Engineering a faster Rubisco in tobacco chloroplasts

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Chen et al. demonstrated that installing a bacterial-type fast Rubisco into tobacco chloroplasts to support photosynthesis. The Plant Cell (2023). https://doi.org/10.1093/plcell/koac348

By Taiyu Chen and Lu-Ning Liu

Figure legend: Engineering a Form IA Rubisco from the proteobacterium Halothiobacillus neapolitanus into tobacco chloroplasts could support growth of the transgenic tobacco lines (TobHnLS1 and TobHnLS2) in air complemented with 1% CO2, compared with WT (A). (B) Plant heights. (C), leaves numbers.

Background: Rubisco is the key enzyme responsible for fixing CO2. However, due to its intrinsically low catalytic turnover rate, Rubisco represents the ultimate rate-limiting step in plant photosynthesis. Improving Rubisco carboxylation and assembly in plants has been a long-standing challenge in crop engineering to meet the pressing need for increased global food production. There is mounting interest in replacing endogenous plant Rubisco with active non-native Rubisco candidates from other organisms to enhance photosynthetic carbon fixation.

Question: The folding and assembly of Rubisco in chloroplasts are intricate processes that usually require a series of ancillary factors. Seeking a new Rubisco variant that can be produced in chloroplasts with a high yield and high catalytic performance, without the requirement for cognate assembly factors and activases, could help improve carbon fixation in crop plants.

Finding: In this work, we introduced a Rubisco from a proteobacterium into tobacco chloroplasts to replace native tobacco Rubisco. In the proteobacteria, Rubisco is naturally encapsulated at a high density within a CO2-fixing protein organelle, the carboxysome. The foreign Rubisco derived from bacteria formed efficiently and was functional in chloroplasts without the need for exogenous chaperones. Intriguingly, the chloroplast-expressed bacterial Rubisco supported the autotrophic growth of transgenic plants at a similar rate to wild-type plants at 1% CO2.

Next Step: The successful production of functional bacterial Rubisco represents a step towards installing faster, highly active Rubisco, functional carboxysomes, and eventually active CO2-concentration mechanisms into chloroplasts to improve Rubisco carboxylation, with the intent of enhancing crop photosynthesis and crop yield on a global scale.

Reference:

Taiyu Chen, Saba Riaz, Philip Davey, Ziyu Zhao, Yaqi Sun, Gregory F. Dykes, Fei Zhou, James Hartwell, Tracy Lawson, Peter J. Nixon, Yongjun Lin, and Lu-Ning Liu. (2022). Producing fast and active Rubisco in tobacco to enhance photosynthesis. https://doi.org/10.1093/plcell/koac348

Functional and evolutionary analyses of Cullin1 proteins involved in S-RNase-Based Self-Incompatibility

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Sun et al. explore the involvement of CUL1 proteins in S-RNase-based self-incompatibility.

By Linhan Suna and Teh-hui Kaoab

aIntercollege Graduate Degree Program in Plant Biology, The Pennsylvania State University, University Park, Pennsylvania 16802

bDepartment of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, Pennsylvania 16802

Background: For any organism, inbreeding reduces fitness of the progeny.  To prevent inbreeding, plants have adopted a reproductive strategy, self-incompatibility, to allow pistils to reject genetically identical self-pollen and accept nonself pollen for fertilization. In eudicot families, such as Solanaceae, Plantaginaceae, and Rosaceae, the pistil uses a cytotoxic protein, S-RNase, to inhibit growth of self-pollen tubes.  Nonself pollen overcomes S-RNase cytotoxicity using a suite of S-locus F-box (SLF) proteins to mediate degradation of nonself S-RNases.  Each SLF is a component of a protein complex, SCFSLF.  In Petunia inflata (Solanaceae), this complex contains two pollen-specific components, PiSSK1 and PiCUL1-P.

Question: We wished to determine whether PiCUL1-P is essential for pollen to detoxify nonself S-RNases during cross-compatible pollination, and whether PiCUL1-P functions specifically in self-incompatibility. We also wanted to examine the identity of CUL1 proteins potentially involved in S-RNase-based self-incompatibility in other eudicot families.

