A reference genetic linkage map of apomictic Hieracium species based on expressed markers derived from developing ovule transcripts.

BACKGROUND AND AIMS Apomixis in plants generates clonal progeny with a maternal genotype through asexual seed formation. Hieracium subgenus Pilosella (Asteraceae) contains polyploid, highly heterozygous apomictic and sexual species. Within apomictic Hieracium, dominant genetic loci independently regulate the qualitative developmental components of apomixis. In H. praealtum, LOSS OF APOMEIOSIS (LOA) enables formation of embryo sacs without meiosis and LOSS OF PARTHENOGENESIS (LOP) enables fertilization-independent seed formation. A locus required for fertilization-independent endosperm formation (AutE) has been identified in H. piloselloides. Additional quantitative loci appear to influence the penetrance of the qualitative loci, although the controlling genes remain unknown. This study aimed to develop the first genetic linkage maps for sexual and apomictic Hieracium species using simple sequence repeat (SSR) markers derived from expressed transcripts within the developing ovaries. METHODS RNA from microdissected Hieracium ovule cell types and ovaries was sequenced and SSRs were identified. Two different F1 mapping populations were created to overcome difficulties associated with genome complexity and asexual reproduction. SSR markers were analysed within each mapping population to generate draft linkage maps for apomictic and sexual Hieracium species. KEY RESULTS A collection of 14 684 Hieracium expressed SSR markers were developed and linkage maps were constructed for Hieracium species using a subset of the SSR markers. Both the LOA and LOP loci were successfully assigned to linkage groups; however, AutE could not be mapped using the current populations. Comparisons with lettuce (Lactuca sativa) revealed partial macrosynteny between the two Asteraceae species. CONCLUSIONS A collection of SSR markers and draft linkage maps were developed for two apomictic and one sexual Hieracium species. These maps will support cloning of controlling genes at LOA and LOP loci in Hieracium and should also assist with identification of quantitative loci that affect the expressivity of apomixis. Future work will focus on mapping AutE using alternative populations.

[1]  S. Johnson,et al.  Evolution of apomixis loci in Pilosella and Hieracium (Asteraceae) inferred from the conservation of apomixis-linked markers in natural and experimental populations , 2014, Heredity.

[2]  G. Suzuki,et al.  The LOSS OF APOMEIOSIS (LOA) locus in Hieracium praealtum can function independently of the associated large-scale repetitive chromosomal structure. , 2014, The New phytologist.

[3]  Céline Muys,et al.  Integration of AFLPs, SSRs and SNPs markers into a new genetic map of industrial chicory (Cichorium intybus L. var. sativum) , 2014 .

[4]  Matthew R. Tucker,et al.  Enlarging Cells Initiating Apomixis in Hieracium praealtum Transition to an Embryo Sac Program prior to Entering Mitosis1[W][OPEN] , 2013, Plant Physiology.

[5]  O. Savolainen,et al.  Investigating Incipient Speciation in Arabidopsis lyrata from Patterns of Transmission Ratio Distortion , 2013, Genetics.

[6]  H. V. van Leeuwen,et al.  An Ultra-High-Density, Transcript-Based, Genetic Map of Lettuce , 2013, G3: Genes, Genomes, Genetics.

[7]  A. Koltunow,et al.  Genetic separation of autonomous endosperm formation (AutE) from the two other components of apomixis in Hieracium , 2013, Plant Reproduction.

[8]  Michael S. Barker,et al.  Development of an Ultra-Dense Genetic Map of the Sunflower Genome Based on Single-Feature Polymorphisms , 2012, PloS one.

[9]  G. Barcaccia,et al.  Cloning plants by seeds: Inheritance models and candidate genes to increase fundamental knowledge for engineering apomixis in sexual crops. , 2012, Journal of biotechnology.

[10]  Daniel W. A. Buchan,et al.  The tomato genome sequence provides insights into fleshy fruit evolution , 2012, Nature.

[11]  N. Alexandrov,et al.  High Resolution Genetic Mapping by Genome Sequencing Reveals Genome Duplication and Tetraploid Genetic Structure of the Diploid Miscanthus sinensis , 2012, PloS one.

[12]  Matthew R. Tucker,et al.  Sporophytic ovule tissues modulate the initiation and progression of apomixis in Hieracium , 2012, Journal of experimental botany.

[13]  J. Poland,et al.  Development of High-Density Genetic Maps for Barley and Wheat Using a Novel Two-Enzyme Genotyping-by-Sequencing Approach , 2012, PloS one.

[14]  A. Houben,et al.  Chromosomes Carrying Meiotic Avoidance Loci in Three Apomictic Eudicot Hieracium Subgenus Pilosella Species Share Structural Features with Two Monocot Apomicts1[W][OA] , 2011, Plant Physiology.

[15]  G. Suzuki,et al.  Sexual reproduction is the default mode in apomictic Hieracium subgenus Pilosella, in which two dominant loci function to enable apomixis. , 2011, The Plant journal : for cell and molecular biology.

