Examination of the Abscission-Associated Transcriptomes for Soybean, Tomato, and Arabidopsis Highlights the Conserved Biosynthesis of an Extensible Extracellular Matrix and Boundary Layer

Abstract

Abscission zone (AZ) development and the progression of abscission (detachment of plant organs) have been roughly separated into four stages: first, AZ differentiation; second, competence to respond to abscission signals; third, activation of abscission; and fourth, formation of a protective layer and post-abscission trans-differentiation. Stage three, activation of abscission, is when changes in the cell wall and extracellular matrix occur to support successful organ separation. Most abscission research has focused on gene expression for enzymes that disassemble the cell wall within the AZ and changes in phytohormones and other signaling events that regulate their expression. Here, transcriptome data for soybean, tomato and Arabidopsis were examined and compared with a focus not only on genes associated with disassembly of the cell wall but also on gene expression linked to the biosynthesis of a new extracellular matrix. AZ-specific up-regulation of genes associated with cell wall disassembly including cellulases (beta-1,4-endoglucanases, CELs), polygalacturonases (PGs), and expansins (EXPs) were much as expected; however, curiously, changes in expression of xyloglucan endotransglucosylase/hydrolases (XTHs) were not AZ-specific in soybean. Unexpectedly, we identified an early increase in the expression of genes underlying the synthesis of a waxy-like cuticle. Based on the expression data, we propose that the early up-regulation of an abundance of small pathogenesis-related (PR) genes is more closely linked to structural changes in the extracellular matrix of separating cells than an enzymatic role in pathogen resistance. Furthermore, these observations led us to propose that, in addition to cell wall loosening enzymes, abscission requires (or is enhanced by) biosynthesis and secretion of small proteins (15–25 kDa) and waxes that form an extensible extracellular matrix and boundary layer on the surface of separating cells. The synthesis of the boundary layer precedes what is typically associated with the post-abscission synthesis of a protective scar over the fracture plane. This modification in the abscission model is discussed in regard to how it influences our interpretation of the role of multiple abscission signals.

Re-evaluation of the ethylene-dependent and -independent pathways in the regulation of floral and organ abscission

“…Moreover, these 11 genes were actually upregulated in both the hae hsl2 and ida mutants and the WT between stages 12-15 (Niederhuth et al, 2013), indicating that their upregulation in the mutants occurred without the involvement of the IDA-HAE-HSL2 complex, similar to the upregulation of 1772 other genes. The RNA-seq data in the supplementary files of this article were reformulated and presented by Kim et al (2015). The analyzed data showed that most of the genes related to cell wall disassembly and formation of the protective layer were similarly expressed in the receptacles of the WT and the hae-hsl2 mutant, and some of these genes were even upregulated in the hae-hsl2 mutant compared to the WT (Kim et al, 2015).…”

“…The RNA-seq data in the supplementary files of this article were reformulated and presented by Kim et al (2015). The analyzed data showed that most of the genes related to cell wall disassembly and formation of the protective layer were similarly expressed in the receptacles of the WT and the hae-hsl2 mutant, and some of these genes were even upregulated in the hae-hsl2 mutant compared to the WT (Kim et al, 2015). The minor delay in the decrease of petal breakstrength obtained in the ida and hae hsl2 compared to the WT (Liu et al, 2013), as well as the reformatted results by Kim et al (2015), indicate that the final cell separation step controlled by the IDA-HAE-HSL2 pathway is effected by a low number of the cell wall hydrolyzing enzymes.…”

“…However, it should be emphasized that the process of cell wall remodeling requires the involvement of many gene families related to cell wall degradation, defense, and development of a boundary layer that are specifically upregulated in the AZ. Numerous such genes were detected in various abscission systems including tomato flowers (Meir et al, 2010;Kim et al, 2015), fruits of apple (Zhu et al, 2011), melon (Corbacho et al, 2013) and olive (Gil-Amado and Gomez-Jimenez, 2013), fruitlets of litchi (Li et al, 2015) and citrus (Xie et al, 2018), soybean leaves (Kim et al, 2015), and lupine florets (Glazinska et al, 2017). It seems therefore, that the IDA-HAE-HSL2 pathway appears to regulate only a subset of genes encoding cell wall modifying proteins expressed in AZ cells.…”

Comparative Proteomics Profiling Illuminates the Fruitlet Abscission Mechanism of Sweet Cherry as Induced by Embryo Abortion

“…Several genes regulate the functioning of the plant cell wall. Changes in their expression are associated with aging [5], organ growth and development [5,44], maturation of fruits [45], and organ abscission [46].…”

Chemical Defoliant Promotes Leaf Abscission by Altering ROS Metabolism and Photosynthetic Efficiency in Gossypium hirsutum

“…Our findings not only provide important insights into leaf shedding-associated changes induced by TDZ in cotton, but also highlight the possibility that the ROS and photosynthesis may play a critical role in the organ shedding process in other crops.Previous studies have found that ethylene accelerates organ abscission, while auxin inhibits this process [5][6][7][8][9]. Meanwhile, researchers have paid attention to the fact that multiple cell wall-degrading enzymes are activated to dissolve the cell wall and middle lamella of abscission zone, including cellulases, pecticlyases, polygalactosidases [10][11][12]. Some research has found that hydrogen peroxide (H 2 O 2 ) acts downstream from ethylene and plays a role in the cell-wall degradation process in abscission signaling [13,14].Reactive oxygen species (ROS), including H 2 O 2 , superoxide, singlet oxygen, and the hydroxyl radical, are produced in response to environmental stress [13].…”