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

Abstract

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.

Keywords: crop feralization; germination strategy; rapid adaptation; standing genetic variation; weedy rice.

Figure 1

Sampling sites for 20 weedy rice populations investigated in northeastern and eastern China.

Figure 2

Germination ratio (left) and germination time (right) of weedy rice seeds from 8 populations at 9, 12, and 15°C, respectively. Vertical bars indicate the standard error of the mean. Germination tests were conducted at 6 (A), 12 (B), and 24 (C) months after collection, respectively.

Figure 3

Frequencies of the northeastern weedy rice-specific predominant alleles in wild rice (Wild), japonica rice (JAP), northeastern weedy rice (NE_W), Jiangsu weedy rice (JS_W), and indica rice (IND) populations. Each dot represents a SNP allele. The horizontal bars indicate the mean allele frequency in each population. The red, blue, yellow, green, and orange dots represent the alleles located in Os03g0122600, Os10g0136150, Os10g0155800, Os11g0191300, and Os08g0227200, respectively. Their espression patterns were validated by qRT-PCR.

Figure 4

Genotype frequencies (left) and expression patterns (right) of 5 genes containing potential adaptive SNPs. (A–E) represent Os03g0122600, Os10g0136150, Os10g0155800, Os11g0191300, Os08g0227200, respectively. Ref, the homozygote of the reference base; Var, the homozygote of the variant base; Heter, the heterozygote of the reference and variant bases. HLJ_W, weedy rice from HLJ province; LN_W, weedy rice from LN province; JS_W, weedy rice from JS province; jap_C, the co-existing japonica rice.