Findings: Using CRISPR/Cas9-mediated gene knockout, we found that, in Petunia inflata, pollen lacking functional PiCUL1-P could still detoxify nonself S-RNases during cross-compatible pollination, whereas pollen lacking both PiCUL1-P and another CUL1, PiCUL1-B, could not, suggesting functional redundancy of these two CUL1 proteins.  In Petunia hybrida, we found a transposable element inserted in the promoter region of CUL1-B, which might result in drastic reduction of its transcript level, rendering PhCUL1-P essential for cross-compatibility.  We did not find CUL1-B in the other Solanaceae species examined.  Analyses of CUL1 evolution in eudicots revealed that all CUL1s involved, or potentially involved, in self-incompatibility possibly share a common ancestor.

Next steps: At the biochemical level, we want to determine the amino acids of Petunia CUL1-P and CUL1-B that are responsible for their specific interactions with SSK1 to form SCFSLF complexes.  At the evolutionary level, we want to investigate whether the CUL1 and SSK1 components of SCFSLF complexes might have co-evolved in eudicots.

Linhan Sun, Shiyun Cao, Ning Zheng, and Teh-hui Kao. (2023). Analyses of Cullin1 homologs reveal functional redundancy in S-RNase-based self-incompatibility and evolutionary relationships in eudicots https://doi.org/10.1093/plcell/koac357

Pablo González-Suárez: Plant Physiology First Author

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Pablo González-Suárez, first author of “FLOWERING LOCUS T mediates photo-thermal timing of inflorescence meristem arrest in Arabidopsis thaliana“

Current Position: PhD Student at the University of Leeds, UK.

Education: B.Sc. in Environmental Biology (Autonomous University of Barcelona), M.Sc. in Plant Biotechnology (University of Oviedo), M.Sc. in Bioinformatics and Biostatistics (Open University of Catalonia-University of Barcelona).

Non-scientific Interests: Playing the ukelele, jogging and spending time with my friends and family.

Brief bio: I am a plant biologist at heart since I discovered plant physiology and botany during my B.Sc. degree. The curiosity to understand how plants work has taken me to work with endangered species in a botanical garden, study pine trees in a forestry research industry and, more recently, embark in the Ph.D. journey. I am currently finishing my Ph.D. in the University of Leeds, where I investigate the effect of environmental conditions on the end of flowering in both Arabidopsis thaliana and wheat (Triticum aestivum).

Kang Li: The Plant Cell First Author

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Kang Li, co-first author of “Structural basis and evolution of the photosystem I–light-harvesting supercomplex of cryptophyte algae”

Current Position: staff, Pilot National Laboratory for Marine Science and Technology，China

Education:  Ph.D., Shandong University, China

Non-scientific Interests: Badminton

Brief bio: I joined Prof. Yuzhong Zhang’s lab at Shandong University for Ph.D. Based on atomic force microscopy and electron microscopy, my research focused on exploring the structure and function of peptidoglycan and important proteins of bacterial cell wall. Then I joined the Cryo-EM Center of QNLM Laboratory to explore the structure and function of important biological macromolecules such as marine viruses and light-harvesting complexes.

 

姓名：李康

目前职位：职员，崂山实验室

教育经历：山东大学微生物学博士

兴趣爱好：羽毛球

个人简介：博士期间在山东大学张玉忠课题组从事细菌细胞壁结构的研究，基于原子力显微镜和电子显微镜，探索细菌细胞壁肽聚糖及重要蛋白质的结构及功能。之后加入崂山实验室冷冻电镜中心，探索海洋病毒、捕光复合物等重要生物大分子的结构与功能。

 

Peng Wang: The Plant Cell First Author

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Peng Wang, co-first author of “Structural basis and evolution of the photosystem I–light-harvesting supercomplex of cryptophyte algae”

Current position：Associate professor, College of Marine Life Sciences, Ocean University of China, China

Education：Ph.D (2017), School of Life Sciences, Shandong University.

