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Seed Evolution: Parental Conflicts in a Multi-Generational Household

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Seed Evolution: Parental Conflicts in a Multi-Generational Household Zurich Open Repository and Archive University of Zurich Main Library Strickhofstrasse 39 CH-8057 Zurich www.zora.uzh.ch Year: 2014 Seed evolution: parental conflicts in a multi-generational household Pires, Nuno D Abstract: Seeds are multi-generational structures containing a small embryonic plant enclosed in layers of diverse parental origins. The evolution of seeds was a pinnacle in an evolutionary trend towards a progressive retention of embryos and gametes within parental tissue. This strategy, which dates back to the first land plants, allowed an increased protection and nourishing of the developing embryo. Flowering plants took parental control one step further with the evolution of a biparental endosperm that derives from a second parallel fertilization event. The endosperm directly nourishes the developing embryo and allows not only the maternal genes, but also paternal genes, to play an active role during seed development. The appearance of an endosperm set the conditions for the manifestation of conflicts of interest between maternal and paternal genomes over the allocation of resources to the developing embryos. As a consequence, a dynamic balance was established between maternal and paternal gene dosage in the endosperm, and maintaining a correct balance became essential to ensure a correct seed development. This balance was achieved in part by changes in the genetic constitution of the endosperm and through epigenetic mechanisms that allow a differential expression of alleles depending on their parental origin. This review discusses the evolutionary steps that resulted in the appearance of seeds and endosperm, and the epigenetic and genetic mechanisms that allow a harmonious coinhabitance of multiple generations within a single seed. DOI: https://doi.org/10.1515/bmc-2013-0034 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-106919 Journal Article Published Version Originally published at: Pires, Nuno D (2014). Seed evolution: parental conflicts in a multi-generational household. BioMolecular Concepts, 5(1):71-86. DOI: https://doi.org/10.1515/bmc-2013-0034 DOI 10.1515/bmc-2013-0034 BioMol Concepts 2014; 5(1): 71–86 Review Nuno D. Pires* Seed evolution: parental conflicts in a multi-generational household Abstract: Seeds are multi-generational structures contain- Introduction ing a small embryonic plant enclosed in layers of diverse parental origins. The evolution of seeds was a pinnacle in Seeds were one of the key innovations that allowed gym- an evolutionary trend towards a progressive retention of nosperms and angiosperms to dominate terrestrial eco- embryos and gametes within parental tissue. This strat- systems during the last 300 million years. The protection egy, which dates back to the first land plants, allowed an and nourishment offered to the plant embryos is a costly increased protection and nourishing of the developing strategy, but one that greatly increases their chances of embryo. Flowering plants took parental control one step survival and dispersion on land. The evolution of seeds further with the evolution of a biparental endosperm that followed a trend that started with the first land plants and derives from a second parallel fertilization event. The consisted of the retention of a fertilized zygote and result- endosperm directly nourishes the developing embryo ing diploid generation within maternal tissue. Subsequent and allows not only the maternal genes, but also pater- plant lineages elaborated on this strategy to the point of nal genes, to play an active role during seed development. angiosperm seeds forming a multi-generational structure The appearance of an endosperm set the conditions for comprising an embryo enveloped in sibling biparental the manifestation of conflicts of interest between mater- endosperm and two ancestral generations of maternal nal and paternal genomes over the allocation of resources tissue. The evolution of a biparental endosperm in angio- to the developing embryos. As a consequence, a dynamic sperms was a particularly important innovation because balance was established between maternal and paternal it allowed fathers to be directly involved in embryogenesis gene dosage in the endosperm, and maintaining a correct and compete with other parents for resource allocation for balance became essential to ensure a correct seed devel- their progeny. Importantly, the endosperm also allowed a opment. This balance was achieved in part by changes in more sophisticated regulation of the epigenetic develop- the genetic constitution of the endosperm and through ment of embryos. The balancing of parental information epigenetic mechanisms