The chytrids (phylum Chytridiomycota) are a major, predominantly unicellular fungal lineage of ecological importance. For example, some chytrid species are the causative agents of the global amphibian panzootic (Fisher and Garner, 2020) and virulent crop pests (van de Vossenberg et al., 2019), whilst others are algal parasites and saprotrophs in marine and freshwater ecosystems (Frenken et al., 2017; Grossart et al., 2019; Klawonn et al., 2021). Chytrid zoospores contain large amounts of intracellular storage lipids that are consumed by grazing zooplankton, making them responsible for a significant form of trophic upgrading in aquatic ecosystems (Kagami et al., 2017; Kagami et al., 2014; Kagami et al., 2007; Rasconi et al., 2020). Chytrids are also important from an evolutionary perspective as they retain cellular traits from the last common ancestor of branching fungi (Figure 1A) that are now absent in hyphal fungi (Berbee et al., 2017; Nagy et al., 2018), as well as traits from the common ancestor of animals and fungi in the Opisthokonta (Medina et al., 2016; Prostak et al., 2021). This makes chytrids powerful models to explore the origin and evolution of innovations in fungal cell biology and the wider eukaryotic tree of life. To help fully appreciate chytrids in terms of their ecological and evolutionary contexts, it is necessary to resolve their core cell biology (Laundon and Cunliffe, 2021).

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Central to chytrid cell biology is their distinctive dimorphic life cycle, consisting of a motile free-swimming uniflagellate zoospore that transforms into a sessile walled thallus with anucleate attaching and feeding rhizoids (Figure 1B; Laundon et al., 2020; Medina et al., 2020). The cell body component of the thallus develops into the zoosporangium from which the next generation of zoospores are produced (Figure 1B). Any biological life cycle inherently represents a temporal progression, yet the chytrid life cycle can be categorised into four distinctive contiguous life stages (Berger et al., 2005). The first stage is the motile ‘zoospore’ which lacks a cell wall, does not feed, and colonises substrates or hosts. Even though zoospores are metabolically active, they are transcriptionally and translationally inactive, with dormant ribosomes containing maternally derived mRNA (Medina and Buchler, 2020). The second stage is the sessile ‘germling’ which develops immediately after zoospore settlement following flagellar retraction (or sometimes detachment), cell wall production (encystment), and initiation of rhizoid growth from an initial germ tube. The third stage is the vegetative ‘immature thallus’ which is associated with the highest levels of rhizoid development and overall cellular growth (Laundon et al., 2020). The cell plan of the immature thallus can be divided into three parts (Figure 1B): the cell body which is ultimately destined for reproduction (zoosporogenesis), the rhizoid for attachment and feeding, and (in some chytrid species) a bulbous swelling between the cell body and rhizoid termed the ‘apophysis’, the function of which is currently poorly understood (Laundon and Cunliffe, 2021). The final life stage is the reproductive ‘mature zoosporangium’, which appears once the immature thallus has reached maximum cell size and the cell body cytoplasm is cleaved into the next generation of zoospores (Figure 1B).

Representative model strains have an important role to play in understanding the biology of chytrids (Laundon and Cunliffe, 2021). Rhizoclosmatium globosum is a widespread aquatic saprotroph and the strain R. globosum JEL800 has emerged as a promising model organism in laboratory investigations (Laundon et al., 2020; Roberts et al., 2020; Venard et al., 2020) due to an available genome (Mondo et al., 2017), easy axenic culture, and amenability to live-cell fluorescent microscopy (Laundon et al., 2020). R. globosum JEL800 exhibits an archetypal chytrid cell plan (Figure 1B) and rapid life cycle, making it a powerful model system to interrogate chytrid cellular development (Laundon et al., 2020; Laundon and Cunliffe, 2021).

The chytrid life cycle has so far been characterised with largely descriptive approaches (e.g. Berger et al., 2005) with only a few quantitative studies focusing on specific processes, such as rhizoid morphogenesis (Dee et al., 2019; Laundon et al., 2020) and actin formation (Medina et al., 2020; Prostak et al., 2021). These important studies provide a foundation on which to develop a quantitative approach to understand the biology of the chytrid cell plan and the drivers of the transitions between the life stages. To investigate the cellular and molecular underpinnings of the chytrid life cycle and associated cell biology, we studied the four major life stages of R. globosum by combining quantitative volume electron microscopy and transcriptomics (Figure 1C), with the addition of supplementary targeted live-cell fluorescent microscopy and lipid analysis. The aim of our approach was to quantify the cellular traits that define the major chytrid life stages and identify the biological processes that take place during the developmental transitions between them. As such, we have created a developmental ‘atlas’ with R. globosum for the archetypal chytrid life cycle, which in turn generated specific avenues for targeted investigation of important biological processes, namely lipid biology, apophysis function, and zoosporogenesis.

By culturing R. globosum and sampling the populations at different stages through their temporal development (0 hr zoospore, 1.5 hr germling, 10 hr immature thallus, and a 24 hr mixed population including mature zoosporangia) (Figure 1C; Figure 1—figure supplement 1), we examined chytrid populations with both 3D reconstructions by serial block face scanning electron microscopy (SBF-SEM) and mRNA sequencing. We used single-cell SBF-SEM reconstructions (n = 5 cells per life stage) to quantify the cellular structures at each life stage and population-level transcriptomic analysis of significant Kyoto Encyclopedia of Genes and Genomes (KEGG) pathway categories (n = 3 populations per life stage, differentially expressed genes [DEGs]) to summarise the major biological differences between the life stages through temporal development (Figure 1C). As these stages represent key time points in the progression of the linear temporal chytrid life cycle, pairwise comparison of transcriptomes from contiguous life stages achieved an account of the major putative biological transitions (e.g. germling vs. zoospore, immature thallus vs. germling). Our findings provide insights into chytrid developmental processes and serve as a resource from which to resolve the biology of this ecologically and evolutionary important fungal lineage.

This study into the cellular and molecular biology of R. globosum has generated a novel developmental atlas of an archetypal chytrid life cycle, shedding light on the cell patterns of major life stages and the biological processes governing the transitions between them. Our key findings are summarised in Figure 7.

