Differential Expression and Internal Feedback Regulation of 1-Aminocyclopropane-1-Carboxylate Synthase, 1-Aminocyclopropane-1-Carboxylate Oxidase, and Ethylene Receptor Genes in Tomato Fruit during Development and Ripening

Abstract

We investigated the feedback regulation of ethylene biosynthesis in tomato (Lycopersicon esculentum) fruit with respect to the transition from system 1 to system 2 ethylene production. The abundance of LE-ACS2, LE-ACS4, and NR mRNAs increased in the ripening fruit concomitant with a burst in ethylene production. These increases in mRNAs with ripening were prevented to a large extent by treatment with 1-methylcyclopropene (MCP), an ethylene action inhibitor. Transcripts for the LE-ACS6 gene, which accumulated in preclimacteric fruit but not in untreated ripening fruit, did accumulate in ripening fruit treated with MCP. Treatment of young fruit with propylene prevented the accumulation of transcripts for this gene. LE-ACS1A, LE-ACS3, and TAE1 genes were expressed constitutively in the fruit throughout development and ripening irrespective of whether the fruit was treated with MCP or propylene. The transcripts for LE-ACO1 and LE-ACO4 genes already existed in preclimacteric fruit and increased greatly when ripening commenced. These increases in LE-ACO mRNA with ripening were also prevented by treatment with MCP. The results suggest that in tomato fruit the preclimacteric system 1 ethylene is possibly mediated via constitutively expressed LE-ACS1A and LE-ACS3 and negatively feedback-regulated LE-ACS6 genes with preexisting LE-ACO1 and LE-ACO4 mRNAs. At the onset of the climacteric stage, it shifts to system 2 ethylene, with a large accumulation of LE-ACS2, LE-ACS4, LE-ACO1, and LE-ACO4 mRNAs as a result of a positive feedback regulation. This transition from system 1 to system 2 ethylene production might be related to the accumulated level of NR mRNA.

The fading distinctions between classical patterns of ripening in climacteric and non-climacteric fruit and the ubiquity of ethylene—An overview

“…2). Both of these enzymes are encoded by multigene families in various plants and regulated by number of factors (Fluhr and Mattoo 1996;Lelievre et al 1997;Nakatsuka et al 1998;Barry et al 2000;Alexander and Grierson 2002). Ethylene (which is the final product of the above reactions) itself also strongly regulates the expression and activity of ACS and ACO (Lelievre et al 1997) (Fig.…”

“…It is regulated in an autoinductive manner (Fig. 2) (Oetiker and Yang 1995;Lelievre et al 1997;Nakatsuka et al 1998;Inaba 2007). This means that exogenous ethylene when applied to climacteric fruits (at mature stage) stimulates ethylene biosynthesis and generally induces rapid fruit ripening.…”

“…Now, it is only in presence of action inhibitors of ethylene that the response towards the exogenously applied ethylene or auto-inductive rise in the production of ethylene can be suppressed. Tomato possesses at least nine ACS (LeACS1A, LeACS1B, and LeACS2-8) and five ACO (LeACO1-5) genes (Zarem-binski and Theologis 1994; Barry et al 1996;Oetiker et al 1997;Nakatsuka et al 1998;Van-derHoeven et al 2002). Expression analysis studies have revealed that at least four ACS (LeACS1A, LeACS2, LeACS4, LeACS6) and three ACO (LeACO1, LeACO3, LeACO4) genes are differentially expressed in tomato fruit (Rottmann et al 1991;Nakatsuka et al 1998;Barry et al 1996Barry et al , 2000Barry and Giovannoni 2007) (Fig.…”

“…Transcripts of each of these genes were found to increase at the onset of ripening when the fruit shows transition from system 1 to system 2 of ethylene production. During ripening, LeACO1 and LeACO4 are sustained in expression, whereas the increase in expression of LeACO3 is transient (Barry et al 1996;Nakatsuka et al 1998). Studies on the regulation of ACS gene expression during fruit ripening by Barry et al (2000) and Barry and Giovannoni (2007) revealed the following information 1.…”

“…4) proposed a model to explain the transition from system 1 to system 2. Ethylene in system 1 is produced via LeACS1A and LeACS6, which are regulated by negative feedback (Nakatsuka et al 1998;Barry et al 2000;Alexander and Grierson 2002). Transition of system 1 to system 2, under natural conditions i.e., in absence of exogenous ethylene and stress, occurs mainly via limited expression of LeACS2 and LeACS4.…”