Ecological and Genetic Investigations of the Nickel Hyperaccumulator Streptanthus polygaloides (Brassicaceae)

Abstract

Hyperaccumulators are plants that take up, transport, and sequester large amounts of an element in their tissues. By doing this, they often achieve tissue concentrations that are toxic to most organisms. In this dissertation, I combined DNA sequence analyses with ecological studies of allocation strategies and herbivory to broaden our knowledge of the Ni hyperaccumulator Streptanthus polygaloides Gray, a species restricted to California serpentine soils. First, I assembled and annotated complete chloroplast genome sequences for all four morphs of S. polygaloides. Phylogenetic analyses strongly supported clades aligning with geographic collection localities. Second, I evaluated if seeds of the Ni hyperaccumulator, and a congeneric non-hyperaccumulator species also found on California serpentine soils (Streptanthus insignis Jepson), are resistant to predation by a generalist granivore, Tribolium confusum Jaquelin du Val. In addition, I investigated Ni toxicity to the granivore using an artificial diet study. I determined that Ni in S. polygaloides seeds can, due to its toxicity, act as an elemental defense against seed herbivores even at 300 µg Ni g-1, a level below the 1000 µg Ni g-1 hyperaccumulation threshold concentration. In contrast, seeds of the congeneric non-hyperaccumulator species (S. insignis) contained little Ni (~5 µg Ni g-1) and their consumption did not affect T. confusum. Third, I evaluated if Ni hyperaccumulation is associated with herbivory tolerance by applying levels of artificial herbivory to S. polygaloides and S. insignis plants grown in either control or Ni-amended soil. Plants of S. polygaloides receiving greater damage produced significantly more flowers, and had greater biomass, when grown in Ni-amended soil than plants in unamended soil, but this effect did not occur with the non-hyperaccumulator S. insignis. I conclude that S. polygaloides better tolerates herbivory when hyperaccumulating Ni, thus increasing plant fitness when herbivory damage is severe. Lastly, I compared root proliferation of S. polygaloides and S. insignis in control and Ni-amended soil. Root proliferation by S. polygaloides was two-fold greater in Ni-amended soil, but S. insignis demonstrated no differential response to soil Ni. Directional root growth to Ni also was measured in seedlings of the two species germinated on agar medium. Roots of S. polygaloides tended to grow toward a Ni source (the source created a Ni concentration gradient in the agar), produced more lateral roots in the direction of the Ni source, and lateral roots were longer the direction of the Ni source. In contrast, roots of S. insignis did not respond to the Ni concentration gradient. I concluded that S. polygaloides exhibited several positive root foraging responses to Ni (biomass, directional growth, elongation, and lateral root initiation) that may enhance its Ni uptake ability and suggest the term “nickelophilic root foraging” for this behavior. Overall, my research increases our knowledge of this Ni hyperaccumulator species and expands our understanding of the potential functions of hyperaccumulation in plants.