Pub Date : 2025-11-17DOI: 10.1007/s11120-025-01184-z
Vladimir I Novoderezhkin
We model the energy transfers between two B850 antenna units using the hybrid hierarchical equation (HEOM) method, where intra-B850 dynamics is evaluated nonperturbatively using HEOM, whereas inter-B850 transfers are treated by the generalized Förster theory. To account for a conformation-induced energetic disorder we use a realistic model emerging from a quantitative explanation of the single molecule spectral fluctuations in the B850 antenna. The disorder produces a variety of configurations including realizations where the exciton states are predominantly localized at the red-shifted sites. A slow detrapping of excitation from the red states can compete with the transfers to the adjacent B850 unit, thus slowing down the whole equilibration dynamics. In order to highlight the interplay between intra-B850 dynamics and migration to neighboring B850 complex we analyze the diversity of scenarios produced by specific disorder patterns within both donor and acceptor units.
{"title":"Energy transfers between the B850 antennas: hybrid hierarchical equation approach.","authors":"Vladimir I Novoderezhkin","doi":"10.1007/s11120-025-01184-z","DOIUrl":"10.1007/s11120-025-01184-z","url":null,"abstract":"<p><p>We model the energy transfers between two B850 antenna units using the hybrid hierarchical equation (HEOM) method, where intra-B850 dynamics is evaluated nonperturbatively using HEOM, whereas inter-B850 transfers are treated by the generalized Förster theory. To account for a conformation-induced energetic disorder we use a realistic model emerging from a quantitative explanation of the single molecule spectral fluctuations in the B850 antenna. The disorder produces a variety of configurations including realizations where the exciton states are predominantly localized at the red-shifted sites. A slow detrapping of excitation from the red states can compete with the transfers to the adjacent B850 unit, thus slowing down the whole equilibration dynamics. In order to highlight the interplay between intra-B850 dynamics and migration to neighboring B850 complex we analyze the diversity of scenarios produced by specific disorder patterns within both donor and acceptor units.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"61"},"PeriodicalIF":3.7,"publicationDate":"2025-11-17","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145541907","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-11-12DOI: 10.1007/s11120-025-01180-3
Gabriella Dickinson, Lauren R Stutts, Scott Latimer, Nathan Smith, Zhaniya Batyrshina, Monika Kula-Maximenko, Ireneusz Ślesak, Anna K Block, Mark A Wilson, Gilles J Basset
Cyanobacteria and plastids harbor two prenylated quinones that serve as vital photosynthetic cofactors. One is a naphthoquinone (phylloquinone or menaquinone depending on the species), the naphthalene ring of which is always methylated in ortho of the prenyl chain. The other one is a benzoquinone, called plastoquinone-9, the benzenoid ring of which is, in contrast, never methylated at this position. In oxygenic phototrophs, such an arrangement is thought to have driven the evolution and retention of unique quinol C-methyltransferases that act exclusively on naphthoquinol substrates. Here, we identified quinol C-methyltransferases in two extant taxa of early cyanobacterial lineages, Gloeobacter violaceus and Synechococcus sp. JA-2-3B'a, that did not discriminate between naphthoquinol and benzoquinol substrates when these enzymes were expressed in Escherichia coli. Quinone analysis showed, however, that G. violaceus extracts did not contain any detectable amounts of methyl-plastoquinone-9. Furthermore, functional complementation assays in the cyanobacterium Synechocystis sp. PCC 6803 revealed that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases displayed either strict or marked substrate preference for demethyl-phylloquinol. Taken together, these data suggest that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases are the remnants of a promiscuous enzyme present during the emergence of plastoquinone as a photosynthetic electron carrier.
