Little White Lies: Pericarp Color Provides Insights into the Origins and Evolution of Southeast Asian Weedy Rice

Abstract

Weedy rice is a conspecific form of cultivated rice (Oryza sativa L.) that infests rice fields and results in severe crop losses. Weed strains in different world regions appear to have originated multiple times from different domesticated and/or wild rice progenitors. In the case of Malaysian weedy rice, a multiple-origin model has been proposed based on neutral markers and analyses of domestication genes for hull color and seed shattering. Here, we examined variation in pericarp (bran) color and its molecular basis to address how this trait evolved in Malaysian weeds and its possible role in weed adaptation. Functional alleles of the Rc gene confer proanthocyanidin pigmentation of the pericarp, a trait found in most wild and weedy Oryzas and associated with seed dormancy; nonfunctional rc alleles were strongly favored during rice domestication, and most cultivated varieties have nonpigmented pericarps. Phenotypic characterizations of 52 Malaysian weeds revealed that most strains are characterized by the pigmented pericarp; however, some weeds have white pericarps, suggesting close relationships to cultivated rice. Phylogenetic analyses indicate that the Rc haplotypes present in Malaysian weeds likely have at least three distinct origins: wild O. rufipogon, white-pericarp cultivated rice, and red-pericarp cultivated rice. These diverse origins contribute to high Rc nucleotide diversity in the Malaysian weeds. Comparison of Rc allelic distributions with other rice domestication genes suggests that functional Rc alleles may confer particular fitness benefits in weedy rice populations, for example, by conferring seed dormancy. This may promote functional Rc introgression from local wild Oryza populations.

Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia

“…Because rice is a genomic model species with a well‐annotated reference genome and molecularly well‐characterized domestication genes, evidence for such adaptive introgression can be explicitly examined using dense, genome‐wide SNP markers (Hufford et al., ). This genome‐wide approach can serve as a useful complement to recent candidate gene studies which have suggested adaptive introgression of wild rice alleles conferring shattering ( sh4 , Song et al., ) and seed dormancy ( Rc , Cui et al., ) in some Malaysian weedy rice strains.…”

Discordant Patterns of Introgression Suggest Historical Gene Flow into Thai Weedy Rice from Domesticated and Wild Relatives

“…For such traits, introgression from wild populations rather than crop varieties could be adaptive for allowing the weeds to persist and proliferate in agricultural fields. Comparisons of the distributions of crop versus wild alleles at multiple domestication genes can thus provide insights on patterns of adaptive introgression into weed populations from domesticated and wild relatives (Song et al 2014;Cui et al 2016;Huang et al 2018).…”

“…Comparative analyses of domestication genes and neutral markers have proved particularly insightful in evolutionary studies of weedy rice (Song et al 2014;Cui et al 2016;Huang et al 2018). These analyses have largely relied on 3 well-characterized rice domestication genes: sh4 (controlling loss of shattering in the crop), Rc (controlling loss of pericarp pigmentation and seed dormancy in the crop), and Bh4 (controlling loss of dark-pigmented hulls in the crop).…”

“…Most modern cultivated rice varieties carry a 14-bp frameshift deletion in exon 7 that generates a nonfunctional gene product and nonpigmented or "white" pericarps (bran) (Sweeney et al 2007). Unlike sh4, this rc domestication allele is not present in most weedy rice; instead, most weed strains carry functional Rc alleles (Gross et al 2010;Cui et al 2016). This suggests that most weedy rice strains are not descended from modern rice varieties, but rather that they evolved from dark-pericarp landraces that predate modern light-pericarp varieties.…”

“…This suggests that most weedy rice strains are not descended from modern rice varieties, but rather that they evolved from dark-pericarp landraces that predate modern light-pericarp varieties. The high frequency of the functional Rc allele in weedy rice populations has been proposed to reflect strong selection for seed dormancy, as this is a critical trait for weed persistence in crop fields (Cui et al 2016).…”