An official website of the United States government
SUMMARY The repeated evolution of high seed shattering during multiple independent de‐domestications of cultivated Asian rice (Oryza sativa) into weedy rice (Oryzaspp.) is a prime example of convergent evolution. Weedy rice populations converge in histological features of the abscission zone (AZ), a crucial structure for seed abscission, while ancestral cultivated rice populations exhibit varied AZ morphology and levels of shattering. However, the genetic bases of these phenotypic patterns remain unclear. We examined the expression profiles of the AZ region and its surrounding tissues at three developmental stages in two low‐shattering cultivars ofausandtemperate japonicadomesticated groups and in two genotypes of their derived high‐shattering weed groups, Blackhull Awned (BHA) and Spanish Weedy Rice (SWR), respectively. Consistent with the greater alteration of AZ morphology during the de‐domestication of SWR than BHA, fewer genes exhibited a comparable AZ‐region exclusive expression pattern between weed and crop in thetemperate japonicalineage than in theauslineage. Transcription factors related to the repression of lignin and secondary cell wall deposition, such as,OsWRKY102andOsXND‐1‐like, along with certain known shattering genes involved in AZ formation, likely played a role in maintaining AZ region identity in both lineages. Meanwhile, most genes exhibiting AZ‐region exclusive expression patterns do not overlap between the two lineages and the genes exhibiting differential expression in the AZ region between weed and crop across the two lineages are enriched for different gene ontology terms. Our findings suggest genetic flexibility in shaping AZ morphology, while genetic constraints on AZ identity determination in these two lineages.
more »
« less
A derived weedy rice × ancestral cultivar cross identifies evolutionarily relevant weediness QTLs
Abstract Weedy rice (Oryzaspp.) is a weedy relative of the cultivated rice that competes with the crop and causes significant production loss. The BHA (blackhull awned) US weedy rice group has evolved fromauscultivated rice and differs from its ancestors in several important weediness traits, including flowering time, plant height and seed shattering. Prior attempts to determine the genetic basis of weediness traits in plants using linkage mapping approaches have not often considered weed origins. However, the timing of divergence between crossed parents can affect the detection of quantitative trait loci (QTL) relevant to the evolution of weediness. Here, we used a QTL‐seq approach that combines bulked segregant analysis and high‐throughput whole genome resequencing to map the three important weediness traits in an F2population derived from a cross between BHA weedy rice with an ancestralauscultivar. We compared these QTLs with those previously detected in a cross of BHA with a more distantly related crop,indica. We identified multiple QTLs that overlapped with regions under selection during the evolution of weedy BHA rice and some candidate genes possibly underlying the evolution weediness traits in BHA. We showed that QTLs detected with ancestor–descendant crosses are more likely to be involved in the evolution of weediness traits than those detected from crosses of more diverged taxa.
more »
« less
- Award ID(s):
- 1947609
- PAR ID:
- 10472853
- Publisher / Repository:
- Wiley-Blackwell
- Date Published:
- Journal Name:
- Molecular Ecology
- Volume:
- 32
- Issue:
- 22
- ISSN:
- 0962-1083
- Format(s):
- Medium: X Size: p. 5971-5985
- Size(s):
- p. 5971-5985
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Registration of two rice mapping populations using weedy rice ecotypes as a novel germplasm resourceAbstract Two mapping populations were developed from crosses of the Asianindicarice (Oryza sativaL.) cultivar ‘Dee Geo Woo Gen’ (DGWG; PI 699210 Parent, PI 699212 Parent) and two weedy rice ecotypes, an early‐flowering straw hull (SH) biotype AR‐2000‐1135‐01 (PI 699209 Parent) collected in Arkansas and a late‐flowering black hull (BHA) biotype MS‐1996‐9 (PI 699211 Parent) collected in Mississippi. The weed and crop‐based rice recombinant inbred line (RIL) mapping populations have been used to identify genomic regions associated with weedy traits as well as resistance to sheath blight and rice blast diseases. The mapping population consists of 185 (DGWG/SH; Reg. no. MP‐9, NSL 541035 MAP) and 234 (BHA/DGWG; Reg. no. MP‐10, NSL 541036 MAP) F8RILs, of which 175 (DGWG/SH) and 224 (BHA/DGWG) were used to construct two linkage maps using single nucleotide polymorphic markers to identify weedy traits, sheath blight, and blast resistance loci. These mapping populations and related datasets represent a valuable resource for basic rice evolutionary genomic research and applied marker‐assisted breeding efforts in disease resistance.more » « less
