n-Feng Li

Signatures of adaptation in the weedy rice genome

Crop domestication provided the calories that fueled the rise of civilization. For many crop species, domestication was accompanied by the evolution of weedy crop relatives, which aggressively outcompete crops and reduce harvests. Understanding the genetic mechanisms that underlie the evolution of weedy crop relatives is critical for agricultural weed management and food security. Here we use whole-genome sequences to examine the origin and adaptation of the two major strains of weedy rice found in the United States. We find that de-domestication from cultivated ancestors has had a major role in their evolution, with relatively few genetic changes required for the emergence of weediness traits. Weed strains likely evolved both early and late in the history of rice cultivation and represent an under-recognized component of the domestication process. Genomic regions identified here that show evidence of selection can be considered candidates for future genetic and functional analyses for rice improvement.

A re‐evaluation of the homoploid hybrid origin of Aegilops tauschii, the donor of the wheat D‐subgenome

Hybridization is a prominent evolutionary force promoting plant diversification, either with or without subsequent genome doubling (Abbott et al., 2013; Soltis et al., 2014; Yakimowski & Rieseberg, 2014). The Aegilops–Triticum complex is an ideal system to investigate how natural hybridization and allopolyploidization have caused species diversification (Matsuoka, 2011). Recently,Marcussen et al. (2014) proposed the tantalizing scenario that the ancestralD lineage originated via homoploid hybridization between ancient A and B lineages some 5 million years ago (Mya) (the definition of A, B andD lineages shown inFig. 1). Evidence for this mode of origin was derived from phylogenomic and population genetic analyses of nuclear genes, but without taking into account the evolutionary history and chloroplast topology of this species complex. Meanwhile, in a recent issue of New Phytologist, Gornicki et al. (2014) reported the chloroplast phylogeny of the Triticum–Aegilops complex based on 25 chloroplast genomes of eight modern A, S and D genome diploid species and four polyploidwheat species, but they did not address the origin of theD genome. Here, by re-analyzing critical data used by both studies and additional data, we present evidence for amore complex hybrid origin of the D genome of A. tauschii.

Transcriptome shock invokes disruption of parental expression-conserved genes in tetraploid wheat

Allopolyploidy often triggers phenotypic novelty and gene expression remolding in the resulting polyploids. In this study, we employed multiple phenotypic and genetic approaches to investigate the nature and consequences of allotetraploidization between A- and S-subgenome of tetraploid wheat. Results showed that karyotype of the nascent allopolyploid plants (AT2) is stable but they showed clear novelty in multiple morphological traits which might have positively contributed to the initial establishment of the tetraploids. Further microarray-based transcriptome profiling and gene-specific cDNA-pyrosequencing have documented that transcriptome shock was exceptionally strong in AT2, but a substantial proportion of the induced expression changes was rapidly stabilized in early generations. Meanwhile, both additive and nonadditive expression genes showed extensive homeolog expression remodeling and which have led to the subgenome expression dominance in leaf and young inflorescence of AT2. Through comparing the homeolog-expressing patterns between synthetic and natural tetraploid wheats, it appears that the shock-induced expression changes at both the total expression level and subgenome homeolog partitioning are evolutionarily persistent. Together, our study shed new light on how gene expression changes have rapidly occurred at the initial stage following allotetraploidization, as well as their evolutionary relevance, which may have implications for wheat improvements.

To Have and to Hold: Selection for Seed and Fruit Retention During Crop Domestication.

Crop domestication provides a useful model system to characterize the molecular and developmental bases of morphological variation in plants. Among the most universal changes resulting from selection during crop domestication is the loss of seed and fruit dispersal mechanisms, which greatly facilitates harvesting efficiency. In this review, we consider the molecular genetic and developmental bases of the loss of seed shattering and fruit dispersal in six major crop plant families, three of which are primarily associated with seed crops (Poaceae, Brassicaceae, Fabaceae) and three of which are associated with fleshy-fruited crops (Solanaceae, Rosaceae, Rutaceae). We find that the developmental basis of the loss of seed/fruit dispersal is conserved in a number of independently domesticated crops, indicating the widespread occurrence of developmentally convergent evolution in response to human selection. With regard to the molecular genetic approaches used to characterize the basis of this trait, traditional biparental quantitative trait loci mapping remains the most commonly used strategy; however, recent advances in next-generation sequencing technologies are now providing new avenues to map and characterize loss of shattering/dispersal alleles. We anticipate that continued application of these approaches, together with candidate gene analyses informed by known shattering candidate genes from other crops, will lead to a rapid expansion of our understanding of this critical domestication trait.

To Have and to Hold

Crop domestication provides a useful model system to characterize the molecular and developmental bases of morphological variation in plants. Among the most universal changes resulting from selection during crop domestication is the loss of seed and fruit dispersal mechanisms, which greatly facilitates harvesting efficiency. In this review, we consider the molecular genetic and developmental bases of the loss of seed shattering and fruit dispersal in six major crop plant families, three of which are primarily associated with seed crops (Poaceae, Brassicaceae, Fabaceae) and three of which are associated with fleshy-fruited crops (Solanaceae, Rosaceae, Rutaceae). We find that the developmental basis of the loss of seed/fruit dispersal is conserved in a number of independently domesticated crops, indicating the widespread occurrence of developmentally convergent evolution in response to human selection. With regard to the molecular genetic approaches used to characterize the basis of this trait, traditional biparental quantitative trait loci mapping remains the most commonly used strategy; however, recent advances in next-generation sequencing technologies are now providing new avenues to map and characterize loss of shattering/dispersal alleles. We anticipate that continued application of these approaches, together with candidate gene analyses informed by known shattering candidate genes from other crops, will lead to a rapid expansion of our understanding of this critical domestication trait.

