A simple change determines male vs female organ development in flowers

ResearchBlogging.org Gene duplication is a  major source of genomic novelty for evolution to work on.  When genes duplicate, the extra copy of the gene is often redundant – it might degrade and become a pseudogene or take on a completely new function.  Alternatively, the function of the original gene might become partitioned between the two duplicates in a process known as subfunctionalization.  An excellent example of this has recently been reported in the genes that control male and female organ development in the flower, and it’s (almost) all down to a single amino acid change between the duplicate genes.

Development of male and female reproductive organs in flowers is controlled largely by a group of genes called MADS-box transcription factors. Different versions of these transcription factors (known as A, B or C function genes) are expressed in different parts of the developing flower, acting either alone or together to produce sepals, petals, stamens (male) or carpels (female)*.

Much of what we know about flower development comes from studies on two “model” plants – Arabidopsis (rockcress) and Antirrhinum (snapdragon).  In these species, and in many other flowering plants, the MADs-box C-function gene that controls the production of carpels vs stamens has duplicated. In Arabidopsis, one of the copies (called AG) makes both male and female organs, but the other copy has taken on the completely new function of making seed pods shatter (and is appropriately called SHATTERPROOF).  However, in Antirrhinum both copies still play a role in sex organ development: one copy (called FAR) makes only male parts, while the other copy (PLE) makes mainly female parts but also has a small role in making male parts.

Thus in Antirrhinum, the function of the original gene (making both male and female parts) has almost been split between the two duplicate copies.  In a study published online in PNAS last week, researchers at the University of Leeds, led by Professor Brendan Davies,  found a surprisingly simple difference in the two copies has led to their profoundly different roles.

Davies and colleagues created chimeric versions of PLE and FAR, swapping domains between the proteins to determine exactly what parts of the different proteins are responsible for their differing function.  They narrowed down the difference between the two genes to a single amino acid that is present in FAR but not in PLE. When this amino acid was removed from FAR, the gene switched to making both female and male parts.  FAR and PLE are estimated to have duplicated around 120 million years ago, and the researchers estimate that the mutation responsible for inserting the extra amino acid into FAR happened around 20 million years after the duplication.

Duplicated genes often take on new functions because changes in their regulatory regions change how and where they are expressed.  Thus, finding an example such as this one, where a simple change in the protein coding sequence causes a profound change in function is somewhat unusual.  However, these proteins don’t act in isolation – they are just one part of a network of genes that must work together to control sex organ development.  Davies and colleagues found that the single amino acid change alters the ability of the protein to interact with other proteins in this network.

The additional amino acid in FAR is found in the part of the protein that interacts with other types of MADs-box proteins called SEP proteins.  C-function genes without the additional amino acid (like PLE) can interact with 3 different SEP proteins (SEP1, SEP2 and SEP3), but proteins with the additional amino acid (like FAR) can only interact with SEP3.  The SEP3 gene is not expressed in the first whorl of the flower, where female parts are produced, so FAR doesn’t have anything to interact with in this whorl and therefore doesn’t produce female parts.

Davies describes this as “an excellent example of how a chance imperfection sparks evolutionary change”.  It is also a nice example of subfunctionalization in action, where a simple amino acid change provides a means of separating the functions of the duplicate copies by causing a change in how the protein operates in a larger regulatory network.

Reference: Airoldi CA, Bergonzi S, & Davies B (2010). Single amino acid change alters the ability to specify male or female organ identity. Proceedings of the National Academy of Sciences of the United States of America PMID: 20956314

*For more on the ABC model of plant development, see here or here.

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