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    ABSTRACT: Genes encoding plant nucleotide-binding leucine-rich repeat (NB-LRR) proteins confer dominant resistance to diverse pathogens. The wild-type potato NB-LRR protein Rx confers resistance against a single strain of potato virus X (PVX), whereas LRR mutants protect against both a second PVX strain and the distantly related poplar mosaic virus (PopMV). In one of the Rx mutants there was a cost to the broad-spectrum resistance because the response to PopMV was transformed from a mild disease on plants carrying wild-type Rx to a trailing necrosis that killed the plant. To explore the use of secondary mutagenesis to eliminate this cost of broad-spectrum resistance, we performed random mutagenesis of the N-terminal domains of this broad-recognition version of Rx and isolated four mutants with a stronger response against the PopMV coat protein due to enhanced activation sensitivity. These mutations are located close to the nucleotide-binding pocket, a highly conserved structure that likely controls the "switch" between active and inactive NB-LRR conformations. Stable transgenic plants expressing one of these versions of Rx are resistant to the strains of PVX and the PopMV that previously caused trailing necrosis. We conclude from this work that artificial evolution of NB-LRR disease resistance genes in crops can be enhanced by modification of both activation and recognition phases, to both accentuate the positive and eliminate the negative aspects of disease resistance.
    Proceedings of the National Academy of Sciences 12/2013;
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    ABSTRACT: The C4 photosynthesis carbon concentrating mechanism (CCM) in maize has two CO2 delivery pathways to the Bundle Sheath (BS) (respectively via malate, MAL or aspartate, ASP), and rates of PGA reduction, starch synthesis and PEP regeneration also vary between BS and Mesophyll (M) cells. The theoretical partitioning of ATP supply between M and BS cells was derived for these metabolic activities from simulated profiles of light penetration across a leaf, with a potential 3-fold difference in the fraction of ATP produced in the BS relative to M, (from 0.29 to 0.96). A steady-state metabolic model was tested using varying light quality to differentially stimulate M or BS photosystems. CO2 uptake, ATP production rate (JATP derived with a low O2 / chlorophyll fluorescence method) and carbon isotope discrimination were measured on plants under a low light intensity, which is considered to affect C4 operating efficiency. The light quality treatments did not change the empirical ATP cost of gross assimilation (JATP / GA). Using the metabolic model, measured JATP / GA was compared to the predicted ATP demand as metabolic functions were varied between M and BS. Transamination and the two decarboxylase systems (NADPME and PEPCK) were critical for matching ATP and NADPH demand in BS and M when light capture was varied under contrasting light qualities.
    Plant physiology 11/2013;
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    ABSTRACT: There is currently significant interest in engineering the two-celled C4 photosynthesis pathway into crops such as rice in order to increase yield. This will require alterations to the biochemistry of photosynthesis in both mesophyll (M) and bundle-sheath (BS) cells, but also alterations to leaf anatomy. For example, the BS of C4 species is enlarged compared with that in C3 species. Because cell and nucleus size are often correlated, this study investigated whether nuclear endoreduplication is associated with increased differentiation and expansion of BS cells. Nuclei in the BS of C4 Cleome gynandra were tagged with green fluorescent protein. Confocal laser-scanning microscopy and flow cytometry of isolated nuclei were used to quantify size and DNA content in BS cells. The results showed a significant endoreduplication in BS cells of C. gynandra but not in additional C4 lineages from both the monocotyledonous and dicotyledenous plants. Furthermore, in the C3 species Arabidopsis thaliana, BS cells undergo endoreduplication. Due to this significant endoreduplication in the small BS cells of C3 A. thaliana, it was concluded that endoreduplication of BS nuclei in C4 plants is not linked to expansion and differentiation of BS cells, and therefore that alternative strategies to increase this compartment need to be sought in order to engineer C4 traits into C3 crops such as rice.
