Chloroplast-mediated regulation of CO2-concentrating mechanism by Ca2+-binding protein CAS in the green alga Chlamydomonas reinhardtii

Lianyong Wang, Takashi Yamano, Shunsuke Takane, Yuki Niikawa, Chihana Toyokawa, Shin Ichiro Ozawa, Ryutaro Tokutsu, Yuichiro Takahashi, Jun Minagawa, Yu Kanesaki, Hirofumi Yoshikawa, Hideya Fukuzawa

Research output: Contribution to journalArticlepeer-review

35 Citations (Scopus)

Abstract

Aquatic photosynthetic organisms, including the green alga Chlamydomonas reinhardtii, induce a CO2-concentrating mechanism (CCM) to maintain photosynthetic activity in CO2-limiting conditions by sensing environmental CO2 and light availability. Previously, a novel high-CO2-requiring mutant, H82, defective in the induction of the CCM, was isolated. A homolog of calcium (Ca2+)-binding protein CAS, originally found in Arabidopsis thaliana, was disrupted in H82 cells. Although Arabidopsis CAS is reported to be associated with stomatal closure or immune responses via a chloroplast-mediated retrograde signal, the relationship between a Ca2+ signal and the CCM associated with the function of CAS in an aquatic environment is still unclear. In this study, the introduction of an intact CAS gene into H82 cells restored photosynthetic affinity for inorganic carbon, and RNAseq analyses revealed that CAS could function in maintaining the expression levels of nuclear-encoded CO2-limiting-inducible genes, including the HCO3 - transporters high-light activated 3 (HLA3) and low-CO2-inducible gene A (LCIA). CAS changed its localization from dispersed across the thylakoid membrane in high-CO2 conditions or in the dark to being associated with tubule-like structures in the pyrenoid in CO2-limiting conditions, along with a significant increase of the fluorescent signals of the Ca2+ indicator in the pyrenoid. Chlamydomonas CAS had Ca2+-binding activity, and the perturbation of intracellular Ca2+ homeostasis by a Ca2+-chelator or calmodulin antagonist impaired the accumulation of HLA3 and LCIA. These results suggest that Chlamydomonas CAS is a Ca2+-mediated regulator of CCM-related genes via a retrograde signal from the pyrenoid in the chloroplast to the nucleus.

Original languageEnglish
Pages (from-to)12586-12591
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume113
Issue number44
DOIs
Publication statusPublished - Nov 1 2016

Keywords

  • Acclimation
  • Bicarbonate transporter
  • Calcium signaling
  • Photosynthesis
  • Pyrenoid

ASJC Scopus subject areas

  • General

Fingerprint

Dive into the research topics of 'Chloroplast-mediated regulation of CO<sub>2</sub>-concentrating mechanism by Ca<sup>2+</sup>-binding protein CAS in the green alga Chlamydomonas reinhardtii'. Together they form a unique fingerprint.

Cite this