Multiple rounds of ancient and recent hybridizations have occurred within the Aegilops–Triticum complex

We agree with Sandve et al. (2015) that the nomenclature of Aegilops/Triticum lineages is complex. Indeed, there is a contradiction in how they themselves have defined ‘theDgenome lineage’ in their Letter (Sandve et al., 2015), compared to their earlier paper (Marcussen et al., 2014). Fig. 1 of Sandve et al. (2015) defines it as a clade comprising D + S* + M genome species; this definition is consistent with the clade we identified in our cpDNA phylogeny (Fig. 1 of Li et al., 2015). By contrast, the nuclear gene phylogeny of Marcussen et al. (2014) places M-genome species (e.g. Ae. comosa) within theB-genome lineage, not theD-genome lineage (see Fig. S6 of Marcussen et al., 2014). This contradiction between the chloroplast and nuclear phylogenies is consistent with our previous inference of a complex hybridization history for the D-genome lineage. It is not consistent with a single homoploid hybrid origin of the D + S* +M clade, as inferred by Sandve et al. (2015). Moreover, contrary to the assertion by Sandve et al. (2015) that we confounded the modern D genome and the D-genome lineage (as defined in Fig. 1 of Sandve et al., 2015), we explicitly drew this distinction in our analyses (e.g. Table 2 of Li et al., 2015; showing results both for extant D-genome species and for ‘the ancient D-genome lineage’). We also explicitly considered the single homoploid hybrid originmodel favored by Sandve et al. (2015) for the D-genome lineage (see Fig. 2a of Li et al., 2015); however, the conflicting chloroplast and nuclear phylogenies described earlier led to our inference of a more complex hybridization history.

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

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

Agricultural weeds serve as productive models for studying the genetic basis of rapid adaptation, with weed‐adaptive traits potentially evolving multiple times independently in geographically distinct but environmentally similar agroecosystems. Weedy relatives of domesticated crops can be especially interesting systems because of the potential for weed‐adaptive alleles to originate through multiple mechanisms, including introgression from cultivated and/or wild relatives, standing genetic variation, and de novo mutations. Weedy rice populations have evolved multiple times through dedomestication from cultivated rice. Much of the genomic work to date in weedy rice has focused on populations that exist outside the range of the wild crop progenitor. In this study, we use genome‐wide SNPs generated through genotyping‐by‐sequencing to compare the evolution of weedy rice in regions outside the range of wild rice (North America, South Korea) and populations in Southeast Asia, where wild rice populations are present. We find evidence for adaptive introgression of wild rice alleles into weedy rice populations in Southeast Asia, with the relative contributions of wild and cultivated rice alleles varying across the genome. In addition, gene regions underlying several weed‐adaptive traits are dominated by genomic contributions from wild rice. Genome‐wide nucleotide diversity is also much higher in Southeast Asian weeds than in North American and South Korean weeds. Besides reflecting introgression from wild rice, this difference in diversity likely reflects genetic contributions from diverse cultivated landraces that may have served as the progenitors of these weedy populations. These important differences in weedy rice evolution in regions with and without wild rice could inform region‐specific management strategies for weed control.

Genomic Clues for Crop–Weed Interactions and Evolution

Agronomically critical weeds that have evolved alongside crop species are characterized by rapid adaptation and invasiveness, which can result in an enormous reduction in annual crop yield worldwide. We discuss here recent genome-based research studies on agricultural weeds and crop-weed interactions that reveal several major evolutionary innovations such as de-domestication, interactions mediated by allelochemical secondary metabolites, and parasitic genetic elements that play crucial roles in enhancing weed invasiveness in agricultural settings. We believe that these key studies will guide future research into the evolution of crop-weed interactions, and further the development of practical applications in agricultural weed control and crop breeding.

The Role of Standing Variation in the Evolution of Weediness Traits in South Asian Weedy Rice (Oryza spp.)

Weedy rice (Oryza spp.) is a problematic weed of cultivated rice (O. sativa) around the world. Recent studies have established multiple independent evolutionary origins of weedy rice, raising questions about the traits and genes that are essential for the evolution of this weed. Among world regions, South Asia stands out due to the heterogeneity of its weedy rice populations, which can be traced to at least three origins: two through de-domestication from distinct cultivated rice varieties, and one from local wild rice (O. rufipogon/O. nivara). Here we examine five traits considered typical of or advantageous to weedy rice in weedy, cultivated and wild rice samples from South Asia. We establish that convergence among all three weed groups occurs for easy seed shattering, red pericarp color, and compact plant architecture, suggesting that these traits are essential for weed success in the South Asian agricultural environment. A high degree of convergence for black hull color is also seen among weeds with wild ancestors and weeds evolved from the aus cultivated rice group. We also examine polymorphism in five known domestication candidate genes, and find that Rc and Bh4 are associated with weed seed pericarp color and hull color, respectively, and weedy alleles segregate in the ancestral populations, as do alleles for the seed dormancy-linked gene Sdr4. The presence of a domestication related allele at the seed shattering locus, sh4, in weedy rice populations with cultivated ancestry supports a de-domestication origin for these weedy groups, and raises questions about the reacquisition of the shattering trait in these weedy populations. Our characterization of weedy rice phenotypes in South Asia and their associated candidate genes contribute to the emerging understanding of the mechanisms by which weedy rice evolves worldwide, suggesting that standing ancestral variation is often the source of weedy traits in independently evolved groups, and highlighting the reservoir of genetic variation that is present in cultivated varieties as well as in wild rice, and its potential for phenotypic evolution.