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All sourcesNASA NTRSDOE OSTI
DOE OSTI2024

Cytochrome b5 diversity in green lineages preceded the evolution of syringyl lignin biosynthesis

Abstract Lignin production marked a milestone in vascular plant evolution, and the emergence of syringyl (S) lignin is lineage specific. S-lignin biosynthesis in angiosperms, mediated by ferulate 5-hydroxylase (F5H, CYP84A1), has been considered a recent evolutionary event. F5H uniquely requires the cytochrome b5 protein CB5D as an obligatory redox partner for catalysis. However, it remains unclear how CB5D functionality originated and whether it coevolved with F5H. We reveal here the ancient evolution of CB5D-type function supporting F5H-catalyzed S-lignin biosynthesis. CB5D emerged in charophyte algae, the closest relatives of land plants, and is conserved and proliferated in embryophytes, especially in angiosperms, suggesting functional diversification of the CB5 family before terrestrialization. A sequence motif containing acidic amino residues in Helix 5 of the CB5 heme-binding domain contributes to the retention of CB5D function in land plants but not in algae. Notably, CB5s in the S-lignin–producing lycophyte Selaginella lack these residues, resulting in no CB5D-type function. An independently evolved S-lignin biosynthetic F5H (CYP788A1) in Selaginella relies on NADPH-dependent cytochrome P450 reductase as sole redox partner, distinct from angiosperms. These results suggest that angiosperm F5Hs coopted the ancient CB5D, forming a modern cytochrome P450 monooxygenase system for aromatic ring meta-hydroxylation, enabling the reemergence of S-lignin biosynthesis in angiosperms.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2024

The DYRKP1 kinase regulates cell wall degradation in Chlamydomonas by inducing matrix metalloproteinase expression

Abstract The cell wall of plants and algae is an important cell structure that protects cells from changes in the external physical and chemical environment. This extracellular matrix, composed of polysaccharides and glycoproteins, must be constantly remodeled throughout the life cycle. However, compared to matrix polysaccharides, little is known about the mechanisms regulating the formation and degradation of matrix glycoproteins. We report here that a plant kinase belonging to the dual-specificity tyrosine phosphorylation-regulated kinase (DYRKP1) family present in all eukaryotes regulates cell wall degradation after mitosis of Chlamydomonas reinhardtii by inducing the expression of matrix metalloproteinases. Without DYRKP1, daughter cells cannot disassemble parental cell walls and remain trapped inside for more than 10 days. On the other hand, the dual-specificity tyrosine phosphorylation-regulated kinase complementation lines show normal degradation of the parental cell wall. Transcriptomic and proteomic analyses indicate a marked downregulation of MMP gene expression and accumulation, respectively, in the dyrkp1 mutants. The mutants deficient in matrix metalloproteinases retain palmelloid structures for a longer time than the background strain, like dyrkp1 mutants. Our findings show that dual-specificity tyrosine phosphorylation-regulated kinase, by ensuring timely MMP expression, enables the successful execution of the cell cycle. Altogether, this study provides insight into the life cycle regulation in plants and algae.

Kim, Minjae (ORCID:0000000223561295)↗
DOE OSTI2020

Large fluxes of fatty acids from membranes to triacylglycerol and back during N-deprivation and recovery in Chlamydomonas

Abstract Microalgae accumulate triacylglycerol (TAG) during nutrient deprivation and break it down after nutrient resupply, and these processes involve dramatic shifts in cellular carbon allocation. Due to the importance of algae in the global carbon cycle, and the potential of algal lipids as feedstock for chemical and fuel production, these processes are of both ecophysiological and biotechnological importance. However, the metabolism of TAG is not well understood, particularly the contributions of fatty acids (FAs) from different membrane lipids to TAG accumulation and the fate of TAG FAs during degradation. Here, we used isotopic labeling time course experiments on Chlamydomonas reinhardtii to track FA synthesis and transfer between lipid pools during nitrogen (N)-deprivation and resupply. When cells were labeled before N-deprivation, total levels of label in cellular FAs were unchanged during subsequent N-deprivation and later resupply, despite large fluxes into and out of TAG and membrane lipid pools. Detailed analyses of FA levels and labeling revealed that about one-third of acyl chains accumulating in TAG during N-deprivation derive from preexisting membrane lipids, and in total, at least 45% of TAG FAs passed through membrane lipids at one point. Notably, most acyl chains in membrane lipids during recovery after N-resupply come from TAG. Fluxes of polyunsaturated FAs from plastidic membranes into TAG during N-deprivation were particularly noteworthy. These findings demonstrate a high degree of integration of TAG and membrane lipid metabolism and highlight a role for TAG in storage and supply of membrane lipid components.

