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

Abstract

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.

Keywords: Climate changes; Flowering time; Genome scan; O. glaberrima; O. sativa; Rice; Selection footprint; Temporal cline.

Fig. 1

Pattern of deviation of the annual rainfall total during the crop growth season (GSART) from the normal reference, during the 1961–2010 period, in Kankan (10°23′01.65″ N; 9°18′18.72″ W) and N’Zérekoré (7°’48′53.2″ N; 8°42′14.11″ W) sites of Guinea

Fig. 2

Pattern of deviation of the annual average minimum (T-Min) and maximum (T-Max) temperature from the normal reference, during the 1961–2010 period, in Kankan (10°23′01.65″ N; 9°18′18.72″ W) and N’Zérekoré (7°’48′53.2″ N; 8°42′14.11″ W) sites of Guinea

Fig. 3

Distribution of frequency of accessions of the two collect times (Collect-1 and Collect-2) in different classes of duration of the vegetative phase expressed in number of days between the sowing date and the heading date (DTHD)

Fig. 4

Unweighted neighbor-joining tree of simple matching distances constructed from genotypes of 530 rice accessions at 1130 SNP loci. Tree branches bearing green, red and blue colors correspond to O. glaberrima, O. sativa indica and O. sativa japonica groups, respectively. Within each branch, accessions from the first collect time (Og-1, Osi-1 and Osj-1) are shown in black

Fig. 5

Patterns of decay in the r² estimate of linkage disequilibrium (LD), in the rice populations collected in 1980 (xx-1) and in 2011 (xx-2); Og-1 and Og-2: O. glaberrima; Osj-1 and Osj-2: O. sativa japonica; Osi-2, O. sativa indica. The LD was estimated from 6250 SNP, 9282 SNP and 14,775 SNP loci for Og, Osj and Osi populations, respectively. The curve represents the average r² according to pairwise distance between markers among the 12 chromosomes and the bars represent the associated standard deviation

Fig. 6

Plot of the joint distribution of F_ST and heterozygosity within populations for the observed loci (circles) and the one-sided confidence interval limits obtained from simulated data (dashed lines). Loci departing from neutrality hypothesis at 1% and 5% significance levels are indicated in red and blue circles, respectively. The number of observed loci was 6250 for O. glaberrima, 9282 for O. sativa japonica