Transcriptional Regulation of Abscission Zones

Abstract

Precise and timely regulation of organ separation from the parent plant (abscission) is consequential to improvement of crop productivity as it influences both the timing of harvest and fruit quality. Abscission is tightly associated with plant fitness as unwanted organs (petals, sepals, filaments) are shed after fertilization while seeds, fruits, and leaves are cast off as means of reproductive success or in response to abiotic/biotic stresses. Floral organ abscission in Arabidopsis has been a useful model to elucidate the molecular mechanisms that underlie the separation processes, and multiple abscission signals associated with the activation and downstream pathways have been uncovered. Concomitantly, large-scale analyses of omics studies in diverse abscission systems of various plants have added valuable insights into the abscission process. The results suggest that there are common molecular events linked to the biosynthesis of a new extracellular matrix as well as cell wall disassembly. Comparative analysis between Arabidopsis and soybean abscission systems has revealed shared and yet disparate regulatory modules that affect the separation processes. In this review, we discuss our current understanding of the transcriptional regulation of abscission in several different plants that has improved on the previously proposed four-phased model of organ separation.

Keywords: abscission; abscission zone; boundary layer; comparative analysis; extracellular matrix; regulatory modules; transcriptional regulation.

Figure 1

A schematic model of abscission in plants. The working model for abscission consists of largely four basic phases. First, differentiation of abscission zone (AZ); second, acquisition of the competence of the AZ to respond to abscission signals (e.g., decline in auxin); third, cell wall modifications and cell separation; and fourth, trans-differentiation of the AZ and formation of a protective layer. Based on recent transcriptome analyses (Kim et al., 2015, Kim et al., 2016), roles of transcription factors (TFs) that define the boundary layer cells in the AZs (Organ boundary TFs, Phase 2) and genes linked to the synthesis of flexible extracellular matrix (outcome of Phase 3) are implemented on the previously proposed four phases of separation processes (modified from Patterson, 2001 and Kim, 2014). In Phase 1, both tomato (Xu et al., 2016) and Arabidopsis (McKim et al., 2008) BOP TFs, and a tomato MADS-box TF of JOINTLESS (Mao et al., 2000) are known to be critical in establishment of AZ. MADS-box TFs (e.g., AGL15, AGL18, AGL24) affect timing of abscission in Arabidopsis (Phase 2). In addition, a membrane traffic regulator (NEVERSHED, NEV) and a small signaling peptide (INFLORESCENCE DEFICIENT IN ABSCISSION, IDA) are associated with cell wall disassembly and modifications in Phase 3 and Phase 4 of Arabidopsis, but their specific roles in other species have not been determined.

Figure 2

Representatives of the transcriptional modules associated with the formation of separation layer in the AZ of soybean leaf abscission. Transcription factors (TFs) that may define the separation layer in the AZs (Phase 2 possibly through Phase 3) are shown with their cognate regulators. Although Auxin response factors 2 and 7 (ARF2/7) were not identified in the transcriptome data of soybean leaf abscission, gene expression of its upstream regulator, SOLITARY ROOT (SLR), was up-regulated at the onset of abscission, Phase 2 (Table 1 in Kim et al., 2016). The representative modules constitute ANT/AIL6 and GNC/GNL TFs that are possibly regulated by ARFs and their upstream regulator of SLR, which balance between cell proliferation and differentiation in the AZ at the onset of abscission. In addition, YAB and AS1 TFs may control the expression of KNAT6 gene to regulate Phase 2 of abscission through the establishment of separation layer cells within the AZ.