Hopeful monsters: Evolutionary relevance and ecology of polyploid plants in the Arctic

publishedVersio

Evolusjon av blomstringstilpassingar i tempererte gras

Grasses (Poaceae) represent an unparalleled evolutionary success story and are particularly well adapted to the environmental challenges posed by temperate habitats. Crucial to their evolutionary success in temperate ecosystems is their ability to align phenological events coordinating growth and reproduction with predictable, seasonal variations in temperature and daylength. However, only a few subfamilies of grasses have spread to temperate niches, a biogeographic bias that renders grasses a good system for comparative analyses of physiological and phenological traits that facilitate adaptive radiations in temperate habitats. The work presented in this thesis identified and characterised molecular mechanisms that determine the rules for seasonal flowering, driving one of the most successful adaptive radiations among flowering plants. Many temperate grasses synchronise flowering with favourable conditions within the relatively short growing season through a two-step process. First, prolonged cold exposure enhances their ability to flower, a process known as vernalisation. Transition from vegetative to reproductive growth is then further accelerated by long photoperiod in spring. This warrants the subsequent emergence inflorescences under suitable environmental conditions, timed to utilise a limited growing season. This development is controlled by interlocked genetic networks that integrate mechanisms for sensing cold, photoperiod, and timing. In this doctoral project, I examined the evolutionary history of adaptations to temperate climates in various subfamilies of grasses and potential implications for shifts between biological niches from their original tropical to increasingly temperate habitats. The research was focused on mechanisms that control flowering in model and temperate cereal species to investigate whether these are conserved within and between Pooideae and other temperate subfamilies. I employed a wide range of methodological approaches, such as growth experiments, phylogenetic reconstruction, comparative transcriptomics, and functional data analysis for these purposes. The results indicate that a portion of the genetic basis for adaptation to long photoperiods evolved early within the Pooideae subfamily, and that vernalisation responses have arisen multiple times in different subfamilies through a parallel evolutionary process. Nevertheless, it was demonstrated that many of the investigated genetic processes had undergone extensive lineage-specific evolution, and that minor changes in how these genes are regulated in response to external cues are sufficient to promote transitions between habitats with different demands for physiological and phenological adaptations such as floral onset, especially within the early-diverging Pooideae lineage Stipeae.Gras (Poaceae) er ein evolusjonær suksesshistorie utan like og særleg godt tillempa dei miljø- messige utfordringane tempererte habitat byr på. Utslagsgjevande for grasa sin evolusjonære framgang i tempererte økosystem er deira evne til å høve fenologiske hendingar som samordnar vekst og formeiring med føreseielege, årstidsbundne variasjonar i temperatur og daglengd. Likevel har berre nokre få underfamiliar av gras spreidd seg til tempererte nisjar, ei biogeografisk skeivfordeling som gjer grasfamilien til eit godt døme for samanliknande analyse av fysiologiske og fenologiske trekk som fremjar adaptive radiasjonar i tempererte habitat. Arbeidet lagt fram i denne avhandlinga identifiserte og karakteriserte molekylære mekanismar som fastset reglane for årstidsbunden blomstring, noko som driv ei av dei mest suksessrike adaptive radiasjonane blant blomsterplanter. Mange tempererte planter samkøyrer blomstring med gunstige tilhøve i den høvesvis korte vekstsesongen gjennom ein to-stegsprosess. Fyrst aukar langvarig kulde evna til å blomstre i ein prosess som kallast vernalisering. Overgangen frå vegetativ til reproduktiv vekst vert ytterlegare framskunda av lang fotoperiode på våren. Dette tryggjar påfølgjande framvekst av blomsterstand under høvelege forhold, tidsnok til å nytte seg av ein tidsavgrensa vekstsesong. Denne utviklinga styrast av samanvovne genetiske nettverk som knyter saman mekanismar for sansing av kulde, fotoperiode og tidtaking. I dette doktorgradsprosjektet undersøkte eg den evolusjonære historia til tilpassingar til tempererte klima i ulike underfamiliar av gras og mogelege fylgjer for skift mellom biologiske nisjar frå deira opphavleg tropiske til stadig meir tempererte habitat. Forskinga vart retta mot mekanismar som styrer blomstring i modell- og tempererte kornartar for å undersøkje om desse er konservert innanfor og mellom Pooideae og andre tempererte underfamiliar. Eg nytta eit breitt register av metodologiske tilnærmingar slik som vekstforsøk, fylogenetisk rekonstruksjon, samanliknande transkriptomikk og funksjonell data-analyse til desse føremål. Resultata peiker mot at ein del av det genetiske grunnlaget for tilpassing til lang fotoperiode utvikla seg tidleg i Pooideae-underfamilien og at vernaliseringsrespons har oppstått fleire gongar i ulike underfamiliar av gras gjennom ein parallell evolusjonær prosess. Likevel vart det vist at mange av dei undersøkte genetiske prosessane hadde gjennomgått omfattande linjespesifikk evolusjon og at små endringar i korleis desse gen regulerast av og i høve til ytre påverknadar er tilstrekkelege til å fremje overgang mellom habitat med ulike krav til fysiologiske og fenologiske tilpassingar slik som blomstringstid, særleg i den tidlegskilde Pooideae-linja Stipeae

