Evolutionary patterns of salt tolerance in angiosperms

Date

2015

Authors

Moray, Camile

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Abstract

Global food production is threatened by increasing land salinization triggered by climate change, land clearing, and irrigation. Salinity is toxic to most plants, including most crop species. A tremendous research effort has focused on understanding how a rare set of naturally salt tolerant plants, halophytes, are able to cope with soil salinity, as a model for producing salt tolerant crops. One largely unexplored area of research is the evolution of salt tolerance. Previous studies show that salt tolerance has evolved multiple times across the angiosperms, but little is known about the patterns and processes that underlie the evolution of salt tolerance. In my thesis I addressed several questions relating to the evolution of salt tolerance in angiosperms using a broad-scale, macroevolutionary approach. I first used taxonomic and phylogenetic comparative techniques to assess the evolutionary patterns of salt tolerance in angiosperms. I found that over one-third of angiosperm families contain halophytes and that salt tolerance appears to have evolved hundreds of times in the angiosperms. In over half of the family phylogenies analyzed, salt tolerance appeared evolutionarily labile: the origins of salt tolerance were scattered across phylogenies and generally gave rise to only one or a few halophytes. I also explored the association between salt tolerance and another trait associated with anthropogenic environmental change, heavy metal hyperaccumulation: the ability to accumulate high concentrations of heavy metals/metalloids. Taxonomic and physiological similarities suggest that salt tolerance may be associated with hyperaccumulation. I test the suggested relationship between these abilities using taxonomic and phylogenetic analyses. Significantly more angiosperm families contain both halophytes and hyperaccumulators and significantly more species are reported as both halophytes and hyperaccumulators than expected given the rarity of each trait. In several families, halophytes and hyperaccumulators are more closely related than expected if the two traits evolved independently. These results support the observation that salt tolerance and heavy metal hyperaccumulation are associated in angiosperms. Prolonged or repeated exposure to salinity can cause oxidative stress that may lead to increased mutation rates. These mutations may lead to increased substitution rates in halophytes compared to non-salt tolerant relatives. We tested this idea by comparing DNA sequences of multiple genes from the chloroplast, mitochondrial, and nuclear genomes from several halophytes with their non-salt tolerant relatives. We found that halophytes have significantly increased total substitution rates compared to their non-salt tolerant relatives in mitochondrial genes. This finding provides evidence that environmental factors may be associated with molecular rates. The goal of developing salt tolerant crops has proved incredibly difficult, which may be partly due to loss in genetic variation associated with domestication. Yet several studies suggest that domesticated animals and plants may have increased rates of molecular evolution, which could lead to increased variation. We test whether domesticates have consistently increased rates of molecular evolution by comparing the mitochondrial genomes of domesticated mammals and birds to their wild relatives. While a few domesticates exhibited higher rates, in general we found no consistent difference in mitochondrial rates of domesticated animals compared to their wild relatives. Keywords: comparative analysis, phylogenetics, domestication, macroevolution, rates of molecular evolution, halophytes

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comparative analysis, phylogenetics, domestication, macroevolution, rates of molecular evolution, halophytes

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Thesis (PhD)

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