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Reduced expression of chlorophyllide a oxygenase (CAO) decreases the metabolic flux for chlorophyll synthesis and downregulates photosynthesis in tobacco plants

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Abstract

Chlorophyll b is synthesized from chlorophyllide a, catalyzed by chlorophyllide a oxygenase (CAO). To examine whether reduced chlorophyll b content regulates chlorophyll (Chl) synthesis and photosynthesis, we raised CAO transgenic tobacco plants with antisense CAO expression, which had lower chlorophyll b content and, thus, higher Chl a/b ratio. Further, these plants had (i) lower chlorophyll b and total Chl content, whether they were grown under low or high light; (ii) decreased steady-state levels of chlorophyll biosynthetic intermediates, due, perhaps, to a feedback-controlled reduction in enzyme expressions/activities; (iii) reduced electron transport rates in their intact leaves, and reduced Photosystem (PS) I, PS II and whole chain electron transport activities in their isolated thylakoids; (iv) decreased carbon assimilation in plants grown under low or high light. We suggest that reduced synthesis of chlorophyll b by antisense expression of CAO, acting at the end of Chl biosynthesis pathway, downregulates the chlorophyll b biosynthesis, resulting in decreased Chl b, total chlorophylls and increased Chl a/b. We have previously shown that the controlled up-regulation of chlorophyll b biosynthesis and decreased Chl a/b ratio by over expression of CAO enhance the rates of electron transport and CO2 assimilation in tobacco. Conversely, our data, presented here, demonstrate that-antisense expression of CAO in tobacco, which decreases Chl b biosynthesis and increases Chl a/b ratio, leads to reduced photosynthetic electron transport and carbon assimilation rates, both under low and high light. We conclude that Chl b modulates photosynthesis; its controlled down regulation/ up regulation decreases/ increases light-harvesting, rates of electron transport, and carbon assimilation.

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Abbreviations

ALA:

5-Aminolevulinic acid

ALAD:

5-Aminolevulinic acid dehydratase

cDNA:

Complementary DNA

CAO:

Chlorophyllide a oxygenase

CAOas:

Chlorophyllide a oxygenase antisense

CaMV:

Cauliflower mosaic virus

Chl:

Chlorophyll

Chlide:

Chlorophyllide

ETR:

Electron Transport Rate

GSA:

Glutamate-1-semialdehyde

IRGA:

Infra-Red Gas Analyzer

LHCP:

Light harvesting Chl protein

PAM:

Pulse amplitude modulation

PBGD:

Porphobilinogen deaminase

PCR:

Polymerase chain reaction

POR:

Protochlorophyllide oxidoreductase

Proto IX:

Protoporphyrin IX

PROTOX:

Protoporphyrinogen oxidase

ROS:

Reactive oxygen species

LL:

Low light

HL:

High light

MPE:

Mg-protoporphyrin IX monoester

WT:

Wild type

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Acknowledgements

This work was supported by J.C. Bose Fellowship grant from the Science and Engineering Research Board (SERB), Government of India to BCT.

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Author notes

  1. Ajaya K. Biswal and Gopal K. Pattanayak have contributed equally to this article.

Authors and Affiliations

  1. School of Life Sciences, Jawaharlal Nehru University, New Delhi, 110067, India

    Ajaya K. Biswal, Gopal K. Pattanayak, Kamal Ruhil, Deepika Kandoi, Sushree S. Mohanty, Govindjee Govindjee & Baishnab C. Tripathy

  2. Department of Life Sciences, Sharda University, Greater Noida, UP, India

    Deepika Kandoi

  3. International Center for Genetic Engineering and Biotechnology, New Delhi, 110067, India

    Sadhu Leelavati & Vanga S. Reddy

  4. Department of Plant Biology, Department of Biochemistry, and Center of Biophysics & Quantitative Biology, University of Illinois at Urbana-Champaign, Urbana, IL, 61801, USA

    Govindjee Govindjee

  5. Department of Biotechnology, Sharda University, Greater Noida, UP, 201310, India

    Baishnab C. Tripathy

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  1. Ajaya K. Biswal
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Contributions

AKB, GKP, KR, SSM and SL carried out experiments. AKB, GKP and BCT designed the experiments and analyzed the data. AKB, GKP, DK, GG, and BCT wrote the manuscript.

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Correspondence to Baishnab C. Tripathy.

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Fig. S1. Chlorophyll a content of wild-type (WT) and CAO antisense (CAOas) tobacco plants grown under low-light (LL) and high-light (HL) in the greenhouse. Plants were grown for up to 30 days under light intensity of 300 µmol photons m-2s-1; then, they were transferred to LL (70–80 µmol photons m-2s-1) and HL (700–800 µmol photons m-2s-1) for additional 4 weeks. Each data point is the average of seven replicates and error bars represent the mean ±SE; asterisks indicate significant differences determined by ANOVA-test along with Dunnett’s post hoc test compared to WT (*P < 0.05, **P < 0.01). Statistical tests were conducted between WT and mutant within the same treatment. Fig. S2. Effective quantum yield of PSII (φPSII) of WT and CAOas plants. LL- and HL-grown WT and CAOas plants were dark adapted for 20 min before measurements were made, using PAM 2100 fluorometer. фPSII was estimated from data obtained by this fluorometer at different light intensities (up to 900 µmol photons m-2s-1) as described in the methods. Each data point is the average of five replicates; error bars represent the ±SE; asterisks indicate significant differences determined by ANOVA-test along with Dunnett’s post hoc test compared to WT (*P < 0.05, **P < 0.01). Statistical tests were conducted between WT and mutant within the same treatment. Fig. S3. Non-photochemical quenching (NPQ) of WT and CAOas plants. LL- and HL-grown WT and CAOas plants were dark adapted for 20 min before measurements were made, using PAM 2100 fluorometer. NPQ of excited states of chlorophyll was estimated from data obtained by this fluorometer at different light intensities (up to 900 µmol photons m-2s-1) as described in the methods. Each data point is the average of five replicates; error bars represent the ±SE; asterisks indicate significant differences determined by ANOVA-test along with Dunnett’s post hoc test compared to WT (*P < 0.05, **P < 0.01). The experiment was done three times. Statistical tests were conducted between WT and mutant within the same treatment. (PPTX 68 kb)

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Biswal, A.K., Pattanayak, G.K., Ruhil, K. et al. Reduced expression of chlorophyllide a oxygenase (CAO) decreases the metabolic flux for chlorophyll synthesis and downregulates photosynthesis in tobacco plants. Physiol Mol Biol Plants 30, 1–16 (2024). https://doi.org/10.1007/s12298-023-01395-5

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