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Title: Grain shattering by cell death and fracture in Eragrostis tef
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.  more » « less
Award ID(s):
1938093 1938086
NSF-PAR ID:
10414595
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Plant Physiology
Volume:
192
Issue:
1
ISSN:
0032-0889
Page Range / eLocation ID:
222 to 239
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Summary

    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 andSetaria. In rice,SH1inhibits lignification specifically in the AZ. However, the AZ ofSetariais nonlignified throughout, raising the question of howSH1functions in species without lignification.

    Crispr‐Cas9 knockout mutants ofSH1were generated inSetaria viridisand characterized with histology, cell wall and auxin immunofluorescence, transmission electron microscopy, hormonal treatment and RNA‐Seq analysis.

    Thesh1mutant lacks shattering, as expected. No differences in cell anatomy or cell wall components including lignin were observed betweensh1and 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 andsh1, with the signal of an antibody to auxin detected in thesh1chloroplast.

    SH1inSetariais required for activation of abscission through auxin signaling, which is not reported in other grass species.

     
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  2. Grasses are among the most resilient plants, and some can survive prolonged desiccation in semiarid regions with seasonal rainfall. However, the genetic elements that distinguish grasses that are sensitive versus tolerant to extreme drying are largely unknown. Here, we leveraged comparative genomic approaches with the desiccation-tolerant grass Eragrostis nindensis and the related desiccation-sensitive cereal Eragrostis tef to identify changes underlying desiccation tolerance. These analyses were extended across C4 grasses and cereals to identify broader evolutionary conservation and divergence. Across diverse genomic datasets, we identified changes in chromatin architecture, methylation, gene duplications, and expression dynamics related to desiccation in E. nindensis . It was previously hypothesized that transcriptional rewiring of seed desiccation pathways confers vegetative desiccation tolerance. Here, we demonstrate that the majority of seed-dehydration–related genes showed similar expression patterns in leaves of both desiccation-tolerant and -sensitive species. However, we identified a small set of seed-related orthologs with expression specific to desiccation-tolerant species. This supports a broad role for seed-related genes, where many are involved in typical drought responses, with only a small subset of crucial genes specifically induced in desiccation-tolerant plants. 
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  4. Summary

    Abscission is a process in which plants shed their parts, and is mediated by a particular set of cells, the abscission zone (AZ). In grasses (Poaceae), the position of the AZ differs among species, raising the question of whether its anatomical structure and genetic control are conserved.

    The ancestral position of the AZ was reconstructed. A combination of light microscopy, transmission electron microscopy, RNA‐Seq analyses and RNAin situhybridisation were used to compare three species, two (weedy rice andBrachypodium distachyon) with the AZ in the ancestral position and one (Setaria viridis) with the AZ in a derived position below a cluster of flowers (spikelet).

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    Transcriptional regulation of AZ development appears to be extensively rewired among the three species, leading to distinct anatomical and morphological outcomes.

     
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  5. Premise

    Abscission zones (AZ) are specialized cell layers that separate plant parts at the organ junction upon developmental or environmental signals. Fruit or seed abscission has been well studied in model species because of its crucial role for seed dispersal. Previous work showed thatAZlocalization differs among species of Poaceae and thatAZformation is histologically and genetically distinct in three distantly related grass species, refuting the idea of a broadly conserved module. However, whetherAZstructure is consistent within subfamilies is unknown.

    Methods

    Eleven species were selected from six subfamilies of Poaceae, and theirAZwas investigated using paraffin‐embedded, stained material. Observations were added from the literature for an additional six species. Data were recorded onAZlocation and whether cells in theAZwere distinguishable by size or lignification. Characteristics of theAZwere mapped on the phylogeny using maximum likelihood.

    Results

    Abscission zone anatomy and histology vary among species, and characteristics of theAZdo not correlate with phylogeny. Twelve of the seventeen studied species have anAZin which the cells are significantly smaller than surrounding cells. Of these, eight have differential lignification. Differential lignification is often associated with differential cell size, but not vice versa.

    Conclusions

    Neither smaller cells in theAZnor differential lignification between the AZand surrounding cells is required for abscission, although differential cell size and lignification are often correlated. Abscission zone anatomy does not correlate with phylogeny, suggesting its rapid change over evolutionary time.

     
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