Figure 7

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In the R. globosum zoospore cell body, the ribosome cluster is a distinctive and dominating feature. Historically called the ‘nuclear cap’, ribosome clusters have been observed in zoospores throughout the Chytridiomycota (e.g. Koch, 1961) and in the closely related Blastocladiomycota (e.g. Lovett, 1963). Lovett, 1963, showed in Blastocladiella (Blastocladiomycota), as we show here with R. globosum, the ribosome cluster dissipates during the transition between the free-swimming zoospore and germling stages causing the release of the previously contained ribosomes throughout the cell. Lovett, 1968; Lovett, 1963, related the Blastocladiella zoospore ribosome cluster and subsequent dissipation with the biological activity of the cell during the zoospore-germling transition, proposing the role of the cluster was to maintain the ribosomes through the zoospore stage and to spatially isolate the ribosomes to prevent translation occurring until when the cluster dissipates (i.e. the germling stage) and protein synthesis is initiated. Subsequent investigations into transcription and translation in chytrids and the Blastocladiomycota established that these processes are inactive in zoospores which contain maternally provisioned mRNA and dormant ribosomes (Barstow and Lovett, 1974; Jaworski, 1976; LéJohn and Lovett, 1966; Lovett, 1968; Schmoyer and Lovett, 1969; Silva et al., 1987).

Our transcriptome data add molecular detail to understanding the biology of the zoospore-germling transition, with KEGG categories related to ribosome maintenance downregulated and categories associated with translation and biosynthesis upregulated in the germling life stage compared to zoospore mRNA. Similarly, Rosenblum et al., 2008, detected high levels of transcripts associated with posttranslational protein modification in Batrachochytrium dendrobatidis (Bd) zoospores, but low transcriptional activity. Taken together, the chytrid zoospore represents a sophisticated and well-adapted life stage specialised for dispersal to new growth substrates or hosts rather than general metabolism, which is only initiated by the release of the ribosome cluster at the germling stage once favourable conditions are found. The germling stage is characterised by major cell plan remodelling, including rhizoid growth, and concomitant activation of diverse metabolic pathways. Similar upregulation of metabolic pathways has been observed at the transcriptional level associated with conidial germination in dikaryan fungi (Sharma et al., 2016; Zhou et al., 2018).

Interestingly, we detected the upregulation of proteasome genes in the germling relative to the zoospore mRNA content, which are also necessary for dikaryan germination (Seong et al., 2008; Wang et al., 2011). A previous study into flagellar retraction in R. globosum showed that the internalised flagellum is disassembled and degraded in the germling stage, at least partially by proteasome-dependent proteolysis (Venard et al., 2020). Our finding of increased proteasome-associated mRNA may likewise be associated with flagellar degradation and the recycling of redundant zoospore machinery in the germling.

The immature thallus displayed increased cellular and molecular signatures associated with the reproductive cell cycle, intracellular trafficking, and protein processing. A key structural development was the vacuolisation of the cell body. Highly vacuolated dikaryan cells (El Ghaouth et al., 1994; Gow and Gooday, 1987) are associated with diverse cellular processes including general homeostasis, protein sorting, cell cycling, and intracellular trafficking (Veses et al., 2008), any of which could at least partially explain the high vacuolisation of immature chytrid thalli. Noticeable in the context of chytrid cell biology however is the increased mRNA for actin-driven cytoskeletal genes, including those assigned to the Arp2/3 complex. The role of actin in vacuolisation and endocytosis has been demonstrated in yeast (Eitzen et al., 2002; Gachet and Hyams, 2005), similar to our observations here in R. globosum. Arp2/3-dependent actin dynamics drive crawling α-motility in some chytrid zoospores when moving freely in the environment (Fritz-Laylin et al., 2017; Medina et al., 2020) and the presence of animal-like actin components that have been lost in multicellular fungi makes chytrids useful models to investigate the evolution of the fungal cytoskeleton (Prostak et al., 2021). Although R. globosum zoospores do not crawl, the immature thallus has actin patches, cables, and perinuclear shells (Prostak et al., 2021). Here, we show that, for a non-crawling chytrid, actin-associated gene transcripts are increased in immature thalli and that this life stage is associated with high vacuolisation and possible endocytosis, which together could be associated with the early onset of zoosporogenesis.

We did not find any differences in molecular signatures related to cell wall synthesis between the different life stages at the higher categorical level in R. globosum, instead we observed individual differentially transcribed genes suggesting that the process is dynamic and complex. Higher levels of putative chitin synthase gene transcripts (e.g. ORY39038) in wall-less zoospores was coupled with the detection of precursory cell wall material at the base of the R. globosum flagellum. Bd transcriptomes also suggest some chitin synthases to be more abundant in zoospores than in sessile thalli (Rosenblum et al., 2008). Chitin synthase activity has been shown to be associated with the Blastocladiella emersonii zoospore membrane (Dalley and Sonneborn, 1982). Initiation of cell wall synthesis warrants further study and may explain why early chemical inhibition induces phenotypic disruptions to normal development in chytrids (Laundon et al., 2020). This emphasises the need to include the wall-less zoospore stage in investigations into chytrid cell wall biology.

This study has highlighted the complexity of lipid dynamics across the R. globosum life cycle. Our data show that the volume of the lipid globule, total lipid by volume, and lipid as a percentage of dry mass remain unchanged between zoospores and germlings, yet we observed a shift in lipid type, moving from sphingolipids and neutral glycolipids (likely storage triacylglycerides) to polar lipids (likely membrane-associated phospholipids) between zoospores and germlings. Similarly, during the B. emersonii zoospore-germling transition glycolipids decrease and phospholipids increase (Dalley and Sonneborn, 1982). Previous research has characterised fatty acid profiles in chytrids (Akinwole et al., 2014; Gerphagnon et al., 2019; Rasconi et al., 2020) and shown differences between chytrid zoospores and sessile thalli of the same species (Taube et al., 2019). As the Nile Red emission spectrum undergoes a red shift in increasingly polar environments (Bertozzini et al., 2011), we propose that our live-cell data do not quantify the structural degradation of the lipid globule per se but rather biochemical polarisation as neutral storage lipids are catabolised and polar phospholipids are synthesised. The larger volumetric proportion of glycogen stores in developing zoospores over mature free-swimming zoospores also indicates that glycogen catabolism between the two stages contributes to the zoospore energy budget during motility as previously proposed (Powell, 1979).

