Journal
PROTOPLASMA
Volume 259, Issue 3, Pages 487-593Publisher
SPRINGER WIEN
DOI: 10.1007/s00709-021-01665-7
Keywords
Glaucophyta; Rhodelphis; Picozoa; Transitional plate; Acorn-V filaments; Infrakingdom Rhodaria
Categories
Funding
- NERC [NE/C510975/1]
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The author thoroughly discusses the evolution of ciliary transition zones, highlighting previously overlooked ultrastructural details and establishing fundamental principles throughout eukaryotes. The integration of TZ/ciliary evolution with multiprotein trees has led to the recognition of new major eukaryote clades and the revision of the megaclassification of the basal kingdom Protozoa. The discovery of non-photosynthetic phagotrophic flagellates with genome-free plastids and the similarities between Rhodelphis and Picomonas shed light on early plant and chromist evolution.
I thoroughly discuss ciliary transition zone (TZ) evolution, highlighting many overlooked evolutionarily significant ultrastructural details. I establish fundamental principles of TZ ultrastructure and evolution throughout eukaryotes, inferring unrecognised ancestral TZ patterns for Fungi, opisthokonts, and Corticata (i.e., kingdoms Plantae and Chromista). Typical TZs have a dense transitional plate (TP), with a previously overlooked complex lattice as skeleton. I show most eukaryotes have centriole/TZ junction acorn-V filaments (whose ancestral function was arguably supporting central pair microtubule-nucleating sites; I discuss their role in centriole growth). Uniquely simple malawimonad TZs (without TP, simpler acorn) pinpoint the eukaryote tree's root between them and TP-bearers, highlighting novel superclades. I integrate TZ/ciliary evolution with the best multiprotein trees, naming newly recognised major eukaryote clades and revise megaclassification of basal kingdom Protozoa. Recent discovery of non-photosynthetic phagotrophic flagellates with genome-free plastids (Rhodelphis), the sister group to phylum Rhodophyta (red algae), illuminates plant and chromist early evolution. I show previously overlooked marked similarities in cell ultrastructure between Rhodelphis and Picomonas, formerly considered an early diverging chromist. In both a nonagonal tube lies between their TP and an annular septum surrounding their 9+2 ciliary axoneme. Mitochondrial dense condensations and mitochondrion-linked smooth endomembrane cytoplasmic partitioning cisternae further support grouping Picomonadea and Rhodelphea as new plant phylum Pararhoda. As Pararhoda/Rhodophyta form a robust clade on site-heterogeneous multiprotein trees, I group Pararhoda and Rhodophyta as new infrakingdom Rhodaria of Plantae within subkingdom Biliphyta, which also includes Glaucophyta with fundamentally similar TZ, uniquely in eukaryotes. I explain how biliphyte TZs generated viridiplant stellate-structures.
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