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Abstract Abscission, known as shattering in crop species, is a highly regulated process by which plants shed parts. Although shattering has been studied extensively in cereals and a number of regulatory genes have been identified, much diversity in the process remains to be discovered. Teff (Eragrostis tef) is a crop native to Ethiopia that is potentially highly valuable worldwide for its nutritious grain and drought tolerance. Previous work has suggested that grain shattering in Eragrostis might have little in common with other cereals. In this study, we characterize the anatomy, cellular structure, and gene regulatory control of the abscission zone (AZ) in E. tef. We show that the AZ of E. tef is a narrow stalk below the caryopsis, which is common in Eragrostis species. X-ray microscopy, scanning electron microscopy, transmission electron microscopy, and immunolocalization of cell wall components showed that the AZ cells are thin walled and break open along with programmed cell death (PCD) at seed maturity, rather than separating between cells as in other studied species. Knockout of YABBY2/SHATTERING1, documented to control abscission in several cereals, had no effect on abscission or AZ structure in E. tef. RNA sequencing analysis showed that genes related to PCD and cell wall modification are enriched in the AZ at the early seed maturity stage. These data show that E. tef drops its seeds using a unique mechanism. Our results provide the groundwork for understanding grain shattering in Eragrostis and further improvement of shattering in E. tef.
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The YABBY gene SHATTERING1 controls activation rather than patterning of the abscission zone in Setaria viridis
Abscission is predetermined in specialized cell layers called the abscission zone (AZ) and activated by developmental or environmental signals. In the grass family, most identified AZ genes regulate AZ anatomy, which differs among lineages. A YABBY transcription factor, SHATTERING1 (SH1), is a domestication gene regulating abscission in multiple cereals, including rice and Setaria. In rice, SH1 inhibits lignification specifically in the AZ. However, the AZ of Setaria is nonlignified throughout, raising the question of how SH1 functions in species without lignification. Crispr-Cas9 knockout mutants of SH1 were generated in Setaria viridis and characterized with histology, cell wall and auxin immunofluorescence, transmission electron microscopy, hormonal treatment and RNA-Seq analysis. The sh1 mutant lacks shattering, as expected. No differences in cell anatomy or cell wall components including lignin were observed between sh1 and the wild-type (WT) until abscission occurs. Chloroplasts degenerated in the AZ of WT before abscission, but degeneration was suppressed by auxin treatment. Auxin distribution and expression of auxin-related genes differed between WT and sh1, with the signal of an antibody to auxin detected in the sh1 chloroplast. SH1 in Setaria is required for activation of abscission through auxin signaling, which is not reported in other grass species.
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- PAR ID:
- 10506925
- Publisher / Repository:
- New Phytologist Foundation
- Date Published:
- Journal Name:
- New Phytologist
- Volume:
- 240
- Issue:
- 2
- ISSN:
- 0028-646X
- Page Range / eLocation ID:
- 846 to 862
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Tranbarger, Timothy J (Ed.)The abscission zone (AZ) consists of specialized cell layers where cell separation or breakage occurs that result in organ detachment. Microscopic observation of the AZ is crucial for understanding its function. The AZ undergoes cellular and physiological changes prior to abscission, such as cell death, loss of chlorophyll, and the production of reactive oxygen species (ROS). These changes can be visualized using specific dyes and indicators under light or fluorescent microscopes. However, one challenge of using these dyes is their inefficient penetration into the tissue, especially when the epidermal layer has thick secondary cell walls. In this chapter, a detailed protocol to overcome this challenge is described. Using the fruit AZ of Setaria viridis, in which the epidermal cell wall is thick and lignified, we gently fix the dissected tissue, embed it in the Cryomatrix, and trim off the outer cell layers using a cryostat. The tissue with exposed inner cells can then be stained with fluorescent dyes to visualize organelles of interest, or 3,3′-diaminobenzidine (DAB) to visualize hydrogen peroxide accumulated in the tissue.more » « less
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Bartlett, Madelaine; Richardson, Annis (Ed.)Cereal shattering and threshability, both involving disarticulation of grains from the mother plant, are important traits for cereal domestication and improvement. Recent studies highlighted diverse mechanisms influencing shattering and threshability, either through development of the disarticulation zone or floral structures enclosing or supporting the disarticulation unit. Differential lignification in the disarticulation zone is essential for rice shattering but not required for many other grasses. During shattering, the disarticulation zone undergoes either abscission leading to cell separation or cell breakage. Threshability can be affected by the morphology and toughness of the enclosing floral structures, and in some species, by the inherent weakness of the disarticulation zone. Fine-tuning shattering and threshability is essential for breeding wild and less domesticated cereals.more » « less
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Lunn, John (Ed.)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.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/nph.19157