{"title":"Quinol C-methyltransferases from extant species of early cyanobacterial lineages shed light on the emergence of plastoquinone in oxygenic phototrophs.","authors":"Gabriella Dickinson, Lauren R Stutts, Scott Latimer, Nathan Smith, Zhaniya Batyrshina, Monika Kula-Maximenko, Ireneusz Ślesak, Anna K Block, Mark A Wilson, Gilles J Basset","doi":"10.1007/s11120-025-01180-3","DOIUrl":"10.1007/s11120-025-01180-3","url":null,"abstract":"<p><p>Cyanobacteria and plastids harbor two prenylated quinones that serve as vital photosynthetic cofactors. One is a naphthoquinone (phylloquinone or menaquinone depending on the species), the naphthalene ring of which is always methylated in ortho of the prenyl chain. The other one is a benzoquinone, called plastoquinone-9, the benzenoid ring of which is, in contrast, never methylated at this position. In oxygenic phototrophs, such an arrangement is thought to have driven the evolution and retention of unique quinol C-methyltransferases that act exclusively on naphthoquinol substrates. Here, we identified quinol C-methyltransferases in two extant taxa of early cyanobacterial lineages, Gloeobacter violaceus and Synechococcus sp. JA-2-3B'a, that did not discriminate between naphthoquinol and benzoquinol substrates when these enzymes were expressed in Escherichia coli. Quinone analysis showed, however, that G. violaceus extracts did not contain any detectable amounts of methyl-plastoquinone-9. Furthermore, functional complementation assays in the cyanobacterium Synechocystis sp. PCC 6803 revealed that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases displayed either strict or marked substrate preference for demethyl-phylloquinol. Taken together, these data suggest that G. violaceus and S. sp. JA-2-3B'a quinol C-methyltransferases are the remnants of a promiscuous enzyme present during the emergence of plastoquinone as a photosynthetic electron carrier.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"59"},"PeriodicalIF":3.7,"publicationDate":"2025-11-12","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145506308","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
In this study, we aimed to understand the role of cyclic electron transport (CET) in the acclimation process in response to high salinity stress by comparing wild-type Chlamydomonas reinhardtii with CET deficient mutants, Proton Gradient Regulation 5 (PGR5), and Proton Gradient Regulation Like 1 (PGRL1). Cells grown in photoautotrophic conditions under salt stress resulted in a primary reduction in growth and chlorophyll fluorescence, as well as OJIP transient kinetics under salt stress, indicative of diminished photochemical efficiency. Notably, all strains exhibited a decrease in the variable fluorescence, and the non-photochemical quenching was accompanied by an increase in non-regulated energy dissipation. Additionally, salt treatment resulted in a reduction in total chlorophyll content and a related increase in carotenoid levels like violaxanthin, zeaxanthin, and lutein, and these levels were more pronounced in the pgr5. These alterations are likely linked to enhanced reactive oxygen species (ROS) generation under salt stress. The mutants were more sensitive to ROS and showed more carotenoid content than the wild type, suggesting a compensatory photoprotective mechanism. The circular dichroism data showed that the salt stress caused changes in pigment-pigment and pigment-protein interactions, which were more significant in mutants. When cells are exposed to high salt, there is a dynamic change in the core proteins, but light-harvesting complexes and antenna proteins of photosystem (PS) I and PSII are not much affected. Further, changes in cell morphology and thylakoid membrane organization were also observed in high salt stress. These data indicate PSI remodeling, defined here as stress-induced dissociation/rearrangement of PSI-LHCI(-LHCII) super complexes, reductions in PsaA/B abundance consistent with PSI core destabilization, and loss of thylakoid macro-domain order, particularly pronounced in pgr5.