Non-scientific interests：Puzzle games and traveling

Brief bio：Since graduate school, I have been working in Yu-zhong Zhang’s lab on how marine microorganisms affect marine energy conversion and material cycles. Marine microorganisms play a crucial role in both material synthesis and metabolism. The unique life processes exhibited by marine microorganisms in driving the marine biogeochemical cycle are fascinating. In the beginning, I focused on the catabolism of marine sulfur/nitrogen organic matter and its ecological impact. Recently, I have also taken up the study of solar energy capture and anabolism. I am pleased to continue my work and make progress in this area.

 

个人简介：

自读研以来，我一直在张玉忠教授的实验室工作，研究海洋微生物如何影响海洋生态环境中的能量转换和物质循环。海洋微生物在海洋物质合成和分解代谢过程中发挥着至关重要的作用。海洋微生物在驱动海洋生物地球化学循环中表现出的独特生命过程令人着迷。最开始，我主要研究海洋硫/氮有机物的分解代谢及其环境生态效应。最近，我也开始研究光能捕获和有机质的合成。未来，我将继续我的工作，并在努力这一领域取得进展。

Longsheng Zhao: The Plant Cell First Author

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Longsheng Zhao, co-first author of “Structural basis and evolution of the photosystem I–light-harvesting supercomplex of cryptophyte algae” 

Current Position: Postdoctoral fellow in State Key Laboratory of Microbial Technology, and Marine Biotechnology Research Center, Shandong University, Qingdao 266237, China.

Education: Ph.D in State Key Laboratory of Microbial Technology, Shandong University, Jinan, China.

Non-scientific Interests: music, movie, badminton, cooking

Brief bio: I got my bachelor’s degree in School of Life Science, Shandong University and doctorate in the group of Prof. Yuzhong Zhang, State Key Laboratory of Microbial Technology, Shandong University. During my Ph.D, I mainly focused on the native supramolecular architecture of photosynthetic membrane in red algae, including single-cell Porphyridium cruentum and multi-cell Polysiphonia urceolata and Porphyra yezoensis, using atomic force microscope (AFM). After I got my Ph.D, I went to UK and worked in University of Liverpool as a research associate in the group of Prof. Luning Liu. Currently, I’m working in State Key Laboratory of Microbial Technology, Shandong University as a postdoctoral fellow under the supervision of Prof. Yuzhong Zhang. With the help of Prof. Liu and Prof. Zhang, I studied the structural variability, coordination and adaptation

of cyanobacterial thylakoid membranes and cryo-EM structure of cryptophyte PSI–LHCI. We applied high-resolution AFM imaging to draw a landscape view of the native arrangement of membrane complexes in the thylakoid membranes from cyanobacteria. Our results provide insight into the heterogeneity, compartmentalization, and functional regulation of the cyanobacterial photosynthetic apparatus, which is extendable to other membrane systems in bacteria, chloroplasts and mitochondria. The naturally occurring organizational features of thylakoid membranes could be important considerations for the future engineering of artificial photosynthetic systems to underpin biofuel production. The unique cryptophyte PSI–LHCI structure provides a framework for delineating the mechanisms of energy transfer and quenching in cryptophyte PSI–LHCI and understanding the evolution of red lineage photosynthesis by secondary endosymbiosis.

姓名：赵龙生

职位：博士后

工作单位：山东大学微生物技术国家重点实验室

工作简介：博士毕业于山东大学微生物技术国家重点实验室，2017年获得博士学位后，进入山东大学微生物技术国家重点实验室开展博士后研究工作。长期从事藻类光合作用的研究，以原子力显微镜藻类光合膜的超分子结构及调控机制，以冷冻电镜单颗粒分析技术研究藻类光系统超复合物结构。旨在揭示光合作用的结构基础及调控机制，为设计高效的光合作用系统以及光能生物转化系统等合成生物学研究提供理论基础。研究工作从纳米水平上展示了蓝藻光合膜上光合复合物的天然结构及相互结合方式，并解释了光合膜结构和功能的光适应调节机制。以此为基础，进一步研究了快速生长生态型蓝藻进行高效光合作用的光合膜超分子结构基础。利用冷冻电镜技术，解析了隐藻光系统I的原子分辨率结构，揭示了其能量转化机制，并为PSI的结构进化提供了重要线索。

