Abstract

Ethylene has long been known to be a critical signal controlling the ripening of climacteric fruits; however, the signaling mechanism underlying ethylene production during fruit development is unknown. Here, we report that two FERONIA-like receptor kinases (FERLs) regulate fruit ripening by modulating ethylene production in the climacteric fruit, apple (Malus×domestica). Bioinformatic analysis indicated that the apple genome contains 14 members of the FER family (MdFERL1–17), of these 17 FERLs, MdFERL6 was expressed at the highest level in fruit. Heterologous expression of MdFERL6 or MdFERL1, the apple homolog of Arabidopsis FER, in another climacteric fruit, tomato (Solanum lycopersicum) fruit delayed ripening and suppressed ethylene production. Overexpression and antisense expression of MdFERL6 in apple fruit calli inhibited and promoted ethylene production, respectively. Additionally, virus-induced gene silencing (VIGS) of SlFERL1, the tomato homolog of FER, promoted tomato fruit ripening and ethylene production. Both MdFERL6 and MdFERL1 physically interacted with MdSAMS (S-adenosylmethionine synthase), a key enzyme in the ethylene biosynthesis pathway. MdFERL6 was expressed at high levels during early fruit development, but dramatically declined when fruit ripening commenced, implying that MdFERL6 might limit ethylene production prior to fruit development and the ethylene production burst during fruit ripening. These results indicate that FERLs regulate apple and tomato fruit ripening, shedding light on the molecular mechanisms underlying ripening in climacteric fruit.

Highlights

  • Fleshy fruits are physiologically classified as climacteric or non-climacteric

  • Since a dramatic increase in ethylene biosynthesis is a critical signal controlling apple and tomato fruit development and ripening, we examined the effects of MdFERL1 and MdFERL6 on ethylene production

  • To further reveal how MdFERL6 regulates fruit ripening and to identify its precise role in ethylene-mediated fruit ripening, we examined the expression of various genes involved in the regulation of ethylene biosynthesis, ethylene signaling transduction, and fruit ripening in apple fruit calli in which the levels of MdFERL6 had been manipulated

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Summary

Introduction

Fleshy fruits are physiologically classified as climacteric or non-climacteric. Climacteric fruits exhibit an increase in respiration at the onset of ripening (Nitsch, 1953; Coombe, 1976; Brady, 1987). Studies of the mechanisms regulating fruit ripening began in the 1920s (Brady, 1987) and a major focus has been identifying the critical internal factors or signals governing this process. Ethylene has long been known to be a critical signal controlling the ripening of climacteric fruit (Biale, 1964; Burg and Burg, 1965; Alexander and Grierson, 2002), which exhibit a large increase in ethylene production at the onset of ripening. Exposure to exogenous ethylene can initiate the ripening of climacteric fruits (Seymour et al, 2013), and its effect is so great that limiting ethylene production in fruits or ethylene exposure for harvested fruit has become a major concern in the commercial cultivation industry (Brady, 1987).

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