Can chromosome reorganisation aid adaptation to drought?

Informations projet

CondensDrought

N° de convention de subvention: 101029312

DOI

10.3030/101029312

Projet clôturé

Date de signature de la CE 4 Mai 2021

Date de début 1 Septembre 2022

Date de fin 31 Août 2024

Financé au titre de

• EXCELLENT SCIENCE - Marie Skłodowska-Curie Actions

Coût total

€ 174 167,04

Contribution de l’UE

€ 174 167,04

Coordonné par

UNIVERSITAT WIEN
Austria

Periodic Reporting for period 1 - CondensDrought (Can chromosome reorganisation aid adaptation to drought?)

Période du rapport: 2022-09-01 au 2024-08-31

Résumé du contexte et des objectifs généraux du projet

Whole genome duplication (WGD) events, followed by reductions in chromosome number (referred to as descending dysploidy), are known to have had a significant impact on the structure and function of modern plant genomes. Despite the numerous WGD events in plant evolutionary history, many extant plant species, particularly herbaceous, self-pollinating, and annual species, exhibit surprisingly low chromosome numbers and relatively small genomes. While some explanations for genome downsizing after WGD have been proposed, the evolutionary drivers behind chromosome number reduction remain poorly understood. This project seeks to address this gap by exploring the hypothesis that reductions in chromosome number are driven by natural selection to create linkage groups that are favorable for adaptation to specific environments, particularly arid habitats. This hypothesis, initially proposed by Darlington and further developed by Stebbins, suggests that chromosome condensation may provide selective advantages by maintaining favorable gene combinations and reducing recombination rates. These effects could be particularly beneficial in species inhabiting harsh, stable environments, where maintaining a highly fit population structure is crucial. To test this hypothesis, this project explored the evolution of Nicotiana section Suaveolentes, a group of plant species that have undergone rapid radiation in Australia and display a wide variation in chromosome numbers and genome sizes. This group is particularly interesting due to its adaptation to diverse environmental conditions, ranging from mesic (moderate) to highly arid habitats. The project aimed to investigate whether chromosome condensation and associated genomic rearrangements are linked to adaptation to arid environments and rapid species diversification in this group.

Understanding the evolutionary mechanisms that enable plants to adapt to extreme environments, such as arid regions, is crucial for addressing several challenges, particularly in the context of climate change. Additionally, the project has implications for biodiversity conservation, as many species are under threat due to habitat loss and environmental changes.

The overall objectives of this project were:
To test the hypothesis that chromosome condensation aids adaptation to arid habitats, specifically within the Nicotiana section Suaveolentes.
To detect large-scale genomic variations and investigate whether genomic rearrangements cluster genes responsible for adaptation to extreme environments.
To infer past population demography and recombination heterogeneity, investigating whether adaptation to extreme habitats occurred alongside significant genetic bottlenecks and to characterize spatial variation in recombination rates along chromosomes.

Travail effectué depuis le début du projet jusqu’à la fin de la période considérée dans le rapport et principaux résultats atteints jusqu’à présent

This project focused on: exploring the evolutionary history and population dynamics of the species in Nicotiana section Suaveolentes and understanding the genomic basis of their drought adaptation. For the evolutionary history, biogeography and population genomics, a total of 437 accessions from different species within Nicotiana section Suaveolentes were collected and RADseq data were obtained. To identify candidate genes involved in drought response and to investigate the genome reorganisation with potential links to adaptation, we generated PacBio and RNAseq data.

Our results confirmed that the adaptive radiation of Nicotiana section Suaveolentes occurred approximately 2 million years ago, after Australia’s transition to arid conditions. Using coalescent-based species tree analysis and molecular clock methods, we estimated divergence times and better understood how environmental pressures shaped the evolution of these species. Population genomics analysis revealed extensive ancient migration between populations, indicating historical genetic connectivity. However, contemporary gene flow has become limited, with only a few population pairs maintaining genetic exchange, suggesting increased genetic isolation across most populations.

In terms of drought adaptation, a controlled drought experiment was performed on selected species pairs, with RNAseq data collected from leaf and root tissues under both drought and control conditions. Differential gene expression (DGE) analysis highlighted distinct drought adaptation strategies between sister species. Drought-resistant species exhibited downregulation of genes involved in photosynthesis and stress responses, while drought-susceptible species showed upregulation of genes related to oxidative stress and phytohormone signaling pathways. These divergent gene regulatory responses highlight the varied strategies species employ to cope with drought stress, which has important implications for understanding how plants adapt to arid environments. Furthermore, we obtained PacBio long-read sequence data for the species pairs to test for structural rearrangements.

The project’s results have been actively disseminated through peer-review publication and in scientific events. The results were presented in two talks during the XX International Botanical Congress in Madrid (2024), a talk at the Systematics Association International Biennial Conference in Reading (2024), and a poster at the Society for Molecular Biology and Evolution (SMBE23) conference in Ferrara, Italy, in 2023. The fellow of the project also presented the results in a symposium at the 2024 International Congress of the Brazilian Genetics Society - 69º CBG, where he was invited as speaker. Furthermore, I the project was presented in seminars at the Natural History Museum in Vienna, the State University of Campinas in Brazil, and the Royal Botanic Gardens in Peradeniya, Sri Lanka. Additionally, the fellow also promoted a bioinformatics workshop to graduate students in Sri Lanka, further extending the project’s educational impact.

Progrès au-delà de l’état des connaissances et impact potentiel prévu (y compris l’impact socio-économique et les conséquences sociétales plus larges du projet jusqu’à présent)

By the project’s conclusion, further detailed analysis of the identified candidate genes and structural rearrangements is expected to provide a comprehensive understanding of the genetic and genomic basis of drought adaptation in Nicotiana. The potential socio-economic and wider societal implications of the project are substantial. One of the most pressing challenges of the 21st century is developing agricultural systems that can withstand the growing impacts of climate change, including increased drought frequency and severity. The project’s results on drought adaptation mechanisms have direct implications for crop breeding and agricultural sustainability. By identifying key genetic pathways and genomic rearrangements involved in drought tolerance, the project provides valuable tools for developing more resilient crop varieties. These findings can contribute to improving food security in arid and semi-arid regions, which are particularly vulnerable to climate change.In addition to its agricultural applications, the project also holds significant value for biodiversity conservation. As natural habitats face increasing environmental stress, understanding how species adapt to extreme conditions is crucial for developing effective conservation strategies. The insights gained from this research can guide efforts to protect and preserve species that are adapted to arid environments, many of which are at risk due to habitat loss and climate change.

Habitat diversity, mesic and arid, among species of Nicotiana section Suaveolentes in the Australia.