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Evolution of genomic imprinting in the Capsella genus

Hatorangan, Marcelinus Rocky (2017). Evolution of genomic imprinting in the Capsella genus. Diss. (sammanfattning/summary) Uppsala : Sveriges lantbruksuniv., Acta Universitatis agriculturae Sueciae, 1652-6880 ; 2017:85
ISBN 978-91-7760-060-2
eISBN 978-91-7760-061-9
[Doctoral thesis]

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Abstract

According to the biological species concept, species are defined as groups of interbreeding populations reproductively isolated from other such groups. Hybrid seed lethality is a common reproductive barrier between plant species. Most frequently its developmental cause lies in the endosperm, but its molecular basis is not well understood. Hybrid seed defects differ depending on the cross direction, suggesting parent-of-origin-specific effects at work. Therefore, genomic imprinting, leading to the parent-of-origin-specific expression of genes in the endosperm, has been proposed to underlie hybrid seed lethality. Nevertheless, this hypothesis remains to be thoroughly tested.
Therefore, the main goal of this thesis was to explore the link between genomic imprinting and hybrid seed lethality in Capsella. The first part of this work aimed at characterizing the imprintome (the set of imprinted genes) of Capsella rubella and to compare it with the imprintome of the closely related species Arabidopsis thaliana (10-14 million years apart). This revealed that the imprintomes of both species are poorly conserved. Nevertheless, the pathways regulating genomic imprinting target transposable elements (TEs) in both species. Furthermore, studying the imprintomes of three Capsella species supported the notion of poor imprinting conservation between related species. This work also revealed that imprintome divergence between Capsella species is based on the divergence of TE insertions and consequent silencing mechanisms. Furthermore, this work discovered that hybrid seed lethality is widespread between each of the Capsella species. This phenomenon originates in the endosperm and exhibits a parent-of-origin pattern. Importantly, this work revealed that endosperm-based hybridization barriers in Capsella correlate with the number and expression of paternally-expressed imprinted genes (PEGs). In addition, the mating system strongly impacts on the number of PEGs, which suggests that transitions of mating systems fuel the establishment of postzygotic hybridization barriers.
Altogether, this thesis proposes a molecular and evolutionary explanation for the arising of endosperm-based hybridization barriers, in connection with genomic imprinting, TE dynamics and mating system. These data are expected to have a strong impact on plant breeding strategies and to promote further studies in this direction of research.

Authors/Creators:Hatorangan, Marcelinus Rocky
Title:Evolution of genomic imprinting in the Capsella genus
Alternative abstract:
LanguageAbstract
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Menurut konsep spesiasi biologi, spesies didefinisikan sebagai kelompok populasi antarbiak yang saling terisolasi secara reproduktif. Letalitas benih hibrida adalah sawar reproduksi umum antara spesies tanaman. Seringkali penyebabnya terpaut dengan endosperma tapi dasar molekularnya belum dipahami secara utuh. Kecacatan berbeda benih hibrida, menunjukkan efek khas induk asal memainkan peranan penting dalam membentuk sawar hibridisasi pascazigotik. Oleh sebab itu, rekaman genomik yang mengarahkan ekspresi gen khas induk asal di endosperma diusulkan sebagai penyebab letalitas benih hibrida. Walaupun demikian, hipotesis ini belum sepenuhnya teruji.
Oleh sebab itu, tujuan utama disertasi ini adalah untuk menjelajahi hubungan antara rekaman genomik dan letalitas benih hibrida pada Capsella. Bagian pertama karya ini ditujukan pada karakterisasi imprintom (himpunan gen-gen terekam) dari Capsella rubella dan membandingkannya dengan imprintom spesies berkekerabatan dekat, Arabidopsis thaliana (10-14 juta tahun terpisah). Hasilnya menunjukkan imprintom kedua spesies tidak dilestarikan dengan baik. Meskipun demikian, lintasan yang mengatur rekaman genomik menyasar transposon pada kedua spesies. Selanjutnya, imprintom dari tiga spesies Capsella, dibangun dan dibandingkan. Hasilnya semakin mendukung buruknya pelestarian rekaman antar spesies berkekerabatan dekat. Perbandingan wilayah pengapit gen-gen terekam menunjukkan bahwa perbedaan imprintom antar spesies Capsella terletak pada divergensi penyisipan transposon dan kelangsungan mekanisme penyenyapan. Selanjutnya, karya ini menemukan adanya persebaran letalitas benih hibrida antar spesies Capsella. Fenomena ini konsisten muncul di dalam endosperma dan menampilkan pola induk asal. Puncaknya, karya ini menunjukkan bahwa sawar hibridisasi berbasis endosperma pada Capsella berkorelasi dengan jumlah dan ekspresi gen terekam sebapak (GTB). Akhirnya, sistem penyilangan sangat berpengaruh terhadap jumlah GTB dan transisi sistem penyilangan memacu pembentukan sawar hibridisasi pascazigotik.
Secara keseluruhan, disertasi ini mengusulkan penjelasan molekular dan evolusioner bagi kemunculan sawar hibridisasi berbasis endosperma dalam hubungannya dengan rekaman genomik, dinamika transposon, dan sistem penyilangan. Data ini diharapkan memiliki dampak yang kuat terhadap strategi pembiakan tanaman dan upaya mempromosikan studi lebih lanjut searah dengan tujuan riset ini.

