SlERF52 regulates SlTIP1;1 expression to accelerate tomato pedicel abscission

Authors: WANG, RONG - Shenyang Agricultural University; LI, RUIZHEN - Shenyang Agricultural University; CHENG, LINA - Shenyang Agricultural University; WANG, XIAOYANG - Shenyang Agricultural University; FU, XIN - Shenyang Agricultural University; DONG, XIUFEN - Shenyang Agricultural University; QI, MINGFANG - Shenyang Agricultural University; Jiang, Cai-Zhong; XU, TAO - Shenyang Agricultural University; LI, TAINLAI - Shenyang Agricultural University

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/8/2021
Publication Date: 1/28/2021
Citation: Wang, R., Li, R., Cheng, L., Wang, X., Fu, X., Dong, X., Qi, M., Jiang, C., Xu, T., Li, T. 2021. SlERF52 regulates SlTIP1;1 expression to accelerate tomato pedicel abscission. Plant Physiology. 185:1829-1846. https://doi.org/10.1093/plphys/kiab026.
DOI: https://doi.org/10.1093/plphys/kiab026

Interpretive Summary: Plant organ abscission occurs during vegetative and reproductive growth and is triggered by both developmental signals and environmental stimuli. The biotic or abiotic stresses reduced the transport of the phytohormone auxin (IAA) from the distal organ (i.e., the flower and fruit) to the abscission zone (AZ). Depletion of IAA sensitizes the AZ to ethylene. Although much research has supported the central role of auxin and ethylene in mediating abscission, little is known about the factors involved in the shift from the auxin-sensitive stage to the ethylene-sensitive stage. Oxidative stress and related stress-inducing agents have been noted for their role in auxin antagonism such as inhibiting root elongation and limiting cotyledon and leaf expansion. Reactive oxygen species (ROS) may affect auxin response at multiple levels. Firstly, oxidative stress-induced upregulation of peroxidases (Prxs) might perturb auxin homeostasis due to their auxin oxidase activity. Secondly, H2O2 could trigger cellular mitogen-activated protein kinase (MAPK) pathways and repress auxin dependent signaling. Thirdly, ROS might enhance AUX/IAA stability and, consequently, suppress auxin response factor (ARF) activity. Interestingly, peroxidases, MAPK pathways, and ARF are all reported to be involved in abscission. ROS production occurs mostly in the apoplast and is catalyzed by NADPH-dependent oxidases (RBOHs), which are essential for normal growth and development. Furthermore, ROS are also known to be involved in ethylene biosynthesis and signaling. During leaf pulvinus abscission induced via water-deficit stress in Cassava, the enhanced proline and polyamines induced ROS production in the AZs, thereby contributing to ethylene production. The abscission of a leaves, flowers, or fruits involves degradation of the primary cell wall or middle lamella pectin of AZ tissues by polygalacturonases and xyloglucan endotransglucosylases/hydrolases. A reduction in cell wall rigidity in AZ cells allows for their expansion, which provides the force for the abscission of the distal organ. Aquaporins (AQPs) physically interact with themselves or other AQP monomers to assemble into homo- and heterotetrameric units, which act as functional channels for water, urea, glycerol, H2O2, and CO2 transport across cell membranes in all living cells. The influx of H2O2, which results in a transient rise in cellular H2O2 levels, can trigger redox-sensitive transcription factors (TFs) and MAPK pathways to mediate cell hormone signaling and metabolism. In addition, there is considerable evidence that AQPs are involved in controlling cell expansion. Disruption of the undifferentiated cells in a meristem in order to initiate differentiation, such as expansion and separation of meristem-like AZ cells, requires molecular mechanisms to gate water and H2O2 transport; however, the underlying mechanisms are unknown. Here, we tested the hypothesis that AQP-mediated H2O2 and H2O transportation is important for tomato flower pedicel abscission; further, we described the characterization of the associated ethylene and auxin regulatory frameworks in cell separation. We found that the expression of the tonoplast intrinsic proteins (TIPs) which belong to the aquaporin (AQP) family in the AZ was important for tomato pedicel abscission. Knockout of SlTIP1;1 resulted in delayed abscission, whereas the overexpression of SlTIP1;1 accelerated abscission. Further analysis indicated that SlTIP1;1 mediated abscission via gating of cytoplasmic H2O2 concentrations and osmotic water permeability (Pf). The elevated cytoplasmic levels of H2O2 caused a suppressed auxin signal in the early abscission stage and enhanced ethylene production during abscission. Furthermore, we found that increasing Pf was required to enhance the turgor pressure to supply the break force for AZ cell separation. Moreover, we observed t

Technical Abstract: The abscission of plant organs is induced by developmental signals and a variety of environmental stimuli, and involves multiple regulatory networks, e.g., biotic or abiotic stress-impaired auxin flux in the abscission zone (AZ). Depletion of IAA activates abscission zone (AZ) ethylene production and signals the acceleration of abscission, a process that is known to also require hydrogen peroxide (H2O2). However, the interaction between these networks and the underlying mechanisms that control abscission are not well understood. Here, we found that the expression of the tonoplast intrinsic proteins (TIPs) which belong to the aquaporin (AQP) family in the AZ was important for tomato pedicel abscission. Liquid chromatography–mass spectrometry (LC-MS)/MS and in situ hybridization revealed that SlTIP1;1 was most abundant and specifically present in the tomato pedicel AZ. The SlTIP1;1 localized in the plasma membrane and tonoplast. Knockout of SlTIP1;1 resulted in delayed abscission, whereas the overexpression of SlTIP1;1 accelerated abscission. Further analysis indicated that SlTIP1;1 mediated abscission via gating of cytoplasmic H2O2 concentrations and osmotic water permeability (Pf). The elevated cytoplasmic levels of H2O2 caused a suppressed auxin signal in the early abscission stage and enhanced ethylene production during abscission. Furthermore, we found that increasing Pf was required to enhance the turgor pressure to supply the break force for AZ cell separation. Moreover, we observed that SlERF52 bound directly to the SlTIP1;1 promoter to regulate its expression, demonstrating a positive loop, as follows—cytoplasmic H2O2 activates ethylene production, which then activates SlERF52; this, in turn, induces SlTIP1;1, which leads to elevated levels of cytoplasmic H2O2 and water influx. This observation significantly advances our knowledge regarding the regulatory aspects of abscission in tomato flowers, which are likely relevant to the abscission processes of plants in general.