Another novel aspect of our study shows that changes in lipid profiles are apparently coupled with subcellular ultrastructure in R. globosum. The enzymatic function of LRM-associated microbodies as lipolytic organelles has been previously proposed (Powell, 1979; Powell, 1977; Powell, 1976), where evidence suggests that enzymatic activity increases following germination (Powell, 1976). From our data, this organelle may have bidirectional function and be associated with lipid production (anabolism and conversion) as well as catabolism. A key component of the LRM is the enigmatic chytrid rumposome, which was larger in zoospores than germlings. Previous hypotheses have proposed that this organelle is associated with environmental reception and signal transduction in flagellar regulation (Dorward and Powell, 1983). An enlarged rumposome in motile zoospores would support a flagellar role, but its retention in germlings implies additional functions, unless there is a prolonged delay in its degradation. The bulk of lipids in immature thalli during anabolism were intravacuolar and comparable intravacuolar inclusions have been identified in chytrid and dikaryan fungi in the past (Beakes et al., 1992; Bourett and Howard, 1994; Lösel, 1990). Intravacuolar lipid droplets have been previously investigated in yeast but in a catabolic capacity (van Zutphen et al., 2014; Vevea et al., 2015). Although de novo storage lipid synthesis is associated with the ER (Vevea et al., 2015), the vacuoles identified here may cache and aggregate nascent globules as part of the lipid anabolic pathway.

The function of the chytrid apophysis has long been overlooked, despite its ubiquity in the Chytridiomycota (Powell, 1974; Powell and Gillette, 1987; Taylor and Fuller, 1980). Here, we provide evidence that the apophysis acts as a junction for dynamic intracellular trafficking from the multiple branches of the rhizoid network into the central cell body. The localisation of high endomembrane activity in the apophysis and subsequent passage through the annular pore in the pseudo-septum into the cell body implicates this structure as a possible sorting intermediary consolidating the rhizoid network. The ability of multicellular dikaryan fungi to translocate assimilated nutrients through their hyphal network from the site of uptake is sophisticated (van’t Padje et al., 2021; Whiteside et al., 2019), and the observed analogous endomembrane flow from feeding rhizoids to the cell body in chytrids is perhaps not surprising. However, the localisation of high endomembrane activity to the functionally delineated apophysis and through the pseudo-septum into the cell body implicates this structure as a specialised junction.

The pseudo-septation of the apophysis and rhizoids from the cell body is evidence for functional compartmentation (i.e. feeding vs. reproduction) within the thallus of a unicellular fungus. Comparable structures are also present in other chytrid species (e.g. Barr, 1970; Beakes et al., 1992). Division of multicellular dikaryan fungi by septa, where continuity between distinct cytoplasmic compartments is maintained by septal pores, is integral to multicellularity, cellular differentiation, and resilience (Bleichrodt et al., 2015; Bleichrodt et al., 2012). The origin of hyphal septa was a major innovation in fungal evolution (Berbee et al., 2017; Nagy et al., 2020) occurring at the node shared by hyphal and rhizoidal fungi (Berbee et al., 2017). The role of the apophysis-cell body pseudo-septum (or an analogous structure) in chytrids in delineating functionally dedicated subcellular compartments may represent an evolutionary precursor to dikaryan septa differentiation and multicellularity. Therefore, investigating the chytrid apophysis is not only important for understanding intracellular trafficking biology in the phylum, but also the evolution of multicellularity more widely across the fungal kingdom.

Our quantitative reconstructions of individual developing zoospores in the zoosporangium and comparison with their free-swimming counterparts have added to understanding the underpinning biology of chytrid zoosporogenesis. Perhaps our most striking finding is the amoeboid morphology of developing zoospores, potentially resulting from endocytotic engulfment, and trafficking structures, suggesting that developing zoospores assimilate material from the maternal cytoplasm post-cleavage. Although dikaryan sporogenesis is complex and diverse, it typically involves the septation of hyphal cytoplasm via cell wall synthesis and dikaryan spores are therefore incapable of such engulfment activity (Cole, 1986; Money, 2016). Phagocytosis has not been observed generally in the fungi (Yutin et al., 2009), however in representatives of the basal Opisthosporidia, wall-less endoparasites such as Rozella (Cryptomycota) and Aphelidium (Aphelida) have been shown to consume host cytoplasm material via phagocytosis (Powell et al., 2017; Karpov et al., 2014). Nucleariid amoebae (Yoshida et al., 2009), choanoflagellates (Laundon et al., 2019), and various animal cell types (Bayne, 1990) also exhibit analogous endocytotic engulfment behaviour as we provide evidence for here in chytrid zoospores. Chytrid zoosporogenesis warrants further study, however the apparent conservation may indicate that such engulfment behaviour to assimilate subcellular cargo during sporogenesis of wall-less zoospores existed in the last common ancestor of branching fungi and was lost in dikaryan fungi as spores became walled.

In conclusion, our characterisation of the R. globosum life cycle has revealed changes in cell structure and biological processes associated with chytrid development, some of which show analogies in dikaryan fungi and others in ‘animal like’ cells. As important saprotrophs, parasites, and pathogens, our findings provide information into the cellular processes that underpin the ecological importance of chytrids. In addition, our characterisation of a fungus that retains cellular characteristics from the last common ancestor of branching fungi is a step forward in reconstructing the putative biology of this organism. This study demonstrates the utility of developmental studies with model chytrids such as R. globosum and reiterates the need for fundamental biology in investigating the function of chytrid cells.

All 3D objects, raw datasets associated with figures, image analysis scripts, processed SBF-SEM stacks, and model files, are available for download from Figshare at: https://tinyurl.com/yww6h9d9. Raw sequencing reads are deposited in the Sequence Read Archive (SRA) (PRJNA789147).

1. 1. Laundon D
   2. Chrismas N
   3. Bird K
   4. Thomas S
   5. Mock T
   6. Cunliffe M

   (2021) NCBI BioProject

   ID PRJNA789147. Mapping of a cellular and molecular atlas reveals the basis of chytrid development.

   https://www.ncbi.nlm.nih.gov/bioproject/PRJNA789147/

1. 1. Akinwole PO
   2. Lefevre E
   3. Powell MJ
   4. Findlay RH

   (2014) Unique odd-chain polyenoic phospholipid fatty acids present in chytrid fungi

   Lipids 49:933–942.

   https://doi.org/10.1007/s11745-014-3934-3

   • PubMed
   • Google Scholar
2. 1. Barr DJS

   (1970) Phlyctochytrium arcticum n. sp. (Chytridiales); morphology and physiology

   Canadian Journal of Botany 48:2279–2283.

   https://doi.org/10.1139/b70-330

   • Google Scholar
3. 1. Barr DJS

   (1986) Allochytridium expandens rediscovered: morphology, physiology and zoospore ultrastructure

   Mycologia 78:439.

   https://doi.org/10.2307/3793048

   • Google Scholar
4. 1. Barstow WE
   2. Lovett JS

   (1974) Apical vesicles and microtubules in rhizoids of Blastocladiella emersonii: effects of actinomycin D and cycloheximide on development during germination