Plant Sciences↗
DOE OSTI2023

Restricting electron flow at cytochrome b6f when downstream electron acceptors are severely limited

Abstract Photosynthetic organisms frequently experience abiotic stress that restricts their growth and development. Under such circumstances, most absorbed solar energy cannot be used for CO2 fixation and can cause the photoproduction of reactive oxygen species (ROS) that can damage the photosynthetic reaction centers of PSI and PSII, resulting in a decline in primary productivity. This work describes a biological “switch” in the green alga Chlamydomonas reinhardtii that reversibly restricts photosynthetic electron transport (PET) at the cytochrome b6f (Cyt b6f) complex when the capacity for accepting electrons downstream of PSI is severely limited. We specifically show this restriction in STARCHLESS6 (sta6) mutant cells, which cannot synthesize starch when they are limited for nitrogen (growth inhibition) and subjected to a dark-to-light transition. This restriction represents a form of photosynthetic control that causes diminished electron flow to PSI and thereby prevents PSI photodamage but does not appear to rely on a ΔpH. Furthermore, when electron flow is restricted, the plastid alternative oxidase (PTOX) becomes active, functioning as an electron valve that dissipates some excitation energy absorbed by PSII and allows the formation of a proton motive force (PMF) that would drive some ATP production (potentially sustaining PSII repair and nonphotochemical quenching [NPQ]). The restriction at the Cyt b6f complex can be gradually relieved with continued illumination. This study provides insights into how PET responds to a marked reduction in availability of downstream electron acceptors and the protective mechanisms involved.

Plant Sciences↗
DOE OSTI2018

Delocalized excitons in natural light-harvesting complexes

Natural organisms such as photosynthetic bacteria, algae, and plants employ complex molecular machinery to convert solar energy into biochemical fuel. An important common feature shared by most of these photosynthetic organisms is that they capture photons in the form of excitons typically delocalized over a few to tens of pigment molecules embedded in protein environments of light harvesting complexes (LHCs). Delocalized excitons created in such LHCs remain well protected despite being swayed by environmental fluctuations and are delivered successfully to their destinations over 100 nanometer distances in about 100 ps times. Decades of experimental and theoretical investigation have produced a large body of information offering insight into major structural, energetic, and dynamical features contributing to LHCs’ extraordinary capability to harness photons using delocalized excitons. The objective of this review is (i) to provide a comprehensive account of major theoretical, computational, and spectroscopic advances that have contributed to this body of knowledge, and (ii) to clarify the issues concerning the role of delocalized excitons in achieving efficient energy transport mechanisms. The focus of this review is on three representative systems: the Fenna-Matthews-Olson complex of green sulfur bacteria, the light harvesting 2 complex of purple bacteria, and phycobiliproteins of cryptophyte algae. Although we offer a more in-depth and detailed description of theoretical and computational aspects, major experimental results and their implications are also assessed in the context of achieving excellent light-harvesting functionality. Future theoretical and experimental challenges to be addressed in gaining a better understanding and utilization of delocalized excitons are also discussed.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2014

The Regulation of Photosynthetic Structure and Function during Nitrogen Deprivation in Chlamydomonas reinhardtii

