FERONIA/FER-like receptor kinases integrate and modulate multiple signaling pathways in fruit development and ripening.

Ripening of fleshy fruits is a complex process that involves dramatic changes in color, texture, flavor, and aroma, which is essentially regulated by multiple hormone signals. Although the metabolic mechanisms for the regulation of fruit development and ripening have been studied extensively, little is known about the signaling mechanisms underlying this process. FERONIA has been increasingly suggested to be implicated in multiple signaling pathways. In a recent publication, we showed that a FERONIA/FER -like receptor kinase, FaMRLK47, playes an important role in the regulation of fruit ripening in strawberry (Fragaria × ananassa, a typical non-climacteric fruit) fruit. Over-expression orRNAi-mediated down regulation of FaMRLK47 caused a delay or acceleration, respectively, of fruit ripening progress. Meanwhile, overexpression orRNAi-mediated down regulation of FaMRLK47 caused a decrease or increase, respectively, in the ABA-induced expression of a series of ripening-related genes. More recently, we also found that MdFERL1, a FERONIA/FER-like receptor kinase in tomato plant, was implicated in the regulation of tomato fruit ripening via modulating ethylene production. We propose that FERONIA/FER-like receptor kinases may function to regulate fruit development and ripening via integrate multiple signaling pathways in both climacteric and non-climacteric fruits.

Fleshy fruits are physiologically classified as climacteric or non-climacteric. For both climacteric and non-climacteric fruits, fruit development and ripening is a complex process that involves dramatic changes in a series of physiologic and biochemical metabolisms, such as sugar/acid metabolism, cell wall metabolism, color, flavor, etc. Among these changes, in our opinion, the change in cell wall metabolism may be the most important event, since a change in fruit firmness as determined by cell wall metabolism is tightly associated with all other ripening-related events. Therefore, we are particularly interested in signaling mechanisms associated with the regulation of cell wall metabolism or cell metabolism-initiated signaling events. Recently, plasma membrane-anchored receptor-like kinases (RLKs) have attracted much attention due to their roles in sensing cell wall integrity. Malectin is a membrane-anchored protein of the endoplasmic reticulum. It can recognize and bind to oligosachrides. The Arabidopsis genome contains 17 members of Malectin-domain containing RLKs, in which FERONIA /FER was first identified and functionally characterized for its role in fertilization in Arabidopsis. We searched Malectin-domain containing RLKs in the genome of strawberry, a non-climacteric fruit, and identified 62 members of the Malectin-domain containing RLKs, designated as FaMRLK1 to FaMRLK62. In recently published paper, we reported that FaMRLK47, a homolog of FERONIA /FER, was implicated in the regulation of strawberry fruit ripening. Manipulation of FaMRLK47 expression could modulate strawberry fruit ripening. FaMRLK47 was shown to physically interact with ABi1 thereby modulating ABA signaling during strawberry fruit development and ripening. Notably, FaMRLK47 was found to play a particular role in the regulation of sucrose accumulation, implying that FaMRLK47 was implicated in the signaling pathway associated with sugar metabolism. More recently, we found a FERONIA /FER-like RLK, MdFERL1, functioned to regulate ethylene production therefore playing a critical role in the regulation of tomato fruit ripening (unpublished). Collectively, our researches suggested that FERONIA /FER-like RLKs might function to regulate fruit development and ripening in both climacteric and non-climacteric fruits.

Although ethylene has long been known as a critical signal controlling ripening of climacteric fruits, the regulatory mechanisms for non-climacteric fruit development and ripening has been largely unknown. Previous studies reported that auxin (IAA) was a key regulator of fruit ripening of strawberry. In recent years, a crucial role of ABA in strawberry fruit ripening has gain particular interests and attention. Strikingly, besides the potential roles of IAA and ABA, it has been increasingly demonstratedthat strawberry fruit development and ripening is regulated by multiple phyto-hormones, such as jasmonic acid (JA), sucrose, and so on. Even in climacteric fruit, it has been suggested that ABA may play a crucial role in the regulation of fruit growth and development. Collectively, for both climacteric and non-climacteric fruits, fruit development and ripening is essentially controlled by an integrated action of multiple signaling pathways.

Since FERONIA /FER was functionally identified for its role in fertilization in Arabidopsis, the signaling mechanisms of FERONIA /FER has attracted particular interests from plant scientists. FERONIA/FER was reported to be a key modulator of brassinosteroids and ethylene responsiveness in Arabidopsis hypocotyls. More recently, Stegmann et al. reported that FER acted as a scaffold that modulated the receptor kinase complex assembly of EFR (immune receptor kinases EF-TU RECEPTOR), FLS2 (FLAGELLIN-SENSING 2) and BAK1 (the co-receptor of BR receptor, BRASSINOSTEROID INSENSITIVE 1). Yu et al. (2012) reported that FERONIA functioned to suppress ABA signaling in Arabidopsis by activating ABI2 phosphatase. Similarly, the FERONIA/FER-like kinase, FaMRLK47, was demonstrated to be capable of physically interacting with FaABI1. Given that fleshy fruit development and ripening is regulated by an integration of multiple hormones and that FERONIA/FER functions to modulate the cross-talking signaling of the hormones, we propose that FERONIA/FER-like kinases may be the key regulators of fruit development and ripening via its integration of hormone signaling in both climacteric and non-climateric fruits (Fig 1).

Figure 1.

Diagram of integration and modulation of multiple signaling pathways via FERONIA-like protein kinase. FERONIA-like protein kinases likely act to integrate multiple signaling pathways implicated in the regulation of fruit ripening and quality formation, especially the ethylene, ABA, and BR signaling pathways; thereby modulating the hormone sensitivity. A change in wall metabolism is believed to be a critical event during fruit ripening and quality formation, and as malectin domain containing protein kinases, FERONIA-like protein kinases likely act to sense and mediate cell wall integrity -associated signaling (CWI). Accordingly, besides the integration of multiple hormones signaling, FERONIA-like protein kinases can be also proposed to integrate signaling pathways between hormone and (CWI).