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1.
Plant Cell ; 35(5): 1334-1359, 2023 04 20.
Article in English | MEDLINE | ID: mdl-36691724

ABSTRACT

Gynandropsis gynandra (Cleomaceae) is a cosmopolitan leafy vegetable and medicinal plant, which has also been used as a model to study C4 photosynthesis due to its evolutionary proximity to C3 Arabidopsis (Arabidopsis thaliana). Here, we present the genome sequence of G. gynandra, anchored onto 17 main pseudomolecules with a total length of 740 Mb, an N50 of 42 Mb and 30,933 well-supported gene models. The G. gynandra genome and previously released genomes of C3 relatives in the Cleomaceae and Brassicaceae make an excellent model for studying the role of genome evolution in the transition from C3 to C4 photosynthesis. Our analyses revealed that G. gynandra and its C3 relative Tarenaya hassleriana shared a whole-genome duplication event (Gg-α), then an addition of a third genome (Th-α, +1×) took place in T. hassleriana but not in G. gynandra. Analysis of syntenic copy number of C4 photosynthesis-related gene families indicates that G. gynandra generally retained more duplicated copies of these genes than C3T. hassleriana, and also that the G. gynandra C4 genes might have been under positive selection pressure. Both whole-genome and single-gene duplication were found to contribute to the expansion of the aforementioned gene families in G. gynandra. Collectively, this study enhances our understanding of the polyploidy history, gene duplication and retention, as well as their impact on the evolution of C4 photosynthesis in Cleomaceae.


Subject(s)
Arabidopsis , Brassicaceae , Magnoliopsida , Gene Duplication , Magnoliopsida/genetics , Brassicaceae/genetics , Arabidopsis/genetics , Photosynthesis/genetics , Evolution, Molecular
2.
New Phytol ; 225(3): 1383-1396, 2020 02.
Article in English | MEDLINE | ID: mdl-31550387

ABSTRACT

Nodulin 26-like intrinsic proteins (NIPs) play essential roles in transporting the nutrients silicon and boron in seed plants, but the evolutionary origin of this transport function and the co-permeability to toxic arsenic remains enigmatic. Horizontal gene transfer of a yet uncharacterised bacterial AqpN-aquaporin group was the starting-point for plant NIP evolution. We combined intense sequence, phylogenetic and genetic context analyses and a mutational approach with various transport assays in oocytes and plants to resolve the transorganismal and functional evolution of bacterial and algal and terrestrial plant NIPs and to reveal their molecular transport specificity features. We discovered that aqpN genes are prevalently located in arsenic resistance operons of various prokaryotic phyla. We provided genetic and functional evidence that these proteins contribute to the arsenic detoxification machinery. We identified NIPs with the ancestral bacterial AqpN selectivity filter composition in algae, liverworts, moss, hornworts and ferns and demonstrated that these archetype plant NIPs and their prokaryotic progenitors are almost impermeable to water and silicon but transport arsenic and boron. With a mutational approach, we demonstrated that during evolution, ancestral NIP selectivity shifted to allow subfunctionalisations. Together, our data provided evidence that evolution converted bacterial arsenic efflux channels into essential seed plant nutrient transporters.


Subject(s)
Arsenic/metabolism , Evolution, Molecular , Membrane Proteins/genetics , Nitrogen/metabolism , Phosphorus/metabolism , Plant Proteins/genetics , Plants/metabolism , Animals , Aquaporins/metabolism , Bacteria/metabolism , Biodegradation, Environmental , Biological Transport , Boric Acids/metabolism , Boron/metabolism , Bryophyta/metabolism , Cell Membrane/metabolism , Diffusion , Metalloids/metabolism , Mutation/genetics , Oocytes/metabolism , Phenotype , Phylogeny , Recombinant Fusion Proteins/metabolism , Silicic Acid/metabolism , Water/metabolism , Xenopus/metabolism
3.
BMC Genomics ; 14: 442, 2013 Jul 03.
Article in English | MEDLINE | ID: mdl-23822863