Independent recruitment of FRUITFULL-like transcription factors in the convergent origins of vernalization-responsive grass flowering

Flowering in response to low temperatures (vernalization) has evolved multiple times independently across angiosperms as an adaptation to match reproductive development with the short growing season of temperate habitats. Despite the context of a generally conserved flowering time network, evidence suggests that the genes underlying vernalization responsiveness are distinct across major plant clades. Whether different or similar mechanisms underlie vernalization-induced flowering at narrower (e.g., family-level) phylogenetic scales is not well understood. To test the hypothesis that vernalization responsiveness has evolved convergently in temperate species of the grass family (Poaceae), we carried out flowering time experiments with and without vernalization in several representative species from different subfamilies. We then determined the likelihood that vernalization responsiveness evolved through parallel mechanisms by quantifying the response of Pooideae vernalization pathway FRUITFULL (FUL)-like genes to extended periods of cold. Our results demonstrate that vernalization- induced flowering has evolved multiple times independently in at least five grass subfamilies, and that different combinations of FUL-like genes have been recruited to this pathway on several occasions.Independent recruitment of FRUITFULL-like transcription factors in the convergent origins of vernalization-responsive grass floweringpublishedVersio

Major niche transitions in Pooideae correlate with variation in photoperiodic flowering and evolution of CCT domain genes

The external cues that trigger timely flowering vary greatly across tropical and temperate plant taxa, the latter rely- ing on predictable seasonal fluctuations in temperature and photoperiod. In the grass family (Poaceae) for example, species of the subfamily Pooideae have become specialists of the northern temperate hemisphere, generating the hypothesis that their progenitor evolved a flowering response to long days from a short-day or day-neutral ancestor. Sampling across the Pooideae, we found support for this hypothesis, and identified several secondary shifts to day- neutral flowering and one to short-day flowering in a tropical highland clade. To explain the proximate mechanisms for the secondary transition back to short-day-regulated flowering, we investigated the expression of CCT domain genes, some of which are known to repress flowering in cereal grasses under specific photoperiods. We found a shift in CONSTANS 1 and CONSTANS 9 expression that coincides with the derived short-day photoperiodism of our exem- plar species Nassella pubiflora. This sets up the testable hypothesis that trans- or cis-regulatory elements of these CCT domain genes were the targets of selection for major niche shifts in Pooideae grasses.Major niche transitions in Pooideae correlate with variation in photoperiodic flowering and evolution of CCT domain genespublishedVersio

Molecular genetic characterisation of vernalisation response in PACMAD grasses

Many plants rely on a mechanism called vernalisation response to match reproductive output with favourable environmental conditions. This trait is an important adaptation to seasonal climates, like for example at high latitudes. In grasses (Poaceae), evolution of seasonally-cued flowering was one of the traits enabling certain lineages to move out of their tropical origins and diversify in temperate zones. Due to its ecological and agricultural importance, the genetic basis of vernalisa- tion response is particularly well-studied in Pooideae grasses that predominates temperate habit- ats. However, little is known about vernalisation systems in other grass lineages that are adapted to cool and seasonal climates. In this study, I ask whether vernalisation response is found in a grass lineage called the pacmad clade. To disentangle the molecular machinery governing this trait, I quantified the expression of two paralogous FRUITFULL-like (FUL-like) vernalisation genes. My results demonstrate that vernalisation response is widespread in pacmad grasses, and found in at least four subfamilies with temperate representatives. Moreover, I found evidence for the co- option of a novel vernalisation gene (FUL2) into the vernalisation gene network Arundinoideae species Molinia caerulea.Yara Norge AS ; NMBUs forskningsfond ; Nordisk jordbruksforskeres forening (NJF), avdeling NorgesubmittedVersionM-BIO

