C4 species utilize fluctuating light less efficiently than C3 species

Li, Yuting; Jun, Luo; Liu, Peng; Zhang, Zishan

doi:10.1093/plphys/kiab411

Cited by 25 publications

(38 citation statements)

References 13 publications

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“…Greater losses of photosynthetic efficiency have previously been observed in C 4 grown under dynamic light in comparison to C 3 species and linked to mechanisms involving photosynthetic induction ( Kubásek et al., 2013 ). Further fluctuating light work on plants grown under constant light (including C 4 F. bidentis ) has also shown an increased lag in CO 2 assimilation in C 4 compared to C 3 species following step-increases in light intensity ( Li et al., 2021 ). Similarly, in a study comparing a selection of C 3 and C 4 grasses ( Lee et al., 2022 ), a biphasic increase in assimilation during the low to high light transition was the most significant limitation in maize and big bluestem, again emphasizing the C 4 lag in CO 2 assimilation.…”

Section: Discussionmentioning

confidence: 99%

“…The increased efficiency of the C 4 pathway relative to the C 3 ancestral state is especially apparent under constant high light ( Wang et al., 2012 ). However, during changes in light intensity, some C 4 species display impaired carbon assimilation in comparison to C 3 species ( Kubásek et al., 2013 ; Slattery et al., 2018 ; Li et al., 2021 ). Decreases in photosynthetic efficiency during light induction (in response to an increase in light intensity) occur irrespective of photosynthetic pathway and are often explained by lags in regeneration of ribulose-1,5-biphosphate (RuBP) within the C 3 cycle, Rubisco activation, and stomatal opening ( Pearcy and Seemann, 1990 ; Pearcy, 1990 ; Sassenrath-Cole and Pearcy, 1992 ; Mott and Woodrow, 2000 ).…”

Section: Introductionmentioning

confidence: 99%

“…Whilst the experimental evidence and putative mechanisms detailed above may indeed suggest that C 4 species could be more affected by transient decreases in photosynthetic efficiency during induction relative to steady state than C 3 species, most of the work does not directly compare C 3 and C 4 species in a common experiment, but instead often focuses on a single species, such as maize ( Zelitch et al., 2009 ; Kromdijk et al., 2010 ; Medeiros et al., 2022 ). Some direct comparisons between C 3 and C 4 photosynthesis have been made in sets of contrasting grass species ( Lee et al., 2022 ) and species within the same genus ( Kubásek et al., 2013 ), but so far the only C 3 and C 4 species studied that share a relatively recent common ancestor are Flaveria ( Li et al., 2021 ). Phylogenetic distance can strongly confound the apparent photosynthetic differences observed ( Taylor et al., 2010 ) and to confirm whether observed differences are due to photosynthetic pathway or evolutionary variation, studies conducted on phylogenetically linked C 3 and C 4 species are necessary.…”

Section: Introductionmentioning

confidence: 99%

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Activation of CO2 assimilation during photosynthetic induction is slower in C4 than in C3 photosynthesis in three phylogenetically controlled experiments

et al. 2023

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IntroductionDespite their importance for the global carbon cycle and crop production, species with C4 photosynthesis are still somewhat understudied relative to C3 species. Although the benefits of the C4 carbon concentrating mechanism are readily observable under optimal steady state conditions, it is less clear how the presence of C4 affects activation of CO2 assimilation during photosynthetic induction.MethodsIn this study we aimed to characterise differences between C4 and C3 photosynthetic induction responses by analysing steady state photosynthesis and photosynthetic induction in three phylogenetically linked pairs of C3 and C4 species from Alloteropsis, Flaveria, and Cleome genera. Experiments were conducted both at 21% and 2% O2 to evaluate the role of photorespiration during photosynthetic induction.ResultsOur results confirm C4 species have slower activation of CO2 assimilation during photosynthetic induction than C3 species, but the apparent mechanism behind these differences varied between genera. Incomplete suppression of photorespiration was found to impact photosynthetic induction significantly in C4Flaveria bidentis, whereas in the Cleome and Alloteropsis C4 species, delayed activation of the C3 cycle appeared to limit induction and a potentially supporting role for photorespiration was also identified.DiscussionThe sheer variation in photosynthetic induction responses observed in our limited sample of species highlights the importance of controlling for evolutionary distance when comparing C3 and C4 photosynthetic pathways.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Activation of CO2 assimilation during photosynthetic induction is slower in C4 than in C3 photosynthesis in three phylogenetically controlled experiments

et al. 2023

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“…A better mechanistic understanding of the impact of low irradiance on C 4 photosynthesis has implications for improving the effectiveness of C 4 photosynthesis in the field after the canopy has closed and leaves experience low irradiance ( Sales et al . , 2021 ), for understanding which factors decrease the efficiency of C 4 photosynthesis in fluctuating light ( Kubasek et al, 2013 ; Li et al, 2021 ), as well as for ecological questions related to why C 4 photosynthesis did not evolve often in shrubs or trees with bushy canopies ( Sage, 2014 ).…”

