Genome Scan of Rice Landrace Populations Collected Across Time Revealed Climate Changes’ Selective Footprints in the Genes Network Regulating Flowering Time

Analyses of the genetic bases of plant adaptation to climate changes, using genome-scan approaches, are often conducted on natural populations, under hypothesis of out-crossing reproductive regime. We report here on a study based on diachronic sampling (1980 and 2011) of the autogamous crop species, Oryza sativa and Oryza glaberrima, in the tropical forest and the Sudanian savannah of West Africa. First, using historical meteorological data we confirmed changes in temperatures (+ 1 °C on average) and rainfall regime (less predictable and reduced amount) in the target areas. Second, phenotyping the populations for phenology, we observed significantly earlier heading time in the 2010 samples. Third, implementing two genome-scan methods (one of which specially developed for selfing species) on genotyping by sequencing genotypic data of the two populations, we detected 31 independent selection footprints. Gene ontology analysis detected significant enrichment of these selection footprints in genes involved in reproductive processes. Some of them bore known heading time QTLs and genes, including OsGI, Hd1 and OsphyB. This rapid adaptive evolution, originated from subtle changes in the standing variation in genetic network regulating heading time, did not translate into predominance of multilocus genotypes, as it is often the case in selfing plants, and into notable selective sweeps. The high adaptive potential observed results from the multiline genetic structure of the rice landraces, and the rather large and imbricated genetic diversity of the rice meta-population at the farm, the village and the region levels, that hosted the adaptive variants in multiple genetic backgrounds before the advent of the environmental selective pressure. Our results illustrate the evolution of in situ diversity through processes of human and natural selection, and provide a model for rice breeding and cultivars deployment strategies aiming resilience to climate changes. It also calls for further development of population genetic models for adaptation of plant populations to environmental changes. To our best knowledge, this is the first study dealing with climate-changes’ selective footprint in crops. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12284-023-00633-4.