The accumulation of carbon storage compounds by many unicellular algae after nutrient deprivation occurs despite declines in their photosynthetic apparatus. To understand the regulation and roles of photosynthesis during this potentially bioenergetically valuable process, we analyzed photosynthetic structure and function after nitrogen deprivation in the model alga Chlamydomonas reinhardtii. Transcriptomic, proteomic, metabolite, and lipid profiling and microscopic time course data were combined with multiple measures of photosynthetic function. Levels of transcripts and proteins of photosystems I and II and most antenna genes fell with differing trajectories; thylakoid membrane lipid levels decreased, while their proportions remained similar and thylakoid membrane organization appeared to be preserved. Cellular chlorophyll (Chl) content decreased more than 2-fold within 24 h, and we conclude from transcript protein and 13 C labeling rates that Chl synthesis was down-regulated both pre- and posttranslationally and that Chl levels fell because of a rapid cessation in synthesis and dilution by cellular growth rather than because of degradation. Photosynthetically driven oxygen production and the efficiency of photosystem II as well as P700 + reduction and electrochromic shift kinetics all decreased over the time course, without evidence of substantial energy overflow. The results also indicate that linear electron flow fell approximately 15% more than cyclic flow over the first 24 h. Comparing Calvin-Benson cycle transcript and enzyme levels with changes in photosynthetic 13 CO 2 incorporation rates also pointed to a coordinated multilevel down-regulation of photosynthetic fluxes during starch synthesis before the induction of high triacylglycerol accumulation rates.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2016

Metagenomics unveils the attributes of the alginolytic guilds of sediments from four distant cold coastal environments: Alginolytic guilds from cold sediments

Alginates are abundant polysaccharides in brown algae that constitute an important energy source for marine heterotrophic bacteria. Despite the key role of alginate assimilation processes in the marine carbon cycle, little information is available on the bacterial populations involved in these processes. The goal of this work was to gain insight into the structure and functional traits of the alginolytic communities from sediments of cold coastal environments. Sediment metagenomes from high-latitude regions of both Hemispheres were interrogated for alginate lyase gene homolog sequences and their genomic context. Sediments contained highly abundant and diverse bacterial assemblages with alginolytic potential, including members of Bacteroidetes and Proteobacteria, as well as several poorly characterized taxa. Temperature and salinity were correlated to the variation in community structure. The microbial communities in Arctic and Antarctic sediments exhibited the most similar alginolytic profiles, whereas brackish sediments had a higher proportion of novel members. Examination of the gene context of the alginate lyase homologs revealed distinct patterns according to the phylogenetic origin of the scaffolds, with evidence of evolutionary relationships among lineages. This information is relevant for understanding carbon fluxes in cold coastal environments and provides valuable information for the development of biotechnological applications from brown algae biomass.

Matos, Marina N.↗
DOE OSTI2019

Phytochrome evolution in 3D: deletion, duplication, and diversification

Canonical plant phytochromes are master regulators of photomorphogenesis and the shade avoidance response. They are also part of a widespread superfamily of photoreceptors with diverse spectral and biochemical properties. Plant phytochromes belong to a clade including other phytochromes from glaucophyte, prasinophyte, and streptophyte algae (all members of the Archaeplastida) and those from cryptophyte algae. This is consistent with recent analyses supporting the existence of an AC (Archaeplastida + Cryptista) clade. AC phytochromes have been proposed to arise from ancestral cyanobacterial genes via endosymbiotic gene transfer (EGT), but most recent studies instead support multiple horizontal gene transfer (HGT) events to generate extant eukaryotic phytochromes. In principle, this scenario would be compared to the emerging understanding of early events in eukaryotic evolution to generate a coherent picture. Unfortunately, there is currently a major discrepancy between the evolution of phytochromes and the evolution of eukaryotes; phytochrome evolution is thus not a solved problem. We therefore examine phytochrome evolution in a broader context. Within this context, we can identify three important themes in phytochrome evolution: deletion, duplication, and diversification. These themes drive phytochrome evolution as organisms evolve in response to environmental challenges.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2015

Large‐scale insertional mutagenesis of Chlamydomonas supports phylogenomic functional prediction of photosynthetic genes and analysis of classical acetate‐requiring mutants

Summary Chlamydomonas reinhardtii is a unicellular green alga that is a key model organism in the study of photosynthesis and oxidative stress. Here we describe the large‐scale generation of a population of insertional mutants that have been screened for phenotypes related to photosynthesis and the isolation of 459 flanking sequence tags from 439 mutants. Recent phylogenomic analysis has identified a core set of genes, named GreenCut2, that are conserved in green algae and plants. Many of these genes are likely to be central to the process of photosynthesis, and they are over‐represented by sixfold among the screened insertional mutants, with insertion events isolated in or adjacent to 68 of 597 GreenCut2 genes. This enrichment thus provides experimental support for functional assignments based on previous bioinformatic analysis. To illustrate one of the uses of the population, a candidate gene approach based on genome position of the flanking sequence of the insertional mutant CAL 027_01_20 was used to identify the molecular basis of the classical C. reinhardtii mutation ac17 . These mutations were shown to affect the gene PDH 2 , which encodes a subunit of the plastid pyruvate dehydrogenase complex. The mutants and associated flanking sequence data described here are publicly available to the research community, and they represent one of the largest phenotyped collections of algal insertional mutants to date.

