Anaplerotic flux into the Calvin-Benson cycle. Integration in carbon and energy metabolism of Helianthus annuus

Plants assimilate carbon primarily via the Calvin-Benson cycle. Two companion papers reports evidence for anaplerotic carbon flux into this cycle. To estimate flux rates in Helianthus annuus leaves based on gas exchange measurements, we here expanded Farquhar-von Caemmerer-Berry photosynthesis models by terms accounting for anaplerotic respiration and energy recycling. In line with reported isotope evidence (companion papers), we found relative increases in anaplerotic flux as intercellular CO2 concentrations, Ci, decrease below a change point. At Ci=136 and 202 ppm, we found absolute rates of 2.99 and 2.39 μmol Ru5P m-2 s-1 corresponding to 58.3 and 28.2% of net CO2 assimilation, 13.1 and 10.7% of ribulose 1,5-bisphosphate regeneration, and 22.2 and 15.8% of Rubisco carboxylation (futile carbon cycling), respectively. Anaplerotic respiration governs total day respiration with contributions of 81.3 and 77.6%, and anaplerotic relative to photorespiratory CO2 release amounts to 63.9 and 67%, respectively. Furthermore, anaplerotic flux significantly increases absolute ATP demands and ATP-to-NADPH demand ratios of photosynthesis and may explain increasing sucrose-to-starch carbon partitioning ratios with decreasing Ci. We propose that anaplerotic flux can occur under both Rubisco and RuBP-limited growth conditions. Overall, our work introduces the anaplerotic pathway as central component in carbon and energy metabolism of C3 plants.

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Anaplerotic flux into the Calvin-Benson cycle. Isotope evidence for in vivo occurrence in Helianthus annuus

10.1101/2021.07.30.454453 ◽

2021 ◽

Author(s):

Thomas Wieloch ◽

Angela Augusti ◽

Juergen Schleucher

Keyword(s):

Helianthus Annuus ◽

Carbon Flux ◽

Normal Growth ◽

Growth Conditions ◽

Pentose Phosphate ◽

Response Change ◽

Isotope Evidence ◽

Life On Earth ◽

Anaplerotic Pathway

As the central carbon uptake pathway in photosynthetic cells, the Calvin-Benson cycle is among the most important biochemical cycles for life on Earth. Recently, anaplerotic carbon flux (through the chloroplast-localised oxidative branch of the pentose phosphate pathway) into this cycle was proposed. Here, we measured intramolecular deuterium abundances in leaf starch of Helianthus annuus grown at varying ambient CO2 concentrations, Ca. Additionally, we modelled deuterium fractionations expected for the anaplerotic pathway and compared modelled with measured fractionations. We report deuterium fractionation signals at starch glucose H1 and H2. Below a response change point, these signals increase with decreasing Ca consistent with modelled fractionations by anaplerotic flux. Under normal growth conditions (Ca≥450 ppm corresponding to intercellular CO2 concentrations, Ci, ≥328 ppm), we estimate negligible anaplerotic flux. At Ca=180 ppm (Ci=140 ppm), we estimate that of the glucose 6-phosphate entering the starch biosynthesis pathway more than 11.5% is diverted into the anaplerotic pathway. In conclusion, we report evidence consistent with anaplerotic carbon flux into the Calvin-Benson cycle in vivo. We propose the flux may help to (i) maintain high levels of ribulose 1,5-bisphosphate under source-limited growth conditions to facilitate photorespiratory nitrogen assimilation required to build-up source strength and (ii) counteract oxidative stress.

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Utilization of leaf temperature for the selection of leaf gas-exchange traits to induce heat resistance in sunflower (Helianthus annuus L.)

