. From labelling of the four branches where C4 is hypothesized to have developed (foreground branches), residue 733 (maize numbering) was identified to be under positive selection with a posterior probability >0.99 and residue 868 at the >0.95 interval using Bayes empirical Bayes (BEB). When labelling all the branches within C4 clades, the branch-site test identified 13 codons to be under selection with a posterior probability >0.95 by BEB; this is discussed considering current information on functional residues. The signature C4 substitution of an alanine for a serine at position 780 in the C-terminal end (which is considered a major determinant of affinity for PEP) was only found in four of the C4 species sampled, while eight of the C4 species and all the C3 species have an alanine residue; indicating that this substitution is not a requirement for C4 function.
| S-EPMC4085955 | biostudies-literature
Project description:Photosynthesis underpins the viability of most ecosystems, with C4 plants that exhibit âKranzâ anatomy being the most efficient primary producers. Kranz anatomy is characterized by closely spaced veins that are encircled by two morphologically distinct photosynthetic cell types. Although Kranz anatomy evolved multiple times, the underlying genetic mechanisms remain largely elusive, with only the maize scarecrow gene so far implicated in Kranz patterning. To provide a broader insight into the regulation of Kranz differentiation, we performed a genome-wide comparative analysis of developmental trajectories in Kranz (foliar leaf blade) and non-Kranz (husk leaf sheath) leaves of the C4 plant maize. Using profile classification of gene expression in early leaf primordia, we identified cohorts of genes associated with procambium initiation and vascular patterning. In addition, we used supervised classification criteria inferred from anatomical and developmental analyses of five developmental stages to identify candidate regulators of cell-type specification. Our analysis supports the suggestion that Kranz anatomy is patterned, at least in part, by a SCARECROW/SHORTROOT regulatory network, and suggests likely components of that network. Furthermore, the data imply a role for additional pathways in the development of Kranz leaves.
2013-07-29 | E-MTAB-4134 | biostudies-arrayexpress
Project description:Portulacaceae is a family that has considerable diversity in photosynthetic phenotypes. It is one of 19 families of terrestrial plants where species having C4 photosynthesis have been found. Most species in Portulaca are in the alternate-leaved (AL) lineage, which includes one clade (Cryptopetala) with taxa lacking C4 photosynthesis and three clades having C4 species (Oleracea, Umbraticola and Pilosa). All three species in the Cryptopetala clade lack Kranz anatomy, the leaves have C3-like carbon isotope composition and they have low levels of C4 cycle enzymes. Anatomical, biochemical and physiological analyses show they are all C3-C4 intermediates. They have intermediate CO2 compensation points, enrichment of organelles in the centripetal position in bundle sheath (BS) cells, with selective localization of glycine decarboxylase in BS mitochondria. In the three C4 clades there are differences in Kranz anatomy types and form of malic enzyme (ME) reported to function in C4 (NAD-ME versus NADP-ME): Oleracea (Atriplicoid, NAD-ME), Umbraticola (Atriplicoid, NADP-ME) and Pilosa (Pilosoid, NADP-ME). Structural and biochemical analyses were performed on Pilosa clade representatives having Pilosoid-type leaf anatomy with Kranz tissue enclosing individual peripheral vascular bundles and water storage in the center of the leaf. In this clade, all species except P. elatior are NADP-ME-type C4 species with grana-deficient BS chloroplasts and grana-enriched M chloroplasts. Surprisingly, P. elatior has BS chloroplasts enriched in grana and NAD-ME-type photosynthesis. The results suggest photosynthetic phenotypes were probably derived from an ancestor with NADP-ME-type C4, with two independent switches to NAD-ME type.
| S-EPMC5853368 | biostudies-literature
Project description:C4 plants exhibit significantly higher photosynthetic, water and nutrient use efficiency compared with C3 plants. Kranz anatomy is associated with many C4 plants in which bundle sheath cells surround the veins and are themselves surrounded by mesophyll cells. This specialized Kranz anatomy is elucidated as an important contributor to C4 photosynthetic activities in C4 plant. Characterizing the molecular basis of Kranz structure formation has become a key objective for studies of C4 photosynthesis. However, severe mutants that specifically disrupt Kranz anatomy have not been identified. In this study, we detected 549 stable ethyl methane sulfonate-induced foxtail millet (cultivar Yugu1) mutants related to leaf development and photosynthesis among 2,709 mutants screened (M3/M4 generation). The identified mutants included 52 that had abnormal leaf veins (with abnormal starch accumulation based on iodine staining). Each of the 52 mutants was characterized through an analysis of leaf morphology, and through microscopic observations of leaf tissue sections embedded in resin and paraffin. In total, 14 mutants were identified with abnormal Kranz structures exemplified by small bundle sheath cell size. Additional phenotypes of the mutants included poorly differentiated mesophyll and bundle sheath cells, increased vein density and the absence of chloroplasts in the bundle sheath cells. Kranz structure mutations were accompanied by varying leaf thickness, implying these mutations induced complex effects. We identified mutations related to Kranz structure development in this trial, which may be useful for the mapping and cloning of genes responsible for mediating Kranz structure development.
