Maya Matsumoto, Clare Hanneman, A. G. Camara, Stacy A. Krueger-Hadfield, Trinity L. Hamilton, Robin B. Kodner
{"title":"Hypothesized life cycle of the snow algae Chlainomonas sp. (Chlamydomonadales, Chlorophyta) from the Cascade Mountains, USA","authors":"Maya Matsumoto, Clare Hanneman, A. G. Camara, Stacy A. Krueger-Hadfield, Trinity L. Hamilton, Robin B. Kodner","doi":"10.1111/jpy.13454","DOIUrl":"10.1111/jpy.13454","url":null,"abstract":"<p><i>Chlainomonas</i> (Chlamydomonadales, Chlorophyta) is one of the four genera of snow algae known to produce annual pink or red blooms in alpine snow. No <i>Chlainomonas</i> species have been successfully cultured in the laboratory, but diverse cell types have been observed from many field-collected samples, from multiple species. The diversity of morphologies suggests these algae have complex life cycles with changes in ploidy. Over 7 years (2017–2023), we observed seasonal blooms dominated by a <i>Chlainomonas</i> species from late spring through the summer months on a snow-on-lake habitat in an alpine basin in the North Cascade Mountains of Washington, USA. The Bagley Lake <i>Chlainomonas</i> is distinct from previously reported species based on morphology and sequence data. We observed a similar collection of cell types observed in other <i>Chlainomonas</i> species, with the addition of swarming biflagellate cells that emerged from sporangia. We present a life cycle hypothesis for this species that links cell morphologies observed in the field to seasonally available habitat. The progression of cell types suggests cells are undergoing both meiosis and fertilization in the life cycle. Since the life cycle is the most fundamental biological feature of an organism, with direct consequences for evolutionary processes, it is critical to understand how snow algal life cycles will influence their responses to changes in their habitat driven by climate warming. For microbial taxa that live in extreme environments and are difficult to culture, temporal field studies, such as we report here, may be key to creating testable hypotheses for life cycles.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"724-740"},"PeriodicalIF":2.9,"publicationDate":"2024-05-02","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140828240","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}
{"title":"Diversity of genome size and chromosome number in homothallic and heterothallic strains of the Closterium peracerosum–strigosum–littorale complex (Desmidiales, Zygnematophyceae, Streptophyta)","authors":"Yuki Tsuchikane, Misaki Watanabe, Yawako W. Kawaguchi, Koichi Uehara, Tomoaki Nishiyama, Hiroyuki Sekimoto, Takashi Tsuchimatsu","doi":"10.1111/jpy.13457","DOIUrl":"10.1111/jpy.13457","url":null,"abstract":"<p>The evolutionary transitions of mating systems between outcrossing and self-fertilization are often suggested to associate with the cytological and genomic changes, but the empirical reports are limited in multicellular organisms. Here we used the unicellular zygnematophycean algae, the <i>Closterium peracerosum–strigosum–littorale</i> (<i>C. psl.</i>) complex, to address whether genomic properties such as genome sizes and chromosome numbers are associated with mating system transitions between homothallism (self-fertility) and heterothallism (self-sterility). Phylogenetic analysis revealed the polyphyly of homothallic strains, suggesting multiple transitions between homothallism and heterothallism in the <i>C. psl.</i> complex. Flow cytometry analysis identified a more than 2-fold genome size variation, ranging from 0.53 to 1.42 Gbp, which was positively correlated with chromosome number variation between strains. Although we did not find consistent trends in genome size change and mating system transitions, the mean chromosome sizes tend to be smaller in homothallic strains than in their relative heterothallic strains. This result suggests that homothallic strains possibly have more fragmented chromosomes, which is consistent with the argument that self-fertilizing populations may tolerate more chromosomal rearrangements.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"654-667"},"PeriodicalIF":2.9,"publicationDate":"2024-04-28","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140812112","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}