Dent, Rachel M.↗
DOE OSTI2015

Light stress and photoprotection in Chlamydomonas reinhardtii

Summary Plants and algae require light for photosynthesis, but absorption of too much light can lead to photo‐oxidative damage to the photosynthetic apparatus and sustained decreases in the efficiency and rate of photosynthesis (photoinhibition). Light stress can adversely affect growth and viability, necessitating that photosynthetic organisms acclimate to different environmental conditions in order to alleviate the detrimental effects of excess light. The model unicellular green alga, Chlamydomonas reinhardtii , employs diverse strategies of regulation and photoprotection to avoid, minimize, and repair photo‐oxidative damage in stressful light conditions, allowing for acclimation to different and changing environments.

Erickson, Erika↗
DOE OSTI2018

High-throughput sequencing of the chloroplast and mitochondrion of Chlamydomonas reinhardtii to generate improved de novo assemblies, analyze expression patterns and transcript speciation, and evaluate diversity among laboratory strains and wild isolates

Chlamydomonas reinhardtii is a unicellular chlorophyte alga that is widely studied as a reference organism for understanding photosynthesis, sensory and motile cilia, and for development of an algal-based platform for producing biofuels and bio-products. Its highly repetitive, ~205-kbp circular chloroplast genome and ~15.8-kbp linear mitochondrial genome were sequenced prior to the advent of high-throughput sequencing technologies. Here, high coverage shotgun sequencing was used to assemble both organellar genomes de novo. These new genomes correct dozens of errors in the prior genome sequences and annotations. Gen-ome sequencing coverage indicates that each cell contains on average 83 copies of the chloroplast genome and 130 copies of the mitochondrial genome. Using protocols and analyses optimized for organellar tran-scripts, RNA-Seq was used to quantify their relative abundances across 12 different growth conditions. Forty-six percent of total cellular mRNA is attributable to high expression from a few dozen chloroplast genes. RNA-Seq data were used to guide gene annotation, to demonstrate polycistronic gene expression, and to quantify splicing of psaA and psbA introns. In contrast to a conclusion from a recent study, we found that chloroplast transcripts are not edited. Unexpectedly, cytosine-rich polynucleotide tails were observed at the 3’-end of all mitochondrial transcripts. A comparative genomics analysis of eight laboratory strains and 11 wild isolates of C. reinhardtii identified 2658 variants in the organellargenomes, which is 1/10th as much genetic diversity as is found in the nucleus.

ftsH↗
DOE OSTI2018

Subdiffraction-resolution live-cell imaging for visualizing thylakoid membranes

© 2018 The Authors The Plant Journal © 2018 John Wiley & Sons Ltd The chloroplast is the chlorophyll-containing organelle that produces energy through photosynthesis. Within the chloroplast is an intricate network of thylakoid membranes containing photosynthetic membrane proteins that mediate electron transport and generate chemical energy. Historically, electron microscopy (EM) has been a powerful tool for visualizing the macromolecular structure and organization of thylakoid membranes. However, an understanding of thylakoid membrane dynamics remains elusive because EM requires fixation and sectioning. To improve our knowledge of thylakoid membrane dynamics we need to consider at least two issues: (i) the live-cell imaging conditions needed to visualize active processes in vivo; and (ii) the spatial resolution required to differentiate the characteristics of thylakoid membranes. Here, we utilize three-dimensional structured illumination microscopy (3D-SIM) to explore the optimal imaging conditions for investigating the dynamics of thylakoid membranes in living plant and algal cells. We show that 3D-SIM is capable of examining broad characteristics of thylakoid structures in chloroplasts of the vascular plant Arabidopsis thaliana and distinguishing the structural differences between wild-type and mutant strains. Using 3D-SIM, we also visualize thylakoid organization in whole cells of the green alga Chlamydomonas reinhardtii. These data reveal that high light intensity changes thylakoid membrane structure in C. reinhardtii. Moreover, we observed the green alga Chromochloris zofingiensis and the moss Physcomitrella patens to show the applicability of 3D-SIM. This study demonstrates that 3D-SIM is a promising approach for studying the dynamics of thylakoid membranes in photoautotrophic organisms during photoacclimation processes.

