Genomic insights into the evolution of Echinochloa species as weed and orphan crop.

As one of the great survivors of the plant kingdom, barnyard grasses (Echinochloa spp.) are the most noxious and common weeds in paddy ecosystems. Meanwhile, at least two Echinochloa species have been domesticated and cultivated as millets. In order to better understand the genomic forces driving the evolution of Echinochloa species toward weed and crop characteristics, we assemble genomes of three Echinochloa species (allohexaploid E. crus-galli and E. colona, and allotetraploid E. oryzicola) and re-sequence 737 accessions of barnyard grasses and millets from 16 rice-producing countries. Phylogenomic and comparative genomic analyses reveal the complex and reticulate evolution in the speciation of Echinochloa polyploids and provide evidence of constrained disease-related gene copy numbers in Echinochloa. A population-level investigation uncovers deep population differentiation for local adaptation, multiple target-site herbicide resistance mutations of barnyard grasses, and limited domestication of barnyard millets. Our results provide genomic insights into the dual roles of Echinochloa species as weeds and crops as well as essential resources for studying plant polyploidization, adaptation, precision weed control and millet improvements.

Population genomic analysis reveals domestication of cultivated rye from weedy rye.

Rye (Secale cereale) is an important crop with multiple uses and a valuable genetic resource for wheat breeding. However, due to its complex genome and outcrossing nature, the origin of cultivated rye remains elusive. The geneticist N.I. Vavilov proposed that cultivated rye had been domesticated from weedy rye, rather than directly from wild species like other crops. Unraveling the domestication history of rye will extend our understanding of crop evolution and upend our inherent understanding of agricultural weeds. To this end, in this study we generated the 8.5 Tb of whole-genome resequencing data from 116 worldwide accessions of wild, weedy, and cultivated rye, and demonstrated that cultivated rye was domesticated directly from weedy relatives with a similar but enhanced genomic selection by humans. We found that a repertoire of genes that experienced artificial selection is associated with important agronomic traits, including shattering, grain yield, and disease resistance. Furthermore, we identified a composite introgression in cultivated rye from the wild perennial Secale strictum and detected a 2-Mb introgressed fragment containing a candidate ammonium transporter gene with potential effect on the grain yield and plant growth of rye. Taken together, our findings unravel the domestication history of cultivated rye, suggest that interspecific introgression serves as one of the likely causes of obscure species taxonomy of the genus Secale, and provide an important resource for future rye and wheat breeding.

The complete chloroplast genome of Echinochloa haploclada.

The genus Echinochloa (Poaceae) includes orphan crops and important agricultural weeds. Here, we assembled the complete chloroplast genome of a diploid Echinochloa species (E. haploclada). The chloroplast genome is 139,844 bp in length, which includes a large single copy region (81,893 bp), a small single copy region (12,533 bp) and two separated inverted repeat regions (45,418 bp). A total of 119 unique genes were annotated, consisting of 83 protein-coding genes, 32 tRNA genes and 4 rRNA genes. Hexaploid E. crus-galli, one of the most serious weeds worldwide, was derived from a hybrid between tetraploid E. oryzicola and an unknown diploid species. Based on chloroplast genomes of eight Echinochloa species (varieties), the phylogenetic analysis showed that E. crus-galli clustered firstly with diploid E. haploclada rather than tetraploid E. oryzicola, supporting previous assumption that E. oryzicola is the paternal donor of E. crus-galli.

De-Domestication: An Extension of Crop Evolution.

De-domestication or feralization is an interesting phenomenon in crops and livestock. Previously, evidence for crop de-domestication was based mainly on studies using phenotypic and genotypic data from limited molecular markers or gene segments. Recent genomic studies in rice, barley, and wheat provide comprehensive landscapes of de-domestication on a whole-genome scale. Here, we summarize crop de-domestication processes, ecological roles of de-domesticates, mechanisms underlying crop de-domestication syndromes, and conditions potentially favoring de-domestication events. We further explain how recent de-domestication studies have expanded our understanding of the complexity of crop evolution, and highlight the genetic novelties of de-domesticates beneficial for modern crop breeding.

The Genomes of the Allohexaploid Echinochloa crus-galli and Its Progenitors Provide Insights into Polyploidization-Driven Adaptation.

The hexaploid species Echinochloa crus-galli is one of the most detrimental weeds in crop fields, especially in rice paddies. Its evolutionary history is similar to that of bread wheat, arising through polyploidization after hybridization between a tetraploid and a diploid species. In this study, we generated and analyzed high-quality genome sequences of diploid (E. haploclada), tetraploid (E. oryzicola), and hexaploid (E. crus-galli) Echinochloa species. Gene family analysis showed a significant loss of disease-resistance genes such as those encoding NB-ARC domain-containing proteins during Echinochloa polyploidization, contrary to their significant expansionduring wheat polyploidization, suggesting that natural selection might favor reduced investment in resistance in this weed to maximize its growth and reproduction. In contrast to the asymmetric patterns of genome evolution observed in wheat and other crops, no significant differences in selection pressure were detected between the subgenomes in E. oryzicola and E. crus-galli. In addition, distinctive differences in subgenome transcriptome dynamics during hexaploidization were observed between E. crus-galli and bread wheat. Collectively, our study documents genomic mechanisms underlying the adaptation of a major agricultural weed during polyploidization. The genomic and transcriptomic resources of three Echinochloa species and new insights into the polyploidization-driven adaptive evolution would be useful for future breeding cereal crops.