Exploring the potential of plastid biology and biotechnology DOI Open Access
Rose McNelly, Angel Vergara Cruces, David J. Lea‐Smith

et al.

New Phytologist, Journal Year: 2023, Volume and Issue: 240(6), P. 2187 - 2190

Published: Oct. 3, 2023

Plastids are a family of organelles that likely originate from the endosymbiosis cyanobacteria (Howe et al., 2008) and exhibit diverse morphologies biochemical capabilities (Fig. 1). The chloroplast is most well-studied plastid type performs photosynthesis in plants algae thus responsible for food production on planet. However, there other important functions performed by plastids, including synthesis storage some carbohydrates, pigment production, fatty acid nitrogen sulphur assimilation. Plants have specialised types carry out these functions, such as starch-storing amyloplasts pigment-producing chromoplasts annual Plastid Preview Meeting took place 1–2 September 2022 Norwich (UK), jointly hosted John Innes Centre University East Anglia. Since 1970s, has showcased cutting-edge research PhD students early career postdoctoral scientists investigating fundamental applied biology. Research presented throughout years not only addressed questions but also areas chlorophyll biosynthesis, starch metabolism, carbon fixation, gene expression transformation. In meeting, it was apparent significant progress being made addressing long-standing with aid technological developments, machine learning, editing cryo-EM approaches to study protein structure, combined ability explore previously untapped biological diversity rapid expansion genome sequences. Three major domains were covered: first concerned 'understanding plastid', probing mechanisms govern second 'optimising plastid' focussed processes could increase productivity resilience cyanobacteria, plants. third 'utilising specifically use plastid-containing organisms biotechnology produce high-value proteins metabolites. Here, we highlight exciting work encompassing three covered at meeting. into processes, biogenesis, expression, import division, required understand how metabolism occur integrated within organelle. Protein prime example process influences many an area active discussion majority proteome encoded nucleus, imported organelle through recognition plastid-localisation signals, translocation membranes delivery appropriate location plastid. This heavily function, recent implicated ubiquitination this (Ling & Jarvis, 2015). Ling al. (2012) discovered cytosolic ubiquitin-mediated degradation pathway regulates components machinery. More recently, been observed broad range Arabidopsis, those involved photosynthesis, oxidative stress metabolic pathways (Sun 2022). opens new about role regulation well its relevance broader species types, crops. We discussed links emerging between division (Fang While nucleus can influence possesses reciprocal signal status back known retrograde signalling. Many aspects communication fully understood, several uncovered, tetrapyrroles reactive oxygen (Chan 2016). accumulate due defect allowing sense chloroplast. sensitive perturbations environmental conditions, makes ideal sentinel general cell status. As such, signalling response both abiotic biotic stresses 2016; Littlejohn 2021). An meeting pathogen infection affect nuclear genes encoding plastid-localised resistance (Corredor-Moreno Uncovering effectors hijack during roles interactions lead novel protect pathogens. Photosynthesis central chloroplasts main source energy cyanobacteria. inefficiencies RuBisCo described detail (Flamholz 2019). It be partly attributed slow evolution enzyme (Bouvier 2022) requirement balance carboxylation rates CO2/O2 specificity. highlighted strategies overcome activity. strategy based harnessing pre-existing RuBisCo. There large variation kinetics phototrophs (Savir 2010) potentially exploited replace native enzymes more efficient versions, if localised CO2 concentrations increased. Extensive modelling shows replacing wheat C4 significantly efficiency uptake (Iqbal 2021), experimentally implementing predictions may validate route increasing photosynthetic efficiency. Furthermore, where reported, particularly nonmodel species. learning becomes increasingly prevalent, employed predict sequences potential improve photosynthesis. via concentrating (CCMs). CCMs biophysical, like algal pyrenoids cyanobacterial carboxysomes, or biochemical, Recent developing mechanistic understanding form function. One breakthrough discovery Chlamydomonas reinhardtii EPYC1, which physically pyrenoid (Mackinder enhanced our assembly opened possibility engineering (Adler Similar transfer carboxysomes follow, benefitting insights structure α-carboxysome (Ni Beyond chloroplasts, manipulated crop quality, carotenoid elaioplasts Specifically, wheat, two distinct granules, A-type small B-type granules. MRC formation granules introduce desirable changes granule size properties milling industries (Chen Further come exploiting intra- interspecies will drive improvements nutritional functional quality similar way Biotechnological using biofactory key theme meetings. provides environment rest producing valuable Much attention fallen algae, especially newly fast-growing Synechococcus sp. PCC 11901 (Włodarczyk 2020), volumes cells cultivated ease smaller space compared numerous examples C. vaccine subunits, antibacterial compounds antibodies (Dyo Purton, 2018). A primary focus techniques cyanobacterial, plant biotechnology. Regulators transgenes great interest, allow robust control easy on/off switching expression. Riboswitches, instance thiamine pyrophosphate riboswitch, solution (Mehrshahi further switches tandem expand existing toolkit. Another targeting heterologous subcompartments, thylakoid lumen. would produced stable stroma (Chin-Fatt Menassa, To ensure biotechnological realised, priority toolkit transformation technologies. includes improved synthetic biology tools, example, MoClo cloning systems compatible across (Vasudevan expect Cas enzymes, beyond Cas9, function adapting base technology plastome editing. additional challenge when multiple plastids per achieving homoplasmy, (Okuzaki 2020). These methods result widespread adoption utilisation biofactories remains guided goal shining light beyond. field – variety studied, differences much natural unexplored technologies continue evolve, adopting combining different fields. Exploiting essential understand, utilise further, no doubt future Previews. thank all presenters attendees 2022, apologise whose here restrictions. possible financial support New Phytologist Foundation, Gatsby Society Experimental Biology, Li-Cor, Algae-UK, Anglia Institute Development Grant. acknowledge funding Foundation (Rotation studentships RM ÁV-C; Chris J. Leaver Fellowship DS), Royal (Research grant RGS/R2/222157 MW) Biotechnology Biological Sciences Council, UK grants BB/S020365/1 DL-S BB/W015935/1 DS; Strategic Programmes BB/X01102X/1 BB/X01097X/1 Centre). ÁV-C contributed equally work.