   Protoplasma 82:103–117.

   https://doi.org/10.1007/BF01276874

   • PubMed
   • Google Scholar
5. 1. Bayne CJ

   (1990) Phagocytosis and non-self recognition in invertebrates

   Bioscience 40:723–731.

   https://doi.org/10.2307/1311504

   • Google Scholar
6. 1. Beakes GW
   2. Canter HM
   3. Jaworski GHM

   (1992) Comparative ultrastructural ontogeny of zoosporangia of Zygorhizidium affluens and Z. planktonicum, chytrid parasites of the diatom Asterionella formosa

   Mycological Research 96:1047–1059.

   https://doi.org/10.1016/S0953-7562(09)80115-9

   • Google Scholar
7. 1. Belevich I
   2. Joensuu M
   3. Kumar D
   4. Vihinen H
   5. Jokitalo E

   (2016) Microscopy Image Browser: a platform for segmentation and analysis of multidimensional datasets

   PLOS Biology 14:e1002340.

   https://doi.org/10.1371/journal.pbio.1002340

   • Google Scholar
8. 1. Berbee ML
   2. James TY
   3. Strullu-Derrien C

   (2017) Early diverging fungi: diversity and impact at the dawn of terrestrial life

   Annual Review of Microbiology 71:41–60.

   https://doi.org/10.1146/annurev-micro-030117-020324

   • PubMed
   • Google Scholar
9. 1. Berger L
   2. Hyatt AD
   3. Speare R
   4. Longcore JE

   (2005) Life cycle stages of the amphibian chytrid Batrachochytrium dendrobatidis

   Diseases of Aquatic Organisms 68:51–63.

   https://doi.org/10.3354/dao068051

   • PubMed
   • Google Scholar
10. 1. Bertozzini E
    2. Galluzzi L
    3. Penna A
    4. Magnani M

    (2011) Application of the standard addition method for the absolute quantification of neutral lipids in microalgae using Nile red

    Journal of Microbiological Methods 87:17–23.

    https://doi.org/10.1016/j.mimet.2011.06.018

    • PubMed
    • Google Scholar
11. 1. Bleichrodt RJ
    2. van Veluw GJ
    3. Recter B
    4. Maruyama JI
    5. Kitamoto K
    6. Wösten HAB

    (2012) Hyphal heterogeneity in Aspergillus oryzae is the result of dynamic closure of septa by Woronin bodies

    Molecular Microbiology 86:1334–1344.

    https://doi.org/10.1111/mmi.12077

    • PubMed
    • Google Scholar
12. 1. Bleichrodt RJ
    2. Hulsman M
    3. Wösten HAB
    4. Reinders MJT

    (2015) Switching from a unicellular to multicellular organization in an Aspergillus niger hypha

    MBio 6:e00111.

    https://doi.org/10.1128/mBio.00111-15

    • PubMed
    • Google Scholar
13. 1. Bligh EG
    2. Dyer WJ

    (1959) A rapid method of total lipid extraction and purification

    Canadian Journal of Biochemistry and Physiology 37:911–917.

    https://doi.org/10.1139/o59-099

    • PubMed
    • Google Scholar
14. 1. Bourett TM
    2. Howard RJ

    (1994) Enhanced labelling of concanavalin a binding sites in fungal endomembranes using a double-sided, indirect method

    Mycological Research 98:769–775.

    https://doi.org/10.1016/S0953-7562(09)81053-8

    • Google Scholar
15. 1. Cardona A
    2. Saalfeld S
    3. Schindelin J
    4. Arganda-Carreras I
    5. Preibisch S
    6. Longair M
    7. Tomancak P
    8. Hartenstein V
    9. Douglas RJ

    (2012) TrakEM2 software for neural circuit reconstruction

    PLOS ONE 7:e38011.

    https://doi.org/10.1371/journal.pone.0038011

    • PubMed
    • Google Scholar
16. 1. Cole GT

    (1986) Models of cell differentiation in conidial fungi

    Microbiological Reviews 50:95–132.

    https://doi.org/10.1128/mr.50.2.95-132.1986

    • PubMed
    • Google Scholar
17. 1. Conway JR
    2. Lex A
    3. Gehlenborg N

    (2017) UpSetR: an R package for the visualization of intersecting sets and their properties

    Bioinformatics (Oxford, England) 33:2938–2940.

    https://doi.org/10.1093/bioinformatics/btx364

    • PubMed
    • Google Scholar
18. 1. Dalley NE
    2. Sonneborn DR

    (1982) Evidence that Blastocladiella emersonii zoospore chitin synthetase is located at the plasma membrane

    Biochimica et Biophysica Acta (BBA) - Biomembranes 686:65–76.

    https://doi.org/10.1016/0005-2736(82)90152-3

    • Google Scholar
19. 1. Dee JM
    2. Landry BR
    3. Berbee ML

    (2019) Actin guides filamentous rhizoid growth and morphogenesis in the zoosporic fungus Chytriomyces hyalinus

    Mycologia 111:904–918.

    https://doi.org/10.1080/00275514.2019.1669999

    • Google Scholar
20. 1. Dorward DW
    2. Powell MJ

    (1983) Cytochemical detection of polysaccharides and the ultrastructure of the cell coat of zoospores of Chytriomyces aureus and Chytriomyces hyalinus

    Mycologia 75:209–220.

    https://doi.org/10.1080/00275514.1983.12021657

    • Google Scholar
21. 1. Eitzen G
    2. Wang L
    3. Thorngren N
    4. Wickner W

    (2002) Remodeling of organelle-bound actin is required for yeast vacuole fusion

    The Journal of Cell Biology 158:669–679.

    https://doi.org/10.1083/jcb.200204089

    • PubMed
    • Google Scholar
22. 1. El Ghaouth A
    2. Arul J
    3. Wilson C
    4. Benhamou N

    (1994) Ultrastructural and cytochemical aspects of the effect of chitosan on decay of bell pepper fruit

    Physiological and Molecular Plant Pathology 44:417–432.

    https://doi.org/10.1016/S0885-5765(05)80098-0

    • Google Scholar
23. 1. Fisher MC
    2. Garner TWJ

    (2020) Chytrid fungi and global amphibian declines

    Nature Reviews. Microbiology 18:332–343.

