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Coordination between photorespiration and carbon concentrating mechanism in Chlamydomonas reinhardtii: transcript and protein changes during light-dark diurnal cycles and mixotrophy conditions

  • S. Tirumani
  • K.M. Gothandam
  • Basuthkar J Rao
Original Article

Abstract

Carbon concentrating mechanism (CCM) and photorespiration (PR) are interlinked and co-regulated in Chlamydomonas reinhardtii, but conditions where co-regulation alters are not sufficiently explored. Here, we uncover that PR gene transcripts, like CCM transcripts, are induced even in the dark when both processes are not active. Such diurnal cycles show that transcript levels peak in the middle of 12 h day, decline by early part of 12-h dark followed by their onset again at mid-dark. Interestingly, the onset in the mid-dark phase is sensitive to high CO2, implying that the active carbon sensing mechanism operates even in the dark. The rhythmic alterations of both CCM and PR transcript levels are unlinked to circadian clock: the “free-running state” reveals no discernible rhythmicity in transcript changes. Only continuous light leads to high transcript levels but no detectable transcripts were observed in continuous dark. Asynchronous continuous light cultures, upon shifting to low from high CO2 exhibit only transient induction of PR transcripts/proteins while CCM transcript induction is stable, indicating the loss of co-regulation between PR and CCM gene transcription. Lastly, we also describe that both CCM and PR transcripts/proteins are induced in low CO2 even in mixotrophic cultures, but only in high light, the same being attenuated in high CO2, implying that high light is a mandatory “trigger” for CCM and PR induction in low CO2 mixotrophy. Our study provides comprehensive analyses of conditions where CCM and PR were differently regulated, setting a paradigm for a detailed mechanistic probing of these responses.

Keywords

Carbon concentrating mechanism Circadian clock Transcriptional regulation Light-dark cycles Mixotrophy Photorespiration 

Abbreviations

AAT1

Alanine:α-ketoglutarate aminotransf erase

CAH3

Carbonic anhydrase 3

CCM

Carbon concentrating mechanism

CCP1

Chloroplast carrier protein 1

D1

Photosystem II protein D1

GDCH

Glycine decarboxylase H protein

GDH

Glycolate dehydrogenase

HPR

Hydroxypyruvate reductase

LCIB

Low CO2 inducible membrane protein

LCI1

Low CO2 inducible membrane protein

LHCSR3

Light harvesting complex stress-related chlorophyll a/b binding protein

PGP1

Phosphoglycolate phosphatase

PR

Photorespiration

RuBisCO

Ribulose-1,5-bisphosphate carboxylase-oxygenase

SGAT

Serine:glyoxylate aminotransferase

TAP medium

Tris acetate phosphate medium

TP medium

Tris phosphate medium

Notes

Acknowledgements

This work was supported by J.C. Bose Fellowship Grant, DST (10X-217) and Department of Atomic Energy Grant, Government of India (12P0123) to Prof. Basuthkar Jagadeeshwar Rao. We also thank Soumajit Saha for his help in microscopy imaging and valuable inputs throughout the project.

Authors’ contribution

BJ and TS conceived and designed the research. TS conducted the experiments. BJ contributed new reagents or analytical tools. BJ, TS, and KM analyzed the data. BJ wrote the manuscript. All authors read and approved the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

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ESM 1

(PNG 654 kb)

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High resolution image (TIF 4874 kb)

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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  • S. Tirumani
    • 1
    • 2
  • K.M. Gothandam
    • 2
  • Basuthkar J Rao
    • 1
    • 3
  1. 1.B-202, Department of Biological SciencesTata Institute of Fundamental ResearchMumbaiIndia
  2. 2.School of Bio Sciences and TechnologyVIT UniversityVelloreIndia
  3. 3.Indian Institute of Science Education and ResearchTirupatiIndia

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