Language: Английский

Rubisco Function, Evolution, and Engineering DOI Creative Commons
Noam Prywes, Naiya R. Phillips, Owen T. Tuck

et al.

Annual Review of Biochemistry, Journal Year: 2023, Volume and Issue: 92(1), P. 385 - 410

Published: April 26, 2023

Carbon fixation is the process by which CO2 converted from a gas into biomass. The Calvin-Benson-Bassham cycle (CBB) dominant carbon-consuming pathway on Earth, driving >99.5% of ∼120 billion tons carbon that are to sugar plants, algae, and cyanobacteria. carboxylase enzyme in CBB, ribulose-1,5-bisphosphate carboxylase/oxygenase (rubisco), fixes one molecule per turn bioavailable sugars. Despite being critical assimilation carbon, rubisco's kinetic rate not very fast, limiting flux through pathway. This bottleneck presents paradox: Why has rubisco evolved be better catalyst? Many hypothesize catalytic mechanism subject or more trade-offs variants have been optimized for their native physiological environment. Here, we review evolution biochemistry lens structure order understand what limit its improvement. We also many attempts improve itself thereby promote plant growth.

Language: Английский

Citations

61

Evolution of increased complexity and specificity at the dawn of form I Rubiscos DOI
Luca Schulz, Zhijun Guo, Jan Zarzycki

et al.

Science, Journal Year: 2022, Volume and Issue: 378(6616), P. 155 - 160

Published: Oct. 13, 2022

The evolution of ribulose-1,5-bisphosphate carboxylase/oxygenases (Rubiscos) that discriminate strongly between their substrate carbon dioxide and the undesired side dioxygen was an important event for photosynthetic organisms adapting to oxygenated environment. We use ancestral sequence reconstruction recapitulate this event. show Rubisco increased its specificity carboxylation efficiency through gain accessory subunit before atmospheric oxygen present. Using structural biochemical approaches, we retrace how gained became essential. Our work illuminates emergence adaptation rising ambient levels, provides a template investigating function interactions have remained elusive because essentiality, sheds light on determinants in Rubisco.

Language: Английский

Citations

67

The diversity and coevolution of Rubisco and CO2 concentrating mechanisms in marine macrophytes DOI Creative Commons
Sebastià Capó‐Bauçà, Concepción Iñíguez, Jeroni Galmés

et al.

New Phytologist, Journal Year: 2024, Volume and Issue: 241(6), P. 2353 - 2365

Published: Jan. 10, 2024

The kinetic properties of Rubisco, the most important carbon-fixing enzyme, have been assessed in a small fraction estimated existing biodiversity photosynthetic organisms. Until recently, one significant gaps knowledge Rubisco kinetics was marine macrophytes, an ecologically relevant group including brown (Ochrophyta), red (Rhodophyta) and green (Chlorophyta) macroalgae seagrasses (Streptophyta). These organisms express various types predominantly possess CO

Language: Английский

Citations

2

Response to Tcherkez and Farquhar: Rubisco adaptation is more limited by phylogenetic constraint than by catalytic trade-off DOI Creative Commons
Jacques W. Bouvier, Steven Kelly

