The pyrenoid is the site of ribulose 1,5-bisphosphate carboxylase/oxygenase accumulation in the hornwort (Bryophyta: Anthocerotae) chloroplast

Vaughn, Kevin C.; Campbell, Ella O.; Hasegawa, Jiro; Owen, Heather A.; Renzaglia, Karen S.

doi:10.1007/bf01560650

Cited by 52 publications

(37 citation statements)

References 17 publications

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“…8 for algae with CCMs despite lacking pyrenoids) (Table S2). Hornworts without pyrenoids have the RuBisCO enzyme distributed throughout the stroma, similar to the condition in the remaining land plants (6). Hornworts with pyrenoids have a larger DiC pool and lower photorespiration than liverworts, which rely on the C 3 pathway (17,18).…”

Section: Resultsmentioning

confidence: 78%

Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years

Villarreal

Renner

2012

Proc. Natl. Acad. Sci. U.S.A.

115

105

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Ribulose-1,5-Biphosphate-carboxylase-oxygenase (RuBisCO) has a crucial role in carbon fixation but a slow catalytic rate, a problem overcome in some plant lineages by physiological and anatomical traits that elevate carbon concentrations around the enzyme. Such carbon-concentrating mechanisms are hypothesized to have evolved during periods of low atmospheric CO 2 . Hornworts, the sister to vascular plants, have a carbon-concentrating mechanism that relies on pyrenoids, proteinaceous bodies mostly consisting of RuBisCO. We generated a phylogeny based on mitochondrial and plastid sequences for 36% of the approximately 200 hornwort species to infer the history of gains and losses of pyrenoids in this clade; we also used fossils and multiple dating approaches to generate a chronogram for the hornworts. The results imply five to six origins and an equal number of subsequent losses of pyrenoids in hornworts, with the oldest pyrenoid gained ca. 100 Mya, and most others at <35 Mya. The nonsynchronous appearance of pyrenoid-containing clades, the successful diversification of pyrenoid-lacking clades during periods with low [CO 2 ], and the maintenance of pyrenoids during episodes of high [CO 2 ] all argue against the previously proposed relationship between pyrenoid origin and low [CO 2 ]. The selective advantages, and costs, of hornwort pyrenoids thus must relate to additional factors besides atmospheric CO 2 . independent origins T he enzyme most important in photosynthesis is Ribulose-1,5-Biphosphate-carboxylase-oxygenase, or RuBisCO. This enzyme has a low CO 2 attraction and catalytic rate, which plants compensate for by increasing their CO 2 affinity, synthesizing large quantities of the enzyme, or increasing the CO 2 concentration near it (1-3). Among green organisms (algae and land plants), CO 2 -concentrating mechanisms (CCMs, also referred to as carbonconcentrating mechanisms) have evolved in numerous lineages to increase the CO 2 :O 2 ratio inside their photosynthetic cells. These mechanisms are C 4 photosynthesis, Crassulacean acid metabolism, and the pyrenoids found in algae and hornworts (4, 5).

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Section: Resultsmentioning

confidence: 78%

Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years

Villarreal

Renner

2012

Proc. Natl. Acad. Sci. U.S.A.

115

105

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“…While there are undoubtedly some CCM systems which function in the absence of a pyrenoid (Raven 1997a,b;Raven et al 2008), we contend that the majority of the significant aquatic global carbon fixation mediated by noncyanobacterial microbes (Raven et al 2008) is mediated by a pyrenoid-based CCM. To date, there are no candidate genes, proteins or specific structures which are thought to comprise a pyrenoid, other than the associated starch sheath (Izumo et al 2007), and internal pyrenoid complement of rubisco (Lacoste-Royal & Gibbs 1987;Vaughn et al 1990;Borkhsenious et al 1998), rubisco activase (McKay et al 1991), nitrate reductase (Okabe & Okada 1990), Calvin cycle enzymes, photosystem I and lumenal carbonic anhydrase-enriched trans-thylakoid lamellae (Villarejo et al 1998;Moroney & Ynalvez 2007). While we are currently undertaking work on a pyrenoid proteome and also investigating the relationship between rubisco structure and function in the chloroplast pyrenoid, our closest guess to the normal pyrenoid structure is some type of aggregation mechanism associated with rubisco, which may be related either to rubisco holoenzyme amino acid residue interactions or some additional plastoskeleton structures.…”