{"title":"Investigating the role of PGR5 and PGRL1 in photosynthetic acclimation to salt stress in Chlamydomonas reinhardtii.","authors":"Siva Naga Sai Damaraju, Ranay Mohan Yadav, Namrata Dubey, Pavithra Ramachandran, Jyoti Ranjan Rath, Jerome Xavier Gunasekaran, Shriya Sharma, Rajagopal Subramanyam","doi":"10.1007/s11120-025-01179-w","DOIUrl":"10.1007/s11120-025-01179-w","url":null,"abstract":"<p><p>In this study, we aimed to understand the role of cyclic electron transport (CET) in the acclimation process in response to high salinity stress by comparing wild-type Chlamydomonas reinhardtii with CET deficient mutants, Proton Gradient Regulation 5 (PGR5), and Proton Gradient Regulation Like 1 (PGRL1). Cells grown in photoautotrophic conditions under salt stress resulted in a primary reduction in growth and chlorophyll fluorescence, as well as OJIP transient kinetics under salt stress, indicative of diminished photochemical efficiency. Notably, all strains exhibited a decrease in the variable fluorescence, and the non-photochemical quenching was accompanied by an increase in non-regulated energy dissipation. Additionally, salt treatment resulted in a reduction in total chlorophyll content and a related increase in carotenoid levels like violaxanthin, zeaxanthin, and lutein, and these levels were more pronounced in the pgr5. These alterations are likely linked to enhanced reactive oxygen species (ROS) generation under salt stress. The mutants were more sensitive to ROS and showed more carotenoid content than the wild type, suggesting a compensatory photoprotective mechanism. The circular dichroism data showed that the salt stress caused changes in pigment-pigment and pigment-protein interactions, which were more significant in mutants. When cells are exposed to high salt, there is a dynamic change in the core proteins, but light-harvesting complexes and antenna proteins of photosystem (PS) I and PSII are not much affected. Further, changes in cell morphology and thylakoid membrane organization were also observed in high salt stress. These data indicate PSI remodeling, defined here as stress-induced dissociation/rearrangement of PSI-LHCI(-LHCII) super complexes, reductions in PsaA/B abundance consistent with PSI core destabilization, and loss of thylakoid macro-domain order, particularly pronounced in pgr5.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"58"},"PeriodicalIF":3.7,"publicationDate":"2025-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145445524","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-10-30DOI: 10.1007/s11120-025-01176-z
Wojciech Giera, Krzysztof Gibasiewicz
{"title":"Photophysical model of primary charge separation in green algal photosystem I based on combined analysis of time-resolved absorption and fluorescence spectra.","authors":"Wojciech Giera, Krzysztof Gibasiewicz","doi":"10.1007/s11120-025-01176-z","DOIUrl":"10.1007/s11120-025-01176-z","url":null,"abstract":"","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"57"},"PeriodicalIF":3.7,"publicationDate":"2025-10-30","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12575488/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145409715","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-10-24DOI: 10.1007/s11120-025-01177-y
K K Naidoo, G Naidoo
{"title":"Photosynthetic response of the invasive weed Chromolaena odorata to glyphosate.","authors":"K K Naidoo, G Naidoo","doi":"10.1007/s11120-025-01177-y","DOIUrl":"10.1007/s11120-025-01177-y","url":null,"abstract":"","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"55"},"PeriodicalIF":3.7,"publicationDate":"2025-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145355712","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-10-23DOI: 10.1007/s11120-025-01178-x
Győző Garab
The technique of chlorophyll-a fluorescence induction (ChlF) is widely used in plant biology. The 'mainstream', so-called QA model of ChlF, posits that the reaction centers (RCs) of Photosystem-II (PSII) exist in two states, quenched (Fo) or open (PSIIO), and unquenched (Fm) or closed (PSIIC), containing the primary quinone acceptor, QA, in oxidized and reduced state, respectively; and that the quantum yield of PSII photochemistry of a dark-adapted sample is Y(II) = Fv/Fm, where Fv=Fm-Fo. The widespread application of ChlF, with user-friendly instruments, and the use of the QA model, have substantially contributed to our understanding of the operation of the photosynthetic machineries under different environmental conditions. However, recent experimental data - multiple light-induced fluorescence increments in PSIIC; the complex, pH and temperature dependent kinetic and spectral features of key ChlF parameters; twith enhanced stabilization of the charges - cannot be reconciled with the QA model. These features are explained by subtle conformational transitions driven by stationary and transient electric fields and associated dielectric relaxation processes. This interpretation, while invites further studies, places the hitherto unknown structural and functional plasticity of the RC matrix in the context of its physiological significance.
