Maize and Arabidopsis ARGOS Proteins Interact with Ethylene Receptor Signaling Complex, Supporting a Regulatory Role for ARGOS in Ethylene Signal Transduction

Abstract

The phytohormone ethylene regulates plant growth and development as well as plant response to environmental cues. ARGOS genes reduce plant sensitivity to ethylene when overexpressed in transgenic Arabidopsis (Arabidopsis thaliana) and maize (Zea mays). A previous genetic study suggested that the endoplasmic reticulum and Golgi-localized maize ARGOS1 targets the ethylene signal transduction components at or upstream of CONSTITUTIVE TRIPLE RESPONSE1, but the mechanism of ARGOS modulating ethylene signaling is unknown. Here, we demonstrate in Arabidopsis that ZmARGOS1, as well as the Arabidopsis ARGOS homolog ORGAN SIZE RELATED1, physically interacts with Arabidopsis REVERSION-TO-ETHYLENE SENSITIVITY1 (RTE1), an ethylene receptor interacting protein that regulates the activity of ETHYLENE RESPONSE1. The protein-protein interaction was also detected with the yeast split-ubiquitin two-hybrid system. Using the same yeast assay, we found that maize RTE1 homolog REVERSION-TO-ETHYLENE SENSITIVITY1 LIKE4 (ZmRTL4) and ZmRTL2 also interact with maize and Arabidopsis ARGOS proteins. Like AtRTE1 in Arabidopsis, ZmRTL4 and ZmRTL2 reduce ethylene responses when overexpressed in maize, indicating a similar mechanism for ARGOS regulating ethylene signaling in maize. A polypeptide fragment derived from ZmARGOS8, consisting of a Pro-rich motif flanked by two transmembrane helices that are conserved among members of the ARGOS family, can interact with AtRTE1 and maize RTL proteins in Arabidopsis. The conserved domain is necessary and sufficient to reduce ethylene sensitivity in Arabidopsis and maize. Overall, these results suggest a physical association between ARGOS and the ethylene receptor signaling complex via AtRTE1 and maize RTL proteins, supporting a role for ARGOS in regulating ethylene perception and the early steps of signal transduction in Arabidopsis and maize.

ARGOS8 variants generated by CRISPR‐Cas9 improve maize grain yield under field drought stress conditions

“…The 7‐bp duplication may be a footprint left behind by a transposon excision event (Scott et al ., ). Like the long version from B73 (Shi et al ., , ), the short version of ARGOS8 also reduces ethylene responses when overexpressed, as demonstrated in Arabidopsis transgenic plants. In the ethylene triple response assay (Bleecker et al ., ), hypocotyls and roots of the etiolated 35S: ARGOS8 Arabidopsis seedlings were longer than that in WT controls in the presence of the ethylene precursor aminocyclopropane‐1‐carboxylic acid (Figure ).…”

“…The 7-bp duplication may be a footprint left behind by a transposon excision event (Scott et al, 1996). Like the long version from B73 (Shi et al, 2015(Shi et al, , 2016, the short version of ARGOS8 also reduces ethylene responses when overexpressed, as demonstrated in Arabidopsis transgenic plants.…”

Manipulation of Auxin Response Factor 19 affects seed size in the woody perennial Jatropha curcas

“…5a), providing molecular explanations for the increased cell number in JcARF19 overexpression Jatropha seeds. We found that the expression of several genes encoding important regulators in cell differentiation and cytoskeletal dynamics have been enhanced including ARGOS46, small GTPases auxin-Rho of Plants (ROP), ROP-interactive protein RIC and receptor-like auxin-(Transmembrane Kinase) TMK4748, either in early or middle stages of seed development of J. curcas (Fig. 5b), which also explain the cell size expansion in JcARF19 ectopic expression Jatropha seeds.…”

“…Ectopic expression of ARGOS prolongs the expression of AINTEGUMENTA (ANT) and cell cycle regulator CycD3; as well as the neoplastic activity of leaf cells45. Overexpression of ARGOS genes modifies plant sensitivity to Ethylene, leading to improved drought tolerance in both Arabidopsis and maize46. The auxin-(Transmembrane Kinase) TMK sensing and auxin-Rho of Plants (ROP) signaling networks have been demonstrated to control auxin signaling pathway4748.…”

Exploring the protein–protein interaction landscape in plants

“…An additional advantage is the direct visualization of PPIs in living plant cells, thus providing information about the subcellular localization of the interaction. BiFC assays have been successfully applied in a variety of plant species, including Arabidopsis (Shi, Drummond, Wang, Archibald, & Habben, ), Nicotiana spp. (Wang, Zhang, et al, ), Allium spp.…”