    https://doi.org/10.1038/s41579-020-0335-x

    • PubMed
    • Google Scholar
24. 1. Frenken T
    2. Alacid E
    3. Berger SA
    4. Bourne EC
    5. Gerphagnon M
    6. Grossart H-P
    7. Gsell AS
    8. Ibelings BW
    9. Kagami M
    10. Küpper FC
    11. Letcher PM
    12. Loyau A
    13. Miki T
    14. Nejstgaard JC
    15. Rasconi S
    16. Reñé A
    17. Rohrlack T
    18. Rojas-Jimenez K
    19. Schmeller DS
    20. Scholz B
    21. Seto K
    22. Sime-Ngando T
    23. Sukenik A
    24. Van de Waal DB
    25. Van den Wyngaert S
    26. Van Donk E
    27. Wolinska J
    28. Wurzbacher C
    29. Agha R

    (2017) Integrating chytrid fungal parasites into plankton ecology: research gaps and needs

    Environmental Microbiology 19:3802–3822.

    https://doi.org/10.1111/1462-2920.13827

    • PubMed
    • Google Scholar
25. 1. Fritz-Laylin LK
    2. Lord SJ
    3. Mullins RD

    (2017) WASP and SCAR are evolutionarily conserved in actin-filled pseudopod-based motility

    The Journal of Cell Biology 216:1673–1688.

    https://doi.org/10.1083/jcb.201701074

    • PubMed
    • Google Scholar
26. 1. Gachet Y
    2. Hyams JS

    (2005) Endocytosis in fission yeast is spatially associated with the actin cytoskeleton during polarised cell growth and cytokinesis

    Journal of Cell Science 118:4231–4242.

    https://doi.org/10.1242/jcs.02530

    • PubMed
    • Google Scholar
27. 1. Gerphagnon M
    2. Agha R
    3. Martin-Creuzburg D
    4. Bec A
    5. Perriere F
    6. Rad-Menéndez C
    7. Gachon CMM
    8. Wolinska J

    (2019) Comparison of sterol and fatty acid profiles of chytrids and their hosts reveals trophic upgrading of nutritionally inadequate phytoplankton by fungal parasites

    Environmental Microbiology 21:949–958.

    https://doi.org/10.1111/1462-2920.14489

    • PubMed
    • Google Scholar
28. 1. Gow NAR
    2. Gooday GW

    (1987) Cytological aspects of dimorphism in Candida albicans

    Critical Reviews in Microbiology 15:73–78.

    https://doi.org/10.3109/10408418709104449

    • PubMed
    • Google Scholar
29. 1. Grossart HP
    2. Van den Wyngaert S
    3. Kagami M
    4. Wurzbacher C
    5. Cunliffe M
    6. Rojas-Jimenez K

    (2019) Fungi in aquatic ecosystems

    Nature Reviews Microbiology 17:339–354.

    https://doi.org/10.1038/s41579-019-0175-8

    • Google Scholar
30. 1. James TY
    2. Letcher PM
    3. Longcore JE
    4. Mozley-Standridge SE
    5. Porter D
    6. Powell MJ
    7. Griffith GW
    8. Vilgalys R

    (2006) A molecular phylogeny of the flagellated fungi (Chytridiomycota) and description of a new phylum (Blastocladiomycota)

    Mycologia 98:860–871.

    https://doi.org/10.3852/mycologia.98.6.860

    • PubMed
    • Google Scholar
31. 1. Jaworski AJ

    (1976) Synthesis of polyadenylic acid RNA during zoospore differentiation and germination in Blastocladiella emersonii

    Archives of Biochemistry and Biophysics 173:201–209.

    https://doi.org/10.1016/0003-9861(76)90250-2

    • PubMed
    • Google Scholar
32. 1. Kagami M
    2. von Elert E
    3. Ibelings BW
    4. de Bruin A
    5. van Donk E

    (2007) The parasitic chytrid, Zygorhizidium, facilitates the growth of the cladoceran zooplankter, Daphnia, in cultures of the inedible alga, Asterionella

    Proc. R. Soc. B 274:1561–1566.

    https://doi.org/10.1098/rspb.2007.0425

    • PubMed
    • Google Scholar
33. 1. Kagami M
    2. Miki T
    3. Takimoto G

    (2014) Mycoloop: Chytrids in aquatic food webs

    Frontiers in Microbiology 5:166.

    https://doi.org/10.3389/fmicb.2014.00166

    • Google Scholar
34. 1. Kagami M
    2. Motoki Y
    3. Masclaux H
    4. Bec A

    (2017) Carbon and nutrients of indigestible pollen are transferred to zooplankton by chytrid fungi

    Freshwater Biology 62:954–964.

    https://doi.org/10.1111/fwb.12916

    • Google Scholar
35. 1. Kanopoulos N
    2. Vasanthavada N
    3. Baker RL

    (1988) Design of an image edge detection filter using the Sobel operator

    IEEE Journal of Solid-State Circuits 23:358–367.

    https://doi.org/10.1109/4.996

    • Google Scholar
36. 1. Karpov SA
    2. Mamkaeva MA
    3. Benzerara K
    4. Moreira D
    5. López-García P

    (2014) Molecular phylogeny and ultrastructure of Aphelidium aff. melosirae (Aphelida, Opisthosporidia)

    Protist 165:512–526.

    https://doi.org/10.1016/j.protis.2014.05.003

    • PubMed
    • Google Scholar
37. 1. Klawonn I
    2. Van den Wyngaert S
    3. Parada AE
    4. Arandia-Gorostidi N
    5. Whitehouse MJ
    6. Grossart HP
    7. Dekas AE

    (2021) Characterizing the “fungal shunt”: Parasitic fungi on diatoms affect carbon flow and bacterial communities in aquatic microbial food webs

    PNAS 118:e2102225118.

    https://doi.org/10.1073/pnas.2102225118

    • PubMed
    • Google Scholar
38. 1. Koch WJ

    (1961) Studies of the motile cells of chytrids. III. major types

    American Journal of Botany 48:786.

    https://doi.org/10.2307/2439652

    • Google Scholar
39. 1. Laundon D
    2. Larson BT
    3. McDonald K
    4. King N
    5. Burkhardt P

    (2019) The architecture of cell differentiation in choanoflagellates and sponge choanocytes

    PLOS Biology 17:e3000226.

    https://doi.org/10.1371/journal.pbio.3000226

    • PubMed
    • Google Scholar
40. 1. Laundon D
    2. Chrismas N
    3. Wheeler G
    4. Cunliffe M

    (2020) Chytrid rhizoid morphogenesis resembles hyphal development in multicellular fungi and is adaptive to resource availability

    Proceedings of the Royal Society B Biological Sciences 287:20200433.

    https://doi.org/10.1098/rspb.2020.0433

    • PubMed
    • Google Scholar
41. 1. Laundon D
    2. Cunliffe M

    (2021) A call for A better understanding of aquatic chytrid biology

    Frontiers in Fungal Biology 2:30.