ABSTRACT

BACKGROUND: Abiotic stress causes disturbances in the cellular homeostasis. Re-adjustment of balance in carbon, nitrogen and phosphorus metabolism therefore plays a central role in stress adaptation. However, it is currently unknown which parts of the primary cell metabolism follow common patterns under different stress conditions and which represent specific responses. RESULTS: To address these questions, changes in transcriptome, metabolome and ionome were analyzed in maize source leaves from plants suffering low temperature, low nitrogen (N) and low phosphorus (P) stress. The selection of maize as study object provided data directly from an important crop species and the so far underexplored C4 metabolism. Growth retardation was comparable under all tested stress conditions. The only primary metabolic pathway responding similar to all stresses was nitrate assimilation, which was down-regulated. The largest group of commonly regulated transcripts followed the expression pattern: down under low temperature and low N, but up under low P. Several members of this transcript cluster could be connected to P metabolism and correlated negatively to different phosphate concentration in the leaf tissue. Accumulation of starch under low temperature and low N stress, but decrease in starch levels under low P conditions indicated that only low P treated leaves suffered carbon starvation. CONCLUSIONS: Maize employs very different strategies to manage N and P metabolism under stress. While nitrate assimilation was regulated depending on demand by growth processes, phosphate concentrations changed depending on availability, thus building up reserves under excess conditions. Carbon and energy metabolism of the C4 maize leaves were particularly sensitive to P starvation.


Subject(s)
Adaptation, Physiological , Carbon/metabolism , Nitrogen/metabolism , Phosphorus/metabolism , Plant Leaves/metabolism , Stress, Physiological , Zea mays/metabolism , Adaptation, Physiological/genetics , Gene Expression Profiling , Homeostasis , Photosynthesis , Plant Leaves/genetics , Plant Leaves/physiology , RNA, Messenger/genetics , RNA, Messenger/metabolism , Seedlings/genetics , Seedlings/metabolism , Seedlings/physiology , Stress, Physiological/genetics , Temperature , Zea mays/genetics , Zea mays/physiology
4.
Plant J ; 74(2): 280-93, 2013 Apr.
Article in English | MEDLINE | ID: mdl-23452278

ABSTRACT

The majority of land plants live in symbiosis with arbuscular mycorrhizal fungi from the phylum Glomeromycota. This symbiosis improves acquisition of phosphorus (P) by the host plant in exchange for carbohydrates, especially under low-P availability. The symbiosome, constituted by root cortex cells accommodating arbuscular mycorrhizal fungal hyphae, is the site at which bi-directional exchange of nutrients and metabolites takes place. Uptake of orthophosphate (Pi) in the symbiosome is facilitated by mycorrhiza-specific plant Pi transporters. Modifications of the potato Pi transporter 3 (StPT3) promoter were analysed in transgenic mycorrhizal roots, and it was found that the CTTC cis-regulatory element is necessary and sufficient for a transcriptional response to fungal colonization under low-Pi conditions. Phylogenetic footprinting also revealed binary combination of the CTTC element with the Pi starvation response-associated PHR1-binding site (P1BS) in the promoters of several mycorrhiza-specific Pi transporter genes. Scanning of the Lotus japonicus genome for gene promoters containing both cis-regulatory elements revealed a strong over-representation of genes involved in transport processes. One of these, LjVTI12, encoding a member of the SNARE family of proteins involved in membrane transport, exhibited enhanced transcript levels in Lotus roots colonized with the arbuscular mycorrhizal fungus Glomus intraradices. Down-regulation of LjVTI12 by RNA interference resulted in a mycorrhiza-specific phenotype characterized by distorted arbuscule morphology. The results highlight cooperative cis-regulation which integrates mycorrhiza and Pi starvation signaling with vesicle trafficking in symbiosome development.


