Multiple mechanisms for enhanced plasmodesmata density in disparate subtypes of C4 grasses.
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ABSTRACT:
SUBMITTER: Danila FR
PROVIDER: S-EPMC6018992 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:In plants, an oligogene family encodes NADP-malic enzymes (NADP-me), which are responsible for various functions and exhibit different kinetics and expression patterns. In particular, a chloroplast isoform of NADP-me plays a key role in one of the three biochemical subtypes of C(4) photosynthesis, an adaptation to warm environments that evolved several times independently during angiosperm diversification. By combining genomic and phylogenetic approaches, this study aimed at identifying the molecular mechanisms linked to the recurrent evolutions of C(4)-specific NADP-me in grasses (Poaceae). Genes encoding NADP-me (nadpme) were retrieved from genomes of model grasses and isolated from a large sample of C(3) and C(4) grasses. Genomic and phylogenetic analyses showed that 1) the grass nadpme gene family is composed of four main lineages, one of which is expressed in plastids (nadpme-IV), 2) C(4)-specific NADP-me evolved at least five times independently from nadpme-IV, and 3) some codons driven by positive selection underwent parallel changes during the multiple C(4) origins. The C(4) NADP-me being expressed in chloroplasts probably constrained its recurrent evolutions from the only plastid nadpme lineage and this common starting point limited the number of evolutionary paths toward a C(4) optimized enzyme, resulting in genetic convergence. In light of the history of nadpme genes, an evolutionary scenario of the C(4) phenotype using NADP-me is discussed.
| S-EPMC2817415 | biostudies-literature
Project description:Most physiology comparisons of C3 and C4 plants are made under current or elevated concentrations of atmospheric CO2 which do not reflect the low CO2 environment under which C4 photosynthesis has evolved. Accordingly, photosynthetic nitrogen (PNUE) and water (PWUE) use efficiency, and the activity of the photosynthetic carboxylases [Rubisco and phosphoenolpyruvate carboxylase (PEPC)] and decarboxylases [NADP-malic enzyme (NADP-ME) and phosphoenolpyruvate carboxykinase (PEP-CK)] were compared in eight C4 grasses with NAD-ME, PCK, and NADP-ME subtypes, one C3 grass, and one C3-C4 grass grown under ambient (400 μl l(-1)) and glacial (180 μl l(-1)) CO2. Glacial CO2 caused a smaller reduction of photosynthesis and a greater increase of stomatal conductance in C4 relative to C3 and C3-C4 species. Panicum bisulcatum (C3) acclimated to glacial [CO2] by doubling Rubisco activity, while Rubisco was unchanged in Panicum milioides (C3-C4), possibly due to its high leaf N and Rubisco contents. Glacial CO2 up-regulated Rubisco and PEPC activities in concert for several C4 grasses, while NADP-ME and PEP-CK activities were unchanged, reflecting the high control exerted by the carboxylases relative to the decarboxylases on the efficiency of C4 metabolism. Despite having larger stomatal conductance at glacial CO2, C4 species maintained greater PWUE and PNUE relative to C3-C4 and C3 species due to higher photosynthetic rates. Relative to other C4 subtypes, NAD-ME and PEP-CK grasses had the highest PWUE and PNUE, respectively; relative to C3, the C3-C4 grass had higher PWUE and similar PNUE at glacial CO2. Biomass accumulation was reduced by glacial CO2 in the C3 grass relative to the C3-C4 grass, while biomass was less reduced in NAD-ME grasses compared with NADP-ME and PCK grasses. Under glacial CO2, high resource use efficiency offers a key evolutionary advantage for the transition from C3 to C4 photosynthesis in water- and nutrient-limited environments.
| S-EPMC4085965 | biostudies-literature
Project description:Investigating the cis-Regulatory Basis of C3 and C4 Photosynthesis in Grasses at Single-Cell Resolution
| PRJNA1062455 | ENA
Project description:Grasses using the C(4) photosynthetic pathway dominate grasslands and savannahs of warm regions, and account for half of the species in this ecologically and economically important plant family. The C(4) pathway increases the potential for high rates of photosynthesis, particularly at high irradiance, and raises water-use efficiency compared with the C(3) type. It is therefore classically viewed as an adaptation to open, arid conditions. Here, we test this adaptive hypothesis using the comparative method, analysing habitat data for 117 genera of grasses, representing 15 C(4) lineages. The evidence from our three complementary analyses is consistent with the hypothesis that evolutionary selection for C(4) photosynthesis requires open environments, but we find an equal likelihood of C(4) evolutionary origins in mesic, arid and saline habitats. However, once the pathway has arisen, evolutionary transitions into arid habitats occur at higher rates in C(4) than C(3) clades. Extant C(4) genera therefore occupy a wider range of drier habitats than their C(3) counterparts because the C(4) pathway represents a pre-adaptation to arid conditions. Our analyses warn against evolutionary inferences based solely upon the high occurrence of extant C(4) species in dry habitats, and provide a novel interpretation of this classic ecological association.