Marlene Dordoni, Jörg Tittel, Yvonne Rosenlöcher, Karsten Rinke, Johannes A. C. Barth
{"title":"Metabolic activity of Planktothrix rubescens and its consequences on oxygen dynamics in laboratory experiment: A stable isotope study","authors":"Marlene Dordoni, Jörg Tittel, Yvonne Rosenlöcher, Karsten Rinke, Johannes A. C. Barth","doi":"10.1111/jpy.13455","DOIUrl":"10.1111/jpy.13455","url":null,"abstract":"<p>Fluctuations in dissolved oxygen (DO) contents in natural waters can become intense during cyanobacteria blooms. In a reconnaissance study, we investigated DO concentrations and stable isotope dynamics during a laboratory experiment with the cyanobacterium <i>Planktothrix rubescens</i> in order to obtain insights into primary production under specific conditions. This observation was extended to sub-daily timescales with alternating light and dark phases. Dissolved oxygen concentrations and its isotopes (δ<sup>18</sup>O<sub>DO</sub>) ranged from 0.02 to 0.06 mmol · L<sup>−1</sup> and from +9.6‰ to +23.4‰. The δ<sup>18</sup>O<sub>DO</sub> proved to be more sensitive than concentration measurements in response to metabolic variation and registered earlier shifts to dominance by respiration. Oxygen (O<sub>2</sub>) contents in the headspace and its isotopes (δ<sup>18</sup>O<sub>O2</sub>) ranged from 2.62 to 3.20 mmol · L<sup>−1</sup> and from +9.8‰ to +21.9‰. Headspace samples showed less fluctuations in concentration and isotope trends because aquatic processes were hardly able to alter signals once the gas had reached the headspace. Headspace δ<sup>18</sup>O<sub>O2</sub> values were corrected for gas–water equilibration and were determined to be higher than the mean δ<sup>18</sup>O<sub>H2O</sub> of −8.7‰. This finding suggests that counteracting respiration was important even during the highest photosynthetic activity. Additionally, headspace analyses led to the definition of a fractionation factor for respiration (<i>α</i><sub><i>R</i></sub>) of this cyanobacterium with a value of 0.980. This value confirms the one commonly used for cyanobacteria. Our findings may become important for the management of water bodies where decreases in DO are caused by cyanobacteria.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"642-653"},"PeriodicalIF":2.9,"publicationDate":"2024-04-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140623812","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}
Shiri Graff van Creveld, Sacha N. Coesel, Megan J. Schatz, E. Virginia Armbrust
{"title":"New eukaryotic phytoplankton isolates from the oligotrophic tropical Pacific Ocean","authors":"Shiri Graff van Creveld, Sacha N. Coesel, Megan J. Schatz, E. Virginia Armbrust","doi":"10.1111/jpy.13447","DOIUrl":"10.1111/jpy.13447","url":null,"abstract":"<p>Marine food webs are based primarily upon unicellular phytoplankton that are diverse in their taxonomy, physiology, and cell size. Eukaryotic phytoplankton are present throughout the world's open oceans, yet current culture collections are dominated by isolates derived from coastal and estuarine ecosystems. Consequently, the physiology and distribution patterns of open ocean eukaryotic phytoplankton are poorly described, and their DNA sequences are lacking from marine reference libraries. To address this gap, we isolated 46 unialgal strains of eukaryotic phytoplankton from the tropical Pacific Ocean during two research expeditions. The isolates grouped in 29 distinct V4–V5 regions of 18S rDNA gene with representatives from each of the five major photosynthetic groups: Bacillariophyta (20 distinct sequences), Pelagophyceae (four distinct sequences), Haptophyta (two distinct sequences), Dinophyceae (two distinct sequences), and Chlorophyta (one sequence). Thirty-nine isolates persist in culture and have been deposited into the NCMA culture collection and are available for further study.