-
Convergent evolution of root system architecture in two independently evolved lineages of weedy riceSummary Root system architecture (RSA) is a critical aspect of plant growth and competitive ability. Here we used two independently evolved strains of weedy rice, a de‐domesticated form of rice, to study the evolution of weed‐associatedRSAtraits and the extent to which they evolve through shared or different genetic mechanisms.We characterised 98 two‐dimensional and three‐dimensionalRSAtraits in 671 plants representing parents and descendants of two recombinant inbred line populations derived from two weed × crop crosses. A random forest machine learning model was used to assess the degree to which root traits can predict genotype and the most diagnostic traits for doing so. We used quantitative trait locus (QTL)mapping to compare genetic architecture between the weed strains.The two weeds were distinguishable from the crop in similar and predictable ways, suggesting independent evolution of a ‘weedy’RSAphenotype. Notably, comparativeQTLmapping revealed little evidence for shared underlying genetic mechanisms.Our findings suggest that despite the double bottlenecks of domestication and de‐domestication, weedy rice nonetheless shows genetic flexibility in the repeated evolution of weedyRSAtraits. Whereas the root growth of cultivated rice may facilitate interactions among neighbouring plants, the weedy rice phenotype may minimise below‐ground contact as a competitive strategy.more » « less
-
Societal Impact StatementWeedy plants are a major constraint on agricultural productivity. Weedy rice is a weed that invades rice fields worldwide and is responsible for reductions in rice yields. Studies to date have detected multiple independent weedy rice origins in different parts of the world. We investigated the origin of weedy rice in Spain and Portugal and found that it has evolved from a cultivated rice variety group grown locally. Iberian weeds carry mutations that reverse domesticated pericarp color to its ancestral red color. Our results imply that management strategies are needed to prevent the evolution of troublesome weeds from cultivated ancestors. SummaryWeedy rice, a damaging conspecific weed of cultivated rice, has arisen multiple times independently around the world. Understanding all weedy rice origins is necessary to create more effective weed management strategies. The origins of weedy rice in Spain and Portugal, where there are no nativeOryzaspecies, are unknown. In this study, we try to identify the likely ancestors of Iberian weedy rice and the mechanisms involved in the evolution of two weedy traits, seed shattering, and red pericarps.We used genotyping by sequencing to understand the origin of Iberian weedy rice and its relationship to other weedy, wild, and cultivated rice groups worldwide. We also genotyped candidate genes for shattering and pericarp color.We find that weedy rice in the Iberian Peninsula has primarily evolved through de‐domestication oftemperate japonicacultivars, with minor origins from exotic weedy rice. Iberian weeds have evolved the capacity to shatter seeds via novel loci and have acquired red pericarps via compensatory mutations in theRcdomestication gene. Our results suggest the Iberian weeds have experienced selection at multiple locations in the genome to establish as weeds, likely targeting male fertility genes among other functions.Our characterization of Iberian weedy rice adds to the growing evidence that de‐domestication of cultivated rice varieties is the main source of weedy rice worldwide. Their evolutionary versatility explains why weedy rice continues to be one of the most problematic weeds of cultivated rice.more » « less
-
Abstract Weedy rice is a close relative of cultivated rice that devastates rice productivity worldwide. In the southern United States, two distinct strains have been historically predominant, but the 21stcentury introduction of hybrid rice and herbicide resistant rice technologies has dramatically altered the weedy rice selective landscape. Here, we use whole-genome sequences of 48 contemporary weedy rice accessions to investigate the genomic consequences of crop-weed hybridization and selection for herbicide resistance. We find that population dynamics have shifted such that most contemporary weeds are now crop-weed hybrid derivatives, and that their genomes have subsequently evolved to be more like their weedy ancestors. Haplotype analysis reveals extensive adaptive introgression of cultivated alleles at the resistance geneALS, but also uncovers evidence for convergent molecular evolution in accessions with no signs of hybrid origin. The results of this study suggest a new era of weedy rice evolution in the United States.more » « less
