Transcriptomes of the Parasitic Plant Family Orobanchaceae Reveal Surprising Conservation of Chlorophyll Synthesis

Abstract

Parasitism in flowering plants has evolved at least 11 times [1]. Only one family, Orobanchaceae, comprises all major nutritional types of parasites: facultative, hemiparasitic (partially photosynthetic), and holoparasitic (nonphotosynthetic) [2]. Additionally, the family includes Lindenbergia, a nonparasitic genus sister to all parasitic Orobanchaceae [3-6]. Parasitic Orobanchaceae include species with severe economic impacts: Striga (witchweed), for example, affects over 50 million hectares of crops in sub-Saharan Africa, causing more than $3 billion in damage annually [7]. Although gene losses and increased substitution rates have been characterized for parasitic plant plastid genomes [5, 8-11], the nuclear genome and transcriptome remain largely unexplored. The Parasitic Plant Genome Project (PPGP; http://ppgp.huck.psu.edu/) [2] is leveraging the natural variation in Orobanchaceae to explore the evolution and genomic consequences of parasitism in plants through a massive transcriptome and gene discovery project involving Triphysaria versicolor (facultative hemiparasite), Striga hermonthica (obligate hemiparasite), and Phelipanche aegyptiaca (Orobanche [12]; holoparasite). Here we present the first set of large-scale genomic resources for parasitic plant comparative biology. Transcriptomes of above-ground tissues reveal that, in addition to the predictable loss of photosynthesis-related gene expression in P. aegyptiaca, the nonphotosynthetic parasite retains an intact, expressed, and selectively constrained chlorophyll synthesis pathway.

Mechanistic model of evolutionary rate variation en route to a nonphotosynthetic lifestyle in plants

“…Their plastomes also show more genomic rearrangements than autotrophs and the facultative hemiparasites T. versicolor and Bartsia inaequalis (17). These results are further corroborated by gene expression data from aboveground tissue of S. hermonthica, which expresses nuclear genes for light harvesting and photosystems with lower abundance than T. versicolor (18). The relaxation of purifying selection in both photosynthesis and housekeeping genes (e.g., rpl, rps) (Fig.…”

De Novo Assembly and Characterization of the Transcriptome of the Parasitic Weed Dodder Identifies Genes Associated with Plant Parasitism

“…1C). However, some studies showed that stems of different Cuscuta spp., including dodder, photosynthesize to varying degrees, consistent with other lineages of parasitic plants (Choudhury and Sahu, 1999;Revill et al, 2005;Wickett et al, 2011). Our differential gene expression analysis also showed high expression of photosynthetic genes in dodder seedlings.…”

“…Recently, de novo assembly and analysis of transcriptomes of root parasites, belonging to family Orobanchaceae, provided important insight into the process of parasitism, showing the association of photosynthesis-related genes and cell wall-modifying b-expansin in the process of parasitism (Wickett et al, 2011;Honaas et al, 2013). To understand the molecular mechanisms underlying dynamic morphological and functional changes in haustoria development, however, detailed transcriptional profiling along developmental stages of parasitism is necessary.…”

A Plastid without a Genome: Evidence from the Nonphotosynthetic Green Algal Genus Polytomella

“…Thus, the absence of ptDNA reads from Illumina sequencing data of four different Polytomella spp. is perplexing as is the absence of an obvious plastid gene expression system from P. parva transcriptomic data, especially given that transcriptome sequencing of other colorless algae has consistently uncovered such a system (Bozdech et al, 2003;Borza et al, 2005;Wickett et al, 2011). Nuclear genes encoding proteins involved in the replication, repair, or expression of ptDNA represent a significant proportion (.7%) of the predicted C. reinhardtii plastid proteome (Terashima et al, 2011).…”