Photosynthesis across African cassava germplasm is limited by Rubisco and mesophyll conductance at steady state, but by stomatal conductance in fluctuating light

Improving leaf intrinsic water-use efficiency (iWUE), the ratio of photosynthetic CO2 assimilation to stomatal conductance, could decrease crop freshwater consumption. iWUE has primarily been studied under steady-state light, but light in crop stands rapidly fluctuates. Leaf responses to these fluctuations substantially affect overall plant performance. Notably, photosynthesis responds faster than stomata to decreases in light intensity: this desynchronization results in substantial loss of iWUE. Traits that could improve iWUE under fluctuating light, such as faster stomatal movement to better synchronize stomata with photosynthesis, show significant natural diversity in C3 species. However, C4 crops have been less closely investigated. Additionally, while modification of photosynthetic or stomatal traits independent of one another will theoretically have a proportionate effect on iWUE, in reality these traits are inter-dependent. It is unclear how interactions between photosynthesis and stomata affect natural diversity in iWUE, and whether some traits are more tractable drivers to improve iWUE. Here, measurements of photosynthesis, stomatal conductance and iWUE under steady-state and fluctuating light, along with stomatal patterning, were obtained in 18 field-grown accessions of the C4 crop sorghum. These traits showed significant natural diversity but were highly correlated, with important implications for improvement of iWUE. Some features, such as gradual responses of photosynthesis to decreases in light, appeared promising for improvement of iWUE. Other traits showed tradeoffs that negated benefits to iWUE, e.g., accessions with faster stomatal responses to decreases in light, expected to benefit iWUE, also displayed more abrupt losses in photosynthesis, resulting in overall lower iWUE. Genetic engineering might be needed to break these natural tradeoffs and achieve optimal trait combinations, e.g., leaves with fewer, smaller stomata, more sensitive to changes in photosynthesis. Traits describing iWUE at steady-state, and the change in iWUE following decreases in light, were important contributors to overall iWUE under fluctuating light.

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Modelling photosynthesis in fluctuating light with inclusion of stomatal conductance, biochemical activation and pools of key photosynthetic intermediates

Planta ◽

10.1007/s004250050225 ◽

1997 ◽

Vol 204 (1) ◽

pp. 16-26 ◽

Cited By ~ 52

Author(s):

M. U. F. Kirschbaum ◽

M. Küppers ◽

H. Schneider ◽

C. Giersch ◽

S. Noe

Keyword(s):

Stomatal Conductance ◽

Fluctuating Light ◽

Biochemical Activation

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Increased stomatal conductance induces rapid changes to photosynthetic rate in response to naturally fluctuating light conditions in rice

Plant Cell & Environment ◽

10.1111/pce.13725 ◽

2020 ◽

Vol 43 (5) ◽

pp. 1230-1240 ◽

Cited By ~ 14

Author(s):

Wataru Yamori ◽

Kensuke Kusumi ◽

Koh Iba ◽

Ichiro Terashima

Keyword(s):

Stomatal Conductance ◽

Photosynthetic Rate ◽

Light Conditions ◽

Fluctuating Light ◽

Rapid Changes

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High-yielding rice Takanari has superior photosynthetic response to a commercial rice Koshihikari under fluctuating light

Journal of Experimental Botany ◽

10.1093/jxb/erz304 ◽

2019 ◽

Vol 70 (19) ◽

pp. 5287-5297 ◽

Cited By ~ 6

Author(s):

Shunsuke Adachi ◽

Yu Tanaka ◽

Atsuko Miyagi ◽

Makoto Kashima ◽

Ayumi Tezuka ◽

...

Keyword(s):

Electron Transport ◽

Stomatal Conductance ◽

Metabolic Flux ◽

Electron Transport Rate ◽

Rice Cultivar ◽

Carbon Gain ◽

High Electron ◽

Photosynthetic Induction ◽

Photosynthetic Response ◽

Fluctuating Light

The high-yielding rice cultivar Takanari has fast photosynthetic induction owing to a high electron transport rate, stomatal conductance, and metabolic flux, leading to high daily carbon gain under fluctuating light.

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Phosphate Requirement, Photosynthesis, and Diel Cell Cycle of Scenedesmus obliquas Under Fluctuating Light

Canadian Journal of Fisheries and Aquatic Sciences ◽

10.1139/f87-214 ◽

1987 ◽

Vol 44 (10) ◽

pp. 1753-1758 ◽

Cited By ~ 10

Author(s):

C. N. Shin ◽

G-Y Rhee ◽

J. Chen

Keyword(s):

