Characterization of Transcriptome Dynamics during Early Fruit Development in Olive (Olea europaea L.)

Abstract

In the olive (Olea europaea L.), an economically leading oil crop worldwide, fruit size and yield are determined by the early stages of fruit development. However, few detailed analyses of this stage of fruit development are available. This study offers an extensive characterization of the various processes involved in early olive fruit growth (cell division, cell cycle regulation, and cell expansion). For this, cytological, hormonal, and transcriptional changes characterizing the phases of early fruit development were analyzed in olive fruit of the cv. ‘Picual’. First, the surface area and mitotic activity (by flow cytometry) of fruit cells were investigated during early olive fruit development, from 0 to 42 days post-anthesis (DPA). The results demonstrate that the cell division phase extends up to 21 DPA, during which the maximal proportion of 4C cells in olive fruits was reached at 14 DPA, indicating that intensive cell division was activated in olive fruits at that time. Subsequently, fruit cell expansion lasted as long as 3 weeks more before endocarp lignification. Finally, the molecular mechanisms controlling the early fruit development were investigated by analyzing the transcriptome of olive flowers at anthesis (fruit set) as well as olive fruits at 14 DPA (cell division phase) and at 28 DPA (cell expansion phase). Sequential induction of the cell cycle regulating genes is associated with the upregulation of genes involved in cell wall remodeling and ion fluxes, and with a shift in plant hormone metabolism and signaling genes during early olive fruit development. This occurs together with transcriptional activity of subtilisin-like protease proteins together with transcription factors potentially involved in early fruit growth signaling. This gene expression profile, together with hormonal regulators, offers new insights for understanding the processes that regulate cell division and expansion, and ultimately fruit yield and olive size.

Hormonal Content and Gene Expression during Olive Fruit Growth and Ripening

“…Thus, unlike in small sized fruit, GA 1 levels rose in the large sized fruit during growth by cell expansion after endocarp lignification, indicating that the presence of GA 1 in 'Picual' fruit could be correlated to the fruit size of this cultivar in comparison to the 'Arbequina' cultivar. These results agree with the established notion that GA participates mainly in the cell expansion process in olive fruit [20]. In the 'Picual' cultivar, the level of GA 1 was high at flowering and then fell during the cell division phase, while the levels of GA 1 and GA 4 peaked during the cell expansion phase of early 'Picual' fruit development, in agreement with findings elsewhere for the upregulated expression patterns of OeGA3ox, coding GA 3-oxidase (GA3ox), and OeGID2, coding GA receptor [20].…”

“…This period can oscillate between 5 and 9 months, from anthesis to the fully ripe fruit stage, depending on olive cultivar, climatic conditions, and agricultural practices [1,7,10,[14][15][16][17]. The successful fertilization of the ovule is followed by cell division and expansion, resulting in the rapid growth of the olive fruit [18][19][20]. Subsequently, early fruit growth is due solely to cell expansion until endocarp lignification about 50 days following ovary fertilization [20].…”

“…The successful fertilization of the ovule is followed by cell division and expansion, resulting in the rapid growth of the olive fruit [18][19][20]. Subsequently, early fruit growth is due solely to cell expansion until endocarp lignification about 50 days following ovary fertilization [20]. Next, the late growth of olive fruit comprises mainly pulp cell expansion, which is responsible for the maximum fruit size, and oil accumulation [14,15].…”

“…In this context, the preharvest application of plant hormones to different olive cultivars has recently been reported to increase fruit size and to boost the content of bioactive components and antioxidants, among other components, and thus to preserve the oxidative stability of olive fruits during storage [72][73][74][75][76]. Recently, it has been demonstrated that CKs and SA correlate positively with cell division during early olive fruit development, while GA, auxin, and ABA have higher relative importance in the period when olive fruit growth depends mainly on cell expansion [20].…”

Parthenocarpy-related genes induced by naphthalene acetic acid in oil palm interspecific O × G [Elaeis oleifera (Kunth) Cortés × Elaeis guineensis Jacq.] hybrids

“…On the other hand, the TF probable WRKY transcription factor 72 (WRKY72), ethylene-responsive transcription factor 71 (ERF071), NAC domain-containing protein 58 (NAC58), and transcription factor bHLH162 were found over-expressed as well. Among them, the TF WRKY72 has been reported in the abscisic acid signal and auxin transport pathway in Arabidopsis inflorescence ( Yu et al, 2010 ), the TF ERF071 has been related to sweet cherry fruit development ( Alkio et al, 2014 ) and with the cell expansion during olive fruit development ( Camarero et al, 2023 ). However, NAC58 and bHLH162 have not been reported in fruit development.…”