Exploration Of Genetic Mechanisms Of Plant Adaptation At Different Temporal And Spatial Scales

Adaptive evolution is a dynamic evolutionary process by which organisms respond to environmental changes by altering their fitness through changes in phenotype and genotype.It is the comprehensive result of multiple forms of natural selection,neutral factors and environmental variables.The genetic mechanisms of adaptive evolution also differ at different temporal and spatial scales: for example,the convergent phenotypes of xerophytes diverged over 100 million-year ago on different continents,while the same species show different phenotypes as a response to local differences depending on geographical,environmental distance or interspecific introgression.Although there are many studies on convergent adaptation,local adaptation and adaptive introgression,few have explored the genetic connections between those evolutionary mechanisms at different scales.Here,in order to reveal similarities and differences in mechanisms of adaptive evolution at different temporal and spatial scales we focused on two emblematic cases: we focused on Gymnocarpos przewalskii,an important xerophyte from North-West China and two sympatric widespread East Asian oak species(Quercus acutissima and Q.variabilis).The thesis is mainly divided into three parts: 1)we first test for convergent evolution in plants adapting to extreme environments(e.g.aridity)from the multi-species scale.2)we analyze local adaptation influenced by spatial environment heterogeneity from the multi-population scale after speciation.3)we explore the adaptive evolution caused by interspecific introgression at the population scale in sympatric and closely related species.The main results and conclusions are as follows:(1)Convergent evolution of distantly related xerophytesWe first assembled a high-quality genome of G.przewalskii,and compared it to the genomes of ten xerophytes and four non-xerophytes with an overall divergence time of about 100 Mya: 1)although the influence of genetic drift cannot be ignored,the number of shared genes between xerophytes was significantly higher than that between non-xerophytes or between xerophytes and non-xerophytes,that is,convergent evolution retains more xerophyte-related genes in xerophytes;2)compared with directional selection,stabilizing selection plays a dominant role in the process of convergent evolution.We identified 118 genes involved in convergent adaptation to aridity.Sixty-five G.przewalskii genes were shared across xerophytic species,of which63 were under stabilizing selection and two under directional selection.(2)Local adaptions of xerophyteBefore evaluating local adaptation in G.przewalskii,we inferred population demographic history and population structure.The results showed that: 1)a major migration barrier was centered around the Lop Nur and separated the Tarim populations from others;2)the aridification caused by the uplift of the Qinghai-Tibet Plateau,the retreat of the Paratethys Ocean,orogeny and the final permanent dried up of episodic lakes during the late Miocene to Pliocene transition drove Tarim cluster split from others(～ 5.22Mya).And the ancestral migration also ceased between the Tarim and the three other clusters after the Hami lineage diverged about 2.75 Mya;3)climate changes in the late Pleistocene(～ 56 Kya)drove the population size contractions and fragmentation of G.przewalskii.We tested for evidence of local adaptation by resequencing 177 individuals from 26 populations of G.przewalskii,about 20%(10,516 coding genes)of the total number of genes in G.przewalskii were found to be associated to local adaptation.These genes were significantly enriched in expanded gene families that possibly arised from the recent WGD event of G.przewalskii.Only 13 of those genes were also under convergent adaptation.This indicates that the molecular mechanisms of adaptive evolution at the two-time scale are different.(3)Adaptive introgression among closely related speciesUsing full genome resequencing data from 187 individuals of Q.acutissima and Q.variabilis,we analyzed the introgression pattern among 10 sympatric populations.The result showed that geographical distance and environmental similarity jointly determine the intensity of interspecific introgression.Adaptive introgression sites associated with environmental factors were more likely to be enriched in regions where genetic recombination was suppressed,such as the four regions where recombination was suppressed by chromosomal inversions(Chr.9:39.4 Mb - 51 Mb,Chr.10:29.7 Mb- 34.9 Mb,Chr.11:24.8 Mb - 27.4 Mb,Chr.12:13.4 Mb - 21.5 Mb).The functional classification of adaptive introgression sites found that most of them are located in cisregulatory elements formed by transposable elements(TEs)insertion,that affect the expression regulation of downstream genes by environmental stimuli.The genes that are the most likely to be affected by introgression tend to have more stable expression levels.In summary,populations occupying similar environments tend to have the same genomic regions affected by introgression.The genes have more similar expressions under the same environment.To sum up,our results suggest that plants have diverse adaptive strategies: stability is required for long-term adaptation to extreme environmental stress and is attained by directional selection and stabilizing selection on a group of highly pleiotropic genes;meanwhile,rapid response to recent local environmental changes is highly polygenic at the whole genome level and is attained by diversifying selection,gene family expansion and adaptive introgression.The mechanisms on different time scales are clearly different: the former leads to ‘stability’ of phenotype and fitness,while the latter contributes to the ‘fine-tuning’ of the whole genome.