Structure and Identification of a Pterin Dehydratase-like Protein as a Ribulose-bisphosphate Carboxylase/Oxygenase (RuBisCO) Assembly Factor in the α-Carboxysome

Wheatley, Nicole M.; Sundberg, Christopher; Gidaniyan, Soheil D.; Cascio, Duilio; Yeates, Todd O.

doi:10.1074/jbc.m113.531236

Cited by 58 publications

(48 citation statements)

References 45 publications

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“…Gene‐specific PCR of additional raf2 ‐ 1 mutant individuals and several phenotypically WT cousins confirmed that this insertion was tightly linked to raf2 (Figure S1). In addition, the bacterial homolog of raf2 is encoded in the same operon as Rubisco subunits, and was recently shown to increase the accumulation of bacterial Rubisco when co‐expressed with Rubisco subunits and GroELS (Wheatley et al ., ). Taken together, these findings provide strong support for the conclusion that RAF2 is required for Rubisco accumulation in maize.…”

Section: Resultsmentioning

confidence: 97%

A protein with an inactive pterin‐4a‐carbinolamine dehydratase domain is required for Rubisco biogenesis in plants

et al. 2014

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SUMMARYRibulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) plays a critical role in sustaining life by catalysis of carbon fixation in the Calvin-Benson pathway. Incomplete knowledge of the assembly pathway of chloroplast Rubisco has hampered efforts to fully delineate the enzyme's properties, or seek improved catalytic characteristics via directed evolution. Here we report that a Mu transposon insertion in the Zea mays (maize) gene encoding a chloroplast dimerization co-factor of hepatocyte nuclear factor 1 (DCoH)/pterin4a-carbinolamine dehydratases (PCD)-like protein is the causative mutation in a seedling-lethal, Rubiscodeficient mutant named Rubisco accumulation factor 2 (raf2-1). In raf2 mutants newly synthesized Rubisco large subunit accumulates in a high-molecular weight complex, the formation of which requires a specific chaperonin 60-kDa isoform. Analogous observations had been made previously with maize mutants lacking the Rubisco biogenesis proteins RAF1 and BSD2. Chemical cross-linking of maize leaves followed by immunoprecipitation with antibodies to RAF2, RAF1 or BSD2 demonstrated co-immunoprecipitation of each with Rubisco small subunit, and to a lesser extent, co-immunoprecipitation with Rubisco large subunit. We propose that RAF2, RAF1 and BSD2 form transient complexes with the Rubisco small subunit, which in turn assembles with the large subunit as it is released from chaperonins.

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Section: Resultsmentioning

confidence: 97%

A protein with an inactive pterin‐4a‐carbinolamine dehydratase domain is required for Rubisco biogenesis in plants

et al. 2014

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“…Here, we demonstrate that RAF2 in the C3 plant A . thaliana is involved in RuBisCO holoenzyme accumulation, similar to maize RAF2 (Feiz et al ., ) and the remote cyanobacterial homolog (Wheatley et al ., ). Consequently, when RAF2 is missing in A .…”

Section: Discussionmentioning

confidence: 97%

RAF2 is a RuBisCO assembly factor in Arabidopsis thaliana

Fristedt¹,

Hu²,

Wheatley³

et al. 2018

The Plant Journal

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Ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO) catalyzes the reaction between gaseous carbon dioxide (CO ) and ribulose-1,5-bisphosphate. Although it is one of the most studied enzymes, the assembly mechanisms of the large hexadecameric RuBisCO is still emerging. In bacteria and in the C4 plant Zea mays, a protein with distant homology to pterin-4α-carbinolamine dehydratase (PCD) has recently been shown to be involved in RuBisCO assembly. However, studies of the homologous PCD-like protein (RAF2, RuBisCO assembly factor 2) in the C3 plant Arabidopsis thaliana (A. thaliana) have so far focused on its role in hormone and stress signaling. We investigated whether A. thalianaRAF2 is also involved in RuBisCO assembly. We localized RAF2 to the soluble chloroplast stroma and demonstrated that raf2 A. thaliana mutant plants display a severe pale green phenotype with reduced levels of stromal RuBisCO. We concluded that the RAF2 protein is probably involved in RuBisCO assembly in the C3 plant A. thaliana.

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“…Given that the RbcL subunits of all form I Rubiscos are highly homologous, it is surprising that the Rubisco of higher plants has so far been refractory to reconstitution in E. coli or in vitro. Perhaps additional factors are required for the assembly of the plant enzyme 24,34,35 .…”

Section: Discussionmentioning

confidence: 99%

Structure and mechanism of the Rubisco-assembly chaperone Raf1

Hauser

Bhat

Miličić

et al. 2015

Nat Struct Mol Biol

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Biogenesis of the photosynthetic enzyme Rubisco, a complex of eight large (RbcL) and eight small (RbcS) subunits, requires assembly chaperones. Here we analyzed the role of Rubisco accumulation factor1 (Raf1), a dimer of ∼40-kDa subunits. We find that Raf1 from Synechococcus elongatus acts downstream of chaperonin-assisted RbcL folding by stabilizing RbcL antiparallel dimers for assembly into RbcL8 complexes with four Raf1 dimers bound. Raf1 displacement by RbcS results in holoenzyme formation. Crystal structures show that Raf1 from Arabidopsis thaliana consists of a β-sheet dimerization domain and a flexibly linked α-helical domain. Chemical cross-linking and EM reconstruction indicate that the β-domains bind along the equator of each RbcL2 unit, and the α-helical domains embrace the top and bottom edges of RbcL2. Raf1 fulfills a role similar to that of the assembly chaperone RbcX, thus suggesting that functionally redundant factors ensure efficient Rubisco biogenesis.

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Structure and Identification of a Pterin Dehydratase-like Protein as a Ribulose-bisphosphate Carboxylase/Oxygenase (RuBisCO) Assembly Factor in the α-Carboxysome

Cited by 58 publications

References 45 publications

A protein with an inactive pterin‐4a‐carbinolamine dehydratase domain is required for Rubisco biogenesis in plants

A protein with an inactive pterin‐4a‐carbinolamine dehydratase domain is required for Rubisco biogenesis in plants

RAF2 is a RuBisCO assembly factor in Arabidopsis thaliana

Structure and mechanism of the Rubisco-assembly chaperone Raf1

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