    https://doi.org/10.3389/ffunb.2021.708813

    • Google Scholar
42. 1. LéJohn HB
    2. Lovett JS

    (1966) Ribonucleic acid and protein synthesis in Rhizophlyctis rosea zoospores

    Journal of Bacteriology 91:709–717.

    https://doi.org/10.1128/jb.91.2.709-717.1966

    • Google Scholar
43. 1. Lodhi IJ
    2. Semenkovich CF

    (2014) Peroxisomes: a nexus for lipid metabolism and cellular signaling

    Cell Metabolism 19:380–392.

    https://doi.org/10.1016/j.cmet.2014.01.002

    • PubMed
    • Google Scholar
44. Book

    1. Lösel DM

    (1990) Lipids in the structure and function of fungal membranes biochemistry of cell walls and membranes

    In: Lösel DM, editors. Biochemistry of Cell Walls and Membranes in Fungi. Springer. pp. 119–133.

    https://doi.org/10.1007/978-3-642-74215-6_9

    • Google Scholar
45. 1. Love MI
    2. Huber W
    3. Anders S

    (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

    Genome Biology 15:1–21.

    https://doi.org/10.1186/s13059-014-0550-8

    • PubMed
    • Google Scholar
46. 1. Lovett JS

    (1963) Chemical and physical characterization of “nuclear caps” isolated from Blastocladiella zoospores

    Journal of Bacteriology 85:1235–1246.

    https://doi.org/10.1128/jb.85.6.1235-1246.1963

    • PubMed
    • Google Scholar
47. 1. Lovett JS

    (1968) Reactivation of ribonucleic acid and protein synthesis during germination of Blastocladiella zoospores and the role of the ribosomal nuclear cap

    Journal of Bacteriology 96:962–969.

    https://doi.org/10.1128/jb.96.4.962-969.1968

    • PubMed
    • Google Scholar
48. 1. Medina EM
    2. Turner JJ
    3. Gordân R
    4. Skotheim JM
    5. Buchler NE

    (2016) Punctuated evolution and transitional hybrid network in an ancestral cell cycle of fungi

    eLife 5:e09492.

    https://doi.org/10.7554/eLife.09492

    • Google Scholar
49. 1. Medina EM
    2. Buchler NE

    (2020) Chytrid fungi

    Current Biology 30:R516–R520.

    https://doi.org/10.1016/j.cub.2020.02.076

    • PubMed
    • Google Scholar
50. 1. Medina EM
    2. Robinson KA
    3. Bellingham-Johnstun K
    4. Ianiri G
    5. Laplante C
    6. Fritz-Laylin LK
    7. Buchler NE

    (2020) Genetic transformation of Spizellomyces punctatus, a resource for studying chytrid biology and evolutionary cell biology

    eLife 9:e52741.

    https://doi.org/10.7554/eLife.52741

    • Google Scholar
51. 1. Mondo SJ
    2. Dannebaum RO
    3. Kuo RC
    4. Louie KB
    5. Bewick AJ
    6. LaButti K
    7. Haridas S
    8. Kuo A
    9. Salamov A
    10. Bowen R
    11. Lipzen BP
    12. Sullivan A
    13. Andreopoulos W
    14. Clum BB
    15. Lindquist A
    16. Daum E
    17. Northen C
    18. Kunde-Ramamoorthy TR
    19. Schmitz G
    20. Gryganskyi RJ
    21. Culley A
    22. Magnuson D
    23. James J
    24. Stajich MA
    25. Spatafora JE
    26. Visel JW
    27. Grigoriev I V. A

    (2017) Widespread adenine N6-methylation of active genes in fungi

    Nature Genetics 49:964–968.

    https://doi.org/10.1038/ng.3859

    • Google Scholar
52. Book

    1. Money NP

    (2016) Spore production, discharge, and dispersal

    In: Money NP, editors. The Fungi. Academic Press. pp. 67–97.

    https://doi.org/10.1016/B978-0-12-382034-1.00003-7

    • Google Scholar
53. 1. Nagy LG
    2. Kovács GM
    3. Krizsán K

    (2018) Complex multicellularity in fungi: evolutionary convergence, single origin, or both?

    Biological Reviews of the Cambridge Philosophical Society 93:1778–1794.

    https://doi.org/10.1111/brv.12418

    • PubMed
    • Google Scholar
54. 1. Nagy LG
    2. Varga T
    3. Csernetics Á
    4. Virágh M

    (2020) Fungi took a unique evolutionary route to multicellularity: Seven key challenges for fungal multicellular life

    Fungal Biology Reviews 34:151–169.

    https://doi.org/10.1016/j.fbr.2020.07.002

    • Google Scholar
55. 1. Otsu N

    (1979) A threshold selection method from gray-level histograms

    IEEE Transactions on Systems, Man, and Cybernetics 9:62–66.

    https://doi.org/10.1109/TSMC.1979.4310076

    • Google Scholar
56. 1. Powell MJ

    (1974) Fine structure of plasmodesmata in a chytrid

    Mycologia 66:606.

    https://doi.org/10.2307/3758164

    • Google Scholar
57. 1. Powell MJ

    (1976) Ultrastructure and isolation of glyoxysomes (microbodies) in zoospores of the fungus Entophlyctis sp

    Protoplasma 89:1–27.

    https://doi.org/10.1007/BF01279325

    • Google Scholar
58. 1. Powell MJ

    (1977) Ultrastructural cytochemistry of the diaminobenzidine reaction in the aquatic fungus Entophlyctis variabilis

    Archives of Microbiology 114:123–136.

    https://doi.org/10.1007/BF00410773

    • Google Scholar
59. 1. Powell MJ

    (1979) The structure of microbodies and their associations with other organelles in zoosporangia of Entophlyctis variabilis

    Protoplasma 98:177–198.

    https://doi.org/10.1007/BF01281439

    • Google Scholar
60. 1. Powell MJ

    (1983) Localization of antimonate-mediated precipitates of cations in zoospores of Chytriomyces hyalinus

    Experimental Mycology 7:266–277.

    https://doi.org/10.1016/0147-5975(83)90047-6

    • Google Scholar
61. 1. Powell MJ
    2. Gillette L

    (1987) Septal structure of the chytrid Rhizophlyctis harderi

    Mycologia 79:635–639.

