Unraveling the Mysteries of Brown Algae's Sex Chromosomes

Researchers from the Max Planck Institute for Biology Tübingen made a groundbreaking discovery, revealing that an HMG-box gene in brown algae plays a crucial role in determining male sex.

Unraveling the Mysteries of Brown Algae
Microscopic view of Ectocarpus sp. mature gametophyte filaments. Gametes are produced in plurilocular gametangia, structures that become thicker and dark-brown when mature. Image Credit: Dr. Rémy Luthringer Max Planck Institute for Biology, Germany

This finding significantly enhances the comprehension of sex-determination mechanisms in eukaryotic organisms. Until now, master sex-determination genes have only been identified in a limited number of animals and plants.

The study sheds light on the evolutionary parallels in developmental pathways between animals and seaweeds, despite their millions of years of independent evolution. It underscores the recurring utilization of a shared genetic “toolkit” across distant lineages for essential biological functions. Apart from providing deeper insights into brown algae's reproductive biology, this research delves into distant evolutionary convergences. The study was published in Science.

The Enigmatic U/V Sex Chromosome System in Brown Algae

The genetic regulation that underlies sex determination varies greatly amongst species, despite the fact that most sexually reproducing organisms are frequently clearly male or female. The seemingly uncomplicated appearance of brown algae, which have fascinating sex-determination mechanisms, is another example of this diversity.

Brown algae are photosynthetic, multicellular, marine eukaryotes. These organisms have independently evolved several important biological characteristics, such as multicellularity, complex life cycles, and sex chromosomes, from plants and animals. Brown algae are a great model organism for studying the evolutionary aspects of reproduction because of these special qualities.

Organisms ranging from simple single-celled organisms to intricate multicellular forms are classified as eukaryotes. Different sex chromosomes are seen in eukaryotes.

Males have an X and a Y chromosome in mammals with the XX/XY system. Likewise, in the ZZ/ZW system found in fish, birds, and certain insects, males usually possess both ZZ chromosomes. Animals have two copies of their genome during embryonic development—one copy from each parent—which leads to the XX/XY and ZZ/ZW systems.

Certain master sex-determination factors have been found on the Y and W chromosomes, respectively, and these systems contain specific factors that initiate male or female differentiation. Algae, mosses, and lichens have only been found to have one sex-determining factor, whereas the U/V system has received less research. On the other hand, fungi do not depend on unique sex chromosomes. To identify their sex and potential mates, they use mating-type genes.

The U/V sex chromosome system is one characteristic that sets brown algae apart. Unlike diploid animals with two complete sets of chromosomes, brown algae determine their sexes during their haploid stage, when they have only one copy of their genome. Brown algae are classified as female or male based on which chromosome they carry.

Insights From CRISPR/Cas Genetic Manipulation

In their natural habitat, brown algae gametes engage in a mesmerizing mating dance. Female gametes fix quickly onto substrates and release a pheromone, like a chemical signal, in seawater to attract males. Male gametes actively swim using two flagella in progressively closer circles around the females, attracted by their ‘perfume’.”

Dr. Rémy Luthringer, Head, Algal Culture Facility, Max Planck Institute for Biology Tübingen

These brown algae’s genetic material could be precisely targeted and edited by the researchers thanks to the development of CRISPR/Cas technology, sometimes known as “gene scissors.” By creating mutants with a loss of function, they tested the biological function of MIN using this tool. The outcome was evident.

The intricate male gamete mating dance was absent in the CRISPR mutant lines. Meaning that in the absence of MIN, the gametes became completely insensitive to the female pheromone. When we knocked out MIN, the sex-determinant gene in brown algae, we did not observe a sex reversal. Instead, the males became asexual. This is because they are missing the complementary chromosome, the female U chromosome. This suggests a female-inducer factor on the U chromosome is yet to be discovered.”

Dr. Susana Coelho, Director, Algal Development and Evolution Department, Max Planck Institute for Biology Tübingen

The researchers were able to clarify the complex mechanisms controlling the determination of male sex in brown algae by means of these genetic experiments.

Dr. Coelho remarked, “Identifying an HMG-domain gene as the brown algal master sex factor reveals that animals and seaweeds have independently converged on the same solution for determining male sex.”

The Evolution of Sex Determination, Thanks to a Shared Genetic Toolkit

Exploring the evolutionary timeline, the unicellular last common ancestor shared between algae and animals did not possess the distinct sex chromosomes found in these two groups of organisms.

The origin of the HMG-box domain can be traced back to the last eukaryotic common ancestor, whereas MIN evolved later in the common ancestor of brown algae.”

Dr. Vikram Alva, Project Leader, Protein Bioinformatics, Max Planck Institute for Biology Tübingen

Mammals, fungi, and brown algae all have homologous HMG-box domains shared by their sex-determination factors, suggesting their origins are in common ancestral genetics.

Dr. Alva emphasized, “While MIN and SRY are homologous, they are not orthologous; they were derived before lineages diverged into different organisms. Their functional similarities are an example of convergent evolution, whereby the HMG-box domain adapted a similar role across organisms despite their independent evolution.”

It is like building different genes with Lego bricks from the same box, to put it simply. Functional similarities and shared ancestry can be found in the Lego bricks, but the results differ.  “And in this case, animals and brown algae independently used similar building blocks to reach the same result, male sex determination,” clarified Dr. Josué Barrera-Redondo, a Humboldt Research Fellow in Dr. Coelho’s team.

These scientists' next goals will be to pinpoint the master gene that controls the development of female sex in brown algae and comprehend the asexual phenotype that results from their loss of the U chromosome.

Beyond the conventional animal and plant models, identifying this crucial MIN gene enables researchers to go deeper into the evolutionary dynamics shaping sex-determination mechanisms across the tree of life. This line of inquiry may advance the knowledge of developmental regulation and evolutionary biology by offering a more complete picture of the genetic processes underlying sex determination in brown algae.

Source:
Journal reference:

Luthringer, R., et al., (2024) Repeated co-option of HMG-box genes for sex determination in brown algae and animals. Science. doi.org/10.1126/science.adk5466

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