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. 2017 Aug 1;114(31):E6361-E6370.
doi: 10.1073/pnas.1703088114. Epub 2017 Jul 17.

Insights Into the Red Algae and Eukaryotic Evolution From the Genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

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Free PMC article

Insights Into the Red Algae and Eukaryotic Evolution From the Genome of Porphyra umbilicalis (Bangiophyceae, Rhodophyta)

Susan H Brawley et al. Proc Natl Acad Sci U S A. .
Free PMC article

Abstract

Porphyra umbilicalis (laver) belongs to an ancient group of red algae (Bangiophyceae), is harvested for human food, and thrives in the harsh conditions of the upper intertidal zone. Here we present the 87.7-Mbp haploid Porphyra genome (65.8% G + C content, 13,125 gene loci) and elucidate traits that inform our understanding of the biology of red algae as one of the few multicellular eukaryotic lineages. Novel features of the Porphyra genome shared by other red algae relate to the cytoskeleton, calcium signaling, the cell cycle, and stress-tolerance mechanisms including photoprotection. Cytoskeletal motor proteins in Porphyra are restricted to a small set of kinesins that appear to be the only universal cytoskeletal motors within the red algae. Dynein motors are absent, and most red algae, including Porphyra, lack myosin. This surprisingly minimal cytoskeleton offers a potential explanation for why red algal cells and multicellular structures are more limited in size than in most multicellular lineages. Additional discoveries further relating to the stress tolerance of bangiophytes include ancestral enzymes for sulfation of the hydrophilic galactan-rich cell wall, evidence for mannan synthesis that originated before the divergence of green and red algae, and a high capacity for nutrient uptake. Our analyses provide a comprehensive understanding of the red algae, which are both commercially important and have played a major role in the evolution of other algal groups through secondary endosymbioses.

Keywords: calcium-signaling; carbohydrate-active enzymes; cytoskeleton; stress tolerance; vitamin B12.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Distribution of cytoskeletal motor proteins (kinesin, cytoplasmic dynein, and myosin) in red algae compared with other select groups of Eukarya, showing the reduced cytoskeletal capacity of red algal cells. Standard motor family nomenclatures for dyneins (104), kinesins (105), and myosins (106) are used; for example, kinesins K1, K2, and K3 are cytoskeletal motors that move organelles and vesicles in many eukaryotes. Footnotes: *This may be a contaminating sequence. The Saccharomyces dynein complex has lost much of the functionality found in other organisms (104). Additional, flagellar-related dynein HC are not shown and are absent in red algae and many plants. §Myosins M8 and M11 are vesicle transporters in plants. Galdieria and SCR members of the SCRP clade (SI Appendix, Fig. S11) have a myosin similar to myosin 27 of apicomplexans.
Fig. 2.
Fig. 2.
Conserved gene clusters involved in MAA biosynthesis in P. umbilicalis and related red algae. (A) Biosynthetic pathway from sedoheptulose 7-phosphate to shinorine in cyanobacteria and proposed pathway to porphyra-334 in red algae. (B) Comparison of gene clusters and gene fusions in the cyanobacteria Anabaena and Nostoc and the red algae P. umbilicalis and C. crispus.
Fig. 3.
Fig. 3.
Module structure and presence or absence of different Ca2+ sensor kinases in Porphyra and other eukaryotes: CAMK, CIPK, CDPK, CDTKL. The CDTKLs from Porphyra and other red algae represent a newly recognized family of protein kinases belonging to the TKL family that contains multiple Ca2+-binding EF hands.
Fig. 4.
Fig. 4.
Neighbor-joining phylogenetic tree of GT2 showing the positions of Porphyra sequences (dark triangles) and rooted on bacterial cellulose synthase (bcsA). Red algal cellulose synthases (CESA) cluster most closely with stramenopile oomycete CESAs, whereas bangiophyte CSL enzymes are sister to a clade of green plant CSLs that includes a mannan synthase. Two red algal GT2s are related to bcsA, likely because of horizontal gene transfer. Red algal sequences lie on red branches and triangles group sequences in Viridiplantae (green), stramenopiles (brown), Cyanobacteria (turquoise), Bacteria (pink), and Amoebozoa (gray). The proteins were aligned using MAFFT with the L-INS-I algorithm and the scoring matrix Blosum62 and then manually refined with BIOEDIT. The phylogenetic tree was calculated using maximum likelihood in MEGA 6.06. See SI Appendix, Table S42 for full names and GenBank accession numbers. Bootstrap values ≥ 65% are shown at nodes.
Fig. 5.
Fig. 5.
Phylogenetic profile of FTR1 and FEA/ISIP2a homologs in photosynthetic eukaryotes. Whether each organism is an alga, is multicellular, or lacks true roots is indicated with a colored square, and the presence of a FTR1 or FEA/ISIP2a homolog in that organism is indicated with a colored circle. The same color is used to highlight the cooccurrence between a trait and a gene. Among sequenced algae and plants, FTR1 homologs are only encoded in genomes of organisms that lack true roots, whereas FEA/ISIP2a homologs are only encoded by algal genomes. Multicellularity does not correlate with the presence of either protein family. The roots of Selaginella moellendorffii are morphologically and evolutionarily distinct, but share characteristics with true roots including a root cap and root hairs.

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