Steady State ◽

Average Rate ◽

Scenedesmus Obliquus ◽

Constant Light ◽

Photon Flux ◽

Photon Flux Density ◽

Cell Numbers ◽

P Limitation ◽

Fluctuating Light ◽

Light Fluctuation

The effect of light fluctuation (0.06 Hz) on P requirement, photosynthesis, and the diel cell-division cycle was investigated in Scenedesmus obliquus in a chemostat under a 12 h day: 12 h night cycle. P requirement was much less under oscillating than under constant daylight of the same photon flux density. However, cell chlorophyll a was significantly higher, indicating an increased N requirement. There was little difference in photosynthetic efficiency (the slope of the photosynthesis–light regression) between oscillating and constant light, but photosynthetic capacity was higher in fluctuating light. Cell C was also higher. A strong diel rhythmicity in steady-state cell numbers was observed with little phase difference between oscillating and constant light. Although steady-state cell numbers under P limitation were significantly higher under fluctuating light, there was no difference in instantaneous growth rates and their diel distribution. At a dilution rate of 0.6∙d−1, cell death occurred at an average rate of −0.56∙d−1 between 4 h before and 5 h after the onset of the dark period.

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Oscillatory Transpiration May Complicate Stomatal Conductance and Gas-exchange Measurements

HortScience ◽

10.21273/hortsci.29.6.693 ◽

1994 ◽

Vol 29 (6) ◽

pp. 693-694 ◽

Cited By ~ 6

Author(s):

Mary Ann Rose ◽

Mark A. Rose

Keyword(s):

Steady State ◽

Stomatal Conductance ◽

Gas Exchange ◽

Heat Balance ◽

Sap Flow ◽

Closed Loop ◽

Random Noise ◽

Plant Responses ◽

Whole Plant ◽

Plant Sap

A closed-loop photosynthesis system and a heat-balance sap-flow gauge independently confirmed oscillatory transpiration in a greenhouse-grown Rosa hybrids L. Repetitive sampling revealed 60-minute synchronized oscillations in CO2-exchange rate, stomatal conductance, and whole-plant sap-flow rate. To avoid confusing cyclical plant responses with random noise in measurement, we suggest that gas-exchange protocols begin with frequent, repetitive measurements to determine whether transpiration is stable or oscillating. Single measurements of individual plants would be justified only when transpiration is steady state.

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Diurnal Response of Photosystem I to Fluctuating Light Is Affected by Stomatal Conductance

Cells ◽

10.3390/cells10113128 ◽

2021 ◽

Vol 10 (11) ◽

pp. 3128

Author(s):

Ting-Yu Li ◽

Qi Shi ◽

Hu Sun ◽

Ming Yue ◽

Shi-Bao Zhang ◽

...

Keyword(s):

Stomatal Conductance ◽

Redox State ◽

Electron Flow ◽

High Light ◽

Primary Metabolism ◽

Diurnal Changes ◽

Late Afternoon ◽

Fluctuating Light ◽

Photosynthetic Regulation ◽

Sudden Transition

Upon a sudden transition from low to high light, electrons transported from photosystem II (PSII) to PSI should be rapidly consumed by downstream sinks to avoid the over-reduction of PSI. However, the over-reduction of PSI under fluctuating light might be accelerated if primary metabolism is restricted by low stomatal conductance. To test this hypothesis, we measured the effect of diurnal changes in stomatal conductance on photosynthetic regulation under fluctuating light in tomato (Solanum lycopersicum) and common mulberry (Morus alba). Under conditions of high stomatal conductance, we observed PSI over-reduction within the first 10 s after transition from low to high light. Lower stomatal conductance limited the activity of the Calvin–Benson–Bassham cycle and aggravated PSI over-reduction within 10 s after the light transition. We also observed PSI over-reduction after transition from low to high light for 30 s at the low stomatal conductance typical of the late afternoon, indicating that low stomatal conductance extends the period of PSI over-reduction under fluctuating light. Therefore, diurnal changes in stomatal conductance significantly affect the PSI redox state under fluctuating light. Moreover, our analysis revealed an unexpected inhibition of cyclic electron flow by the severe over-reduction of PSI seen at low stomatal conductance. In conclusion, stomatal conductance can have a large effect on thylakoid reactions under fluctuating light.

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Identification of QTLs for dynamic and steady state photosynthetic traits in a barley mapping population

10.1101/2020.08.09.243352 ◽

2020 ◽

Author(s):

William T. Salter ◽

Si Li ◽

Peter M. Dracatos ◽

Margaret M. Barbour

Keyword(s):