</p><p>The Pacific Ocean covers about one-third of Earth's surface and includes the largest ecosystems on the planet, yet the biological components of these ecosystems remain understudied (Dai et al., <span>2023</span>). Open ocean eukaryotic phytoplankton, particularly from the Pacific Ocean, are underrepresented in algal culture collections and molecular datasets. For example, although diatoms (Bacillariophyta) persist in oligotrophic gyres and thrive in transition zones, in nutrient upwelling regions, and during nutrient enrichment events (Brzezinski et al., <span>1998</span>; Dore et al., <span>2008</span>; Villareal et al., <span>2012</span>), only two diatom strains (CCMP1014, CCMP1120) from the tropical/subtropical Pacific Ocean are available in major algal culture collections (NCMA, RCC, CCAP, NIES), and a single Pacific open ocean diatom has publicly available genome sequence data (GenBank GCA_946965045.2, 2023). Coastal and oceanic isolates of the same species can exhibit differences in growth rate, chlorophyll content, isotope fractionation, and response to elevated CO<sub>2</sub> (McCarthy et al., <span>2012</span>; Sutton et al., <span>2013</span>). As oligotrophic ocean gyres are expected to expand with global warming (Polovina et al., <span>2008</span>), it is increasingly important to understand the physiology, genetics, and genomics of the phytoplankton that fuel these ecosystems.</p><p>Here we report the isolation and taxonomic identification of 46 eukaryotic phytoplankton strains from two expeditions to the tropical Pacific Ocean (Figure 1a,b) in November–December 2021 (Gradients 4, TN397) and January–February 2023 (Gradients 5, TN412). At sea, seawater samples were collected and supplemented to a final concentration of a 100-fold dilution of common algal media (f/2, L1, or K; Haines & Guillard, <span>1974</span>, Guillard & Hargraves, <","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"598-603"},"PeriodicalIF":2.9,"publicationDate":"2024-04-16","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jpy.13447","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140576347","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}
{"title":"From rubies to rosettes","authors":"Thomas Leya","doi":"10.1111/jpy.13445","DOIUrl":"https://doi.org/10.1111/jpy.13445","url":null,"abstract":"","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 2","pages":"273-274"},"PeriodicalIF":2.9,"publicationDate":"2024-04-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140541009","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}
{"title":"Validation of the names Cavernulicolales, Cavernulicolaceae, Cavernulicola, and Cavernulicola chilensis (Rhodophyta)","authors":"Hwan Su Yoon, Emanuele Del Guacchio","doi":"10.1111/jpy.13452","DOIUrl":"10.1111/jpy.13452","url":null,"abstract":"<p>A reclassification of <i>Cyanidium chilense</i> under the new genus <i>Cavernulicola</i> was recently proposed together with a new family (Cavernulicolaceae) and a new order (Cavernulicolales). Unfortunately, due to an error in the required citation of the basionym, the name “<i>Cavernulicola chilensis</i>” was invalid and cannot be accepted as the generitype of <i>Cavernulicola</i>. This means that <i>Cavernulicola</i>, <i>Cavernulicolaceae</i>, and <i>Cavernulicolales</i> are likewise invalid names under the provisions of the International Code of Nomenclature for algae, fungi, and plants (ICN, Shenzhen Code). In this contribution, each of these names is validated.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"778-779"},"PeriodicalIF":2.9,"publicationDate":"2024-04-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140576083","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}
Jaide Phelps, Kenneth Dunton, Brenda Konar, Schery Umanzor, Arley Muth, Katrin Iken
{"title":"The effect of sedimentation on spore settlement and recruitment of the endemic Arctic kelp, Laminaria solidungula (Phaeophyceae)","authors":"Jaide Phelps, Kenneth Dunton, Brenda Konar, Schery Umanzor, Arley Muth, Katrin Iken","doi":"10.1111/jpy.13453","DOIUrl":"10.1111/jpy.13453","url":null,"abstract":"<p>Environmental changes associated with rapid climate change in the Arctic, such as the increased rates of sedimentation from climatic or anthropogenic sources, can enhance the impact of abiotic stressors on coastal ecosystems. High sedimentation rates can be detrimental to nearshore kelp abundance and distribution, possibly due to increased mortality at the spore settlement stage. Spore settlement and viability of the Arctic kelp <i>Laminaria solidungula</i> were examined through a series of lab-based sedimentation