Cytoskeletal Evolution and Eukaryotic Diversity Notes

Cytoskeletal Evolution and Eukaryotic Diversity

Introduction

The diversity of eukaryotic form and function arises from changes in cell shape, movement, and cell-cell interactions, all regulated by the cytoskeleton.

Cytoskeleton Functions

The cytoskeleton regulates various cellular activities:

• Cell shape.

• Cell movement.

• Cell-cell interaction.

• Cell division.

• Intracellular trafficking.

• Phagocytosis.

• Endocytosis.

• Organelle division.

Cytoskeletal changes have significant impacts on eukaryotic phenotype.

Model Species

Model species are used to understand cellular mechanisms driving specific cytoskeletal functions.

Lineage-Level Diversity

Lineage-level diversity is studied to understand the diversification of lineages.

The lineages include:

• Bilaterians

• Cnidarians

• Ctenophores

• Poriferans

• Choanoflagellates

• Filastereans

• Ichthyosporeans

• Ascomycetes

• Basidiomycetes

• Chytrids

• Microsporidians

• Opisthokonts

Reference: PMID: 32251396

Eukaryotic-Level Diversity

Eukaryotic-level diversity is studied to understand eukaryotic diversification, which began over 2 billion years ago.

Cytoskeletal Structures

The core of the cytoskeleton is composed of actin and microtubules.

Dynamics of Actin and Microtubule Structures

Actin and microtubule structures are dynamic networks regulated at multiple levels, including:

• Spontaneous assembly.

• Formin (straight).

• ENA/VASP (straight).

• ARP2/3 Complex (branched).

• ATP to ADP conversion.

• Severing.

• Depolymerization.

• Capping.

• Regrowth / annealing.

• Recycling.

• Bundling / crosslinking.

• Sliding / gliding.

• Nucleation.

• Turnover.

• Organization.

• Polymer interactions.

• Polymer assembly.

Cytoskeletal Network Complexity

The complexity of cytoskeletal networks could explain the diversity of eukaryotic phenotypes.

Cytoskeletal Regulators

The types of cytoskeletal regulators present in different lineages are being studied.

Categories of Regulators

• Polymer assembly:

  • Tubulins and tubulin assembly (Alpha, Beta, Gamma, Other, TbcA-E).

  • Augmin (HAUS6).

  • Tpx2.

  • Mzt1.

  • TACC domain.

  • GCP (GCP2-6).

  • EB1.

• Microtubule dynamics:

  • MAP215/Dis1/chTOG/Msps / MORN1.

  • Orbit /MAST/CLASP.

  • CAP-Gly.

  • CAMSAP/CKK.

  • Asp/ASPM.

  • EMAP.

• Polymer turnover:

  • Katanin (p80).

  • Katanin (p60).

  • Spastin.

  • Fidgetin.

  • TTL.

  • CCP.

  • VASH

• Post-translational modification:

  • aTAT.

• Polymer interactions:

  • PRC1.

  • Doublecortin.

  • MAP2/Tau.

• Bundling and stabilization.

• Motors:

  • Kinesin-1 (KIF5).

  • Kinesin-2 (KIF3).

  • Kinesin-3 (KIF1).

  • Kinesin-4/10 (KIF4A).

  • Kinesin-5 (Eg5).

  • Kinesin-6 (MKLP-1).

  • Kinesin-7 (CENP-E).

  • Kinesin-8 (KIF18A).

  • Kinesin-9 (KIF6).

  • Kinesin-13 (MCAK).

  • Kinesin-14 (KIFC1).

  • Cytoplasmic dynein HC.

  • Axonemal dynein HC, outer arm.

  • Axonemal dynein HC, inner arm.

  • Dynactin (p150glued).

Copy Number

The copy number of cytoskeletal regulators varies across species (Ng Nf Tb Gl Tv Tg Pf Tt Tp Ps Cr At Dd Sr Hs Dm Bd Sc Sp):

• 0

• 1

• 2-3-6

• >6

Conservation of Cytoskeletal Regulators

Cytoskeletal regulators are widely conserved across eukaryotic evolution.

