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Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty.

ABSTRACT: The origin of novel traits is recognized as an important process underlying many major evolutionary radiations. We studied the genetic basis for the evolution of haustoria, the novel feeding organs of parasitic flowering plants, using comparative transcriptome sequencing in three species of Orobanchaceae. 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. Additionally, about 100 shared genes are upregulated in response to haustorium inducing factors prior to host attachment. Collectively, we refer to these newly identified genes as putative "parasitism genes." Most of these parasitism genes are derived from gene duplications in a common ancestor of Orobanchaceae and Mimulus guttatus, a related nonparasitic plant. Additionally, the signature of relaxed purifying selection and/or adaptive evolution at specific sites was detected in many haustorial genes, and may play an important role in parasite evolution. Comparative analysis of gene expression patterns in parasitic and nonparasitic angiosperms suggests that parasitism genes are derived primarily from root and floral tissues, but with some genes co-opted from other tissues. 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.

SUBMITTER: Yang Z

PROVIDER: S-EPMC4327159 | biostudies-literature | 2015 Mar

REPOSITORIES: biostudies-literature

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Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty.

Yang Zhenzhen Z Wafula Eric K EK Honaas Loren A LA Zhang Huiting H Das Malay M Fernandez-Aparicio Monica M Huang Kan K Bandaranayake Pradeepa C G PC Wu Biao B Der Joshua P JP Clarke Christopher R CR Ralph Paula E PE Landherr Lena L Altman Naomi S NS Timko Michael P MP Yoder John I JI Westwood James H JH dePamphilis Claude W CW

Molecular biology and evolution 20141221 3

The origin of novel traits is recognized as an important process underlying many major evolutionary radiations. We studied the genetic basis for the evolution of haustoria, the novel feeding organs of parasitic flowering plants, using comparative transcriptome sequencing in three species of Orobanchaceae. 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 extracell ...[more]

PMID: 25534030

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Project description:Sclerotinia sclerotiorum is a serious pathogen of numerous crops around the world. The major virulence factor of this pathogen is oxalic acid (OA). Mutants that cannot produce OA do not cause disease, and plants that express enzymes that degrade OA, such as oxalate oxidase (OxO), are very resistant to S. sclerotiorum. To examine the effect of OA on plants, we infiltrated soybean leaves with 5 mm OA and examined the gene expression changes at 2 h post-infiltration. By comparing the gene expression levels between leaves of a transgenic soybean carrying an OxO gene (OxO) and its parent AC Colibri (AC) infiltrated with OA (pH 2.4) or water (pH 2.4 or 5.5), we were able to compare the effects of OA dependent or independent of its pH. Gene expression by microarray analysis identified 2390 genes that showed changes in expression, as determined using an overall F-test P-value cut-off of 0.001. The additional requirement that at least one pairwise t-test false discovery rate (FDR)-corrected P value should be less than 0.001 reduced the list of the most highly significant differentially expressed genes to 1054. Independent of pH, OA altered the expression levels of 78 genes, with ferritin showing the strongest induction by OA. The combination of OA plus its low pH caused 1045 genes (99% of all significant genes) to be differentially expressed, with many of the up-regulated genes being related to basal defence, such as genes of the phenylpropanoid pathway and various cytochrome P450s. RNA-seq was also conducted on four samples: OxO and AC genotypes infiltrated with either OA pH 2.4 or water pH 2.4. The RNA-seq analysis also identified ferritin paralogues as being strongly induced by OA. As the expression of ferritin, a gene that encodes for an iron storage protein, is induced by free iron, these results suggest that S. sclerotiorum benefits from the ability of OA to free iron from plant proteins, as this induces host cell death, and also allows the uptake and assimilation of the iron for its own metabolic needs.

Dataset Information

Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty.

Publications

Comparative transcriptome analyses reveal core parasitism genes and suggest gene duplication and repurposing as sources of structural novelty.

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