{"title":"Revisiting the Q<sub>A</sub> model of chlorophyll-a fluorescence induction: new perspectives to monitor the photochemical activity and structural dynamics of photosystem II.","authors":"Győző Garab","doi":"10.1007/s11120-025-01178-x","DOIUrl":"10.1007/s11120-025-01178-x","url":null,"abstract":"<p><p>The technique of chlorophyll-a fluorescence induction (ChlF) is widely used in plant biology. The 'mainstream', so-called Q<sub>A</sub> model of ChlF, posits that the reaction centers (RCs) of Photosystem-II (PSII) exist in two states, quenched (F<sub>o</sub>) or open (PSII<sub>O</sub>), and unquenched (F<sub>m</sub>) or closed (PSII<sub>C</sub>), containing the primary quinone acceptor, Q<sub>A</sub>, in oxidized and reduced state, respectively; and that the quantum yield of PSII photochemistry of a dark-adapted sample is Y(II) = F<sub>v</sub>/F<sub>m</sub>, where F<sub>v</sub>=F<sub>m</sub>-F<sub>o</sub>. The widespread application of ChlF, with user-friendly instruments, and the use of the Q<sub>A</sub> model, have substantially contributed to our understanding of the operation of the photosynthetic machineries under different environmental conditions. However, recent experimental data - multiple light-induced fluorescence increments in PSII<sub>C</sub>; the complex, pH and temperature dependent kinetic and spectral features of key ChlF parameters; twith enhanced stabilization of the charges - cannot be reconciled with the Q<sub>A</sub> model. These features are explained by subtle conformational transitions driven by stationary and transient electric fields and associated dielectric relaxation processes. This interpretation, while invites further studies, places the hitherto unknown structural and functional plasticity of the RC matrix in the context of its physiological significance.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 6","pages":"54"},"PeriodicalIF":3.7,"publicationDate":"2025-10-23","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12549761/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145346376","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Leaf photosynthetic rate serves as a growth indicator in plant science; however, the high cost (exceeding USD 70,000) of traditional measurement system is the main concern when making photosynthesis measurements of interest to a wide range of users. Recently, the availability of inexpensive environmental sensors and single-board microcomputers has increased substantially. In this study, we selected CO2 sensors based on a comparative analysis of four cost-effective sensors. The economical K30 sensor demonstrated a superior response to CO2 fluctuations, compared to the other tested low-cost sensors, and exhibited noise-free stability relative to the values recorded by the high-precision system (LI-850). A closed-chamber system was constructed, incorporating the K30 sensor into a self-made chamber controlled by a single-board microcomputer. The materials for the demo device incurred an approximate cost of USD 200, resulting in a low overall expense. Leaf photosynthesis measurements for sugarcane germplasm from the demo device were compared with those from a standard open system (LI-6400), revealing a significant correlation (p < 0.001). The root mean square error (RMSE) and relative RMSE were 1.4 and 7.6% under artificial light conditions (n = 50) and 3.6 and 13.3% under natural field light conditions (n = 45), respectively. The constructed low-cost photosynthesis measurement system, utilizing the K30 CO₂ sensor and a single-board microcomputer, demonstrated high responsiveness and accuracy comparable to commercial standard systems, thereby making it accessible and practical for a broader range of users. Future work will involve selecting an inexpensive humidity sensor and establishing a system for measuring water-use efficiency.