| S-EPMC6246719 | biostudies-literature
Project description:Leaf senescence is an important biological process that contributes to grain yield in crops. To study the molecular mechanisms underlying natural leaf senescence, we harvested three different developmental ear leaves of maize, mature leaves (ML), early senescent leaves (ESL), and later senescent leaves (LSL), and analyzed transcriptional changes using RNA-sequencing. Three sets of data, ESL vs. ML, LSL vs. ML, and LSL vs. ESL, were compared, respectively. In total, 4,552 genes were identified as differentially expressed. Functional classification placed these genes into 18 categories including protein metabolism, transporters, and signal transduction. At the early stage of leaf senescence, genes involved in aromatic amino acids (AAAs) biosynthetic process and transport, cellular polysaccharide biosynthetic process, and the cell wall macromolecule catabolic process, were up-regulated. Whereas, genes involved in amino acid metabolism, transport, apoptosis, and response to stimulus were up-regulated at the late stage of leaf senescence. Further analyses reveals that the transport-related genes at the early stage of leaf senescence potentially take part in enzyme and amino acid transport and the genes upregulated at the late stage are involved in sugar transport, indicating nutrient recycling mainly takes place at the late stage of leaf senescence. Comparison between the data of natural leaf senescence in this study and previously reported data for Arabidopsis implies that the mechanisms of leaf senescence in maize are basically similar to those in Arabidopsis. A comparison of natural and induced leaf senescence in maize was performed. Athough many basic biological processes involved in senescence occur in both types of leaf senescence, 78.07% of differentially expressed genes in natural leaf senescence were not identifiable in induced leaf senescence, suggesting that differences in gene regulatory network may exist between these two leaf senescence programs. Thus, this study provides important information for understanding the mechanism of leaf senescence in maize.
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Project description:Information about the extra- or intracellular environment is often captured as biochemical signals that propagate through regulatory networks. These signals eventually drive phenotypic changes, typically by altering gene expression programmes in the cell. Reconstruction of transcriptional regulatory networks has given a compelling picture of bacterial physiology, but transcriptional network maps alone often fail to describe phenotypes. Cellular response dynamics are ultimately determined by interactions between transcriptional and non-transcriptional networks, with dramatic implications for physiology and evolution. Here, we provide an overview of non-transcriptional interactions that can affect the performance of natural and synthetic bacterial regulatory networks.
| S-EPMC3755963 | biostudies-literature
Project description:C4 photosynthesis allows highly efficient carbon fixation that originates from tightly regulated anatomical and biochemical modifications of leaf architecture. Recent studies showed that leaf transcriptome modifications during leaf ontogeny of closely related C3 (Tarenaya hassleriana) and C4 (Gynandropsis gynandra) species within the Cleomaceae family existed but they did not identify any dedicated transcriptional networks or factors specifically driving C4 leaf ontogeny. RNAseq analysis provides a steady-state quantification of whole-cell mRNAs but does not allow any discrimination between transcriptional and post-transcriptional processes that may occur simultaneously during leaf ontogeny. Here we use exon-intron split analysis (EISA) to determine the extent to which transcriptional and post-transcriptional processes are involved in the regulation of gene expression between young and expanded leaves in both species. C4-specific changes in post-transcriptional regulation were observed for genes involved in the Calvin-Benson cycle and some photosystem components but not for C4 core-cycle genes. Overall, this study provides an unbiased genome-wide insight into the post-transcriptional mechanisms that regulate gene expression through the control of mRNA levels and could be central to the onset of C4 photosynthesis. This mechanism is cytosolic which implies cell-specific modifications of mRNA stability. Understanding this mechanism may be crucial when aiming to transform C3 crops into C4 crops.
| S-EPMC5853474 | biostudies-literature