Ethylene biosynthesis and signal transduction during ripening and softening in non-climacteric fruits: an overview

Abstract

In recent years, the ethylene-mediated ripening and softening of non-climacteric fruits have been widely mentioned. In this paper, recent research into the ethylene-mediated ripening and softening of non-climacteric fruits is summarized, including the involvement of ethylene biosynthesis and signal transduction. In addition, detailed studies on how ethylene interacts with other hormones to regulate the ripening and softening of non-climacteric fruits are also reviewed. These findings reveal that many regulators of ethylene biosynthesis and signal transduction are linked with the ripening and softening of non-climacteric fruits. Meanwhile, the perspectives of future research on the regulation of ethylene in non-climacteric fruit are also proposed. The overview of the progress of ethylene on the ripening and softening of non-climacteric fruit will aid in the identification and characterization of key genes associated with ethylene perception and signal transduction during non-climacteric fruit ripening and softening.

Keywords: ethylene biosynthesis; ethylene signal transduction; non-climacteric fruit; ripening; softening.

Figure 1

Ethylene biosynthetic pathway. Methionine serves as the precursor of ethylene, and it is catalyzed by SAM synthetase to format S-AdoMet (SAM) at the expense of one molecule of ATP per molecule (Bürstenbinder et al., 2007). Subsequently, SAM is metabolized into 1-aminocyclopropane-1-carboxylic acid (ACC) by ACC synthase (ACS) (Pattyn et al., 2021). Additionally, SAM can be diverted to methylthioadenosine (MTA), which can be recycled back to methionine via α-keto-γ-methylthio-butyric acid (KMB) through the Yang cycle (Bürstenbinder et al., 2007). Finally, the catalytic action of ACC oxidase (ACO) converts ACC into ethylene, initiating downstream ethylene sensing and signaling (Yoon and Kieber, 2013). Furthermore, various transcription factors, ubiquitin ligases, regulators, and environmental stresses are involved in regulating the expression of ACS and ACO expression (Lyzenga and Stone, 2012; Pattyn et al., 2021).

Figure 2

Ethylene signaling transduction pathway. Model of the ethylene signal transduction. Under the mediation of RAN1, which transports copper to ethylene receptors, the presence of ethylene causes the loss of phosphorylation (P) of ethylene receptors (ETRs) at the membrane level (ER) (Binder et al., 2010); following this, the receptor–CTR1 complex is inactivated, the delivery of phosphate groups from CTR1 to EIN2 becomes incapable, and then EIN2 is cleaved and partly enters the nucleus to activate EIN3/EIL1 (Wen et al., 2012). Subsequently, EIN3/EIL1 binds to a conserved motif known as the EIN3 binding site (EBS), which is present within the promoters of ERF1, and this ultimately activates ERF1, which binds to the GCC box in the promoters of many ethylene-inducible, ripening-related genes (Fujimoto et al., 2000). Protein degradation of EIN3/EIL1 is regulated by EBF1/2 via the ubiquitin/26S proteasome pathway, and EIN5/XRN4 5′–3′ exoribonuclease mediated control of EBF1/2 mRNA levels (Potuschak et al., 2003; Olmedo et al., 2006).

Figure 3

Comparative ethylene evolution in representative climacteric and non-climacteric fruit models. (A) Ethylene evolution in the development of the tomato from the immature green to the red ripe stage (Zhang et al., 2009). IG, immature green (20 days after anthesis); MG, mature green (40 days after anthesis); B1, breaker (44 days after anthesis); B2, breaker (45 days after anthesis); T, turning (47 days after anthesis); P, pink (50 days after anthesis); MR, mature red (53 days after anthesis). (B) Ethylene evolution in the development of ‘Camarosa’ strawberry fruit during seven stages (Sun et al., 2013), SG (small green), BG (big green), DG (degreening), Wt (white), IR (initially red), PR (partially red), and FR (fully red), which occurred for 7, 15, 20, 23, 27, 31, and 35 days, respectively, after anthesis. (C) Ethylene evolution in the development of ‘Moldova’ grape fruit during contentious growth points of berry ripening (Xu et al., 2018). (D) Ethylene evolution in the development of attached ‘Valencia’ orange fruit during two growth stages (Katz et al., 2004). Stage I, the cell division stage, starts immediately after fruit set and lasts for approximately 90 days after full bloom (DAFB). Stage II, the cell expansion stage, during which fruit growth continues, mostly by cell expansion, extends until 150–180 DAFB.

Figure 4

Phytohormone crosstalk between ethylene and other hormones in grape, strawberry, and citrus fruits. Note: The hormones and their related components involved in fruit ripening shown in the figure are abscisic acid (ABA), auxin (IAA),1-naphthaleneacetic acid (NAA), ethylene (C₂H₄), brassinosteroids (BRs), gibberellins (GAs), melatonin (MT) and jasmonates (JAs), tryptophan aminotransferase (TAR), auxin response factor (ARF), an auxin/indole-3-acetic acid (Aux/IAA) protein (IAA9), 9-cis-epoxycarotenoid dioxygenase 1 (NCED1), 1-aminocyclopropane-1-carboxylic acid synthase (ACS), and 1-aminocyclopropane-1-carboxylic acid oxidase (ACO). JA, ABA, BRs, and MT in the red fond have a positive effect on fruit ripening (Davies et al., 2006; Sun et al., 2010; Liu et al., 2011; Concha et al., 2013; Delgado et al., 2018; Garrido-Bigotes et al., 2018; Mansouri et al., 2021; Xia et al., 2021); Gas and IAA/NAA in the green fond had a negative effect on fruit ripening (Böttcher et al., 2011; Liu et al., 2011; Ma et al., 2021a, b; Tyagi et al., 2022); and jasmonate-activated fruit ripening is possibly associated with the stimulation of ethylene biosynthesis by an increase in ACO and ACS activities (Mukkun and Singh, 2009), while ABA, BRs, and MT can also stimulate ethylene production (Jiang and Joyce, 2003; Xu et al., 2018). C₂H₄ and IAA/NAA have a mutually reinforcing relationship. NAA can strongly upregulate ACS6 and ACO2 to improve ethylene biosynthesis (Ziliotto et al., 2012). In turn, the elevated concentrations of ethylene may lead to the induction of TAR expression, thus increasing the production of IAA (Böttcher et al., 2013). Ethylene also induces the transcription of VvNCED1 and the synthesis of ABA (Sun et al., 2010). The crosstalk between JAs and ABA, as well as GAs and IAA/NAA, also exists in non-climacteric fruit (Jung et al., 2014; Wang et al., 2015).