that allow a differential expres- in the endosperm became an important process in seed sion of alleles depending on their parental origin. This development, and underlies an important post-zygotic review discusses the evolutionary steps that resulted in hybridization barrier in plants. In this review the genetic the appearance of seeds and endosperm, and the epige- and epigenetic mechanisms that integrate parental infor- netic and genetic mechanisms that allow a harmonious mation during seed development will be discussed within coinhabitance of multiple generations within a single the larger context of plant evolution. seed. Keywords: endosperm; imprinting; MADS; polycomb; triploid block. Land plant reproduction: a strategy of overprotective parenting *Corresponding author: Nuno D. Pires, Institute of Plant Biology and Zürich–Basel Plant Science Center, University of Zürich, One central and defining characteristic of land plants is CH-8008 Zürich, Switzerland, e-mail: [email protected] the alternation of multicellular generations: a haploid entity (the gametophyte) differentiates gametes, gametes fuse to form a zygote, and the zygote gives rise to a diploid entity (the sporophyte), which forms haploid spores by meiosis. In contrast, in the aquatic ancestors of land plants (the charophyte algae) the fertilized zygote is the only Bereitgestellt von | UZH Hauptbibliothek / Zentralbibliothek Zürich Angemeldet Heruntergeladen am | 25.08.18 16:00 72 N.D. Pires: Seed evolution and parental conflicts diploid cell and there is no multicellular spore-producing period (4), perhaps as soon as 50 million years after the generation. Even in derived and complex charophytes, transition to land. such as Coleochaete (where egg cells are enveloped and While the sporophytes grew, the gametophytes protected by a layer of gametophytic cells) the fertilized (which still nourished and protected the embryos) became zygote directly undergoes meiosis to form free-dispersing smaller. Eventually, female gametophytes were themselves haploid spores (1). retained within parental sporophytic tissue (Figure 1). The One of the crucial innovations of the first land plants oldest evidence for these changes is 385 million year-old was an intercalation of mitotic divisions in the zygote fossils of Runcaria (5). Later, the evolution of specialized before meiosis, causing the development of a multicel- integuments resulted in the appearance of the first true lular embryo (a young sporophyte) within gametophytic ovules and seeds around 365 million years old (6). tissue (2, 3). The sheltered multicellular sporophyte These first seeds (and the seeds of modern gymno- increased the number of spores that could be produced sperms) consisted of three distinct genetic generations: from a single water-dependent fertilization event, offering 1) a sporophytic embryo, nourished by 2) a female game- a huge competitive advantage on land. The rapid increase tophyte enveloped in 3) a maternal sporophytic coat in the size and complexity of sporophytes that followed (Figure 1). With the retention of female gametophytes led to an explosion of land plant forms in the Devonian within sporophytic tissues, vascular plants achieved a Embryo (2n) Sporophyte (2n) Endosperm (3n) Gametophyte (n) Seed First Angiosperms Austrobaileyales Most angiosperms and Nymphaeales First vascular plants Gymnosperms Ferns First land plants Doubling of maternal dosage Bryophytes in the endosperm Double fertilisation Endosperm Retention of gametophyte and embryo within maternal sporophyte tissue Increase in sporophyte complexity Retention of a multicellular diploid embryo within maternal gametophyte tissue Figure 1 Progressive retention of the diploid embryo within parental tissues during land plant evolution. Photograph credits: Sandy__RR, ‘Moss 1’, licensed under Creative Commons, downloaded from http://www.flickr.com/photos/35142635@ N05/5475014490/ on 27 October 2013; GaggieITMI, ‘Fern’, licensed under Creative Commons, downloaded from http://www.flickr.com/photos/ gaggieitmi/8154028076/ on 27 October 2013; Scott Robinson, ‘Pine Cones’, licensed under Creative Commons, downloaded from http://www. flickr.com/photos/clearlyambiguous/17204706/on 2 October 2013; Mr. Tonreg, ‘Nuphar lutea’, licensed under Creative Commons, downloaded from http://www.flickr.com/photos/63169246@N00/8444876794/ on 27 October 2013; Tom Hilton, ‘Polygonum paronychia’, licensed under Creative Commons, downloaded from http://commons.wikimedia.org/wiki/File:Polygonum_paronychia.jpg on 27 October 2013. Bereitgestellt von | UZH Hauptbibliothek / Zentralbibliothek Zürich Angemeldet Heruntergeladen am | 25.08.18 16:00 N.D. Pires: Seed evolution and parental conflicts 73 greater independence from water for fertilization, while hegemony over the control of embryogenesis. The intru- the production
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