Series/Journal:Acta Universitatis agriculturae Sueciae (1652-6880)
Year of publishing :26 September 2017
Depositing date:26 September 2017
Volume:2017:85
Number of Pages:65
Papers/manuscripts:
NumberReferences
IHatorangan, M.R., Laenen, B., Steige, K., Slotte, T., Köhler, C*. (2016). Rapid evolution of genomic imprinting in two species of the Brassicaceae. Plant Cell tpc.00304.2016. doi:10.1105/tpc.16.00304
IIRebernig, C.A., Lafon-Placette, C., Hatorangan, M.R., Slotte, T., Köhler, C*. (2015). Non-reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLoS Genet 11, e1005295. doi:10.1371/journal.pgen.1005295
IIILafon-Placette, C.¤, Hatorangan, M.R.¤, Steige, K.A., Cornille, A., Lascoux M., Slotte, T., Köhler, C*. Paternally expressed imprinted genes correlate with hybridization success and likely underpin the Endosperm Balance Number in the Capsella genus. (submitted)
Place of Publication:Uppsala
Publisher:Department of Plant Biology, Swedish University of Agricultural Sciences
ISBN for printed version:978-91-7760-060-2
ISBN for electronic version:978-91-7760-061-9
ISSN:1652-6880
Language:English
Publication Type:Doctoral thesis
Full Text Status:Public
Agris subject categories.:F Plant production > F30 Plant genetics and breeding
Subjects:(A) Swedish standard research categories 2011 > 1 Natural sciences > 106 Biological Sciences (Medical to be 3 and Agricultural to be 4) > Evolutionary Biology
(A) Swedish standard research categories 2011 > 4 Agricultural Sciences > 401 Agricultural, Forestry and Fisheries > Agricultural Science
Agrovoc terms:capsella, arabidopsis, hybridization, gene expression, transposons
Keywords:Capsella, Genomic imprinting, Hybridization barrier, Imprinted genes, Maternally expressed genes, Paternally expressed genes
URN:NBN:urn:nbn:se:slu:epsilon-e-4377
Permanent URL:
http://urn.kb.se/resolve?urn=urn:nbn:se:slu:epsilon-e-4377
ID Code:14578
Faculty:NJ - Fakulteten för naturresurser och jordbruksvetenskap
Department:(NL, NJ) > Department of Plant Biology (from 140101)
Deposited By: Mr Marcelinus Rocky Hatorangan
Deposited On:27 Sep 2017 06:44
Metadata Last Modified:27 Sep 2017 08:48

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