[16]  A. Koltunow,et al.  Apomixis in hawkweed: Mendel's experimental nemesis. , 2011, Journal of experimental botany.

[17]  F. Krahulec,et al.  Expressivity of apomixis in 2n + n hybrids from an apomictic and a sexual parent: insights into variation detected in Pilosella (Asteraceae: Lactuceae) , 2011, Sexual Plant Reproduction.

[18]  An interspecific linkage map of SSR and intronic polymorphism markers in tomato , 2010, Theoretical and Applied Genetics.

[19]  Inanç Birol,et al.  De novo transcriptome assembly with ABySS , 2009, Bioinform..

[20]  F. Krahulec,et al.  Enriching Ploidy Level Diversity: the Role of Apomictic and Sexual Biotypes of Hieracium subgen. Pilosella (Asteraceae) that Coexist in Polyploid Populations , 2009, Folia Geobotanica.

[21]  Shizhong Xu Quantitative Trait Locus Mapping Can Benefit From Segregation Distortion , 2008, Genetics.

[22]  Marta Matvienko,et al.  Multiple paleopolyploidizations during the evolution of the Compositae reveal parallel patterns of duplicate gene retention after millions of years. , 2008, Molecular biology and evolution.

[23]  P. Mráz,et al.  Loss of genetic diversity in isolated populations of an alpine endemic Pilosellaalpicola subsp. ullepitschii: effect of long-term vicariance or long-distance dispersal? , 2008, Plant Systematics and Evolution.

[24]  M. Komjanc,et al.  Identification of microsatellite markers in Hieracium pilosella L. , 2008, Conservation Genetics.

[25]  P. Ozias‐Akins,et al.  Mendelian genetics of apomixis in plants. , 2007, Annual review of genetics.

[26]  G. Evatt,et al.  EST-SSRs as a resource for population genetic analyses , 2007, Heredity.

[27]  S. Pessino,et al.  A genetic map of tetraploid Paspalum notatum Flügge (bahiagrass) based on single-dose molecular markers , 2007, Molecular Breeding.

[28]  B. Jordan,et al.  Deletion mapping of genetic regions associated with apomixis in Hieracium , 2006, Proceedings of the National Academy of Sciences.

[29]  Hidetoshi Shimodaira,et al.  Pvclust: an R package for assessing the uncertainty in hierarchical clustering , 2006, Bioinform..

[30]  I. Donnison,et al.  Molecular cytogenetics and DNA sequence analysis of an apomixis-linked BAC in Paspalum simplex reveal a non pericentromere location and partial microcolinearity with rice , 2006, Theoretical and Applied Genetics.

[31]  John Z. Yu,et al.  Genetic mapping of new cotton fiber loci using EST-derived microsatellites in an interspecific recombinant inbred line cotton population , 2005, Molecular Genetics and Genomics.

[32]  R. Bicknell,et al.  Understanding Apomixis: Recent Advances and Remaining Conundrums , 2004, The Plant Cell Online.

[33]  R. Bicknell,et al.  Quantification of progeny classes in two facultatively apomictic accessions of Hieracium. , 2003, Hereditas.

[34]  Arnaud Estoup,et al.  Homoplasy and mutation model at microsatellite loci and their consequences for population genetics analysis , 2002, Molecular ecology.

[35]  S. Arcioni,et al.  The chromosome segment related to apomixis in Paspalum simplex is homoeologous to the telomeric region of the long arm of rice chromosome 12 , 2001, Molecular Breeding.

[36]  S. Pessino,et al.  A Genetic Linkage Map of Diploid Paspalum notatum , 2001 .

[37]  The Arabidopsis Genome Initiative Analysis of the genome sequence of the flowering plant Arabidopsis thaliana , 2000, Nature.

[38]  S. Johnson,et al.  Apomixis is not developmentally conserved in related, genetically characterized Hieracium plants of varying ploidy , 2000, Sexual Plant Reproduction.

[39]  J. Chrtek,et al.  Autogamy inHieracium Subgen.Pilosella , 1999, Folia Geobotanica.

[40]  R. Bicknell,et al.  Sexual and apomictic development in Hieracium , 1998, Sexual Plant Reproduction.

[41]  R. Bicknell Isolation of a diploid, apomictic plant of Hieracium aurantiacum , 1997, Sexual Plant Reproduction.

[42]  J. Carman Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony , 1997 .

[43]  J. Stougaard Substrate‐dependent negative selection in plants using a bacterial cytosine deaminase gene , 1993 .

[44]  K. Anna The structure of the agamic complex of Hieracium subgen. Pilosella in the Šumava Mts and its comparison with other regions in Central Europe , 2008 .

[45]  J. Ooijen,et al.  JoinMap® 4, Software for the calculation of genetic linkage maps in experimental populations , 2006 .

[46]  R. Voorrips MapChart: software for the graphical presentation of linkage maps and QTLs. , 2002, The Journal of heredity.