PMID- 38241434
OWN - NLM
STAT- MEDLINE
DCOM- 20240122
LR  - 20240201
IS  - 1091-6490 (Electronic)
IS  - 0027-8424 (Print)
IS  - 0027-8424 (Linking)
VI  - 121
IP  - 4
DP  - 2024 Jan 23
TI  - SAGA1 and SAGA2 promote starch formation around proto-pyrenoids in Arabidopsis 
      chloroplasts.
PG  - e2311013121
LID - 10.1073/pnas.2311013121 [doi]
LID - e2311013121
AB  - The pyrenoid is a chloroplastic microcompartment in which most algae and some 
      terrestrial plants condense the primary carboxylase, Rubisco 
      (ribulose-1,5-bisphosphate carboxylase/oxygenase) as part of a 
      CO(2)-concentrating mechanism that improves the efficiency of CO(2) capture. 
      Engineering a pyrenoid-based CO(2)-concentrating mechanism (pCCM) into C3 crop 
      plants is a promising strategy to enhance yield capacities and resilience to the 
      changing climate. Many pyrenoids are characterized by a sheath of starch plates 
      that is proposed to act as a barrier to limit CO(2) diffusion. Recently, we have 
      reconstituted a phase-separated "proto-pyrenoid" Rubisco matrix in the model C3 
      plant Arabidopsis thaliana using proteins from the alga with the most 
      well-studied pyrenoid, Chlamydomonas reinhardtii [N. Atkinson, Y. Mao, K. X. 
      Chan, A. J. McCormick, Nat. Commun. 11, 6303 (2020)]. Here, we describe the 
      impact of introducing the Chlamydomonas proteins StArch Granules Abnormal 1 
      (SAGA1) and SAGA2, which are associated with the regulation of pyrenoid starch 
      biogenesis and morphology. We show that SAGA1 localizes to the proto-pyrenoid in 
      engineered Arabidopsis plants, which results in the formation of atypical 
      spherical starch granules enclosed within the proto-pyrenoid condensate and 
      adjacent plate-like granules that partially cover the condensate, but without 
      modifying the total amount of chloroplastic starch accrued. Additional expression 
      of SAGA2 further increases the proportion of starch synthesized as adjacent 
      plate-like granules that fully encircle the proto-pyrenoid. Our findings pave the 
      way to assembling a diffusion barrier as part of a functional pCCM in vascular 
      plants, while also advancing our understanding of the roles of SAGA1 and SAGA2 in 
      starch sheath formation and broadening the avenues for engineering starch 
      morphology.
FAU - Atkinson, Nicky
AU  - Atkinson N
AUID- ORCID: 0009-0000-4792-4065
AD  - Institute of Molecular Plant Sciences, School of Biological Sciences, University 
      of Edinburgh, Edinburgh EH9 3BF, United Kingdom.
AD  - Centre of Engineering Biology, University of Edinburgh, Edinburgh EH9 3BF, United 
      Kingdom.
FAU - Stringer, Rhea
AU  - Stringer R
AUID- ORCID: 0009-0002-8723-2754
AD  - Department of Biochemistry and Metabolism, John Innes Centre, Norwich Research 
      Park, Norwich NR4 7UH, United Kingdom.
FAU - Mitchell, Stephen R
AU  - Mitchell SR
AUID- ORCID: 0009-0006-5759-4841
AD  - Institute of Molecular Plant Sciences, School of Biological Sciences, University 
      of Edinburgh, Edinburgh EH9 3BF, United Kingdom.
FAU - Seung, David
AU  - Seung D
AUID- ORCID: 0000-0003-3905-3647
AD  - Department of Biochemistry and Metabolism, John Innes Centre, Norwich Research 
      Park, Norwich NR4 7UH, United Kingdom.
FAU - McCormick, Alistair J
AU  - McCormick AJ
AUID- ORCID: 0000-0002-7255-872X
AD  - Institute of Molecular Plant Sciences, School of Biological Sciences, University 
      of Edinburgh, Edinburgh EH9 3BF, United Kingdom.
AD  - Centre of Engineering Biology, University of Edinburgh, Edinburgh EH9 3BF, United 
      Kingdom.
LA  - eng
GR  - WT_/Wellcome Trust/United Kingdom
PT  - Journal Article
DEP - 20240119
PL  - United States
TA  - Proc Natl Acad Sci U S A
JT  - Proceedings of the National Academy of Sciences of the United States of America
JID - 7505876
RN  - EC 4.1.1.39 (Ribulose-Bisphosphate Carboxylase)
RN  - 142M471B3J (Carbon Dioxide)
RN  - 9005-25-8 (Starch)
SB  - IM
MH  - *Arabidopsis/genetics/metabolism
MH  - Ribulose-Bisphosphate Carboxylase/genetics/metabolism
MH  - Carbon Dioxide/metabolism
MH  - Chloroplasts/metabolism
MH  - *Chlamydomonas reinhardtii/genetics/metabolism
MH  - Photosynthesis
MH  - Starch/metabolism
PMC - PMC10823261
OTO - NOTNLM
OT  - Arabidopsis
OT  - CO2-concentrating mechanism
OT  - Chlamydomonas
OT  - EPYC1
OT  - Rubisco
COIS- Competing interests statement:The authors declare no competing interest.
EDAT- 2024/01/19 18:30
MHDA- 2024/01/22 06:42
PMCR- 2024/01/19
CRDT- 2024/01/19 14:13
PHST- 2024/01/22 06:42 [medline]
PHST- 2024/01/19 18:30 [pubmed]
PHST- 2024/01/19 14:13 [entrez]
PHST- 2024/01/19 00:00 [pmc-release]
AID - 202311013 [pii]
AID - 10.1073/pnas.2311013121 [doi]
PST - ppublish
SO  - Proc Natl Acad Sci U S A. 2024 Jan 23;121(4):e2311013121. doi: 
      10.1073/pnas.2311013121. Epub 2024 Jan 19.