The ARGOS gene family functions in a negative feedback loop to desensitize plants to ethylene

Abstract

BackgroundEthylene plays critical roles in plant growth and development, including the regulation of cell expansion, senescence, and the response to biotic and abiotic stresses. Elements of the initial signal transduction pathway have been determined, but we are still defining regulatory mechanisms by which the sensitivity of plants to ethylene is modulated.ResultsWe report here that members of the ARGOS gene family of Arabidopsis, previously implicated in the regulation of plant growth and biomass, function as negative feedback regulators of ethylene signaling. Expression of all four members of the ARGOS family is induced by ethylene, but this induction is blocked in ethylene-insensitive mutants. The dose dependence for ethylene induction varies among the ARGOS family members, suggesting that they could modulate responses across a range of ethylene concentrations. GFP-fusions of ARGOS and ARL localize to the endoplasmic reticulum, the same subcellular location as the ethylene receptors and other initial components of the ethylene signaling pathway. Seedlings with increased expression of ARGOS family members exhibit reduced ethylene sensitivity based on physiological and molecular responses.ConclusionsThese results support a model in which the ARGOS gene family functions as part of a negative feedback circuit to desensitize the plant to ethylene, thereby expanding the range of ethylene concentrations to which the plant can respond. These results also indicate that the effects of the ARGOS gene family on plant growth and biomass are mediated through effects on ethylene signal transduction.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0554-x) contains supplementary material, which is available to authorized users.

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

“…AtRTE1 is a constituent of the ethylene receptor signaling complex; through protein-protein interaction, AtRTE1 stabilizes or promotes the active conformation of the ethylene receptor ETR1 in Arabidopsis (Dong et al, 2008(Dong et al, , 2010. The molecular association of ARGOS proteins with AtRTE1 is consistent with their colocalization in the ER and Golgi membranes (Rai et al, 2015;Shi et al, 2015;Dong et al, 2008). This finding is also consistent with the genetic data indicating that a normal interaction between ETR1 and RTE1 is required for ZmARGOS1 to reduce ethylene sensitivity in Arabidopsis (Shi et al, 2015).…”

“…BiFC signals in hypocotyl cells were associated with small bodies and interconnected threads in the cytoplasm (Fig. 4B), consistent with the subcellular localization of the ARGOS and AtRTE1 proteins in the ER and Golgi (Dong et al, 2008;Feng et al, 2011;Rai et al, 2015;Shi et al, 2015). Strong BiFC signals were detected in the vascular tissues (Fig.…”

“…Maize and Arabidopsis ARGOS genes are negative regulators of ethylene responses recently identified using transgenic plants (Rai et al, 2015;Shi et al, 2015). ARGOS reduces plant sensitivity to ethylene when overexpressed.…”

“…Initially, it was hypothesized that ARGOS may transduce auxin signals downstream of AUXIN RESISTANCE1 to regulate cell proliferation and organ growth through AINTEGUMENTA (Hu et al, 2003). However, two recent studies have shown that ARGOS overexpressing transgenic Arabidopsis plants have reduced response to ethylene (Shi et al, 2015;Rai et al, 2015). The ER-and Golgi-localized ZmARGOS1 is suggested to negatively regulate ethylene signal transduction by affecting ethylene perception or the earlier stages of ethylene signaling (Shi et al, 2015).…”

“…Lowering plant sensitivity to ethylene by overexpressing maize ARGOS8 also enhances plant tolerance to drought and increases maize yield under water-deficit conditions (Shi et al, 2015). ZmARGOS8 is a member of the AUXIN-REGULATED GENE INVOLVED IN ORGAN SIZE (ARGOS) gene family (Hu et al, 2003), which encode integral membrane proteins localized to the endoplasmic reticulum (ER) and Golgi (Rai et al, 2015;Shi et al, 2015). Arabidopsis ARGOS and homologs from other species promote cell division and/or expansion when overexpressed, affecting organ size in transgenic plants (Hu et al, 2003(Hu et al, , 2006Wang et al, 2009;Kuluev et al, 2011;Feng et al, 2011;Guo et al, 2014).…”