{"title":"Establishment of a low-cost photosynthesis measurement system based on a single-board microcomputer and CO<sub>2</sub> sensors.","authors":"Hiroo Takaragawa, Tomoki Asahi, Muneshi Mitsuoka, Eizo Taira, Yoshinobu Kawamitsu","doi":"10.1007/s11120-025-01170-5","DOIUrl":"10.1007/s11120-025-01170-5","url":null,"abstract":"<p><p>Leaf photosynthetic rate serves as a growth indicator in plant science; however, the high cost (exceeding USD 70,000) of traditional measurement system is the main concern when making photosynthesis measurements of interest to a wide range of users. Recently, the availability of inexpensive environmental sensors and single-board microcomputers has increased substantially. In this study, we selected CO<sub>2</sub> sensors based on a comparative analysis of four cost-effective sensors. The economical K30 sensor demonstrated a superior response to CO<sub>2</sub> fluctuations, compared to the other tested low-cost sensors, and exhibited noise-free stability relative to the values recorded by the high-precision system (LI-850). A closed-chamber system was constructed, incorporating the K30 sensor into a self-made chamber controlled by a single-board microcomputer. The materials for the demo device incurred an approximate cost of USD 200, resulting in a low overall expense. Leaf photosynthesis measurements for sugarcane germplasm from the demo device were compared with those from a standard open system (LI-6400), revealing a significant correlation (p < 0.001). The root mean square error (RMSE) and relative RMSE were 1.4 and 7.6% under artificial light conditions (n = 50) and 3.6 and 13.3% under natural field light conditions (n = 45), respectively. The constructed low-cost photosynthesis measurement system, utilizing the K30 CO₂ sensor and a single-board microcomputer, demonstrated high responsiveness and accuracy comparable to commercial standard systems, thereby making it accessible and practical for a broader range of users. Future work will involve selecting an inexpensive humidity sensor and establishing a system for measuring water-use efficiency.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 5","pages":"52"},"PeriodicalIF":3.7,"publicationDate":"2025-10-14","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12521330/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145286720","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2025-09-29DOI: 10.1007/s11120-025-01173-2
Yuan Xu, Stephanie C Schmiege, Thomas D Sharkey
In leaves, major CO₂ fluxes alternate between fixation by the Calvin-Benson-Bassham (CBB) cycle during light and release by the tricarboxylic acid (TCA) cycle in darkness. The speed at which leaf metabolism transitions between these pathways likely influences plant tolerance to fluctuating light conditions. To investigate these rapid metabolic shifts, we exposed leaves to ¹³CO₂ for 20 min to establish a quasi-steady state before abruptly turning off the light while maintaining ¹³CO₂ feeding. Within 10 s of dark transition, 3-phosphoglycerate levels rose significantly while most other CBB cycle intermediates decreased by more than 90%. Simultaneously, carbon accumulated in alanine, likely via pyruvate. Over the subsequent 10 min, six- and five-carbon TCA cycle intermediates steadily increased. In contrast, four-carbon TCA intermediates peaked at one minute, declined at three minutes, and rose again at 10 min, a pattern mirrored by most measured amino acids. These results reveal an exceptionally rapid metabolic reconfiguration from CO₂ fixation by the CBB cycle in light to TCA cycle activation for energy production in darkness, accompanied by substantial changes in amino acid metabolism.
{"title":"Time-resolved targeted metabolomics shows an abrupt switch from Calvin-Benson-Bassham cycle to tricarboxylic acid cycle when the light is turned off.","authors":"Yuan Xu, Stephanie C Schmiege, Thomas D Sharkey","doi":"10.1007/s11120-025-01173-2","DOIUrl":"10.1007/s11120-025-01173-2","url":null,"abstract":"<p><p>In leaves, major CO₂ fluxes alternate between fixation by the Calvin-Benson-Bassham (CBB) cycle during light and release by the tricarboxylic acid (TCA) cycle in darkness. The speed at which leaf metabolism transitions between these pathways likely influences plant tolerance to fluctuating light conditions. To investigate these rapid metabolic shifts, we exposed leaves to ¹³CO₂ for 20 min to establish a quasi-steady state before abruptly turning off the light while maintaining ¹³CO₂ feeding. Within 10 s of dark transition, 3-phosphoglycerate levels rose significantly while most other CBB cycle intermediates decreased by more than 90%. Simultaneously, carbon accumulated in alanine, likely via pyruvate. Over the subsequent 10 min, six- and five-carbon TCA cycle intermediates steadily increased. In contrast, four-carbon TCA intermediates peaked at one minute, declined at three minutes, and rose again at 10 min, a pattern mirrored by most measured amino acids. These results reveal an exceptionally rapid metabolic reconfiguration from CO₂ fixation by the CBB cycle in light to TCA cycle activation for energy production in darkness, accompanied by substantial changes in amino acid metabolism.</p>","PeriodicalId":20130,"journal":{"name":"Photosynthesis Research","volume":"163 5","pages":"51"},"PeriodicalIF":3.7,"publicationDate":"2025-09-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12479584/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"145192380","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}