    https://doi.org/10.1080/00275514.1987.12025436

    • Google Scholar
62. 1. Powell MJ
    2. Letcher PM
    3. James TY

    (2017) Ultrastructural characterization of the host-parasite interface between Allomyces anomalus (Blastocladiomycota) and Rozella allomycis (Cryptomycota)

    Fungal Biology 121:561–572.

    https://doi.org/10.1016/j.funbio.2017.03.002

    • PubMed
    • Google Scholar
63. 1. Prostak SM
    2. Robinson KA
    3. Titus MA
    4. Fritz-Laylin LK

    (2021) The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

    Current Biology: CB 31:1192–1205.

    https://doi.org/10.1016/j.cub.2021.01.001

    • Google Scholar
64. 1. Rasconi S
    2. Ptacnik R
    3. Danner S
    4. Van den Wyngaert S
    5. Rohrlack T
    6. Pilecky M
    7. Kainz MJ

    (2020) Parasitic chytrids upgrade and convey primary produced carbon during inedible algae proliferation

    Protist 171:125768.

    https://doi.org/10.1016/j.protis.2020.125768

    • Google Scholar
65. 1. Roberts C
    2. Allen R
    3. Bird KE
    4. Cunliffe M

    (2020) Chytrid fungi shape bacterial communities on model particulate organic matter

    Biology Letters 16:20200368.

    https://doi.org/10.1098/rsbl.2020.0368

    • Google Scholar
66. 1. Rosenblum EB
    2. Stajich JE
    3. Maddox N
    4. Eisen MB

    (2008) Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis

    PNAS 105:17034–17039.

    https://doi.org/10.1073/pnas.0804173105

    • Google Scholar
67. 1. Schindelin J
    2. Arganda-Carreras I
    3. Frise E
    4. Kaynig V
    5. Longair M
    6. Pietzsch T
    7. Preibisch S
    8. Rueden C
    9. Saalfeld S
    10. Schmid B
    11. Tinevez JY
    12. White DJ
    13. Hartenstein V
    14. Eliceiri K
    15. Tomancak P
    16. Cardona A

    (2012) Fiji: an open-source platform for biological-image analysis

    Nature Methods 9:676–682.

    https://doi.org/10.1038/nmeth.2019

    • PubMed
    • Google Scholar
68. 1. Schmoyer IR
    2. Lovett JS

    (1969) Regulation of protein synthesis in zoospores of Blastocladiella

    Journal of Bacteriology 100:854–864.

    https://doi.org/10.1128/jb.100.2.854-864.1969

    • PubMed
    • Google Scholar
69. 1. Seong KY
    2. Zhao X
    3. Xu JR
    4. Güldener U
    5. Kistler HC

    (2008) Conidial germination in the filamentous fungus Fusarium graminearum

    Fungal Genetics and Biology 45:389–399.

    https://doi.org/10.1016/j.fgb.2007.09.002

    • PubMed
    • Google Scholar
70. 1. Sharma M
    2. Sengupta A
    3. Ghosh R
    4. Agarwal G
    5. Tarafdar A
    6. Nagavardhini A
    7. Pande S
    8. Varshney RK

    (2016) Genome wide transcriptome profiling of Fusarium oxysporum f sp. ciceris conidial germination reveals new insights into infection-related genes

    Scientific Reports 6:1–11.

    https://doi.org/10.1038/srep37353

    • PubMed
    • Google Scholar
71. 1. Silva AM
    2. Maia JC
    3. Juliani MH

    (1987) Changes in the pattern of protein synthesis during zoospore germination in Blastocladiella emersonii

    Journal of Bacteriology 169:2069–2078.

    https://doi.org/10.1128/jb.169.5.2069-2078.1987

    • PubMed
    • Google Scholar
72. 1. Tarling EJ
    2. de Aguiar Vallim TQ
    3. Edwards PA

    (2013) Role of ABC transporters in lipid transport and human disease

    Trends in Endocrinology and Metabolism 24:342–350.

    https://doi.org/10.1016/j.tem.2013.01.006

    • PubMed
    • Google Scholar
73. 1. Taube R
    2. Fabian J
    3. Van den Wyngaert S
    4. Agha R
    5. Baschien C
    6. Gerphagnon M
    7. Kagami M
    8. Krüger A
    9. Premke K

    (2019) Potentials and limitations of quantification of fungi in freshwater environments based on PLFA profiles

    Fungal Ecology 41:256–268.

    https://doi.org/10.1016/j.funeco.2019.05.002

    • Google Scholar
74. 1. Taylor JW
    2. Fuller MS

    (1980) Microtubules, organelle movement, and cross-wall formation at the sporangial-rhizoidal interface in the fungus, Chytridium confervae

    Protoplasma 104:201–221.

    https://doi.org/10.1007/BF01279768

    • Google Scholar
75. 1. Tedersoo L
    2. Sánchez-Ramírez S
    3. Kõljalg U
    4. Bahram M
    5. Döring M
    6. Schigel D
    7. May T
    8. Ryberg M
    9. Abarenkov K

    (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses

    Fungal Diversity 90:135–159.

    https://doi.org/10.1007/s13225-018-0401-0

    • Google Scholar
76. 1. Tinevez JY
    2. Perry N
    3. Schindelin J
    4. Hoopes GM
    5. Reynolds GD
    6. Laplantine E
    7. Bednarek SY
    8. Shorte SL
    9. Eliceiri KW

    (2017) TrackMate: An open and extensible platform for single-particle tracking

    Methods (San Diego, Calif.) 115:80–90.

    https://doi.org/10.1016/j.ymeth.2016.09.016

    • PubMed
    • Google Scholar
77. 1. van de Vossenberg B
    2. Warris S
    3. Nguyen HDT
    4. van Gent-Pelzer MPE
    5. Joly DL
    6. van de Geest HC
    7. Bonants PJM
    8. Smith DS
    9. Lévesque CA
    10. van der Lee TAJ

    (2019) Comparative genomics of chytrid fungi reveal insights into the obligate biotrophic and pathogenic lifestyle of Synchytrium endobioticum

    Scientific Reports 9:1–14.

    https://doi.org/10.1038/s41598-019-45128-9

    • PubMed
    • Google Scholar
78. 1. van der Walt S
    2. Schönberger JL
    3. Nunez-Iglesias J
    4. Boulogne F
    5. Warner JD
    6. Yager N
    7. Gouillart E
    8. Yu T
    9. scikit-image contributors

    (2014) scikit-image: image processing in Python

    PeerJ 2:e453.

    https://doi.org/10.7717/peerj.453

    • PubMed
    • Google Scholar
79. 1. van Zutphen T
    2. Todde V
    3. de Boer R
    4. Kreim M
    5. Hofbauer HF
    6. Wolinski H
    7. Veenhuis M
    8. van der Klei IJ
    9. Kohlwein SD