Subject(s)
Lotus/metabolism , Mycorrhizae/physiology , Plant Proteins/metabolism , Lotus/genetics , Plant Proteins/genetics , RNA Interference , Solanum tuberosum/metabolism , Solanum tuberosum/microbiology
5.
Mol Cell Proteomics ; 11(11): 1306-19, 2012 Nov.
Article in English | MEDLINE | ID: mdl-22891002

ABSTRACT

The Venus flytrap (Dionaea muscipula) is one of the most well-known carnivorous plants because of its unique ability to capture small animals, usually insects or spiders, through a unique snap-trapping mechanism. The animals are subsequently killed and digested so that the plants can assimilate nutrients, as they grow in mineral-deficient soils. We deep sequenced the cDNA from Dionaea traps to obtain transcript libraries, which were used in the mass spectrometry-based identification of the proteins secreted during digestion. The identified proteins consisted of peroxidases, nucleases, phosphatases, phospholipases, a glucanase, chitinases, and proteolytic enzymes, including four cysteine proteases, two aspartic proteases, and a serine carboxypeptidase. The majority of the most abundant proteins were categorized as pathogenesis-related proteins, suggesting that the plant's digestive system evolved from defense-related processes. This in-depth characterization of a highly specialized secreted fluid from a carnivorous plant provides new information about the plant's prey digestion mechanism and the evolutionary processes driving its defense pathways and nutrient acquisition.


Subject(s)
Droseraceae/metabolism , Insecta/metabolism , Plant Exudates/metabolism , Plant Proteins/metabolism , Amino Acid Sequence , Animals , DNA, Complementary/genetics , Droseraceae/enzymology , Droseraceae/genetics , High-Throughput Nucleotide Sequencing , Molecular Sequence Data , Plant Leaves/metabolism , Plant Proteins/chemistry , Proteolysis , Sequence Alignment , Transcriptome
7.
Plant Mol Biol ; 55(1): 17-32, 2004 May.
Article in English | MEDLINE | ID: mdl-15604662

ABSTRACT

When we think of extremophiles, organisms adapted to extreme environments, prokaryotes come to mind first. However, the unicellular red micro-alga Galdieria sulphuraria (Cyanidiales) is a eukaryote that can represent up to 90% of the biomass in extreme habitats such as hot sulfur springs with pH values of 0-4 and temperatures of up to 56 degrees C. This red alga thrives autotrophically as well as heterotrophically on more than 50 different carbon sources, including a number of rare sugars and sugar alcohols. This biochemical versatility suggests a large repertoire of metabolic enzymes, rivaled by few organisms and a potentially rich source of thermo-stable enzymes for biotechnology. The temperatures under which this organism carries out photosynthesis are at the high end of the range for this process, making G. sulphuraria a valuable model for physical studies on the photosynthetic apparatus. In addition, the gene sequences of this living fossil reveal much about the evolution of modern eukaryotes. Finally, the alga tolerates high concentrations of toxic metal ions such as cadmium, mercury, aluminum, and nickel, suggesting potential application in bioremediation. To begin to explore the unique biology of G. sulphuraria , 5270 expressed sequence tags from two different cDNA libraries have been sequenced and annotated. Particular emphasis has been placed on the reconstruction of metabolic pathways present in this organism. For example, we provide evidence for (i) a complete pathway for lipid A biosynthesis; (ii) export of triose-phosphates from rhodoplasts; (iii) and absence of eukaryotic hexokinases. Sequence data and additional information are available at http://genomics.msu.edu/galdieria.


Subject(s)
Carbon/metabolism , Expressed Sequence Tags , Lipid A/biosynthesis , Plastids/metabolism , Rhodophyta/genetics , Algal Proteins/genetics , Amino Acid Sequence , Base Sequence , Biological Transport , DNA, Complementary/chemistry , DNA, Complementary/genetics , Energy Metabolism/genetics , Fatty Acids/metabolism , Gene Library , Hexokinase/genetics , Hydrogen-Ion Concentration , Lipid Metabolism , Molecular Sequence Data , Monosaccharide Transport Proteins/genetics , Oxygen Consumption , Phosphate Transport Proteins/genetics , Photosynthesis/genetics , Phylogeny , Rhodophyta/metabolism , Sequence Alignment , Sequence Analysis, DNA , Sequence Homology, Amino Acid , Sequence Homology, Nucleic Acid , Temperature
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