Skip to main page content
U.S. flag

An official website of the United States government

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
Review
. 2021 Jun 22;72(13):4604-4624.
doi: 10.1093/jxb/erab169.

Orchestral manoeuvres in the light: crosstalk needed for regulation of the Chlamydomonas carbon concentration mechanism

Indu Santhanagopalan  1 , Rachel Wong  1 , Tanya Mathur  1 , Howard Griffiths  1
Affiliations
Review

Orchestral manoeuvres in the light: crosstalk needed for regulation of the Chlamydomonas carbon concentration mechanism

Indu Santhanagopalan et al. J Exp Bot. .

Erratum in

Abstract

The inducible carbon concentration mechanism (CCM) in Chlamydomonas reinhardtii has been well defined from a molecular and ultrastructural perspective. Inorganic carbon transport proteins, and strategically located carbonic anhydrases deliver CO2 within the chloroplast pyrenoid matrix where Rubisco is packaged. However, there is little understanding of the fundamental signalling and sensing processes leading to CCM induction. While external CO2 limitation has been believed to be the primary cue, the coupling between energetic supply and inorganic carbon demand through regulatory feedback from light harvesting and photorespiration signals could provide the original CCM trigger. Key questions regarding the integration of these processes are addressed in this review. We consider how the chloroplast functions as a crucible for photosynthesis, importing and integrating nuclear-encoded components from the cytoplasm, and sending retrograde signals to the nucleus to regulate CCM induction. We hypothesize that induction of the CCM is associated with retrograde signals associated with photorespiration and/or light stress. We have also examined the significance of common evolutionary pressures for origins of two co-regulated processes, namely the CCM and photorespiration, in addition to identifying genes of interest involved in transcription, protein folding, and regulatory processes which are needed to fully understand the processes leading to CCM induction.

Keywords: Chlamydomonas; CIA5; Carbon concentration mechanism (CCM); chaperones; photorespiration; photosynthesis; pyrenoid; retrograde signalling.

PubMed Disclaimer

Figures

Fig. 1.
Fig. 1.
Photorespiratory cycle in Chlamydomonas. The enzymes Rubisco, PGLP (phosphoglycolate phosphatase), GDH (glycolate dehydrogenase), GGT (glutamate glyoxalate aminotransferase), GDC (glycine decarboxylase complex), SHMT (serine hydroxymethyl transferase), SGAT (serine/alanine glyoxalate aminotransferase), HPR1 (hydroxypyruvate reductase), and GLYK (glycerate kinase) are in red. Other abbreviations used: 2-OG, 2-oxoglutarate; Pyr, pyruvate. The enzymes highlighted in bold have expression dependent on both [CO2] and CIA5, similar to several CCM genes (Fang et al., 2012).
Fig. 2.
Fig. 2.
Schematic representation of crosstalk between photosynthetic electron transport (PET), the Calvin–Benson–Basham (CBB) cycle, photorespiration (PR), and the carbon concentration mechanism (CCM) in Chlamydomonas. CCM components: inorganic carbon transporters and carbonic anhydrases, occurring in various parts of the cell are highlighted in grey. *The role of mitochondrial proteins CCP1, CCP2, CAH4, and CAH5 is hypothesized, and remains to be explored. Reactive oxygen species (ROS) generated during PET, and PR metabolites are hypothesized to act as signalling molecules for the CCM.
Fig. 3.
Fig. 3.
Assembly of the pyrenoid. The Rubisco-binding motif (RbM) mediates the formation of three regions of the pyrenoid. The RbM-bearing protein EPYC1 binds to multiple Rubisco holoenzymes and creates a Rubisco–EPYC1 condensate that forms the pyrenoid matrix. The interaction of RbM-bearing thylakoid-anchored proteins RBMP1 and RBMP2 with Rubisco tethers the pyrenoid matrix to the tubule network. The starch sheath is moulded around the pyrenoid matrix through the action of SAGA1 and SAGA2, which bind to Rubisco through their RbM domain and bind to the starch sheath through their starch-binding domain.
Fig. 4.
Fig. 4.
(A) GUN4 retrograde signalling model (after Brzezowski et al., 2014). (i) GUN4 is proposed to be an activator of MgCh activity, interacting with the chlorophyll H subunit to promote the catalytic integration of Mg2+ with ProtoIX to form the chlorophyll biosynthesis pathway intermediate Mg-ProtoIX. (ii) The accumulation of excess tetrapyrrole intermediates, such as ProtoIX, in the chloroplast can lead to generation of ROS. GUN4 is proposed to bind ProtoIX, shielding its reaction with ROS. In shielding ProtoIX, GUN4 may be progressively modified or degraded, with degradation products hypothesized to act as the retrograde signals. (B) A contrasting model for GUN4 (after Tahari Tabrizi et al., 2016). Instead of having a ‘shielding’ effect when bound to ProtoIX, the GUN4–ProtoIX complex appeared to escalate 1O2 generation. The elevated 1O2 produced by GUN4–ProtoIX may be sensed by an 1O2-sensing system (like the Arabidopsis EXECUTER1/EXECUTER2 or EX1/EX2 system) yet to be discovered, that relays a signal to the nucleus.
Fig. 5.
Fig. 5.
A schematic of a tentative mechanism for CAS activity in Chlamydomonas retrograde signalling. (A) Under low light/high CO2 conditions, CAS is dispersed throughout the chloroplast. (B) Under high light/low CO2, the ETC proteins become over-reduced, triggering the movement of CAS into the pyrenoid along the pyrenoid tubules. In the Ca2+-rich pyrenoid, CAS binds to Ca2+ and becomes activated. This form of CAS signals back to the nucleus to modulate target genes. It also induces an increase in intracellular Ca2+.
Fig. 6.
Fig. 6.
Relative expression of PR (top) and CCM (bottom) genes in wild-type (wt) and cia5 Chlamydomonas grown in different [CO2]: <0.02% (V, very low), 0.03–0.05% (L, low), and 5% (H, high). The expression of only genes classified as being in CCM clusters (Fang et al., 2012) is shown here.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Arias C, Obudulub O, Zhaoa X, et al. 2020. Nuclear proteome analysis of Chlamydomonas with response to CO2 limitation. Algal Research 46, 101765.
    1. Armbruster U, Labs M, Pribil M, et al. 2013. Arabidopsis CURVATURE THYLAKOID1 proteins modify thylakoid architecture by inducing membrane curvature. The Plant Cell 25, 2661–2678. - PMC - PubMed
    1. Atkinson N, Feike D, Mackinder LC, Meyer MT, Griffiths H, Jonikas MC, Smith AM, McCormick AJ. 2016. Introducing an algal carbon-concentrating mechanism into higher plants: location and incorporation of key components. Plant Biotechnology Journal 14, 1302–1315. - PMC - PubMed
    1. Atkinson N, Mao Y, Chan KX, McCormick AJ. 2020. Condensation of Rubisco into a proto-pyrenoid in higher plant chloroplasts. Nature Communications 11, 6303. - PMC - PubMed
    1. Badger MR, Kaplan A, Berry JA. 1980. Internal inorganic carbon pool of Chlamydomonas reinhardtii: evidence for a carbon dioxide-concentrating mechanism. Plant Physiology 66, 407–413. - PMC - PubMed

Publication types

LinkOut - more resources