Dataset Information

Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta.

ABSTRACT: Pucciniamonoica is a spectacular plant parasitic rust fungus that triggers the formation of flower-like structures (pseudoflowers) in its Brassicaceae host plant Boecherastricta. Pseudoflowers mimic in shape, color, nectar and scent co-occurring and unrelated flowers such as buttercups. They act to attract insects thereby aiding spore dispersal and sexual reproduction of the rust fungus. Although much ecological research has been performed on P. monoica-induced pseudoflowers, this system has yet to be investigated at the molecular or genomic level. To date, the molecular alterations underlying the development of pseudoflowers and the genes involved have not been described. To address this, we performed gene expression profiling to reveal 256 plant biological processes that are significantly altered in pseudoflowers. Among these biological processes, plant genes involved in cell fate specification, regulation of transcription, reproduction, floral organ development, anthocyanin (major floral pigments) and terpenoid biosynthesis (major floral volatile compounds) were down-regulated in pseudoflowers. In contrast, plant genes involved in shoot, cotyledon and leaf development, carbohydrate transport, wax biosynthesis, cutin transport and L-phenylalanine metabolism (pathway that results in phenylethanol and phenylacetaldehyde volatile production) were up-regulated. These findings point to an extensive reprogramming of host genes by the rust pathogen to induce floral mimicry. We also highlight 31 differentially regulated plant genes that are enriched in the biological processes mentioned above, and are potentially involved in the formation of pseudoflowers. This work illustrates the complex perturbations induced by rust pathogens in their host plants, and provides a starting point for understanding the molecular mechanisms of pathogen-induced floral mimicry.

SUBMITTER: Cano LM

PROVIDER: S-EPMC3775748 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta.

Cano Liliana M LM Raffaele Sylvain S Haugen Riston H RH Saunders Diane G O DG Leonelli Lauriebeth L MacLean Dan D Hogenhout Saskia A SA Kamoun Sophien S

PloS one 20130917 9

Pucciniamonoica is a spectacular plant parasitic rust fungus that triggers the formation of flower-like structures (pseudoflowers) in its Brassicaceae host plant Boecherastricta. Pseudoflowers mimic in shape, color, nectar and scent co-occurring and unrelated flowers such as buttercups. They act to attract insects thereby aiding spore dispersal and sexual reproduction of the rust fungus. Although much ecological research has been performed on P. monoica-induced pseudoflowers, this system has yet ...[more]

PMID: 24069397

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Project description:Wheat stripe rust, caused by Puccinia striiformis f. sp. tritici, is a costly global disease that burdens farmers with yield loss and high fungicide expenses. This sophisticated biotrophic parasite infiltrates wheat leaves and develops infection structures inside host cells, appropriating nutrients while suppressing the plant defense response. Development in most eukaryotes is regulated by small RNA molecules, and the success of host-induced gene silencing technology in Puccinia spp. implies the existence of a functional RNAi system. However, some fungi lack this capability, and small RNAs have not yet been reported in rust fungi. The objective of this study was to determine whether P. striiformis carries an endogenous small RNA repertoire.We extracted small RNA from rust-infected wheat flag leaves and performed high-throughput sequencing. Two wheat cultivars were analyzed: one is susceptible; the other displays partial high-temperature adult plant resistance. Fungal-specific reads were identified by mapping to the P. striiformis draft genome and removing reads present in uninfected control libraries. Sequencing and bioinformatics results were verified by RT-PCR. Like other RNAi-equipped fungi, P. striiformis produces large numbers of 20-22 nt sequences with a preference for uracil at the 5' position. Precise post-transcriptional processing and high accumulation of specific sRNA sequences were observed. Some predicted sRNA precursors possess a microRNA-like stem-loop secondary structure; others originate from much longer inverted repeats containing gene sequences. Finally, sRNA-target prediction algorithms were used to obtain a list of putative gene targets in both organisms. Predicted fungal target genes were enriched for kinases and small secreted proteins, while the list of wheat targets included homologs of known plant resistance genes.This work provides an inventory of small RNAs endogenous to an important plant pathogen, enabling further exploration of gene regulation on both sides of the host/parasite interaction. We conclude that small RNAs are likely to play a role in regulating the complex developmental processes involved in stripe rust pathogenicity.

Project description:Background and aims:In the Brassicaceae family, apomictic development is characteristic of the genus Boechera. Hybridization, polyploidy and environmental adaptation that arose during the evolution of Boechera may serve as (epi)genetic regulators of apomictic initiation in this genus. Here we focus on Boechera stricta, a predominantly diploid species that reproduces sexually. However, apomictic development in this species has been reported in several studies, indicating non-obligate sexuality. Methods:A progressive investigation of flower development was conducted using three accessions to assess the reproductive system of B. stricta. We employed molecular and cyto-embryological identification using histochemistry, transmission electron microscopy and Nomarski and epifluorescence microscopy. Key Results:Data from internal transcribed spacer (ITS) and chloroplast haplotype sequencing, in addition to microsatellite variation, confirmed the B. stricta genotype for all lines. Embryological data indicated irregularities in sexual reproduction manifested by heterochronic ovule development, longevity of meiocyte and dyad stages, diverse callose accumulation during meiocyte-to-gametophyte development, and the formation of triads and tetrads in several patterns. The arabinogalactan-related sugar epitope recognized by JIM13 immunolocalized to one or more megaspores. Furthermore, pollen sterility and a high frequency of seed abortion appeared to accompany reproduction of the accession ES512, along with the initiation of parthenogenesis. Data from flow cytometric screening revealed both sexual and apomictic seed formation. Conclusion:These results imply that B. stricta is a species with an underlying ability to initiate apomixis, at least with respect to the lines examined here. The existence of apomixis in an otherwise diploid sexual B. stricta may provide the genomic building blocks for establishing highly penetrant apomictic diploids and hybrid relatives. Our findings demonstrate that apomixis per se is a variable trait upon which natural selection could act.

Dataset Information

Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta.

Publications

Major transcriptome reprogramming underlies floral mimicry induced by the rust fungus Puccinia monoica in Boechera stricta.

Similar Datasets

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