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Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation.

ABSTRACT: BACKGROUND:Application of apomixis, or asexual seed formation, in crop breeding would allow rapid fixation of complex traits, economizing improved crop delivery. Identification of apomixis genes is confounded by the polyploid nature, high genome complexity and lack of genomic sequence integration with reproductive tissue transcriptomes in most apomicts. RESULTS:A genomic and transcriptomic resource was developed for Hieracium subgenus Pilosella (Asteraceae) which incorporates characterized sexual, apomictic and mutant apomict plants exhibiting reversion to sexual reproduction. Apomicts develop additional female gametogenic cells that suppress the sexual pathway in ovules. Disrupting small RNA pathways in sexual Arabidopsis also induces extra female gametogenic cells; therefore, the resource was used to examine if changes in small RNA pathways correlate with apomixis initiation. An initial characterization of small RNA pathway genes within Hieracium was undertaken, and ovary-expressed ARGONAUTE genes were identified and cloned. Comparisons of whole ovary transcriptomes from mutant apomicts, relative to the parental apomict, revealed that differentially expressed genes were enriched for processes involved in small RNA biogenesis and chromatin silencing. Small RNA profiles within mutant ovaries did not reveal large-scale alterations in composition or length distributions; however, a small number of differentially expressed, putative small RNA targets were identified. CONCLUSIONS:The established Hieracium resource represents a substantial contribution towards the investigation of early sexual and apomictic female gamete development, and the generation of new candidate genes and markers. Observed changes in small RNA targets and biogenesis pathways within sexual and apomictic ovaries will underlie future functional research into apomixis initiation in Hieracium.

SUBMITTER: Rabiger DS

PROVIDER: S-EPMC5054587 | biostudies-literature | 2016 Oct

REPOSITORIES: biostudies-literature

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Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation.

Rabiger David S DS Taylor Jennifer M JM Spriggs Andrew A Hand Melanie L ML Henderson Steven T ST Johnson Susan D SD Oelkers Karsten K Hrmova Maria M Saito Keisuke K Suzuki Go G Mukai Yasuhiko Y Carroll Bernard J BJ Koltunow Anna M G AM

BMC biology 20161006 1

<h4>Background</h4>Application of apomixis, or asexual seed formation, in crop breeding would allow rapid fixation of complex traits, economizing improved crop delivery. Identification of apomixis genes is confounded by the polyploid nature, high genome complexity and lack of genomic sequence integration with reproductive tissue transcriptomes in most apomicts.<h4>Results</h4>A genomic and transcriptomic resource was developed for Hieracium subgenus Pilosella (Asteraceae) which incorporates char ...[more]

PMID: 27716180

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Project description:Background and aimsApomixis or asexual seed reproduction is a key evolutionary mechanism in certain angiosperms providing them with reproductive assurance and isolation. Nevertheless, the frequency of apomixis is largely unknown, especially in groups with autonomous apomixis such as the diploid-polyploid genus Hieracium.MethodsUsing flow cytometric analyses, we determined the ploidy level and reproductive pathways (sexual vs. apomictic) for 7616 seeds originating from 946 plants belonging to >50 taxa sampled at 130 sites across Europe.Key resultsDiploid seeds produced by diploids were formed exclusively by the sexual pathway after double fertilization of reduced embryo sacs. An absolute majority of tri- and tetraploid seeds (99.6 %) produced by tri- and tetrapolyploid taxa were formed by autonomous apomixis. Only 20 polyploid seeds (0.4 %) were formed sexually. These seeds, which originated on seven polyploid accessions of four taxa, were formed after fertilization of either unreduced embryo sacs through a so-called triploid bridge or reduced embryo sacs, and frequently resulted in progeny with an increased ploidy. In addition, the formation of seedlings with increased ploidy (4x and 6x) was found in two triploid plants. This is the first firm evidence on functional facultative apomixis in polyploid members of Hieracium sensu stricto (s.s.).ConclusionsThe mode of reproduction in Hieracium s.s. is tightly associated with ploidy. While diploids produce seeds exclusively sexually, polyploids produce seeds by obligate or almost obligate apomixis. Strict apomixis can increase the reproductive assurance and this in turn can increase the colonization ability of apomicts. Nevertheless, our data clearly show that certain polyploid plants are still able to reproduce sexually and contribute to the formation of new cytotypes and genotypes. The finding of functional facultative apomicts is essential for future studies focused on evolution, inheritance and ecological significance of apomixis in this genus.

Project description:BackgroundApomixis, the asexual reproduction through seeds, occurs in over 40 plant families and avoids the hidden cost of sex. Apomictic plants are thought to have an advantage in sparse populations and when colonizing new areas but may have a disadvantage in changing environments because they propagate via fixed genotypes. In this study, we separated the influences of different genetic backgrounds (potentially reflecting local adaptation) from those of the mode of reproduction, i.e., sexual vs. apomictic, on nine fitness-related traits in Hieracium pilosella L. We aimed to test whether apomixis per se may provide a fitness advantage in different competitive environments in a common garden setting.ResultsTo separate the effects of genetic background from those of reproductive mode, we generated five families of apomictic and sexual full siblings by crossing two paternal with four maternal parents. Under competition, apomictic plants showed reproductive assurance (probability of seeding, fertility), while offspring of sexual plants with the same genetic background had a higher germination rate. Sexual plants grew better (biomass) than apomictic plants in the presence of grass as a competitor but apomictic plants spread further vegetatively (maximum stolon length) when their competitors were sexual plants of the same species. Furthermore, genetic background as represented by the five full-sibling families influenced maximum stolon length, the number of seeds, and total fitness. Under competition with grass, genetic background influenced fecundity, the number of seeds, and germination rate.ConclusionsOur results suggest that both the mode of reproduction as well as the genetic background affect the success of H. pilosella in competitive environments. Total fitness, the most relevant trait for adaptation, was only affected by the genetic background. However, we also show for the first time that apomixis per se has effects on fitness-related traits that are not confounded by-and thus independent of-the genetic background.

Dataset Information

Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation.

Publications

Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation.

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