Photosynthetica ◽

10.1007/s11099-013-0038-x ◽

2013 ◽

Vol 51 (3) ◽

pp. 419-428 ◽

Cited By ~ 7

Author(s):

T. Kalyar ◽

S. Rauf ◽

J. A. Teixeira da Silva ◽

S. Haidar ◽

Z. Iqbal

Keyword(s):

Gas Exchange ◽

Heat Resistance ◽

Helianthus Annuus ◽

Leaf Gas Exchange ◽

Leaf Temperature ◽

Helianthus Annuus L ◽

Selection Of

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Factors Influencing Geosmin Production by the Cyanobacterium Oscillatoria Brevis

Water Science & Technology ◽

10.2166/wst.1988.0233 ◽

1988 ◽

Vol 20 (8-9) ◽

pp. 125-131 ◽

Cited By ~ 17

Author(s):

H. Naes ◽

H. C. Utkilen ◽

A. F. Post

Keyword(s):

Environmental Factors ◽

Dry Weight ◽

Growth Conditions ◽

Limited Extent ◽

Limited Growth ◽

Pigment Synthesis ◽

Factors Affecting ◽

Culture Techniques ◽

Factors Influencing ◽

Effect Of Inhibitors

Environmental factors affecting geosmin production by Oscillatoria brevis have been investigated under laboratory conditions using continuous culture techniques. Transition from light to nutrient limited growth conditions caused a two-fold decrease in geosmin production. However, geosmin content increased relative to pigment content (chlorophyll a and carotenoids). It has been suggested that geosmin biosynthesis in O. brevis proceeds via the isoprenoid pathway as was found in actinomycetes. Accordingly, we investigated the effect of inhibitors of the intermediate stages in this synthetic pathway in order to study the regulation of geosmin production in relation to pigment synthesis. It was concluded that geosmin seemed to function as an overflow metabolite in this pathway. Due to the only modest changes in geosmin production per dry weight compared to changes in biomass levels during light- or nutrient limited growth, contamination of eutrophic fresh waters with geosmin appears to depend mainly on the species present and its biomass level and only to a limited extent on nutrient enhanced synthesis.

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The Transcriptional Landscape of Campylobacter jejuni under Iron Replete and Iron Limited Growth Conditions

PLoS ONE ◽

10.1371/journal.pone.0079475 ◽

2013 ◽

Vol 8 (11) ◽

pp. e79475 ◽

Cited By ~ 30

Author(s):

James Butcher ◽

Alain Stintzi

Keyword(s):

Campylobacter Jejuni ◽

Growth Conditions ◽

Limited Growth ◽

Transcriptional Landscape

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Investment in secreted enzymes during nutrient-limited growth is utility dependent

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1708580114 ◽

2017 ◽

Vol 114 (37) ◽

pp. E7796-E7802 ◽

Cited By ~ 18

Author(s):

Brent Cezairliyan ◽

Frederick M. Ausubel

Keyword(s):

Bacterial Growth ◽

Pathogenic Bacteria ◽

Quantitative Relationship ◽

Growth Conditions ◽

Limited Growth ◽

Protein Substrate ◽

Regulatory Strategy ◽

Rate Of Increase ◽

Secreted Proteases ◽

Secreted Enzymes

Pathogenic bacteria secrete toxins and degradative enzymes that facilitate their growth by liberating nutrients from the environment. To understand bacterial growth under nutrient-limited conditions, we studied resource allocation between cellular and secreted components by the pathogenic bacteriumPseudomonas aeruginosaduring growth on a protein substrate that requires extracellular digestion by secreted proteases. We identified a quantitative relationship between the rate of increase of cellular biomass under nutrient-limiting growth conditions and the rate of increase in investment in secreted proteases. Production of secreted proteases is stimulated by secreted signals that convey information about the utility of secreted proteins during nutrient-limited growth. Growth modeling using this relationship recapitulated the observed kinetics of bacterial growth on a protein substrate. The proposed regulatory strategy suggests a rationale for quorum-sensing–dependent stimulation of the production of secreted enzymes whereby investment in secreted enzymes occurs in proportion to the utility they confer. Our model provides a framework that can be applied toward understanding bacterial growth in many environments where growth rate is limited by the availability of nutrients.

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