Review: Resolving metabolic interaction mechanisms in plant microbiomes

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Life is spurred forward by the power of metabolic interactions. Within the plant microbiome, microbial communities use diverse mechanisms to thrive, survive, and multiply. In this review, Pacheco & Vorholt describe the interplay of metabolic interactions within plant microbiomes and review current approaches. Plants host a wide range of microbes with various metabolic strategies, such as polysaccharide degraders on leaves and pathogens that feed on root exudates. These interactions can significantly impact plant growth, ecosystem productivity, and nutrient use. Despite the challenges posed by the complexity of plant microbiomes, methods have been developed to discover how specific microbe interactions affect the microbiome. The creation of co-occurrence networks via high throughout sequencing melded with microbial lifestyle characteristics can provide insight into interplay of microbial interactions and metabolic reactions. As examples, some bacteria co-occur with others due to cross-feeding, and plant root exudates change upon interaction with some bacteria.  In addition, the authors examine how synthetic communities can reveal how the presence or behavior of one species affects the growth, survival, or reproduction of another species. Furthermore, predictive computational community modeling can be employed to understand community dynamics and integrate the previously described approaches to positively impact crop protection. (Summary by Eric Hobson @ehobs) Curr Opin Microbiol 10.1016/j.mib.2023.102317

Review: Why don’t genetically identical seeds germinate at the same time?

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If you’ve ever conducted a germination experiment, you’ve probably asked yourself: what causes seeds to germinate at different times? The most obvious answer would be to point to genetic differences, but this phenomenon also occurs in genetically identical seeds. In this exciting paper, Sharma and Majee bring us a comprehensive review of the different physiological and molecular mechanisms that have been proposed, including transcriptional heterogeneity and noise, epigenetic diversity, and biomolecular condensates. All these mechanisms point out potential sources of variation in gene expression, phytohormone concentrations and the biochemical availability of these compounds that can lead to a seed germinating more or less quickly. The review also discusses the ecological advantages of seed germination variability and how modern techniques, such as seed priming, can reduce it and ensure higher synchronization in agricultural contexts. While there does not appear to be a definitive answer to explain germination heterogeneity, this review paves the way for future research to help us understand the mechanisms behind it. (Summary by Carlos A. Ordóñez-Parra @caordonezparra) J. Exp. Bot. 10.1093/jxb/erad101

Review: The role of ethylene in plant temperature stress response

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The phytohormone ethylene is known for its importance in plant development and mostly for its role in fruit ripening. However, in this review Huang et al. summarize recent findings on ethylene’s role in temperature (hot and cold) stress response and ethylene crosstalk with other hormones. Interestingly, different plants respond to heat stress differently. For example, heat stress induces ethylene production in Arabidopsis, wheat, and pea whereas it inhibits ethylene production in tomato and lettuce. These effects are also tissue specific; in Arabidopsis, at 45°C ethylene levels in roots and shoot apices remain unchanged but are induced in leaves. Furthermore, thermotolerance of many plants is induced by external application of ACC (an ethylene precursor) or ethephon (converted to ethylene in the plant). Generally, the heat-stress responses are mediated by heat shock proteins, which are induced by heat shock transcription factors, and in Arabidopsis ethylene signaling activates some heat shock transcription factors. Ethylene also mediates freezing tolerance in a species-specific manner. Freezing tolerance in tomato, tobacco and Arabidopsis is increased by ACC application, whereas inhibitors of ethylene synthesis improve freezing tolerance in Medicago truncatula. Thus, effects of ethylene stress response can be positive or negative depending on plant species and developmental stages. Transcription factors in the AP2/ERFs family integrate BR, JA and ABA signaling and could provide targets for genetic efforts to enhance plant tolerance to heat or cold stress. (Summary by Indrani Kakati, @indranikb)  Trends Plant Sci. 10.1016/j.tplants.2023.03.001