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Jan. 11, 2023

Abstract Rubisco is the primary entry point for carbon into biosphere. It has been widely proposed that rubisco highly constrained by catalytic trade-offs due to correlations between enzyme’s kinetic traits across species. In previous work, we have shown these correlations, and thus strength of trade-offs, over-estimated presence phylogenetic signal in trait data (Bouvier et al., 2021). We demonstrated only canonical Michaelis constant CO 2 carboxylase turnover, constants O were robust effects. further constraints limited adaptation a greater extent than combined action trade-offs. Recently, however, our claims contested Tcherkez Farquhar (2021), who argued detect an artefact species sampling, use rbcL-based trees inference, laboratory-to-laboratory variability measurements, homoplasy C 4 trait. present article, respond criticisms on point-by-point basis conclusively show all are either incorrect or invalid. As such, stand original conclusions. Specifically, magnitude overestimated analyses biases, evolution fact more constraint.

Language: Английский

Citations

1

The long and tortuous path towards improving photosynthesis by engineering elevated mesophyll conductance DOI Open Access
Alistair Leverett, Johannes Kromdijk

Authorea (Authorea), Journal Year: 2023, Volume and Issue: unknown

Published: Nov. 16, 2023

The growing demand for global food production is likely to be a defining issue facing humanity over the next 50 years. In order tackle this challenge, there desire bioengineer crops with higher photosynthetic efficiencies, increase yields. Recently, has been interest in engineering leaves mesophyll conductance ( g ), which would allow CO move more efficiently from substomatal cavities chloroplast stroma. However, if crop yield gains are realised through approach, it essential that methodological limitations associated estimating gm fully appreciated. review, we summarise these limitations, and outline uncertainties assumptions can affect final estimation of . Furthermore, critically assess predicted quantitative effect elevating will have on assimilation rates species. We highlight need theoretical modelling determine whether altering truly viable route improve performance. Finally, offer suggestions guide future research , help mitigate uncertainty inherently parameter.

Language: Английский

Citations

1

The evolutionary constraints on angiosperm chloroplast adaptation DOI Creative Commons
Elizabeth H J Robbins, Steven Kelly

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2022, Volume and Issue: unknown

Published: July 12, 2022

Abstract The chloroplast (plastid) arose via endosymbiosis of a photosynthetic cyanobacterium by non-photosynthetic eukaryotic cell approximately 1.5 billion years ago. Although the plastid underwent rapid evolution genome reduction, its rate molecular is low and organisation highly conserved. Here, we investigate factors that have constrained protein coding genes in genome. Through analysis 773 angiosperm genomes show there substantial variation between genes. We strength purifying selection major determinant evolution. further demonstrate distance gene from likely origin replication influences at which it has evolved, consistent with time dependent mutation gradients. In addition, amino acid composition product constraints substitution tolerance, limiting Finally, mRNA abundance key factor determining evolution, suggesting an interaction transcription DNA repair plastid. Collectively, location, composition, expression can account for ≥32% Thus, these three exerted limitation on capacity adaptive genes, evolvability chloroplast.

Language: Английский

Citations

2

Exploring the potential of plastid biology and biotechnology DOI Open Access
Rose McNelly, Angel Vergara Cruces, David J. Lea‐Smith

et al.

