Programmed Cell Death and Aerenchyma Formation in Water-Logged Sunflower Stems and Its Promotion by Ethylene and ROS

Abstract

Previous studies have shown that waterlogging/ hypoxic conditions induce aerenchyma formation to facilitate gas exchange. Ethylene (ET) and reactive oxygen species (ROS), as regulatory signals, might also be involved in these adaptive responses. However, the interrelationships between these signals have seldom been reported. Herein, we showed that programmed cell death (PCD) was involved in aerenchyma formation in the stem of Helianthus annuus. Lysigenous aerenchyma formation in the stem was induced through waterlogging (WA), ethylene and ROS. Pre-treatment with the NADPH oxidase inhibitor diphenyleneiodonium (DPI) partially suppressed aerenchyma formation in the seedlings after treatment with WA, ET and 3-amino-1, 2, 4-triazole (AT, catalase inhibitor). In addition, pre-treatment with the ethylene perception inhibitor 1-methylcyclopropene (1-MCP) partially suppressed aerenchyma formation induced through WA and ET in the seedlings, but barely inhibited aerenchyma formation induced through ROS. These results revealed that ethylene-mediated ROS signaling plays a role in aerenchyma formation, and there is a causal and interdependent relationship during WA, ET and ROS in PCD, which regulates signal networks in the stem of H. annuus.

Internal aeration and respiration of submerged tomato hypocotyls are enhanced by ethylene‐mediated aerenchyma formation and hypertrophy

“…PCD triggered by environmental or developmental signals is known to be mediated by ethylene (Lombardi et al , Petrov et al ). Similar to other species (Gunawardena et al , Joshi and Kumar , Ni et al ), aerenchyma formation in tomato is achieved via ethylene‐mediated PCD of subepidermal and cortical cells (Figs and A–C). In this sense, TUNEL staining was observed in flooded stems unless ethylene action is blocked (Fig.…”

“…ROS involvement in aerenchyma formation has been widely described in rice and recently in sunflower ( Parlanti et al , Steffens et al , Yamauchi et al , Ni et al ). In tomato, we detected a transient presence of H 2 O 2 in submerged tissues suggesting its role as a signal molecule (Fig.…”

“…The accumulation of ethylene up to physiologically saturating levels frequently induces responses in submerged organs (Sasidharan and Voesenek ). For instance, ethylene has been considered the major player that triggers programmed cell death (PCD) during aerenchyma formation through the action of reactive oxygen species (ROS) (Drew et al , Mergemann and Sauter , Visser and Voesenek , Ni et al ). In rice, ethylene participates in the modulation of NADPH oxidase genes (RBOH, Respiratory Burst Oxidase Homolog) involved in ROS production (Yamauchi et al ).…”

Modulatory Role of Reactive Oxygen Species in Root Development in Model Plant of Arabidopsis thaliana

“…However, aerenchyma formation requires Programmed Cell Death (PCD) in the root cortex ( Drew et al., 2000 ; Bartoli et al., 2015 ; Fujimoto et al., 2018 ; Guan et al., 2019 ). Interestingly, both the aerenchyma formation and PCD in waterlogged sunflower stems are promoted by ethylene and ROS ( Steffens et al., 2011 ; Petrov et al., 2015 ; Ni et al., 2019 ). In the root, during lysigenous aerenchyma formation under oxygen-deficient conditions, the precise balancing of ROS production and scavenging serves a crucial role ( Paradiso et al., 2016 ; Yamauchi et al., 2017a ; Yamauchi et al., 2017b ).…”

Enhancement of plasmalemmasome formation in spinach mesophyll cells

“…In Chara cells the basic pH of the medium increased the frequency of charasomes analogous to PLSs (Lucas, Keifer, and Pesacreta 1986). In Helianthus stem a few days of waterlogging induced PLS formation (Ni et al 2019). In Rubia suspension culture cells different fungal elicitors enhanced the occurrence of PLSs (Bóka, Jakab, and Király 2002).…”