The New Is Old: Novel Germination Strategy Evolved From Standing Genetic Variation in Weedy Rice

Feralization of crop plants has aroused an increasing interest in recent years, not only for the reduced yield and quality of crop production caused by feral plants but also for the rapid evolution of novel traits that facilitate the evolution and persistence of weedy forms. Weedy rice (Oryza sativa f. spontanea) is a conspecific weed of cultivated rice, with separate and independent origins. The weedy rice distributed in eastern and northeastern China did not diverge from their cultivated ancestors by reverting to the pre-domestication trait of seed dormancy during feralization. Instead, they developed a temperature-sensing mechanism to control the timing of seed germination. Subsequent divergence in the minimum critical temperature for germination has been detected between northeastern and eastern populations. An integrative analysis was conducted using combinations of phenotypic, genomic and transcriptomic data to investigate the genetic mechanism underlying local adaptation and feralization. A dozen genes were identified, which showed extreme allele frequency differences between eastern and northeastern populations, and high correlations between allele-specific gene expression and feral phenotypes. Trancing the origin of potential adaptive alleles based on genomic sequences revealed the presence of most selected alleles in wild and cultivated rice genomes, indicating that weedy rice drew upon pre-existing, "conditionally neutral" alleles to respond to the feral selection regimes. The cryptic phenotype was exposed by activating formerly silent alleles to facilitate the transition from cultivation to wild existence, promoting the evolution and persistence of weedy forms.