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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.
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Comparative histology of abscission zones reveals the extent of convergence and divergence in seed shattering in weedy and cultivated rice
Abstract The modification of seed shattering has been a recurring theme in rice evolution. The wild ancestor of cultivated rice disperses its seeds, but reduced shattering was selected during multiple domestication events to facilitate harvesting. Conversely, selection for increased shattering occurred during the evolution of weedy rice, a weed invading cultivated rice fields that has originated multiple times from domesticated ancestors. Shattering requires formation of a tissue known as the abscission zone (AZ), but how the AZ has been modified throughout rice evolution is unclear. We quantitatively characterized the AZ characteristics of relative length, discontinuity, and intensity in 86 cultivated and weedy rice accessions. We reconstructed AZ evolutionary trajectories and determined the degree of convergence among different cultivated varieties and among independent weedy rice populations. AZ relative length emerged as the best feature to distinguish high and low shattering rice. Cultivated varieties differed in average AZ morphology, revealing lack of convergence in how shattering reduction was achieved during domestication. In contrast, weedy rice populations typically converged on complete AZs, irrespective of origin. By examining AZ population-level morphology, our study reveals its evolutionary plasticity, and suggests that the genetic potential to modify the ecologically and agronomically important trait of shattering is plentiful in rice lineages.
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- Award ID(s):
- 1947609
- PAR ID:
- 10586079
- Editor(s):
- Lunn, John
- Publisher / Repository:
- Journal of Experimental Botany
- Date Published:
- Journal Name:
- Journal of Experimental Botany
- Volume:
- 75
- Issue:
- 16
- ISSN:
- 0022-0957
- Page Range / eLocation ID:
- 4837 to 4850
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Weeds that infest crops are a primary factor limiting agricultural productivity worldwide. Weedy rice, also called red rice, has experienced independent evolutionary events through gene flow from wild rice relatives and de-domestication from cultivated rice. Each evolutionary event supplied/equipped weedy rice with competitive abilities that allowed it to thrive with cultivated rice and severely reduce yields in rice fields. Understanding how competitiveness evolves is important not only for noxious agricultural weed management but also for the transfer of weedy rice traits to cultivated rice. Molecular studies of weedy rice using simple sequence repeat (SSR), restriction fragment length polymorphism (RFLP), and whole-genome sequence have shown great genetic variations in weedy rice populations globally. These variations are evident both at the whole-genome and at the single-allele level, including Sh4 (shattering), Hd1 (heading and flowering), and Rc (pericarp pigmentation). The goal of this review is to describe the genetic diversity of current weedy rice germplasm and the significance of weedy rice germplasm as a novel source of disease resistance. Understanding these variations, especially at an allelic level, is also crucial as individual loci that control important traits can be of great target to rice breeders.more » « less
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/jxb/erae221
