The role of ethylene in kiwifruit ripening and senescence

Purpose of review: Kiwifruit cv. ‘Hayward’ is considered a fruit with typical climacteric behaviour. Healthy fruit display climacteric behaviour at ambient temperature (~20oC) and non-climacteric behaviour at temperatures ≤10oC. However, it is extremely sensitive to ethylene action even at low temperatures. The behaviour of kiwifruit in relation to ethylene sensitivity and ethylene production is of great importance for long-term storage. This paper discusses the most recent findings concerning the role of ethylene in kiwifruit ripening and senescence. Main findings: Kiwifruit senses propylene at temperatures ranging from 15 to 34C by advancing the onset of ripening and respiration, while the ethylene burst occurs late in the ripening process. The main reason for late ethylene production is the tardy increase of 1aminocyclopropane-1-carboxylate synthase (ACCS) activity. The lag period for ethylene production decreases as temperature increases. Propylene-treated kiwifruit show reduced ethylene production at 38C and almost none at 40C. 1-Aminocyclopropane-1carboxylate oxidase (ACCO) is the first enzyme to be affected at high temperatures, followed by ACCS. Below a critical temperature range (11–14.5oC), kiwifruit lacks the ability to produce ethylene even when treated with propylene. The main reasons for the inhibition of ethylene production at 10C are primarily due to the suppression of the propylene-induced ACCS gene expression and low ACCO activity. However, wounded or Botrytis-infected fruits produce ethylene at low temperatures. A period of about 12 days at low temperature induces autocatalysis of ethylene upon re-warming of kiwifruit, while around 19 days are required when fruit is held continuously at ambient temperatures. Low temperatures slow ripening, while high temperatures block or cause abnormal ripening. Controlled atmosphere (CA) storage in 2% O2 + 5% CO2 and ultra low oxygen (ULO) storage with 1% O2 + 1% CO2 increases storage life compared with conventional storage (CS). Prolonged storage for 60 days at 0C induces ACCS activity but not that of ACCO. Upon re-warming, only fruit stored under CS and CA produced ethylene. ULO-treated fruit lost the ability to produce ethylene, mostly due to reduced ACCO activity. Directions for future research: The atypical behaviour of kiwifruit in relation to ethylene sensitivity and ethylene production at different temperatures and atmosphere compositions makes this fruit a good system for studying the ethylene biosynthetic pathway, and its regulation and action on fruit ripening and senescence. Although some efforts have been made to clarify this behaviour at the physiological level, the means by which the genes of the enzymes of ethylene biosynthesis pathway are regulated in kiwifruit need further research. . Abbreviations Correspondence to: MDC Antunes, Faculdade de Engenharia de Recursos Naturais, Universidade do Algarve, 8005139 FARO, Portugal. email: mantunes@ualg.pt Stewart Postharvest Review 2007, 2:9 Published online 01 April 2007 doi: 10.2212/spr.2007.2.9 ACCO 1-Aminocyclopropane-1-carboxylate Oxidase ACCS 1-Aminocyclopropane-1-carboxylate Synthase CA Controlled Atmosphere CS Conventional Storage ULO Ultra Low Oxygen Antunes / Stewart Postharvest Review 2007, 2:9 2 Introduction Kiwifruit (Actinidia deliciosa [A Chev.] CF Liang et AR Ferguson var. deliciosa ‘Hayward’) is one of the most important commercial fruits. The success of kiwifruit as an export crop depends on the ability to store the fruit for extended periods and to transport them over long distances. Thus, substantial research efforts have been put into its postharvest behaviour in relation to storage quality. Ripening of kiwifruit is associated with changes in respiration, texture, carbohydrates, organic acids, ethylene production and volatile compounds, which give the characteristic aroma [1*]. Kiwifruit is harvested unripe and ripening can be initiated by exposure to exogenous ethylene. Ethylene triggers rapid and dramatic changes in fruit firmness, and advances ripening and subsequent senescence [2**]. The simple gas ethylene is an endogenous regulator of a variety of stress responses and developmental processes [3]. Tucker [4] reported that the conversion of methionine to S-adenosyl-Lmethionine is constant throughout the development and ripening of the fruit. Thus, the two key control enzymes for the biosynthesis of ethylene are 1-aminocyclopropane-1carboxylate synthase (ACCS) and 1-aminocyclopropane-1carboxylate oxidase (ACCO). Tucker [4] and Atta-Aly et al. [5] reported that ACCS may be the key enzyme in the control of ethylene synthesis. Although ACCO is expressed constitutively in most tissues, its synthesis increases during ripening in some fruit [6]. Kiwifruit was believed to be a climacteric fruit whose ripening was mediated by ethylene [7]. The rate of ethylene production by mature kiwifruit at harvest is very low and increases markedly with ripening