    Journal of Experimental Botany 11/2013;
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    ABSTRACT: Hydrogen peroxide is the most stable of the reactive oxygen species (ROS) and is a regulator of development, immunity and adaptation to stress. It frequently acts by elevating cytosolic free Ca(2+) ([Ca(2+) ]cyt ) as a second messenger, with activation of plasma membrane Ca(2+) -permeable influx channels as a fundamental part of this process. At the genetic level, to date only the Ca(2+) -permeable Stelar K(+) Outward Rectifier (SKOR) channel has been identified as being responsive to hydrogen peroxide. We show here that the ROS-regulated Ca(2+) transport protein Annexin 1 in Arabidopsis thaliana (AtANN1) is involved in regulating the root epidermal [Ca(2+) ]cyt response to stress levels of extracellular hydrogen peroxide. Peroxide-stimulated [Ca(2+) ]cyt elevation (determined using aequorin luminometry) was aberrant in roots and root epidermal protoplasts of the Atann1 knockout mutant. Similarly, peroxide-stimulated net Ca(2+) influx and K(+) efflux were aberrant in Atann1 root mature epidermis, determined using extracellular vibrating ion-selective microelectrodes. Peroxide induction of GSTU1 (Glutathione-S-Transferase1 Tau 1), which is known to be [Ca(2+) ]cyt -dependent was impaired in mutant roots, consistent with a lesion in signalling. Expression of AtANN1 in roots was suppressed by peroxide, consistent with the need to restrict further Ca(2+) influx. Differential regulation of annexin expression was evident, with AtANN2 downregulation but upregulation of AtANN3 and AtANN4. Overall the results point to involvement of AtANN1 in shaping the root peroxide-induced [Ca(2+) ]cyt signature and downstream signalling. This article is protected by copyright. All rights reserved.
    The Plant Journal 11/2013;
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    ABSTRACT: The assembly of respiratory complexes is a multistep process, requiring coordinate expression of mitochondrial and nuclear genes and cofactor biosynthesis. We functionally characterized the iron-sulfur protein required for NADH dehydrogenase (INDH) in the model plant Arabidopsis thaliana. An indh knockout mutant lacked complex I but had low levels of a 650-kD assembly intermediate, similar to mutations in the homologous NUBPL (nucleotide binding protein-like) in Homo sapiens. However, heterozygous indh/+ mutants displayed unusual phenotypes during gametogenesis and resembled mutants in mitochondrial translation more than mutants in complex I. Gradually increased expression of INDH in indh knockout plants revealed a significant delay in reassembly of complex I, suggesting an indirect role for INDH in the assembly process. Depletion of INDH protein was associated with decreased (35)S-Met labeling of translation products in isolated mitochondria, whereas the steady state levels of several mitochondrial transcripts were increased. Mitochondrially encoded proteins were differentially affected, with near normal levels of cytochrome c oxidase subunit2 and Nad7 but little Nad6 protein in the indh mutant. These data suggest that INDH has a primary role in mitochondrial translation that underlies its role in complex I assembly.
    The Plant Cell 10/2013;
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    ABSTRACT: Circadian clocks provide a competitive advantage in an environment that is heavily influenced by the rotation of the Earth, by driving daily rhythms in behaviour, physiology and metabolism in bacteria, fungi, plants and animals. Circadian clocks comprise transcription-translation feedback loops, which are entrained by environmental signals such as light and temperature to adjust the phase of rhythms to match the local environment. The production of sugars by photosynthesis is a key metabolic output of the circadian clock in plants. Here we show that these rhythmic, endogenous sugar signals can entrain circadian rhythms in Arabidopsis thaliana by regulating the gene expression of circadian clock components early in the photoperiod, thus defining a 'metabolic dawn'. By inhibiting photosynthesis, we demonstrate that endogenous oscillations in sugar levels provide metabolic feedback to the circadian oscillator through the morning-expressed gene PSEUDO-RESPONSE REGULATOR 7 (PRR7), and we identify that prr7 mutants are insensitive to the effects of sucrose on the circadian period. Thus, photosynthesis has a marked effect on the entrainment and maintenance of robust circadian rhythms in A. thaliana, demonstrating that metabolism has a crucial role in regulation of the circadian clock.
    Nature 10/2013;
  • Science 10/2013; 342(6154):45-46.
