Universität zu Köln

Castellani, Marco ORCID: 0000-0002-5809-9387 (2023). Holocentric plants of the genus Rhynchospora as a new model to study meiotic adaptations to chromosomal structural rearrangements. PhD thesis, Universität zu Köln.

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Abstract

Climate change, world hunger and overpopulation are some of the biggest challenges the world is currently facing. Moreover, they are part of a multidimensional single scenario: as climate change continues to modify our planet, we might see a decrease of arable land and increase in extreme weather patterns, posing a threat to food security. This has a direct impact on regions with high population growth, where food security is already scarce. Considering additionally the unsustainability of intensive global food production and its contribution to greenhouse emissions and biodiversity loss, it´s clear that all these factors are interconnected (Cardinale et al., 2012; Prosekov & Ivanova, 2018; Wiebe et al., 2019). Plants are the main source of staple food in the world and are also the main actors in carbon fixation, they are therefore key protagonists in controlling climate change. Plants are also an essential habitat-defining element balancing our ecosystem. Thus, how we grow plants and crops will, aside from the obvious implications for food security, also have a profound impact on the climate and biodiversity. The natural variability of species is considered an immense pool of genes and traits, and their understanding is key to generate new useful knowledge. For instance, natural populations can be more tolerant to abiotic and biotic stresses, or carry traits that combined together in hybrids, might achieve a higher seed number, or a faster growth. Classical breeding has exploited unrelated varieties to achieve traits of interest like dwarfism and higher grain production. However, only a limited number of crop species have been the focus of recent scientific and technological approaches, and they do not represent the extremely vast natural diversity of species that could generate useful knowledge for future applications (Castle et al., 2006; Pingali, 2012). The key to this natural variability is a process called meiotic recombination, the exchange of genomic material between homologous parental chromosomes. Meiotic recombination takes place during meiosis, a specialized cell division in which sexually reproducing organisms reduce the genomic complement of their gametes by half in preparation for fertilization. Meiotic recombination takes place at the beginning of meiosis, in a stage called prophase I. To exchange DNA sequences, the strands of two homologous chromosomes must be fragmented. This specific process of physiologically induced DNA fragmentation is conserved in the vast majority of eukaryotes (Keeney et al., 1997). After the formation of double-strand breaks, the 3’ ends that are left are targeted by recombinases that help the strands search and invade templates for repair. After invasion, the 3’ end is extended by DNA synthesis, exposing sequences on the opposite strand that can anneal to the other 3’ end of the original double strand break. DNA synthesis at both ends generates a new structure called a double Holliday Junction (dHJ), forming a physical link between homologous chromosomes, named chiasma (Wyatt & West, 2014). The resolutions of these structures are called crossovers (COs), which is the molecular event representing the outcome of meiotic recombination. Other outcomes are possible, like noncrossovers (NCOs). In this case, the invading strand is ejected and anneals to the single-strand 3´end of the original double-strand break (Allers & Lichten, 2001). Crossovers can be divided into two main groups, called class I and class II. COs of the first group are considered to be sensitive to interference, which means that there are mechanisms that prevent two class I COs from happening in proximity of each other. Class II is insensitive to interference. Class I COs are the result of a pathway called ZMM, which involves a group of specialised proteins that are highly conserved among eukaryotes (Lambing et al., 2017; Mercier et al., 2015). Class I COs are the most common, studied and important type of COs. Centromeres are structures, located on regions of the chromosomes, that allow proper chromosome segregation during mitosis and meiosis. Centromeres have a profound effect on plant breeding and crop improvement, as it is known that meiotic recombination is suppressed at centromeres in most eukaryotes. This represents a great limitation for crop improvement, as many possibly useful traits might be in regions not subject to recombination and thus might not be available for breeding purposes. Additionally, the mechanisms behind how recombination is regulated and prevented from happening at centromeres are still unclear. In most model organisms centromeres are single entities localized on specific regions on the chromosomes. This configuration is called monocentric. However, another type of configuration can be found in nature, but is less studied. In fact, some organisms harbour multiple centromeric determinants distributed over their whole chromosomal length. This configuration is called holocentric. The Cyperaceae comprise a vast, diverse family of plants, with a cosmopolitan distribution in all habitats (Spalink et al., 2016). Despite the presence of this family worldwide, knowledge about it is limited. Few genomes are available and molecular insights are scarce. This family is also known to be mainly formed by holocentric species (Melters et al., 2012). Understanding if and how meiotic recombination is achieved in holocentric plants will generate new knowledge that in the future might unlock new traits in elite crops, previously unavailable to breeding, that could help humanity face global climatic, economic and social challenges. Recent studies have reported new knowledge about important meiotic, chromosome and genome adaptions found in species of the Cyperaceae family and in particular the genus Rhynchospora (Marques et al., 2015, 2016a). With the recent publication of the first reference genomes for several Rhynchospora species, we could already perform a comprehensive analysis of their unique genome features and trace the evolutionary history of their karyotypes and how these have been determined by chromosome fusions (Hofstatter et al., 2021, 2022). This new resource paves the way for future research utilising Rhynchospora as a model genus to study adaptations to holocentricity in plants. With this work, my intention is to shed light on the underexplored topic of holocentricity in plants. Using cutting edge techniques, I examine the conservation of meiotic recombination together with other species-specific adaptations like achiasmy and polyploidy in holocentrics. My results reveal new insights into how plant meiotic recombination is regulated when small centromere units are found distributed chromosome-wide, challenging the classic dogma of suppression of recombination at centromeres.

Item Type:	Thesis (PhD thesis)
Translated title:	Title Language Holocentric plants of the genus Rhynchospora as a new model to study meiotic adaptations to chromosomal structural rearrangements English
Creators:	Creators Email ORCID ORCID Put Code Castellani, Marco mcastellani@mpipz.mpg.de orcid.org/0000-0002-5809-9387 UNSPECIFIED
URN:	urn:nbn:de:hbz:38-711453
Date:	2 October 2023
Language:	English
Faculty:	Faculty of Mathematics and Natural Sciences
Divisions:	Außeruniversitäre Forschungseinrichtungen > MPI for Plant Breeding Research
Subjects:	Natural sciences and mathematics
Uncontrolled Keywords:	Keywords Language Holocentric chromosomes UNSPECIFIED Meiotic recombination UNSPECIFIED Plant meiosis UNSPECIFIED
Date of oral exam:	24 July 2023
Referee:	Name Academic Title Mercier, Raphael Prof. Kopriva, Stanislav Prof.
Refereed:	Yes
URI:	http://kups.ub.uni-koeln.de/id/eprint/71145