studying parasite evolution using comparative transcriptomic and phylogenomic analyses

Open Access
Author:
Yang, Zhenzhen
Graduate Program:
Plant Biology
Degree:
Doctor of Philosophy
Document Type:
Dissertation
Date of Defense:
March 29, 2016
Committee Members:
  • Claude W De Pamphilis, Dissertation Advisor
  • Claude W De Pamphilis, Committee Chair
  • Charles T Anderson, Committee Member
  • Yinong Yang, Committee Member
  • Naomi S Altman, Special Member
Keywords:
  • parasitic plants
  • haustoria
  • transcriptome
  • phylogenomic
  • gene duplication
  • co-option
  • horizontal gene transfer
Abstract:
Parasitic plants are plants that form a parasitic association with their host using a connecting organ called the haustorium, a novel feeding structure through which parasites withdraw nutrients such as carbon and nitrogen from the conducting tissues of the host. Orobanchaceae is the only family containing species with the full spectrum of parasitic capabilities, including one nonparasitic autotrophic genus, Lindenbergia, and more than 90 genera (>2000 species) of parasites with varying degrees of photosynthesis and host dependence. To understand the genetic changes that led to a parasitic lifestyle, a transcriptome sequencing project was initialized to interrogate multiple stages of growth and development of three parasitic plants that span the range of parasitic dependence. Around 180 genes are upregulated during haustorial development following host attachment in at least two species, and these are enriched in proteases, cell wall modifying enzymes, and extracellular secretion proteins. The majority of parasitism genes were duplicated before the divergence of Orobanchaceae and Mimulus, a related nonparasitic plant. This suggests that gene duplication plays a role in the origin of parasitism. A comparative analysis of these genes’ homologs in sequenced nonparasitic plant genomes revealed that parasitic plants make haustoria by co-opting genes from root and floral development. Gene duplication, often taking place in a nonparasitic ancestor of Orobanchaceae, followed by regulatory neofunctionalization, was an important process in the origin of parasitic haustoria. Horizontal gene transfer (HGT), acts as another evolutionary force contributing to parasite adaptation. At least 42 gene families accounting for 52 transfers – largely via genomic integration - result in functional transcripts that were primarily involved in translation, defense responses, transposable element (TE), and other diverse roles. Three lines of evidence indicate an adaptive role of HGT in parasite evolution - (i) A majority of HGT genes are upregulated in haustoria-related tissues in the most parasitic Phelipanche aegyptiaca; (ii) A higher frequency of HGTs are observed in parasites with a higher degree of parasitism; (iii) A portion of genes detected to have evolved some adaptive sites under positive selection. The study of strigolactone (SL) pathway in parasitic plants reveals that parasitic plants still retain genes in SL synthesis. Two SL biosynthesis genes and D14 (the receptor) are upregulated in haustorial structures, indicating a possibility of SL in haustoria development.