Cutting edge: exploring evolutionary convergence at the gene level

Dong Zhai Gang national mangrove reservoir

Mangroves are trees that grow in the ocean, but that doesn’t mean they all evolved from a single mangrove predecessor. Instead, they are a diverse group of species distributed across more than 25 families. The mangrove lifestyle has arisen multiple times. Their shared characteristics – tolerance of variable salinities ranging from twice seawater to freshwater, tolerance of flooding and waterlogging (and drying), tolerance of high temperatures and high irradiance, tolerance of UV – are the result of evolutionary convergence at the phenotypic level (a.k.a. phenotypic convergence).

Clearly, phenotypic convergence must somehow reflect changes at the genetic and genomic levels.  At the genomic level, for example, Dassanayake et al reported parallel differences in KEGG pathway representation and transcript profiles for two unrelated mangroves (Heritiera littoralis and Rhizophora mangle) when compared with Populus trichocarpa.

But this is not the same as convergence at the gene level.  That is the new, exciting and unique contribution of the paper by Xu, He et al., Genome-wide convergence during Evolution of Mangroves from Woody Plants

Shaohua Xu, Ziwen He, Zixiao Guo, Zhang Zhang, Gerald J Wyckoff, Anthony Greenberg, Chung-I Wu and Suhua ShiMol. Biol. Evol. (2017) doi:10.1093/molbev/msw277

It turns out that the problem of finding convergent genes is a tricky one. If, hypothetically, you had the genomes for multiple species, and if, again hypothetically, they all diverged from a common ancestor whose genome remained constant for the millions of years since that happened… then the problem would be rather simple. But such a collection of genomes doesn’t yet exist, and that is not the way evolution works. As the authors here note: “the results [of searches for candidate genes] are often controversial… A main reason for the uncertainty is that molecular convergence is a noisy process.” The noise arises because random genetic changes may occur in parallel, without responding to a particular driver. Further, divergence can only be inferred if an ancestral character can be accurately determined. And, getting accurate rates and patterns of nucleotide substitution – and knowing they are accurate – is difficult.

In preparation for this paper, Suhua Shi’s lab sequenced the genomes of Avicennia marinaSonneratia alba and Rhizophora apiculata. For the analysis, these were compared to the available genomes of three non-mangroves and rice. They first used a modeling approach to assess and reduce the noise levels inherent in data sets such as these. This itself is a major contribution of the paper. Then, they applied the methods to the mangroves.

In the end, the authors were able to map 232 candidate genes to the KEGG PATHWAY database, finding two pathways significantly enriched for convergent genes in the mangroves: ubiquitin-mediated proteolysis (12 genes) and N-glycan biosynthesis (5 genes). They concluded that although many of these genes “may seem to be involved in basal functions… Such activities become targets of adaptation when the functions they are involved in are put under stress.” As they note, both of the pathways “are upstream regulation processes” mediating many things, but adaptation to the many stresses facing the plants, and embryo development in viviparous species stand out.

We can now look at this paper as an important first contribution to the subject of gene convergent evolution in plants, and particularly in extremophytes where it may be most critical and (perhaps) most easily separated from the noise of general genetic variations. Dr. Shi has communicated that her lab has now sequenced the genomes for the mangroves, Rhizophora apiculata, Avicennia marina, Sonneratia alba and S. caseolaris and resequenced the whole genomes of R. mangle, R. stylosa and R. mucronata, and three subspecies of A. marina. They hope to get these published this year. When they do, it will open opportunities to continue the work they present here, and for extremophyte workers throughout the world to begin the comparative analyses we have all been talking about for such a long time.

Suhua Shi, Sun Yat-sen University, PI. Her research focuses on adaptive evolution and speciation in mangroves
Mr. Xu Shaohua is a Ph.D candidate of Sun Yat-sen University, studying adaptive evolution of mangrove species using whole genome data.
Dr. He Ziwen is a research fellow of Sun Yat-sen University, who is interested in evolutionary genomics, bioinformatics and molecular ecology in mangroves and rice.


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