SAGA1 and MITH1 produce matrix-traversing membranes in the CO2-fixing pyrenoid
Approximately one-third of global CO<sub>2</sub> assimilation is performed by the pyrenoid, a liquid-like organelle found in most algae and some plants. Specialized pyrenoid-traversing membranes are hypothesized to drive CO<sub>2</sub> assimilation in the pyrenoid by delivering concentrated CO<sub>2</sub>, but how these membranes are made to traverse the pyrenoid matrix remains unknown. Here we show that proteins SAGA1 and MITH1 cause membranes to traverse the pyrenoid matrix in the model alga Chlamydomonas reinhardtii. Mutants deficient in SAGA1 or MITH1 lack matrix-traversing membranes and exhibit growth defects under CO<sub>2</sub>-limiting conditions. Expression of SAGA1 and MITH1 together in a heterologous system, the model plant Arabidopsis thaliana, produces matrix-traversing membranes. Both proteins localize to matrix-traversing membranes. SAGA1 binds to the major matrix component, Rubisco, and is necessary to initiate matrix-traversing membranes. MITH1 binds to SAGA1 and is necessary for extension of membranes through the matrix. Our data suggest that SAGA1 and MITH1 cause membranes to traverse the matrix by creating an adhesive interaction between the membrane and matrix. Our study identifies and characterizes key factors in the biogenesis of pyrenoid matrix-traversing membranes, demonstrates the importance of these membranes to pyrenoid function and marks a key milestone toward pyrenoid engineering into crops for improving yields.
Authors
- Alistair J. McCormick (ORCID: https://orcid.org/0000-0002-7255-872X)
- Nicky Atkinson (ORCID: https://orcid.org/0009-0000-4792-4065)
- Eric Franklin (ORCID: https://orcid.org/0000-0001-7365-6447)
- Friedrich Fauser (ORCID: https://orcid.org/0000-0002-5772-4814)
- Robert E. Jinkerson (ORCID: https://orcid.org/0000-0001-9399-1613)
- Simona Eicke (ORCID: https://orcid.org/0000-0003-4180-2440)
- Lianyong Wang (ORCID: https://orcid.org/0000-0003-0906-8346)
- Samuel C. Zeeman (ORCID: https://orcid.org/0000-0002-2791-0915)
- Sabrina L. Ergun (ORCID: https://orcid.org/0000-0002-6539-8764)
- Yana Kazachkova (ORCID: https://orcid.org/0000-0003-3613-4177)
- Martin C. Jonikas (ORCID: https://orcid.org/0000-0002-9519-6055)
- Jessica H. Hennacy
- Moshe Kafri (ORCID: https://orcid.org/0000-0002-9416-5513)
- Josep Vilarrasa‐Blasi (ORCID: https://orcid.org/0000-0003-4328-4798)
- Angelo Kayser-Browne
Institutions
- University of California, Riverside (US)
- Howard Hughes Medical Institute (US)
- Carnegie Institution for Science (US)
- Princeton University (US)
- ETH Zurich (CH)
- Carnegie Department of Plant Biology (US)
- University of Edinburgh (GB)
Publication Details
- Journal
- Nature Plants
- Published
- 2024-11-15
- DOI
- https://doi.org/10.1038/s41477-024-01847-0
- Citations
- 15
- Primary Topic
- Photosynthetic Processes and Mechanisms
- Type
- article
- Field-Weighted Citation Impact
- 3.51
Funders
- National Science Foundation
- Howard Hughes Medical Institute
- U.S. Department of Energy
- Bill and Melinda Gates Foundation
- Princeton University
- Wellcome Trust
- UK Research and Innovation
- Leverhulme Trust
- Universität Zürich
- Foreign, Commonwealth and Development Office
- National Institutes of Health
- Directorate for Biological Sciences
- Biotechnology and Biological Sciences Research Council
- National Institute of General Medical Sciences
- Division of Molecular and Cellular Biosciences