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Identification, molecular analysis and phylogeographic distribution of the chimeric UPGRADE-2 gene, a candidate for the initiation of unreduced pollen formation in apomictic Boechera (Brassicaceae)

Mau, Martin

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Abstract

In sexual plants meiosis gives rise to recombined and reduced gametes. In diplosporous accessions of the North American genus Boechera meiotic processes are circumvented (i.e. apomeiosis) which lead to a supressed recombination and to production of clonal unreduced male and female gametes. Unreduced male gametes in diplosporous Boechera are required to produce balanced endosperm. The objective of this study was to identify and characterize candidate genetic factors for unreduced pollen formation, and to analyze their genus-wide dynamics in order to contrast the hypotheses whether apomeiosis expression was induced through interspecific hybridization or if it could be an older characteristic of the genus (i.e. pre-Pleistocene). Apomictic Boechera demonstrated high variability for reduced and unreduced meiocyte production. Early flower developmental staging and flow-cytometric analyses together led to the selection of a single pollen mother cell stage at the onset of meiosis for microarray-based comparative gene expression analyses between diploid sexual and diploid apomictic genotypes, and led to the identification of a single highly-upregulated factor (BspUPG-2) which is highly conserved among apomictic Boechera but has no homologue in sexual Boechera or in other taxa. BspUPG-2 exhibits four intron-exon structure variants which suggest alternative splicing, and lack of a prominent open reading frame and no overall sequence homology to known genes suggests that BspUPG-2 belongs to the novel class of long regulatory non-coding mRNA-like RNAs. BspUPG-2 has apparently arisen through a three-step process initiated by ancestral gene duplication of the original non-genic BspUPG-1 locus, followed by sequential insertions of segmentally duplicated gene fragments which led to its chimeric structure and neofunctionalization in apomictic Boechera. Its genesis reflects the hybridization history which characterizes the genus Boechera. Computational analysis demonstrated that portions of BspUPG-2 form secondary structures which were classified as potential primary microRNAs (pri-miRNAs) according to their minimal folding free energy index (MFEI≥0.70) and their A+U content (≥56.70%). One such structure is highly similar to the third exon of a GTP-binding elongation factor Tu/1-A family homolog from Arabidopsis (AT4G02930, E-value=7.00E-24) which could be a potential regulatory target. Two other sequence fragments at the 5`-end of BspUPG-2 are also homologous to known protein-coding genes (AT5G19960 and AT1G18260), hence supporting the hypothesized regulatory function of BspUPG-2. The apomixis-specificity of BspUPG-2 enabled a genus-wide analysis which demonstrated its ubiquity in all Boechera lineages, including the ancient AB haplotype and two single individuals each of one closely-related genus. These results attest to BspUPG-2’s hypothesized importance for unreduced pollen formation and hence for balanced endosperm formation, and point to a single origin of this factor which coincides with the root of the genus Boechera dating to the middle of the Pleistocene.

Document type: Dissertation
Supervisor: Koch, Prof. Dr. Marcus
Date of thesis defense: 4 July 2013
Date Deposited: 10 Jul 2013 07:51
Date: 31 December 2013
Faculties / Institutes: The Faculty of Bio Sciences > Dean's Office of the Faculty of Bio Sciences
Service facilities > Centre for Organismal Studies Heidelberg (COS)
DDC-classification: 500 Natural sciences and mathematics
570 Life sciences
580 Botanical sciences
Controlled Keywords: Pollenkörner, Blütenpollen
Uncontrolled Keywords: Boechera, apomixis, unreduced pollen, UPGRADE, microgametogenesis
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