after 17±7 days [7, 8]. Ethylene plays a crucial role in ripening of kiwifruit [7], and the elucidation of the controlling factors in ethylene biosynthesis is important in prolonging the storage life and maintaining fruit quality during postharvest handling operations. Kiwifruit is highly sensitive to ethylene and concentrations as low as 5-10 ppb are sufficient to induce premature ripening and advance senescence [9]. Many factors can initiate autocatalysis of ethylene production in the harvested fruit and the control of these factors can be of significance in prolonging the storage life and keeping quality. Kiwifruit has an atypical climacteric behaviour, behaving as a climacteric fruit at ambient temperature and nonclimacteric at temperatures ≤10oC, if the fruits are healthy [2**]. This atypical behaviour in relation to ethylene sensitivity and production, and the lack of ability to produce ethylene at low temperatures makes it a good system for analysing the role of ethylene in fruit ripening. This paper discusses the main factors affecting ripening and senescence of kiwifruit, as well as technologies for increasing its storage capacity. Ethylene and fruit ripening Ethylene is a plant hormone that plays a major role in fruit ripening and advances senescence of harvested horticultural crops. It is synthesised in response to different types of stimuli such as wounding, alternate temperatures, treatments with other hormones and attack by pathogens, and by climacteric fruit during ripening [10]. During ripening, several structural and biochemical changes occur in fruit that confer specific organoleptic qualities, such as modifications in the external aspect, texture and flavour of the fruit. Several studies have already demonstrated that ethylene controls most of the events associated with the fruit ripening process [11]. Fruits can be classified into two major groups based on the intervention of ethylene during ripening. Climacteric fruit are characterised by an increased rate of respiration, which occurs at an early stage in the ripening process and is associated with a similar pattern of increased ethylene production. Nonclimacteric fruit do not show any increase in respiration and ethylene during ripening [2, 12]. The application of exogenous ethylene to non-climacteric fruit results in an increased respiration rate proportional to the concentration of ethylene applied and declines to basal levels upon removal of the ethylene. The main effect of applied ethylene, in climacteric fruit, providing fruit are mature enough, is the advancement in time of the fruit’s respiration and ethylene climacteric, whose effect is proportional to the concentration of applied ethylene [2, 13]. Once autocatalytic synthesis is triggered, ethylene levels will increase so that the final respiration rate is independent of the original exogenous ethylene concentration. Although non-climacteric fruit do not produce autocatalytic ethylene, they respond to exogenous ethylene advancing ripening in a climacteric-like manner. Ethylene in kiwifruit ripening Kiwifruit produces very small amounts of ethylene on the vine and, unlike other climacteric fruit, there is no climacteric rise of ethylene production when it is attached to the tree [1*]. However, the fruit shows a tendency to soften and soluble solids content increases on the tree, which is attributed to the conversion of starch to sugars rather than as a result of the ethylene effect [1, 14]. Kiwifruit has been classified as a climacteric fruit [7, 15, 16]. Antunes et al. [2**] confirmed that kiwifruit cv. ‘Hayward’ behaves as a climacteric fruit at ambient temperature (~20oC) by starting autocatalysis of ethylene production, respiration climacteric and ripening approximately 19 days after harvest, reaching a peak in 24 days with almost a 20,000-fold increase in the rate of ethylene production. Respiration of kiwifruit did not change significantly before autocatalysis of ethylene production, and also had a 2.5-fold increase of the rate of CO2 production, which was closely associated with the increase in ethylene production. The same authors proposed that, in the absence of external ethylene, kiwifruit belongs to the group of climacteric fruit that show the respiration rise concomitantly with the rise in ethylene production [4]. Antunes / Stewart Postharvest Review 2007, 2:9 3 It has been reported that the application of increasing concentrations of propylene to kiwifruit at 20C advanced the respiration climacteric and the autocatalysis of ethylene production [2**] (Figure 1) in the same way as for other climacteric fruit [13]. However, the application of propylene changed the climacteric pattern; the rise in respiration rate and ripeningassociated changes started after 4–10 h, while ethylene burst initiated late in the ripening process, after a lag period of 68– 80 h, just preceding fruit senescence [2, 17], making kiwifruit different from most climacteric fruit as reported by Whittaker et al. [16]. Autocata