| S-EPMC2674487 | biostudies-literature
Project description:Grasslands cover more than 20% of the Earth's terrestrial surface, and their rise to dominance is one of the most dramatic events of biome evolution in Earth history. Grasses possess two main photosynthetic pathways: the C(3) pathway that is typical of most plants and a specialized C(4) pathway that minimizes photorespiration and thus increases photosynthetic performance in high-temperature and/or low-CO(2) environments. C(4) grasses dominate tropical and subtropical grasslands and savannas, and C(3) grasses dominate the world's cooler temperate grassland regions. This striking pattern has been attributed to C(4) physiology, with the implication that the evolution of the pathway enabled C(4) grasses to persist in warmer climates than their C(3) relatives. We combined geospatial and molecular sequence data from two public archives to produce a 1,230-taxon phylogeny of the grasses with accompanying climate data for all species, extracted from more than 1.1 million herbarium specimens. Here we show that grasses are ancestrally a warm-adapted clade and that C(4) evolution was not correlated with shifts between temperate and tropical biomes. Instead, 18 of 20 inferred C(4) origins were correlated with marked reductions in mean annual precipitation. These changes are consistent with a shift out of tropical forest environments and into tropical woodland/savanna systems. We conclude that C(4) evolution in grasses coincided largely with migration out of the understory and into open-canopy environments. Furthermore, we argue that the evolution of cold tolerance in certain C(3) lineages is an overlooked innovation that has profoundly influenced the patterning of grassland communities across the globe.
| S-EPMC2823882 | biostudies-literature
Project description:BACKGROUND:Sorghum is the first C4 plant and the second grass with a full genome sequence available. This makes it possible to perform a whole-genome-level exploration of C4 pathway evolution by comparing key photosynthetic enzyme genes in sorghum, maize (C4) and rice (C3), and to investigate a long-standing hypothesis that a reservoir of duplicated genes is a prerequisite for the evolution of C4 photosynthesis from a C3 progenitor. RESULTS:We show that both whole-genome and individual gene duplication have contributed to the evolution of C4 photosynthesis. The C4 gene isoforms show differential duplicability, with some C4 genes being recruited from whole genome duplication duplicates by multiple modes of functional innovation. The sorghum and maize carbonic anhydrase genes display a novel mode of new gene formation, with recursive tandem duplication and gene fusion accompanied by adaptive evolution to produce C4 genes with one to three functional units. Other C4 enzymes in sorghum and maize also show evidence of adaptive evolution, though differing in level and mode. Intriguingly, a phosphoenolpyruvate carboxylase gene in the C3 plant rice has also been evolving rapidly and shows evidence of adaptive evolution, although lacking key mutations that are characteristic of C4 metabolism. We also found evidence that both gene redundancy and alternative splicing may have sheltered the evolution of new function. CONCLUSIONS:Gene duplication followed by functional innovation is common to evolution of most but not all C4 genes. The apparently long time-lag between the availability of duplicates for recruitment into C4 and the appearance of C4 grasses, together with the heterogeneity of origins of C4 genes, suggests that there may have been a long transition process before the establishment of C4 photosynthesis.
| S-EPMC2718502 | biostudies-literature
Project description:C(4) photosynthesis is a series of anatomical and biochemical modifications to the typical C(3) pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C(4) origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C(4) evolvability in certain phylogenetic groups. The C(4) trait has evolved 22-24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C(3) taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C(4) evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C(4) evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C(4) origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C(3) context and preceding the emergence of the C(4) syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.
| S-EPMC3557070 | biostudies-literature
Project description: Not available
| S-EPMC4947885 | biostudies-literature
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:C4 photosynthesis has independently evolved over 62 times within 19 angiosperm families. The recurrent evolution of C4 photosynthesis appears to contradict the complex anatomical and biochemical modifications required for the transition from C3 to C4 photosynthesis. In this study, we conducted an integrated analysis of genomics and transcriptomics to elucidate the molecular underpinnings of convergent C4 evolution in the grass family. Our genome-wide exploration of C4-related gene families suggests that the expansion of these gene families may have played an important role in facilitating C4 evolution in the grass family. A phylogenomic synteny network analysis uncovered the emergence of C4 genes in various C4 grass lineages from a common ancestral gene pool. Moreover, through a comparison between non-C4 and C4 PEPCs, we pinpointed 14 amino acid sites exhibiting parallel adaptations. These adaptations, occurring post the BEP-PACMAD divergence, shed light on why all C4 origins in grasses are confined to the PACMAD clade. Furthermore, our study revealed that the ancestor of Chloridoideae grasses possessed a more favorable molecular preadaptation for C4 functions compared to the ancestor of Panicoideae grasses. This molecular preadaptation potentially explains why C4 photosynthesis evolved earlier in Chloridoideae than in Panicoideae and why the C3-to-C4 transition occurred once in Chloridoideae but multiple times in Panicoideae. Additionally, we found that C4 genes share similar cis-elements across independent C4 lineages. Notably, NAD-ME subtype grasses may have retained the ancestral regulatory machinery of the C4 NADP-ME gene, while NADP-ME subtype grasses might have undergone unique cis-element modifications.
| S-EPMC11319937 | biostudies-literature