New Phytologist, Journal Year: 2023, Volume and Issue: 240(6), P. 2187 - 2190

Published: Oct. 3, 2023

Plastids are a family of organelles that likely originate from the endosymbiosis cyanobacteria (Howe et al., 2008) and exhibit diverse morphologies biochemical capabilities (Fig. 1). The chloroplast is most well-studied plastid type performs photosynthesis in plants algae thus responsible for food production on planet. However, there other important functions performed by plastids, including synthesis storage some carbohydrates, pigment production, fatty acid nitrogen sulphur assimilation. Plants have specialised types carry out these functions, such as starch-storing amyloplasts pigment-producing chromoplasts annual Plastid Preview Meeting took place 1–2 September 2022 Norwich (UK), jointly hosted John Innes Centre University East Anglia. Since 1970s, has showcased cutting-edge research PhD students early career postdoctoral scientists investigating fundamental applied biology. Research presented throughout years not only addressed questions but also areas chlorophyll biosynthesis, starch metabolism, carbon fixation, gene expression transformation. In meeting, it was apparent significant progress being made addressing long-standing with aid technological developments, machine learning, editing cryo-EM approaches to study protein structure, combined ability explore previously untapped biological diversity rapid expansion genome sequences. Three major domains were covered: first concerned 'understanding plastid', probing mechanisms govern second 'optimising plastid' focussed processes could increase productivity resilience cyanobacteria, plants. third 'utilising specifically use plastid-containing organisms biotechnology produce high-value proteins metabolites. Here, we highlight exciting work encompassing three covered at meeting. into processes, biogenesis, expression, import division, required understand how metabolism occur integrated within organelle. Protein prime example process influences many an area active discussion majority proteome encoded nucleus, imported organelle through recognition plastid-localisation signals, translocation membranes delivery appropriate location plastid. This heavily function, recent implicated ubiquitination this (Ling & Jarvis, 2015). Ling al. (2012) discovered cytosolic ubiquitin-mediated degradation pathway regulates components machinery. More recently, been observed broad range Arabidopsis, those involved photosynthesis, oxidative stress metabolic pathways (Sun 2022). opens new about role regulation well its relevance broader species types, crops. We discussed links emerging between division (Fang While nucleus can influence possesses reciprocal signal status back known retrograde signalling. Many aspects communication fully understood, several uncovered, tetrapyrroles reactive oxygen (Chan 2016). accumulate due defect allowing sense chloroplast. sensitive perturbations environmental conditions, makes ideal sentinel general cell status. As such, signalling response both abiotic biotic stresses 2016; Littlejohn 2021). An meeting pathogen infection affect nuclear genes encoding plastid-localised resistance (Corredor-Moreno Uncovering effectors hijack during roles interactions lead novel protect pathogens. Photosynthesis central chloroplasts main source energy cyanobacteria. inefficiencies RuBisCo described detail (Flamholz 2019). It be partly attributed slow evolution enzyme (Bouvier 2022) requirement balance carboxylation rates CO2/O2 specificity. highlighted strategies overcome activity. strategy based harnessing pre-existing RuBisCo. There large variation kinetics phototrophs (Savir 2010) potentially exploited replace native enzymes more efficient versions, if localised CO2 concentrations increased. Extensive modelling shows replacing wheat C4 significantly efficiency uptake (Iqbal 2021), experimentally implementing predictions may validate route increasing photosynthetic efficiency. Furthermore, where reported, particularly nonmodel species. learning becomes increasingly prevalent, employed predict sequences potential improve photosynthesis. via concentrating (CCMs). CCMs biophysical, like algal pyrenoids cyanobacterial carboxysomes, or biochemical, Recent developing mechanistic understanding form function. One breakthrough discovery Chlamydomonas reinhardtii EPYC1, which physically pyrenoid (Mackinder enhanced our assembly opened possibility engineering (Adler Similar transfer carboxysomes follow, benefitting insights structure α-carboxysome (Ni Beyond chloroplasts, manipulated crop quality, carotenoid elaioplasts Specifically, wheat, two distinct granules, A-type small B-type granules. MRC formation granules introduce desirable changes granule size properties milling industries (Chen Further come exploiting intra- interspecies will drive improvements nutritional functional quality similar way Biotechnological using biofactory key theme meetings. provides environment rest producing valuable Much attention fallen algae, especially newly fast-growing Synechococcus sp. PCC 11901 (Włodarczyk 2020), volumes cells cultivated ease smaller space compared numerous examples C. vaccine subunits, antibacterial compounds antibodies (Dyo Purton, 2018). A primary focus techniques cyanobacterial, plant biotechnology. Regulators transgenes great interest, allow robust control easy on/off switching expression. Riboswitches, instance thiamine pyrophosphate riboswitch, solution (Mehrshahi further switches tandem expand existing toolkit. Another targeting heterologous subcompartments, thylakoid lumen. would produced stable stroma (Chin-Fatt Menassa, To ensure biotechnological realised, priority toolkit transformation technologies. includes improved synthetic biology tools, example, MoClo cloning systems compatible across (Vasudevan expect Cas enzymes, beyond Cas9, function adapting base technology plastome editing. additional challenge when multiple plastids per achieving homoplasmy, (Okuzaki 2020). These methods result widespread adoption utilisation biofactories remains guided goal shining light beyond. field – variety studied, differences much natural unexplored technologies continue evolve, adopting combining different fields. Exploiting essential understand, utilise further, no doubt future Previews. thank all presenters attendees 2022, apologise whose here restrictions. possible financial support New Phytologist Foundation, Gatsby Society Experimental Biology, Li-Cor, Algae-UK, Anglia Institute Development Grant. acknowledge funding Foundation (Rotation studentships RM ÁV-C; Chris J. Leaver Fellowship DS), Royal (Research grant RGS/R2/222157 MW) Biotechnology Biological Sciences Council, UK grants BB/S020365/1 DL-S BB/W015935/1 DS; Strategic Programmes BB/X01102X/1 BB/X01097X/1 Centre). ÁV-C contributed equally work.

Language: Английский

Citations

0