Functional trait and life-history variation of arbuscular mycorrhizal fungi during secondary succession

Composition of plant communities during secondary succession are, to a great extent, determined by their arbuscular mycorrhizal (AM) symbionts. However, the role of AM fungi in driving secondary succession of plant communities is still the subject of extensive research. In recent years, e orts have been made to classify plants and AM fungi according to their life history traits. e mutualistic interactions between a plant and an AM fungal species with matching life history traits are very stable over time. In contrast, mutualism is weak between plants and AM fungi with non-complementary strategies. Plants and fungi maximising each other’s tness preferentially interact at the same successional stage. Moreover, there is compelling evidence for AM fungi driving plant–soil feedbacks. While altering feedback dynamics, AM fungi play a signi cant role in driving secondary succession towards climax stages by changing the composition of plant communities and recruiting more competitive or stress-tolerant species during intermediate successional stages. Consequently, community composition and change along successional gradients can be only fully understood when accounting for one of its major determinants: the AM fungi residing below ground.publishedVersio

Molekylærgenetisk karakterisering av vernaliseringsrespons i PACMAD-gras

Many plants rely on a mechanism called vernalisation response to match reproductive output with favourable environmental conditions. This trait is an important adaptation to seasonal climates, like for example at high latitudes. In grasses (Poaceae), evolution of seasonally-cued flowering was one of the traits enabling certain lineages to move out of their tropical origins and diversify in temperate zones. Due to its ecological and agricultural importance, the genetic basis of vernalisa- tion response is particularly well-studied in Pooideae grasses that predominates temperate habit- ats. However, little is known about vernalisation systems in other grass lineages that are adapted to cool and seasonal climates. In this study, I ask whether vernalisation response is found in a grass lineage called the pacmad clade. To disentangle the molecular machinery governing this trait, I quantified the expression of two paralogous FRUITFULL-like (FUL-like) vernalisation genes. My results demonstrate that vernalisation response is widespread in pacmad grasses, and found in at least four subfamilies with temperate representatives. Moreover, I found evidence for the co- option of a novel vernalisation gene (FUL2) into the vernalisation gene network Arundinoideae species Molinia caerulea

Revision of Coelastrella (Scenedesmaceae, Chlorophyta) and first register of this green coccoid microalga for continental Norway.

publishedVersio

Evolution of vernalization response in the PACMAD clade of the grass family (Poaceae)

<div> <div> <div> <div> <p>Vernalization is a physiological process that establishes floral meristem identity in response to prolonged periods of cold. Thereby, production of flowers in overwintering plants is aligned with the onset of spring, synchronizing reproduction with favorable environmental conditions. Proper timing of developmental transitions is crucial to the success of plants in regions with pronounced seasonal variation. Many vernalization systems have evolved in independently in different plant lineages. This allowed the expansion of certain plant groups from their tropical origins into novel habitats at higher latitudes. Due to its significance in agriculture, vernalization mechanisms of species from the mainly temperate grass subfamily Pooideae is well-studied and has been characterized on a molecular level. Recent advances demonstrate that the core regulatory network governing vernalization response is evolutionarily conserved within the Pooideae (McKeown et al. 2016). </p> <p>In this project, we seek to investigate whether this is true for other temperate grass lineages, focusing on species from the monophyletic PACMAD clade comprised of six distinct grass-subfamilies.</p> </div> </div> </div> </div

Major niche transitions in Pooideae correlate with variation in photoperiodic flowering and evolution of CCT domain genes

The external cues that trigger timely flowering vary greatly across tropical and temperate plant taxa, the latter rely- ing on predictable seasonal fluctuations in temperature and photoperiod. In the grass family (Poaceae) for example, species of the subfamily Pooideae have become specialists of the northern temperate hemisphere, generating the hypothesis that their progenitor evolved a flowering response to long days from a short-day or day-neutral ancestor. Sampling across the Pooideae, we found support for this hypothesis, and identified several secondary shifts to day- neutral flowering and one to short-day flowering in a tropical highland clade. To explain the proximate mechanisms for the secondary transition back to short-day-regulated flowering, we investigated the expression of CCT domain genes, some of which are known to repress flowering in cereal grasses under specific photoperiods. We found a shift in CONSTANS 1 and CONSTANS 9 expression that coincides with the derived short-day photoperiodism of our exem- plar species Nassella pubiflora. This sets up the testable hypothesis that trans- or cis-regulatory elements of these CCT domain genes were the targets of selection for major niche shifts in Pooideae grasses