    (2014) Lipid droplet autophagy in the yeast Saccharomyces cerevisiae

    Molecular Biology of the Cell 25:290–301.

    https://doi.org/10.1091/mbc.E13-08-0448

    • PubMed
    • Google Scholar
80. 1. van’t Padje A
    2. Werner GDA
    3. Kiers ET

    (2021) Mycorrhizal fungi control phosphorus value in trade symbiosis with host roots when exposed to abrupt “crashes” and “booms” of resource availability

    The New Phytologist 229:2933–2944.

    https://doi.org/10.1111/nph.17055

    • PubMed
    • Google Scholar
81. 1. Venard CM
    2. Vasudevan KK
    3. Stearns T

    (2020) Cilium axoneme internalization and degradation in chytrid fungi

    Cytoskeleton (Hoboken, N.J.) 77:365–378.

    https://doi.org/10.1002/cm.21637

    • PubMed
    • Google Scholar
82. 1. Veses V
    2. Richards A
    3. Gow NAR

    (2008) Vacuoles and fungal biology

    Current Opinion in Microbiology 11:503–510.

    https://doi.org/10.1016/j.mib.2008.09.017

    • PubMed
    • Google Scholar
83. 1. Vevea JD
    2. Garcia EJ
    3. Chan RB
    4. Zhou B
    5. Schultz M
    6. Di Paolo G
    7. McCaffery JM
    8. Pon LA

    (2015) Role for lipid droplet biogenesis and microlipophagy in adaptation to lipid imbalance in yeast

    Developmental Cell 35:584–599.

    https://doi.org/10.1016/j.devcel.2015.11.010

    • PubMed
    • Google Scholar
84. 1. Virtanen P
    2. Gommers R
    3. Oliphant TE
    4. Haberland M
    5. Reddy T
    6. Cournapeau D
    7. Burovski E
    8. Peterson P
    9. Weckesser W
    10. Bright J
    11. van der Walt SJ
    12. Brett M
    13. Wilson J
    14. Millman KJ
    15. Mayorov N
    16. Nelson ARJ
    17. Jones E
    18. Kern R
    19. Larson E
    20. Carey CJ
    21. Polat İ
    22. Feng Y
    23. Moore EW
    24. VanderPlas J
    25. Laxalde D
    26. Perktold J
    27. Cimrman R
    28. Henriksen I
    29. Quintero EA
    30. Harris CR
    31. Archibald AM
    32. Ribeiro AH
    33. Pedregosa F
    34. van Mulbregt P
    35. SciPy 1.0 Contributors

    (2020) SciPy 1.0: fundamental algorithms for scientific computing in Python

    Nature Methods 17:261–272.

    https://doi.org/10.1038/s41592-019-0686-2

    • PubMed
    • Google Scholar
85. 1. Wang Y
    2. Kim SG
    3. Wu J
    4. Yu S
    5. Kang KY
    6. Kim ST

    (2011) Proteasome inhibitors affect appressorium formation and pathogenicity of the rice blast fungus, Magnaporthe oryzae

    The Plant Pathology Journal 27:225–231.

    https://doi.org/10.5423/PPJ.2011.27.3.225

    • Google Scholar
86. 1. Whiteside MD
    2. Werner GDA
    3. Caldas VEA
    4. Van’t Padje A
    5. Dupin SE
    6. Elbers B
    7. Bakker M
    8. Wyatt GAK
    9. Klein M
    10. Hink MA
    11. Postma M
    12. Vaitla B
    13. Noë R
    14. Shimizu TS
    15. West SA
    16. Kiers ET

    (2019) Mycorrhizal fungi respond to resource inequality by moving phosphorus from rich to poor patches across networks

    Current Biology 29:2043–2050.

    https://doi.org/10.1016/j.cub.2019.04.061

    • PubMed
    • Google Scholar
87. 1. Yoshida M
    2. Nakayama T
    3. Inouye I

    (2009) Nuclearia thermophila sp. nov. (Nucleariidae), a new nucleariid species isolated from Yunoko Lake in Nikko (Japan)

    European Journal of Protistology 45:147–155.

    https://doi.org/10.1016/j.ejop.2008.09.004

    • Google Scholar
88. 1. Yu G
    2. Wang LG
    3. Han Y
    4. He QY

    (2012) clusterProfiler: an R package for comparing biological themes among gene clusters

    Omics 16:284–287.

    https://doi.org/10.1089/omi.2011.0118

    • PubMed
    • Google Scholar
89. 1. Yutin N
    2. Wolf MY
    3. Wolf YI
    4. Koonin EV

    (2009) The origins of phagocytosis and eukaryogenesis

    Biology Direct 4:1–26.

    https://doi.org/10.1186/1745-6150-4-9

    • Google Scholar
90. 1. Zhou T
    2. Wang X
    3. Luo J
    4. Ye B
    5. Zhou Y
    6. Zhou L
    7. Lai T

    (2018) Identification of differentially expressed genes involved in spore germination of Penicillium expansum by comparative transcriptome and proteome approaches

    MicrobiologyOpen 7:e00562.

    https://doi.org/10.1002/mbo3.562

    • PubMed
    • Google Scholar

Author details

1. Davis Laundon

   1. Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, United Kingdom
   2. School of Environmental Sciences, University of East Anglia, Norwich, United Kingdom

   Contribution

   Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Software, Validation, Visualization, Writing - original draft, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-1508-664X

2. Nathan Chrismas

   Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, United Kingdom

   Contribution

   Data curation, Formal analysis, Methodology, Software, Validation, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-2165-3102

3. Kimberley Bird

   Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, United Kingdom

   Contribution

   Investigation, Methodology, Writing – review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-7244-5960

4. Seth Thomas

   Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, United Kingdom

   Contribution

   Formal analysis, Investigation, Methodology, Visualization, Writing – review and editing

   Competing interests

   No competing interests declared

5. Thomas Mock

   School of Environmental Sciences, University of East Anglia, Norwich, United Kingdom

   Contribution

   Supervision, Validation, Writing – review and editing

   Competing interests

   No competing interests declared

6. Michael Cunliffe

   1. Marine Biological Association, The Laboratory, Citadel Hill, Plymouth, United Kingdom
   2. School of Biological and Marine Sciences, University of Plymouth, Plymouth, United Kingdom

   Contribution

   Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Validation, Writing - original draft, Writing – review and editing

   For correspondence

   micnli@mba.ac.uk

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6716-3555

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