Abstract
Apple (Malus×domestica Borkh) fruits are stored for long periods of time at low temperatures (1 °C) leading to the occurrence of physiological disorders. 'Superficial scald' of Granny Smith apples, an economically important ethylene-dependent disorder, was used as a model to study relationships among ethylene action, the regulation of the ROP-GAP rheostat, and maintenance of H2O2 homeostasis in fruits during prolonged cold exposure. The ROP-GAP rheostat is a key module for adaptation to low oxygen in Arabidopsis through Respiratory Burst NADPH Oxidase Homologs (RBOH)-mediated and ROP GTPase-dependent regulation of reactive oxygen species (ROS) homeostasis. Here, it was shown that the transcriptional expression of several components of the apple ROP-GAP machinery, including genes encoding RBOHs, ROPs, and their ancillary proteins ROP-GEFs and ROP-GAPs, is coordinately and negatively regulated by ethylene in conjunction with the progressive impairment of apoplastic H2O2 homeostatic levels. RNA sequencing analyses showed that several components of the known ROP- and ROS-associated transcriptional networks are regulated along with the ROP-GAP rheostat in response to ethylene perception. These findings may extend the role of the ROP-GAP rheostat beyond hypoxic responses and suggest that it may be a functional regulatory node involved in the integration of ethylene and ROS signalling pathways in abiotic stress.
Highlights
Cold stress represents a major environmental abiotic challenge for plants and results in severe crop losses, both in the field and after harvesting (Mahajan and Tuteja, 2005)
In order to identify the genetic components of the apple ROP-GAP rheostat, sequences that encode ROPs in A. thaliana (Vernoud et al, 2003; Molendijk et al, 2004), their positive and negative regulatory proteins ROP-GEFs (GDP/GTP exchange factors) (Berken et al, 2005; Gu et al, 2006) and ROP-GAPs (GTPase activating proteins) (Wu et al, 2000), respectively, and ROP-GDIs (GDP dissociation inhibitors, sequestering ROPs in their inactive state) (Berken and Wittinghofer, 2008), together with Respiratory Burst NADPH Oxidase Homologs (RBOH) (Torres et al, 1998) and PLDα (Qin and Wang, 2002), the latter responsible for the generation of phosphatidic acids regulating RBOH activity (Zhang et al, 2009), were used as queries to search the Rosaceae database
This study showed that an extended apple ROP-GAP rheostat may be a highly regulated and important signalling hub required for adaptation to cold stress, through the control of apoplastic H2O2 levels
Summary
Cold stress represents a major environmental abiotic challenge for plants and results in severe crop losses, both in the field and after harvesting (Mahajan and Tuteja, 2005). ROPs are molecular switches that, in their GTP-bound active state, positively regulate RBOH activity and superoxide/H2O2 production This reaction is negatively regulated by ROP GTPase activating proteins (ROP-GAPs), which inactivate ROPs by enhancing their intrinsic GTPase activity and are transcriptionally induced when H2O2 levels rise over a certain threshold, providing a rheostatic negative-feedback regulatory control (Baxter-Burrell et al, 2002). Based on these data, it was hypothesized that the ROP-GAP rheostat may be a generally conserved regulatory hub for the adaptation of plants to different abiotic stresses. This hypothesis has not been tested further and no data are available to suggest any involvement of ROP proteins in the regulation of cold-stress responses nor any role for ethylene in the regulation of the ROP-GAP rheostat in abiotic stresses in general
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