Steady State ◽

Stomatal Conductance ◽

Doubled Haploid ◽

Mapping Population ◽

Yield Potential ◽

Doubled Haploid Population ◽

Photosynthetic Induction ◽

In Planta ◽

Activation Rate ◽

Rubisco Activation

AbstractEnhancing the photosynthetic induction response to fluctuating light has been suggested as a key target for improvement in crop breeding programs, with the potential to substantially increase whole canopy carbon assimilation and contribute to crop yield potential. Rubisco activation may be the main physiological process that will allow us to achieve such a goal. In this study, we phenotypically assessed the rubisco activation rate in a doubled haploid (DH) barley mapping population [131 lines from a Yerong/Franklin (Y/F) cross] after a switch from moderate to saturating light. Rates of rubisco activation were found to be highly variable across the mapping population, with a median activation rate of 0.1 min−1 in the slowest genotype and 0.74 min−1 in the fastest genotype. A QTL for rubisco activation rate was identified on chromosome 7H. This is the first report on the identification of a QTL for rubisco activation rate in planta and the discovery opens the door to marker assisted breeding to improve whole canopy photosynthesis of barley. Further strength is given to this finding as this QTL colocalised with QTLs identified for steady state photosynthesis and stomatal conductance. Several other distinct QTLs were identified for these steady state traits, with a common overlapping QTL on chromosome 2H, and distinct QTLs for photosynthesis and stomatal conductance identified on chromosomes 4H and 5H respectively. Future work should aim to validate these QTLs under field conditions so that they can be used to aid plant breeding efforts.HighlightSignificant variation exists in the photosynthetic induction response after a switch from moderate to saturating light across a barley doubled haploid population. A QTL for rubisco activation rate was identified on chromosome 7H, as well as overlapping QTLs for steady state photosynthesis and stomatal conductance.

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Artifleck: The Study of Artifactual Responses to Light Flecks with Inappropriate Leaves

Plants ◽

10.3390/plants9070905 ◽

2020 ◽

Vol 9 (7) ◽

pp. 905 ◽

Cited By ~ 2

Author(s):

Thomas E. Marler

Keyword(s):

Zea Mays ◽

Glycine Max ◽

Steady State ◽

Leaf Mass Per Area ◽

Model Species ◽

Leaf Mass ◽

Fluctuating Light ◽

Light Flecks ◽

Photosynthetic Responses ◽

Response Variables

Methods in sunfleck research commonly employ the use of experimental leaves which were constructed in homogeneous light. These experimental organs may behave unnaturally when they are challenged with fluctuating light. Photosynthetic responses to heterogeneous light and leaf macronutrient relations were determined for Cycas micronesica, Glycine max, and Zea mays leaves that were grown in homogeneous shade, heterogeneous shade, or full sun. The speed of priming where one light fleck increased the photosynthesis during a subsequent light fleck was greatest for the leaves grown in heterogeneous shade. The rate of induction and the ultimate steady-state photosynthesis were greater for the leaves that were grown in heterogeneous shade versus the leaves grown in homogeneous shade. The leaf mass per area, macronutrient concentration, and macronutrient stoichiometry were also influenced by the shade treatments. The amplitude and direction in which the three developmental light treatments influenced the response variables were not universal among the three model species. The results indicate that the historical practice of using experimental leaves which were constructed under homogeneous light to study leaf responses to fluctuating light may produce artifacts that generate dubious interpretations.

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Surfing the Hyperbola Equations of the Steady-State Farquhar–von Caemmerer–Berry C3 Leaf Photosynthesis Model: What Can a Theoretical Analysis of Their Oblique Asymptotes and Transition Points Tell Us?

Bulletin of Mathematical Biology ◽

10.1007/s11538-019-00676-z ◽

2019 ◽

Vol 82 (1) ◽

Author(s):

Jon Miranda-Apodaca ◽

Emilio L. Marcos-Barbero ◽

Rosa Morcuende ◽

Juan B. Arellano

Keyword(s):

Steady State ◽

Theoretical Analysis ◽

Nitrogen Assimilation ◽

Theoretical Study ◽

Mesophyll Conductance ◽

Leaf Photosynthesis ◽

Rectangular Hyperbola ◽

Quadratic Equations ◽

Transition Points ◽

Limiting Values

AbstractThe asymptotes and transition points of the net CO2 assimilation (A/Ci) rate curves of the steady-state Farquhar–von Caemmerer–Berry (FvCB) model for leaf photosynthesis of C3 plants are examined in a theoretical study, which begins from the exploration of the standard equations of hyperbolae after rotating the coordinate system. The analysis of the A/Ci quadratic equations of the three limitation states of the FvCB model—abbreviated as Ac, Aj and Ap—allows us to conclude that their oblique asymptotes have a common slope that depends only on the mesophyll conductance to CO2 diffusion (gm). The limiting values for the transition points between any two states of the three limitation states c, j and p do not depend on gm, and the results are therefore valid for rectangular and non-rectangular hyperbola equations of the FvCB model. The analysis of the variation of the slopes of the asymptotes with gm casts doubts about the fulfilment of the steady-state conditions, particularly, when the net CO2 assimilation rate is inhibited at high CO2 concentrations. The application of the theoretical analysis to extended steady-state FvCB models, where the hyperbola equations of Ac, Aj and Ap are modified to accommodate nitrogen assimilation and amino acids export via the photorespiratory pathway, is also discussed.

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