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    ABSTRACT: Appropriate stimulus-response coupling requires that each signal induces a characteristic response, distinct from that induced by other signals and that there is the potential for individual signals to initiate different downstream responses dependent on cell type. How such specificity is encoded in plant signalling is not known. One possibility is that information is encoded in signal transduction pathways to ensure stimulus- and cell-type specific responses. The calcium ion acts as a second messenger in response to mechanical stimulation, H2O2, NaCl and cold in plants and also in circadian timing. We use GAL4 transactivation of aequorin in enhancer trap lines of Arabidopsis thaliana to test the hypothesis that stimulus- and cell-specific information can be encoded in the pattern of dynamical alterations in the concentration of intracellular-free ([Ca2+]i). We demonstrate that mechanically-induced increases in [Ca2+]i are largely restricted to the epidermal pavement cells of leaves, that NaCl induces oscillatory [Ca2+]i signals in spongy mesophyll and vascular bundle cells, but not other cell types and detect circadian rhythms of [Ca2+]i only in the spongy mesophyll. We demonstrate stimulus-specific [Ca2+]i dynamics in response to touch, cold and H2O2, which in the case of the latter two signals are common to all cell types tested. GAL4 transactivation of aequorin in specific leaf cell types has allowed us to bypass the technical limitations associated with fluorescent Ca2+ reporter dyes in chlorophyll-containing tissues to identify cell- and stimulus-specific complexity of [Ca2+]i dynamics in leaves of Arabidopsis and determine from which tissues stress and circadian-regulated [Ca2+]i signals arise.
    Plant physiology 09/2013;
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    ABSTRACT: • Premise of the study: Caryophyllales are highly diverse in the structure of the perianth and androecium and show a mode of floral development unique in eudicots, reflecting the continuous interplay of gynoecium and perianth and their influence on position, number, and identity of the androecial whorls. The floral development of five species from four genera of a paraphyletic Molluginaceae (Limeum, Hypertelis, Glinus, Corbichonia), representing three distinct evolutionary lineages, was investigated to interpret the evolution of the androecium across Caryophyllales.• Methods: Floral buds were dissected, critical-point dried and imaged with SEM. The genera studied are good representatives of the diversity of development of stamens and staminodial petaloids in Caryophyllales.• Key results: Sepals show evidence of petaloid differentiation via marginal hyaline expansion. Corbichonia, Glinus, and Limeum also show perianth differentiation via sterilization of outer stamen tiers. In all four genera, stamens initiate with the carpels and develop centrifugally, but subsequently variation is significant. With the exception of Limeum, the upper whorl is complete and alternisepalous, while a second antesepalous whorl arises more or less sequentially, starting opposite the inner sepals. Loss or sterilization of antesepalous stamens occurs in Glinus and Limeum and is caused by altered carpel merism and inhibition by sepal pressures.• Conclusions: Outer stamens of Hypertelis correspond with petaloids of Caryophyllaceae and suggest that staminodial petaloids and outer alternisepalous stamens are interchangeable in the Caryophyllales. We emphasize a switch in the position of first formed stamens from antesepalous to alternisepalous following the divergence of Limeum; thus stamen position is an important synapomorphy for the globular inclusion clade.
    American Journal of Botany 09/2013;
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    ABSTRACT: C4 plants have a biochemical carbon concentrating mechanism (CCM) that increases CO2 concentration around Rubisco in the bundle sheath (BS). Under limiting light, the activity of the CCM generally decreases, causing an increase in leakiness, (Φ), the ratio of CO2 retrodiffusing from the BS relative to C4 carboxylation processes. Maize plants were grown under high and low light regimes (respectively HL, 600 vs LL, 100 μE m(-2) s(-1) ). Short term acclimation of Φ was compared from isotopic discrimination (Δ), gas exchange and photochemistry. Direct measurement of respiration in the light, and ATP production rate (JATP ), allowed us use a novel approach to derive Φ, compared to the conventional fitting of measured and predicted Δ. HL grown plants responded to decreasing light intensities with the well-documented increase in Φ. Conversely, LL plants showed a constant Φ which has not been observed previously. We explain the pattern by two contrasting acclimation strategies: HL plants maintained a high CCM activity at LL, resulting in high CO2 overcycling and increased Φ; LL plants acclimated by downregulating the CCM, effectively optimising scarce ATP supply. This surprising plasticity may limit the impact of Φ-dependent carbon losses in leaves becoming shaded within developing canopies.
    Plant Cell and Environment 09/2013;
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