Differential Control of Ethylene Responses byGREEN-RIPEandGREEN-RIPE LIKE1Provides Evidence for Distinct Ethylene Signaling Modules in Tomato    

Abstract

The factors that mediate specific responses to the plant hormone ethylene are not fully defined. In particular, it is not known how signaling at the receptor complex can control distinct subsets of ethylene responses. Mutations at the Green-ripe (Gr) and reversion to ethylene sensitivity1 (rte1) loci, which encode homologous proteins of unknown function, influence ethylene responses in tomato (Solanum lycopersicum) and Arabidopsis (Arabidopsis thaliana), respectively. In Arabidopsis, AtRTE1 is required for function of the ETR1 ethylene receptor and acts predominantly through this receptor via direct protein-protein interaction. While most eudicot families including the Brassicaceae possess a single gene that is closely related to AtRTE1, we report that members of the Solanaceae family contain two phylogenetically distinct genes defined by GR and GREEN-RIPE LIKE1 (GRL1), creating the possibility of subfunctionalization. We also show that SlGR and SlGRL1 are differentially expressed in tomato tissues and encode proteins predominantly localized to the Golgi. A combination of overexpression in tomato and complementation of the rte1-3 mutant allele indicates that SlGR and SlGRL1 influence distinct but overlapping ethylene responses. Overexpression of SlGRL1 in the Gr mutant background provides evidence for the existence of different ethylene signaling modules in tomato that are influenced by GR, GRL1, or both. In addition, overexpression of AtRTE1 in tomato leads to reduced ethylene responsiveness in a subset of tissues but does not mimic the Gr mutant phenotype. Together, these data reveal species-specific heterogeneity in the control of ethylene responses mediated by members of the GR/RTE1 family.The gaseous plant hormone ethylene influences many aspects of plant development and mediates responses to biotic and abiotic stresses (Abeles et al., 1992). Impaired ethylene biosynthesis and responsiveness can lead to altered cell expansion, cell elongation, senescence, abscission, cell death, fruit ripening, root hair formation, lateral root development, nodulation, and sex determination (Bleecker et al

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

“…Previously, phylogenetic analysis suggested that members of the RTE1 gene family from different species form two clades, AtRTE1/SlGR and AtRTH/SIGRL2 (Barry and Giovannoni, 2006;Ma et al, 2012). The AtRTE1/SlGR clade consists of the RTE1 homologs that regulate ethylene signal transduction, such as Arabidopsis RTE1, tomato GR and GRL1, and rice RTH1 (Zhang et al, 2012).…”

“…The AtRTE1/SlGR clade consists of the RTE1 homologs that regulate ethylene signal transduction, such as Arabidopsis RTE1, tomato GR and GRL1, and rice RTH1 (Zhang et al, 2012). The AtRTH/ SIGRL2 clade includes AtRTH and SlGRL2, which have no apparent role in ethylene signaling (Resnick et al, 2006;Ma et al, 2012); petunia PhGRL2, which was proposed to regulate ethylene biosynthesis (Tan et al, 2014), and rice RTH3, whose function is unknown (Zhang et al, 2012). ZmRTL4 is more closely related to the AtRTH/SlGRL2 clade, while ZmRTL2 apparently belongs to the AtRTE1/SlGR clade (Supplemental Fig.…”

“…S3) and their functions are unknown. Phylogenetic analysis indicate that ZmRTL1, ZmRTL2, and ZmRTL3 belong to the AtRTE1/SlGR clade of the RTE1 gene family (Barry and Giovannoni, 2006;Ma et al, 2012) while ZmRTL4 is more closely related to the AtRTH/SlGRL2 clade (Supplemental Fig. S4) and therefore, we elected to determine the function of ZmRTL2 and ZmRTL4.…”

“…Transgenic rice (Oryza sativa) plants overexpressing rice REVERSION-TO-ETHYLENE SENSITIVITY1 HOMOLOG1 also showed reduced ethylene responsiveness across a range of biological processes, such as leaf senescence, seedling leaf elongation and development, and coleoptile elongation as well as adventitious root development (Zhang et al, 2012). In the RTE1 gene family, some members, for example, Arabidopsis REVERSION-TO-ETHYLENE SENSITIVITY1 HOMOLOG (RTH) and tomato GRL2, do not appear to play the same role as RTE1 in ethylene signaling (Resnick et al, 2006;Ma et al, 2012). Rice RTH2 and RTH3 were not able to complement the Arabidopsis rte1-2 mutant when their overexpression was driven by the cauliflower mosaic virus 35S promoter (Zhang et al, 2012), but whether they modulate ethylene sensitivity in rice was not determined.…”

“…Arabidopsis RTE1 reduces ethylene responsiveness in an ETR1-dependent manner when overexpressed in Arabidopsis (Resnick et al, 2006;Zhou et al, 2007). Similarly, overexpression of RTE1 tomato (Solanum lycopersicum) homologs GREEN-RIPE (GR) and GREEN-RIPE LIKE1 (GRL1), as well as ectopic expression of the dominant gain-of-function mutant allele Green-ripe (Gr), decreases ethylene response in tomato plants, as shown in seedlings, fruit, abscission zones, and petioles (Barry and Giovannoni, 2006;Ma et al, 2012). Transgenic rice (Oryza sativa) plants overexpressing rice REVERSION-TO-ETHYLENE SENSITIVITY1 HOMOLOG1 also showed reduced ethylene responsiveness across a range of biological processes, such as leaf senescence, seedling leaf elongation and development, and coleoptile elongation as well as adventitious root development (Zhang et al, 2012).…”