46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND ↗
DOE OSTI2024

Identifying the gene responsible for non‐photochemical quenching reversal in Phaeodactylum tricornutum

SUMMARY Algae such as diatoms and haptophytes have distinct photosynthetic pigments from plants, including a novel set of carotenoids. This includes a primary xanthophyll cycle comprised of diadinoxanthin and its de‐epoxidation product diatoxanthin that enables the switch between light harvesting and non‐photochemical quenching (NPQ)‐mediated dissipation of light energy. The enzyme responsible for the reversal of this cycle was previously unknown. Here, we identified zeaxanthin epoxidase 3 (ZEP3) from Phaeodactylum tricornutum as the candidate diatoxanthin epoxidase. Knocking out the ZEP3 gene caused a loss of rapidly reversible NPQ following saturating light exposure. This correlated with the maintenance of high concentrations of diatoxanthin during recovery in low light. Xanthophyll cycling and NPQ relaxation were restored via complementation of the wild‐type ZEP3 gene. The zep3 knockout strains showed reduced photosynthetic rates at higher light fluxes and reduced specific growth rate in variable light regimes, likely due to the mutant strains becoming locked in a light energy dissipation state. We were able to toggle the level of NPQ capacity in a time and dose dependent manner by placing the ZEP3 gene under the control of a β‐estradiol inducible promoter. Identification of this gene provides a deeper understanding of the diversification of photosynthetic control in algae compared to plants and suggests a potential target to improve the productivity of industrial‐scale cultures.

Ware, Maxwell A.↗
DOE OSTI2017

Chlamydomonas reinhardtii LFO1 Is an IsdG Family Heme Oxygenase

Heme is essential for respiration across all domains of life. However, heme accumulation can lead to toxicity if cells are unable to either degrade or export heme or its toxic by-products. Under aerobic conditions, heme degradation is performed by heme oxygenases, enzymes which utilize oxygen to cleave the tetrapyrrole ring of heme. The HO-1 family of heme oxygenases has been identified in both bacterial and eukaryotic cells, whereas the IsdG family has thus far been described only in bacteria. We identified a hypothetical protein in the eukaryotic green alga Chlamydomonas reinhardtii, which encodes a protein containing an antibiotic biosynthesis monooxygenase (ABM) domain consistent with those associated with IsdG family members. This protein, which we have named LFO1, degrades heme, contains similarities in predicted secondary structures to IsdG family members, and retains the functionally conserved catalytic residues found in all IsdG family heme oxygenases. These data establish LFO1 as an IsdG family member and extend our knowledge of the distribution of IsdG family members beyond bacteria. To gain further insight into the distribution of the IsdG family, we used the LFO1 sequence to identify 866 IsdG family members, including representatives from all domains of life. These results indicate that the distribution of IsdG family heme oxygenases is more expansive than previously appreciated, underscoring the broad relevance of this enzyme family. This work establishes a protein in the freshwater alga Chlamydomonas reinhardtii as an IsdG family heme oxygenase. This protein, LFO1, exhibits predicted secondary structure and catalytic residues conserved in IsdG family members, in addition to a chloroplast localization sequence. Additionally, the catabolite that results from the degradation of heme by LFO1 is distinct from that of other heme degradation products. Using LFO1 as a seed, we performed phylogenetic analysis, revealing that the IsdG family is conserved in all domains of life. Also, C. reinhardtii contains two previously identified HO-1 family heme oxygenases, making C. reinhardtii the first organism shown to contain two families of heme oxygenases. These data indicate that C. reinhardtii may have unique mechanisms for regulating iron homeostasis within the chloroplast.