Section: Discussionmentioning

confidence: 99%

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

Meyer

Seibt

Griffiths

2008

Phil. Trans. R. Soc. B

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A comparative study has been made of the photosynthetic physiological ecology and carbon isotope discrimination characteristics for modern-day bryophytes and closely related algal groups. Firstly, the extent of bryophyte distribution and diversification as compared with more advanced land plant groups is considered. Secondly, measurements of instantaneous carbon isotope discrimination (D), photosynthetic CO 2 assimilation and electron transport rates were compared during the drying cycles. The extent of surface diffusion limitation (when wetted), internal conductance and water use efficiency (WUE) at optimal tissue water content (TWC) were derived for liverworts and a hornwort from contrasting habitats and with differing degrees of thallus ventilation (as intra-thalline cavities and internal airspaces). We also explore how the operation of a biophysical carbon-concentrating mechanism (CCM) tempers isotope discrimination characteristics in two other hornworts, as well as the green algae Coleochaete orbicularis and Chlamydomonas reinhardtii. The magnitude of D was compared for each life form over a drying curve and used to derive the surface liquid-phase conductance (when wetted) and internal conductance (at optimal TWC). The magnitude of external and internal conductances, and WUE, was higher for ventilated, compared with non-ventilated, liverworts and hornworts, but the values were similar within each group, suggesting that both factors have been optimized for each life form. For the hornworts, leakiness of the CCM was highest for Megaceros vincentianus and C. orbicularis (approx. 30%) and, at 5%, lowest in C. reinhardtii grown under ambient CO 2 concentrations. Finally, evidence for the operation of a CCM in algae and hornworts is considered in terms of the probable role of the chloroplast pyrenoid, as the origins, structure and function of this enigmatic organelle are explored during the evolution of land plants.

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“…Since this high CO 2 concentration is in the vicinity of Rubisco, the carboxylation reaction will be enhanced at the expense of the oxygenation reaction, hence reducing the photorespiration. In the pyrenoid-containing hornworts, there is also good correlation between the operation of a CCM and the presence of a pyrenoid (Vaughn et al, 1990;Hemsley and Poole, 2004). Besides the role in physical compartmentalization of Rubisco away from the rest of chloroplast stroma, the dynamic nature of pyrenoid in response to environmental changes adds extra complexity to the CCM.…”

Section: Discussionmentioning

confidence: 99%

Identification of a Novel Gene,CIA6, Required for Normal Pyrenoid Formation inChlamydomonas reinhardtii

Pollock

Xiao

et al. 2011

Plant Physiology

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Chlamydomonas reinhardtii possesses a CO 2 -concentrating mechanism (CCM) that allows the alga to grow at low CO 2 concentrations. One common feature seen in photosynthetic organisms possessing a CCM is the tight packaging of Rubisco within the cell. In many eukaryotic algae, Rubisco is localized to the pyrenoid, an electron-dense structure within the chloroplast. In order to identify genes required for a functional CCM, insertional Bleomycin resistance (Ble R ) mutants were generated and screened for growth on minimal medium under high CO 2 conditions (5% CO 2 in air) but only slow or no growth under very low CO 2 conditions (0.01% CO 2 in air). One mutant identified from this screen was named cia6. Physiological studies established that cia6 grows poorly on low levels of CO 2 and has an impaired ability to accumulate inorganic carbon. The inserted Ble R disrupted a gene encoding a protein with sequence similarity to proteins containing SET domain methyltransferase, although experiments using overexpressed CIA6 failed to demonstrate the methyltransferase activity. Electron microscopy revealed that the pyrenoid of cia6 mutant cells is highly disorganized. Complementation of the mutant restored the pyrenoid, the ability to grow under low-CO 2 conditions, and the ability to concentrate inorganic carbon. Quantitative reverse transcriptionpolymerase chain reaction data from a low-CO 2 induction time-course experiment demonstrated that the up-regulation of several CCM components is slower in cia6 compared with the wild type. This slow induction was further confirmed at the protein level using western blots. These results indicated that CIA6 is required for the formation of the pyrenoid and further supported the notion that the pyrenoid is required for a functional CCM in C. reinhardtii.

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The pyrenoid is the site of ribulose 1,5-bisphosphate carboxylase/oxygenase accumulation in the hornwort (Bryophyta: Anthocerotae) chloroplast

Cited by 52 publications

References 17 publications

Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years

Hornwort pyrenoids, carbon-concentrating structures, evolved and were lost at least five times during the last 100 million years

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

Identification of a Novel Gene,CIA6, Required for Normal Pyrenoid Formation inChlamydomonas reinhardtii

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