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Generation of an Integrated Hieracium Genomic and Transcriptomic Resource Enables Exploration of Small RNA Pathways During Apomixis Initiation David S

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Generation of an Integrated Hieracium Genomic and Transcriptomic Resource Enables Exploration of Small RNA Pathways During Apomixis Initiation David S Rabiger et al. BMC Biology (2016) 14:86 DOI 10.1186/s12915-016-0311-0 RESEARCH ARTICLE Open Access Generation of an integrated Hieracium genomic and transcriptomic resource enables exploration of small RNA pathways during apomixis initiation David S. Rabiger1, Jennifer M. Taylor2, Andrew Spriggs2, Melanie L. Hand1, Steven T. Henderson1, Susan D. Johnson1, Karsten Oelkers1, Maria Hrmova3, Keisuke Saito4, Go Suzuki4, Yasuhiko Mukai4, Bernard J. Carroll5 and Anna M. G. Koltunow1* 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. Background followed by parental gamete fusion and embryogenesis Apomixis describes a suite of reproductive processes in at fertilization, apomixis avoids meiosis during female flowering plants that result in asexual seed formation, gamete development, and embryogenesis initiates with- and subsequently give rise to progeny which are clones out fertilization. Use of apomixis in plant breeding could of the maternal parent [1]. Contrary to the sexual economize and speed delivery of new plant varieties by pathway, wherein the diversity of progeny is derived preserving unlinked complex traits, such as heterosis in from meiotic recombination during gamete formation hybrid crops, within a single seed generation. As apomixis is not evident in major seed crops, isolation of * Correspondence: [email protected] genes from apomictic model species with the intention 1Commonwealth Scientific and Industrial Research Organisation Agriculture and Food, Private Bag 2, Glen Osmond, South Australia 5064, Australia Full list of author information is available at the end of the article © 2016 Rabiger et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Rabiger et al. BMC Biology (2016) 14:86 Page 2 of 21 to transfer them to crops has been a major focus of formation pathways [21]. A substantial expressed se- research. quence tag (EST) database from a closer relative within Most apomictic species are polyploids, often with large the Asteraceae, lettuce (Lactuca sativa), also an obligate genomes, and evidence suggests apomixis is generally con- sexual, is publicly available together with a high-density ferred by dominant loci in most examined species [2, 3]. genetic map [22]; however, functional annotation within Apomictic loci are often found to be associated with highly the lettuce EST resource is limited. The availability of a repetitive chromosomal regions where recombination is Hieracium genomic resource coupled with temporally suppressed, and additional loci also appear to influence the staged ovary transcriptomes, where the events of apo- penetrance of the apomixis phenotype [1, 3, 4]. To date, mixis take place, could significantly accelerate the isola- genes within apomictic loci which are capable of conferring tion of apomixis genes and loci. apomixis phenotypes are largely unknown, with the Within aposporous species of Hieracium,specificationof exception of a recently identified gene from apomictic the megaspore mother cell (MMC), meiosis and selection Pennisetum that stimulates fertilization-independent em- of the functional megaspore (FM) occur as found during bryogenesis [5]. typical polygonum-type female gamete development in Identification of genes regulating apomixis has been sexual plant species (Fig. 1) [23]. However, following the hindered due to limited genomic and transcriptomic initiation of meiosis, one or more cells from sporophytic resources available in apomict model species. Several tissue, termed aposporous initial (AI) cells, enlarge near the transcriptomic analyses in apomictic species have been cells undergoing the events of meiosis and megaspore se- published to date, including serial analysis of gene ex- lection in the majority of ovules (Fig. 1). One of the AI cells pression (SAGE), microarray approaches [6–8], and initiates a mitotic gametophyte program which results in more recently de novo sequencing [9, 10]. However, the the formation of an aposporous gametophyte and concur- generation of genomic resources within these species rently leads to degeneration ofthedevelopingsexualfemale has generally been neglected, and an integrated resource gametophyte (Fig. 1). Inhibiting meiosis within the MMC combining genomic and transcriptomic data in any one prevents AI cell initiation, suggesting that ovule cues asso- apomictic species has not yet been realized. Furthermore, ciated with activation and progression of meiosis may genome assembly and annotation has been difficult due to stimulate AI cell development [18]. Transcriptomic analysis the high complexity of polyploid genomes in apomicts, of microdissected AI cells suggests that enlarging AI cells and de novo transcriptomic assemblies are likely to under- do not express key meiosis genes [9]. The egg and central represent the diversity of transcripts actually present due cell in the aposporous embryo sac then undergo to the collapsing of homologous genes with high sequence fertilization-independent embryo and endosperm develop- similarity into chimeric contigs [11, 12]. ment [24]. Hieracium subgenus Pilosella species within the A collection of gamma irradiated deletion mutants within Asteraceae contain both obligate sexual and facultative the aposporous Hieracium species H. praealtum (R35) apomictic species where apomixis is not fully penetrant identified two independent and dominant loci, LOSS OF [13, 14]. Within apomictic species the trait is dominant, APOMEIOSIS (LOA)andLOSS OF PARTHENOGENESIS and apomixis occurs via aposporous embryo sac forma- (LOP), which are required for AI cell initiation and tion (described below). Apomictic Hieracium species are fertilization-independent seed development, respectively also amongst the few known apomicts capable of both [16, 18]. Deletion mutants lacking LOA fail to initiate AI fertilization-independent embryo and endosperm devel- cell development, and therefore sexual gametophytic devel- opment during seed formation [15–18]. Recombination opment progresses to completion. Sexual gametophytes at apomixis loci within the Pilosella subgenus of that inherit a functional LOP locus, in the absence of LOA, Hieracium does occur at low rates when crossed with can still initiate fertilization-independent seed formation sexual species, which in combination with a collection of resulting in plants with reduced ploidy relative to the apomixis deletion mutants, available bacterial artificial parent. Deletion mutants lacking LOP generate unreduced chromosome (BAC) libraries and expressed sequence gametophytes mitotically through AI cells. However, they markers, has aided in the generation of a genetic linkage are not capable of undergoing fertilization-independent map [16–20]. Coupled with a short lifecycle and an embryo or endosperm development and therefore require established transformation capability, these species have fertilization by a male gamete to initiate seed development, been developed into a valuable molecular and genetic resulting in plants with increased ploidy. Deletion of both model for the analysis of apomixis. Currently, the closest loci results in a complete reversion to sexual reproduction, phylogenetic relative to Hieracium with a comprehen-
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