Was low CO2 a driving force of C4 evolution: Arabidopsis responses to long-term low CO2 stress.
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ABSTRACT:
SUBMITTER: Li Y
PROVIDER: S-EPMC4085967 | biostudies-literature |
REPOSITORIES: biostudies-literature
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Project description:BACKGROUND AND AIMS:The stomatal conductance (gs) of most plant species decreases in response to elevated atmospheric CO2 concentration. This response could have a significant impact on plant water use in a future climate. However, the regulation of the CO2-induced stomatal closure response is not fully understood. Moreover, the potential genetic links between short-term (within minutes to hours) and long-term (within weeks to months) responses of gs to increased atmospheric CO2 have not been explored. METHODS:We used Arabidopsis thaliana recombinant inbred lines originating from accessions Col-0 (strong CO2 response) and C24 (weak CO2 response) to study short- and long-term controls of gs. Quantitative trait locus (QTL) mapping was used to identify loci controlling short- and long-term gs responses to elevated CO2, as well as other stomata-related traits. KEY RESULTS:Short- and long-term stomatal responses to elevated CO2 were significantly correlated. Both short- and long-term responses were associated with a QTL at the end of chromosome 2. The location of this QTL was confirmed using near-isogenic lines and it was fine-mapped to a 410-kb region. The QTL did not correspond to any known gene involved in stomatal closure and had no effect on the responsiveness to abscisic acid. Additionally, we identified numerous other loci associated with stomatal regulation. CONCLUSIONS:We identified and confirmed the effect of a strong QTL corresponding to a yet unknown regulator of stomatal closure in response to elevated CO2 concentration. The correlation between short- and long-term stomatal CO2 responses and the genetic link between these traits highlight the importance of understanding guard cell CO2 signalling to predict and manipulate plant water use in a world with increasing atmospheric CO2 concentration. This study demonstrates the power of using natural variation to unravel the genetic regulation of complex traits.
| S-EPMC7304471 | biostudies-literature
Project description:Physiological and molecular evidences have shown earlier that low CO2 might have been a major driving force during the evolution of C4 photosynthesis, not only being a selection pressure but also as a signaling agent. However, a mechanistic linkage between low CO2 and C4 emergence is missing. In this study, using transcriptomics study in model plant Arabidopsis thaliana, we demonstrated that under long-term low CO2 treatments, the up-regulation of C4 related genes were linked to the up-regulation of genes involved in photorespiration, nitrogen assimilation and glycolysis. Plants under low CO2 also showed altered d13C. The carbonic anhydrase (CA), phosphoenolpyruvate carboxylase (PEPC), malate dehydrogenase (MDH), glutamine oxoglutarate aminotransferase (GS-GOGAT), which are required to reassimilate ammonia, were up-regulated under low CO2. Furthermore, under low CO2, genes involved in PEP regeneration from glycolysis were up-regulated while pyruvate orthophosphate dikinase (PPDK) was down-regulated, suggesting a route of PEP regeneration from glycolysis. All these results suggested that under long-term low CO2 treatment, the selection pressure to recapture the released ammonia from the increased photorespiration might have promoted the evolution of mechanisms for generation PEP from glycolysis and enhancement of enzymes catalyzing formation of oxaloacetate, one intermediate which can accept ammonia residue. These adjustments in metabolism provide a mechanistic linkage between low CO2 and evolution of C4 photosynthesis.
2016-12-31 | GSE64547 | GEO
Project description:Physiological response and transcriptome changes were observed to investigate the effects on the growth, metabolism and genetic changes of Pinus densiflora grown for a long time in an environment with an elevated atmospheric CO2 concentration. Pine trees were grown at ambient (400 ppm) and elevated (560 ppm and 720 ppm) CO2 concentrations for 10 years in open-top chambers. The content of nonstructural carbohydrates was significantly increased in elevated CO2. It was notable that the contents of chlorophylls significantly decreased at an elevated CO2. The activities of antioxidants were significantly increased at an elevated CO2 concentration of 720 ppm. We analyzed the differences in the transcriptomes of Pinus densiflora at ambient and elevated CO2 concentrations and elucidated the functions of the differentially expressed genes (DEGs). RNA-Seq analysis identified 2415 and 4462 DEGs between an ambient and elevated CO2 concentrations of 560 ppm and 720 ppm, respectively. Genes related to glycolysis/gluconeogenesis and starch/sucrose metabolism were unchanged or decreased at an elevated CO2 concentration of 560 ppm and tended to increase at an elevated CO2 concentration of 720 ppm. It was confirmed that the expression levels of genes related to photosynthesis and antioxidants were increased at an elevated CO2 concentration of 720 ppm.