experiments. Spores were exposed to increasing sediment loads in three experimental designs simulating different sedimentation scenarios: sediment deposition above settled spores, settlement of spores on sediment-covered substrate, and simultaneous suspension of spores and sediments during settlement. Spore settlement was recorded upon completion of each experiment, and gametophyte abundance was assessed following a growth period with sediments removed to examine short-term spore viability via a gametophyte-to-settled-spore ratio. In all three types of sediment exposure, the addition of sediments caused a 30%–40% reduction in spore settlement relative to a no-sediment control. Spore settlement decreased significantly between the low and high sediment treatments when spores were settled onto sediment-covered substrates. In all experiments, increasing amounts of sediment had no significant effect on spore viability, indicating that spores that had settled under different short-term sediment conditions were viable. Our results indicate that depending on spore-sediment interaction type, higher rates of sedimentation resulting from increased sediment loading could affect <i>L. solidungula</i> spore settlement success with potential impacts on the long-term persistence of a diverse and productive benthic habitat.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"741-754"},"PeriodicalIF":2.9,"publicationDate":"2024-04-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140576162","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}
Juan C. Montes-Herrera, Emiliano Cimoli, Vonda J. Cummings, Roberta D'Archino, Wendy A. Nelson, Arko Lucieer, Vanessa Lucieer
{"title":"Quantifying pigment content in crustose coralline algae using hyperspectral imaging: A case study with Tethysphytum antarcticum (Ross Sea, Antarctica)","authors":"Juan C. Montes-Herrera, Emiliano Cimoli, Vonda J. Cummings, Roberta D'Archino, Wendy A. Nelson, Arko Lucieer, Vanessa Lucieer","doi":"10.1111/jpy.13449","DOIUrl":"10.1111/jpy.13449","url":null,"abstract":"<p>Crustose coralline algae (CCA) are a highly diverse group of habitat-forming, calcifying red macroalgae (Rhodophyta) with unique adaptations to diverse irradiance regimes. A distinctive CCA phenotype adaptation, which allows them to maximize photosynthetic performance in low light, is their content of a specific group of light-harvesting pigments called phycobilins. In this study, we assessed the potential of noninvasive hyperspectral imaging (HSI) in the visible spectrum (400–800 nm) to describe the phenotypic variability in phycobilin content of an Antarctic coralline, <i>Tethysphytum antarcticum</i> (Hapalidiales), from two distinct locations. We validated our measurements with pigment extractions and spectrophotometry analysis, in addition to DNA barcoding using the <i>psb</i>A marker. Targeted spectral indices were developed and correlated with phycobilin content using linear mixed models (<i>R</i><sup>2</sup> = 0.64–0.7). Once applied to the HSI, the models revealed the distinct phycoerythrin spatial distribution in the two site-specific CCA phenotypes, with thin and thick crusts, respectively. This study advances the capabilities of hyperspectral imaging as a tool to quantitatively study CCA pigmentation in relation to their phenotypic plasticity, which can be applied in laboratory studies and potentially in situ surveys using underwater hyperspectral imaging systems.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"695-709"},"PeriodicalIF":2.9,"publicationDate":"2024-04-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jpy.13449","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140336083","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}