Section: Discussionmentioning

confidence: 99%

13CO2 labeling kinetics in maize reveal impaired efficiency of C4 photosynthesis under low irradiance

et al. 2022

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C4 photosynthesis allows faster photosynthetic rates and higher water and nitrogen use efficiency than C3 photosynthesis, but at the cost of lower quantum yield due to the energy requirement of its biochemical carbon concentration mechanism. It has also been suspected that its operation may be impaired in low irradiance. To investigate fluxes under moderate and low irradiance, maize (Zea mays) was grown at 550 µmol photons m−2 s-l and 13CO2 pulse-labelling was performed at growth irradiance or several hours after transfer to 160 µmol photons m−2 s−1. Analysis by liquid chromatography/tandem mass spectrometry or gas chromatography/mass spectrometry provided information about pool size and labelling kinetics for 32 metabolites and allowed estimation of flux at many steps in C4 photosynthesis. The results highlighted several sources of inefficiency in low light. These included excess flux at phosphoenolpyruvate carboxylase, restriction of decarboxylation by NADP-malic enzyme, and a shift to increased CO2 incorporation into aspartate, less effective use of metabolite pools to drive intercellular shuttles, and higher relative and absolute rates of photorespiration. The latter provides evidence for a lower bundle sheath CO2 concentration in low irradiance, implying that operation of the CO2 concentration mechanism is impaired in this condition. The analyses also revealed rapid exchange of carbon between the Calvin-Benson cycle and the CO2-concentration shuttle, which allows rapid adjustment of the balance between CO2 concentration and assimilation, and accumulation of large amounts of photorespiratory intermediates in low light that provides a major carbon reservoir to build up C4 metabolite pools when irradiance increases.

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“…However, Stitt and Zhu (2014) proposed that the two-cell Kranz system of C 4 photosynthesis ensures large pools of metabolites that could drive diffusion between BSCs and mesophyll cells (MC) for buffering ATP and NADPH, which may provide powerful protection against fluctuating light intensities. Recently, Li et al (2021) have proposed that the accumulation and diffusion of metabolites in C 4 plants from MCs to BSCs take more time, which may delay the photosynthetic induction.…”

Section: Introductionmentioning

confidence: 99%

Short-term elevated temperature and CO

Zheng

Kang

2022

Funct. Plant Biol.

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The continuous increases of atmospheric temperature and CO 2 concentration will impact global photosynthesis. However, there are few studies considering the interaction of elevated temperature (eT) and elevated CO 2 (eCO 2 ) on dynamic photosynthesis, particularly for C 4 species. We examine dynamic photosynthesis under four different temperature and [CO 2 ] treatments:(1) 400 ppm × 28°C (CT); (2) 400 ppm × 33°C (CT+); (3) 800 ppm × 28°C (C+T); and (4) 800 ppm × 33°C (C+T+). In Glycine max L., the time required to reach 50% (T 50%A ) and 90% (T 90%A ) of full photosynthetic induction was smaller under the CT+, C+T, and C+T+ treatments than those under the CT treatment. In Amaranthus tricolor L., however, neither T 50%A nor T 90%A was not significantly affected by eT or eCO 2 . In comparison with the CT treatment, the achieved carbon gain was increased by 58.3% (CT+), 112% (C+T), and 136.6% (C+T+) in G. max and was increased by 17.1% (CT+), 2.6% (C+T) and 56.9% (C+T+) in A. tricolor. The increases of achieved carbon gain in G. max were attributable to both improved photosynthetic induction efficiency (IE) and enhanced steady-state photosynthesis, whereas those in A. tricolor were attributable to enhanced steady-state photosynthesis.

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C4 species utilize fluctuating light less efficiently than C3 species

Abstract: Reactivation of photosynthetic carbon assimilation during high light after a low light interval is slower in C4 than in C3 leaves.

Cited by 25 publications

References 13 publications

Activation of CO2 assimilation during photosynthetic induction is slower in C4 than in C3 photosynthesis in three phylogenetically controlled experiments

Activation of CO2 assimilation during photosynthetic induction is slower in C4 than in C3 photosynthesis in three phylogenetically controlled experiments

13CO2 labeling kinetics in maize reveal impaired efficiency of C4 photosynthesis under low irradiance

Short-term elevated temperature and CO

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