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Project description:In the last decades, increasingly robust experimental approaches have formally demonstrated that autoimmunity is a physiological process involved in a large range of functions including cognition. On this basis, the recently enunciated "brain superautoantigens" theory proposes that autoimmunity has been a driving force of cognitive evolution. It is notably suggested that the immune and nervous systems have somehow co-evolved and exerted a mutual selection pressure benefiting to both systems. In this two-way process, the evolutionary-determined emergence of neurons expressing specific immunogenic antigens (brain superautoantigens) has exerted a selection pressure on immune genes shaping the T-cell repertoire. Such a selection pressure on immune genes has translated into the emergence of a finely tuned autoimmune T-cell repertoire that promotes cognition. In another hand, the evolutionary-determined emergence of brain-autoreactive T-cells has exerted a selection pressure on neural genes coding for brain superautoantigens. Such a selection pressure has translated into the emergence of a neural repertoire (defined here as the whole of neurons, synapses and non-neuronal cells involved in cognitive functions) expressing brain superautoantigens. Overall, the brain superautoantigens theory suggests that cognitive evolution might have been primarily driven by internal cues rather than external environmental conditions. Importantly, while providing a unique molecular connection between neural and T-cell repertoires under physiological conditions, brain superautoantigens may also constitute an Achilles heel responsible for the particular susceptibility of Homo sapiens to "neuroimmune co-pathologies" i.e., disorders affecting both neural and T-cell repertoires. These may notably include paraneoplastic syndromes, multiple sclerosis as well as autism, schizophrenia and neurodegenerative diseases. In the context of this theoretical frame, a specific emphasis is given here to the potential evolutionary role exerted by two families of genes, namely the MHC class II genes, involved in antigen presentation to T-cells, and the Foxp genes, which play crucial roles in language (Foxp2) and the regulation of autoimmunity (Foxp3).
| S-EPMC5662758 | biostudies-literature
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
2020-07-28 | GSE146365 | GEO
Project description:C4 photosynthesis was evolved from ancestral C3 photosynthesis by recruited pre-existed genes to perform new functions. Enzymes and transporters required for C4 metabolic pathway has been well documented, however, transcriptional factors (TFs) that regulate those C4 metabolic genes is poorly understood, in particular, how the TF regulatory network of C4 metabolic genes was re-wired, and the involved metabolic functions of those TFs along the evolution of C4 photosynthesis remained unknown. Here, by using RNA-Seq data from growth condition that reported to have effect on C4 photosynthesis, we constructed the TF regulatory network for four evolutionarily closely related species in the genus Flaveria, which represent different stages of the evolution of C4 photosynthesis, namely, C3, type I C3-C4, type II C3-C4 and C4. Our results show that four TFs are conserved along the evolution whose function either relate to stress response or light response. TFs regulating C4 core genes in C3 species involved in functions belong to RNA regulation and nitrogen metabolism, and that in both intermediate species and C4 species involved in photosynthesis and light responsiveness. Moreover, the TF-network of C4 core metabolic genes has the highest network density in type I C3-C4 species and C4 species when consider the fragment of TF-regulatory network that up-regulated under low CO2, suggesting that TFs regulating C4 genes were recruited to photosynthesis at type I C3-C4 both in involved functions and network density. Our results provide a valuable resource for studying molecular regulatory mechanisms underlying C4 metabolic process.
2020-07-27 | GSE143469 | GEO
Project description:Whereas linear electron flow (LEF) in photosynthesis produces both ATP and NADPH, the cyclic electron flow (CEF) around photosystem I has been shown to produce only ATP. Two alternative routes have been shown for CEF; NAD(P)H dehydrogenase (NDH)- and ferredoxin:plastoquinone oxidoreductase (FQR)-dependent flows, but their physiological relevance has not been elucidated in detail. Meanwhile, because C(4) photosynthesis requires more ATP than does C(3) photosynthesis to concentrate CO(2), it has not been clear how the extra ATP is produced. In this study, to elucidate whether CEF contributes to the additional ATP needed in C(4) photosynthesis, we estimated the amounts of PGR5, which participates in FQR-dependent flow, and NDH-H, a subunit of NDH, in four C(4) species. Although the expression profiles of PGR5 did not correlate well with the additional ATP requirement, NDH was greatly expressed in mesophyll cells in the NAD-malic enzyme (ME) species, and in bundle-sheath cells in NADP-ME species, where there is a strong need for ATP in the respective cells. Our results indicate that CEF via NDH plays a central role in driving the CO(2)-concentrating mechanism in C(4) photosynthesis.
| S-EPMC1283823 | biostudies-literature
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: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:Mutation rate is a key determinant of the pace as well as outcome of evolution, and variability in this rate has been shown in different scenarios to play a key role in evolutionary adaptation and resistance evolution under stress caused by selective pressure. Here we investigate the dynamics of resistance fixation in a bacterial population with variable mutation rates, and we show that evolutionary outcomes are most sensitive to mutation rate variations when the population is subject to environmental and demographic conditions that suppress the evolutionary advantage of high-fitness subpopulations. By directly mapping a biophysical fitness function to the system-level dynamics of the population, we show that both low and very high, but not intermediate, levels of stress in the form of an antibiotic result in a disproportionate effect of hypermutation on resistance fixation. We demonstrate how this behavior is directly tied to the extent of genetic hitchhiking in the system, the propagation of high-mutation rate cells through association with high-fitness mutations. Our results indicate a substantial role for mutation rate flexibility in the evolution of antibiotic resistance under conditions that present a weak advantage over wildtype to resistant cells.
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