{"title":"Crocosphaera watsonii – A widespread nitrogen-fixing unicellular marine cyanobacterium","authors":"Takako Masuda, Jan Mareš, Takuhei Shiozaki, Keisuke Inomura, Amane Fujiwara, Ondřej Prášil","doi":"10.1111/jpy.13450","DOIUrl":"10.1111/jpy.13450","url":null,"abstract":"<p><i>Crocosphaera watsonii</i> is a unicellular N<sub>2</sub>-fixing (diazotrophic) cyanobacterium observed in tropical and subtropical oligotrophic oceans. As a diazotroph, it can be a source of bioavailable nitrogen (N) to the microbial community in N-limited environments, and this may fuel primary production in the regions where it occurs. <i>Crocosphaera watsonii</i> has been the subject of intense study, both in culture and in field populations. Here, we summarize the current understanding of the phylogenetic and physiological diversity of <i>C. watsonii</i>, its distribution, and its ecological niche. Analysis of the relationships among the individual <i>Crocosphaera</i> species and related free-living and symbiotic lineages of diazotrophs based on the <i>nif</i>H gene have shown that the <i>C. watsonii</i> group holds a basal position and that its sequence is more similar to <i>Rippkaea</i> and <i>Zehria</i> than to other <i>Crocosphaera</i> species. This finding warrants further scrutiny to determine if the placement is related to a horizontal gene transfer event. Here, the <i>nif</i>H UCYN-B gene copy number from a recent synthesis effort was used as a proxy for relative <i>C. watsonii</i> abundance to examine patterns of <i>C. watsonii</i> distribution as a function of environmental factors, like iron and phosphorus concentration, and complimented with a synthesis of <i>C. watsonii</i> physiology. Furthermore, we have summarized the current knowledge of <i>C. watsonii</i> with regards to N<sub>2</sub> fixation, photosynthesis, and quantitative modeling of physiology. Because N availability can limit primary production, <i>C. watsonii</i> is widely recognized for its importance to carbon and N cycling in ocean ecosystems, and we conclude this review by highlighting important topics for further research on this important species.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"604-620"},"PeriodicalIF":2.9,"publicationDate":"2024-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jpy.13450","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140323686","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}
{"title":"Syncopation and synchrony: Phenological dynamics of Pyropia nereocystis (Bangiophyceae) in central California","authors":"Daniel J. Gossard","doi":"10.1111/jpy.13448","DOIUrl":"10.1111/jpy.13448","url":null,"abstract":"<p><i>Pyropia nereocystis</i> is an annual northeastern Pacific-bladed bangialean species whose macroscopic stage epiphytized the annual canopy forming bull kelp <i>Nereocystis luetkeana</i>. I examined three in situ facets of these epiphyte-host dynamics in the central California region: (1) spatial and temporal variation in the presence of <i>P. nereocystis</i> epiphytes as a function of host density, (2) the relationship between individual host morphology and epiphytic <i>P. nereocystis</i> biomass, and (3) the ecophysiological growth ramifications for subtidal transplants of both life stages of <i>P. nereocystis</i>. Swath canopy surveys and whole host collections were conducted at five sites between November 2017 and February 2019. Additionally, transplants of <i>P. nereocystis</i> gametophytes and sporophytes were conducted across multiple subtidal depths. I observed temporal changes in the proportions of hosts epiphytized by <i>P. nereocystis</i>, with differences in seasonal persistence of <i>P. nereocystis</i> among sites and between years. Biomass of <i>P. nereocystis</i> was positively correlated with individual host stipe length, stipe surface area, and the primary principal component (PC) of stipe morphometrics denoted by principal component analysis (PCA). Gametogenesis in <i>P. nereocystis</i> epiphytes was spatially heterogeneous and limited for the 2018–2019 cohort due to comprehensive removal of hosts by the February 2019 sampling period. Transplants of <i>P. nereocystis</i> gametophytes yielded similar growth responses among depths, and sporophyte (conchocelis) transplant areal growth was positively correlated with transplant depth. These findings detail spatiotemporal complexity and multi-scale (individual, site, and whole region) phenological nuances for central Californian <i>P. nereocystis</i> epiphytes.</p>","PeriodicalId":16831,"journal":{"name":"Journal of Phycology","volume":"60 3","pages":"710-723"},"PeriodicalIF":2.9,"publicationDate":"2024-03-29","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/jpy.13448","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"140318534","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}