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CH↗
DOE OSTI2023

Taxonomic distribution of metabolic functions in bacteria associated with Trichodesmium consortia

The photosynthetic and diazotrophic cyanobacterium Trichodesmium is a key contributor to marine biogeochemical cycles in the subtropical-oligotrophic oceans. Trichodesmium form colonies that harbor a distinct microbial community in comparison to the surrounding seawater. The presence of their associated bacteria can expand Trichodesmium’s functional potential and is predicted to influence the cycling of carbon, nitrogen, phosphorus, and iron (C, N, P, and Fe). To link the bacteria associated with Trichodesmium to key functional traits and elucidate how community structure can influence nutrient cycling, we characterized Red Sea Trichodesmium colonies using metagenomics and metaproteomics. Colonies harbored bacteria that typically associate with algae and particles, such as the ubiquitous Alteromonas macleodii, but also lineages specific to Trichodesmium, such as members from the order Balneolales. The majority of associated bacteria were auxotrophic for different vitamins, indicating their dependency on vitamin production by Trichodesmium. The associated bacteria carry functional traits including siderophore biosynthesis, reduced phosphorus metabolism, and denitrification pathways. The analysis supports Trichodesmium as an active hotspot for C, N, P, Fe, and vitamin exchange. In turn, Trichodesmium may rely on associated bacteria to meet its high Fe demand as several lineages synthesize photolabile siderophores (e.g., vibrioferrin, rhizoferrin, petrobactin) which can enhance the bioavailability of particulate Fe to the entire consortium. Collectively, the results indicate that Trichodesmium colonies provide a structure where these interactions can take place. While further studies are required to clarify the exact nature of these interactions, Trichodesmium’s reliance on particle and algae-associated bacteria and the observed redundancy of key functional traits likely underpins the resilience of Trichodesmium within an ever-changing global environment.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2021

Identification of Effector Metabolites Using Exometabolite Profiling of Diverse Microalgae

Dissolved exometabolites mediate algal interactions in aquatic ecosystems, but microalgal exometabolomes remain understudied. We conducted an untargeted metabolomic analysis of nonpolar exometabolites exuded from four phylogenetically and ecologically diverse eukaryotic microalgal strains grown in the laboratory, freshwater Chlamydomonas reinhardtii, brackish Desmodesmus sp., marine Phaeodactylum tricornutum, and marine Microchloropsis salina, to identify released metabolites based on relative enrichment in the exometabolomes compared to cell pellet metabolomes. Exudates from the different taxa were distinct, but we did not observe clear phylogenetic patterns. We used feature-based molecular networking to explore the identities of these metabolites, revealing several distinct di- and tripeptides secreted by each of the algae, lumichrome, a compound that is known to be involved in plant growth and bacterial quorum sensing, and novel prostaglandin-like compounds. We further investigated the impacts of exogenous additions of eight compounds selected based on exometabolome enrichment on algal growth. Of these compounds, five (lumichrome, 5'-S-methyl-5'-thioadenosine, 17-phenyl trinor prostaglandin A2, dodecanedioic acid, and aleuritic acid) impacted growth in at least one of the algal cultures. Two of these compounds (dodecanedioic acid and aleuritic acid) produced contrasting results, increasing growth in some algae and decreasing growth in others. Together, our results reveal new groups of microalgal exometabolites, some of which could alter algal growth when provided exogenously, suggesting potential roles in allelopathy and algal interactions.

59 BASIC BIOLOGICAL SCIENCES↗
DOE OSTI2019

Comparative and Functional Algal Genomics

Over 100 whole-genome sequences from algae are published or soon to be published. The rapidly increasing availability of these fundamental resources is precipitating a paradigm shift in the way we understand one of the most diverse, complex, and understudied groups of photosynthetic eukaryotes. Genome sequences provide a window into the functional potential of each disparate alga, with phylogenomics and functional genomics as tools for contextualizing and transferring knowledge from reference organisms into less well-characterized systems. Remarkably, over half of the proteins encoded by algal genomes are of unknown function, highlighting the volume of unique functional capabilities yet to be discovered. We provide an overview of publicly available algal genomes, their associated protein inventories, and their quality, with a summary of the statuses of protein function understanding and prediction.

59 BASIC BIOLOGICAL SCIENCES↗