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Phylogenetics and evolution of monocot mycoheterotrophs and a newly demonstrated lineage of carnivorous monocots Lin, Qianshi

Abstract

I used various approaches to investigate mycoheterotrophic and carnivorous monocots, which obtain essential nutrients from soil fungal partners or animal prey, respectively. Fully mycoheterotrophic plants are unable to photosynthesize, and can be difficult to place in plant phylogeny due to substantial morphological modification and elevated substitution rates in all three plant genomes. Mitochondrial genes are expected to be less susceptible to long-branch artefacts in phylogenetic inference than plastid or nuclear genes, as they generally evolve more slowly. I used a phylogenomic approach considering all 37 protein-coding mitochondrial genes to infer the phylogenetic placements of mycoheterotrophic lineages of monocots. I infer that Thismiaceae (excluding Afrothismia) are distantly related to Burmanniaceae, but that fully mycoheterotrophic Afrothismia (Thismiaceae) is the sister group of photosynthetic Taccaceae and core Thismiaceae. The latter finding supports a further independent loss of photosynthesis in Dioscoreales. Scattered distribution of the cox1 intron in distantly related lineages of monocot mycoheterotrophs supports convergent intron gains, potentially consistent with repeated invasions from soil fungal genomes. I demonstrate that Triantha occidentalis (Tofieldiaceae, Alismatales) is a previously overlooked carnivorous lineage with a sticky-trap inflorescence. Field experiments, isotopic data and mixing models demonstrate significant N transfer from prey, with an estimated 68% of leaf N obtained from capture, comparable to levels for co-occurring sundew. Glandular hairs on flowering stems secrete phosphatase, a digestive enzyme seen in other carnivorous plants. Triantha is nearly unique among carnivorous plants in capturing prey on its inflorescence axis close to flowers; however, its glandular hairs capture only small insects. I also studied Triantha phylogeography across its mostly North American range, by surveying 11 plastid-encoded ndh genes from 75 populations. All three North American species are likely monophyletic, although T. occidentalis monophyly requires recognizing T. japonica as a synonym, which is consistent with its nested position in T. occidentalis, as the sister group of populations in Haida Gwaii (Canada). Plastid ndh genes have experienced various degrees of loss or reading frame interruption within T. glutinosa and T. occidentalis, and a strong geographic signal is evident in patterns of ndh gene loss/pseudogenization across the range of T. occidentalis.

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