It's not simply accumulation of complexity.

Cytoskeletal Evolution and Eukaryotic Diversity

How does cytoskeletal evolution give rise to diversity of eukaryotic form and function?

Reference: PMID: 32251396

Diversification of Actin Networks

Most of what we know about actin comes from studying animal cells and yeast.

• Actin patches.

• Actin cables.

• Pseudopods.

• Cortex.

How did the actin networks of animals and yeast diverge from their common ancestor?

Reference: PMID: 16959963

Chytrids

Chytrids have a biphasic lifecycle with features resembling both animal and yeast cells.

• Growth form: “sporangium”.

• Dispersal form: “zoospore”.

• Animal-like flagellum.

• Chitin cell wall.

Chytrid Fungi as Genetic Systems

The lab has developed chytrid fungi as genetic systems to study the evolution of actin phenotypes.

• Chytrids diverged early in fungal evolution.

• Fungi

• Opisthokonts

• Dikarya

Species listed:

• Cryptococcus

• Saccharomyces

• Aspergillus

• Schizosaccharomyces

• Animals

• Chytrids

• Capsaspora

• Monosiga

• Caenorhabditis

• Drosophila

• Danio

• Xenopus

• Homo

• Mus

• Allomyces

• Batrachochytrium

• Spizellomyces

• Rhizoclosmatium

• Ustilago

• Candida

• Neurospora

• Magnaporthe

• Dikarya

References: PMID: 32392127, bioRxiv: 10.1101/2023.10.17.561934

Evolution of Actin Regulators

To trace the evolution of actin phenotypes, we need to trace the evolution of actin regulators.

Categories of Actin Regulators

• Nucleators: Formins, Arp2/3 complex, Spire.

• Arp2/3 complex activators: WASP, Dip1, SCAR Complex, WASH Complex, Cortactin.

• Monomer binding: Profilin, Verprolin/WIP.

• Filament binding: , Tropomyosin, ENA/VASP, MTSS/MIM.

• Capping proteins: Capping Protein, AIP1, Tropomodulin, Eps8.

• Severing proteins: ADF/Cofilin, SRV2, Twinfilin, Gelsolin-family.

• Bundlers/Crosslinkers: Fimbrin/plastin, , EPLIN, Espin, Fascin, Filamin.

• Endo-/ Exocytosis: EPS15, HIP1R, ABP1/Drebrin, Coronin.

• Other: Talin, CARMIL.

Copy Number

The copy number of actin regulators varies (Hs Sp Bd Bs Rg Am Sc Spo Sj Ca An Nc Mo Um):

• 1

• 2

• 3-6

• 0

• >6

Reference: PMID: 33561386

Actin Regulators in Fungi

Dikaryotic fungi are missing many animal actin regulators.

Chytrid fungi have an intermediate complement of actin regulators.

Reference: PMID: 33561386

Functions of Actin Regulators in Chytrids

What do chytrids do with all of these actin regulators?

• Dispersal form: “zoospore”:

  • Cortex.

  • Pseudopods

References: PMID: 33561386, bioRxiv: 10.1101/2023.10.17.561934

• Growth form: “sporangium”:

  • Actin patches.

  • Actin cables.

• Crawling genes.

• Endocytosis genes

References: PMID: 33561386, bioRxiv: 10.1101/2023.10.17.561934

Animal-like
Yeast-like

Evolution of Actin Phenotypes

Yeast evolved from an ancestor with animal-like actin regulators and animal-like phenotypes.

Reference: PMID: 33561386, bioRxiv: 10.1101/2023.10.17.561934

Rule 1: Cytoskeletal Gene Loss

Cytoskeletal gene loss can drive diversification of eukaryotic form and function.

Reference: PMID: 32251396