Multi-scale comparative transcriptome analysis reveals key genes and metabolic reprogramming processes associated with oil palm fruit abscission

Abstract

Background Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ). To determine the mechanisms of fleshy fruit abscission of the monocot oil palm (Elaeis guineensis Jacq.) compared with other abscission systems, we performed multi-scale comparative transcriptome analyses on fruit targeting the developing primary AZ and adjacent tissues. Results Combining between-tissue developmental comparisons with exogenous ethylene treatments, and naturally occurring abscission in the field, RNAseq analysis revealed a robust core set of 168 genes with differentially regulated expression, spatially associated with the ripe fruit AZ, and temporally restricted to the abscission timing. The expression of a set of candidate genes was validated by qRT-PCR in the fruit AZ of a natural oil palm variant with blocked fruit abscission, which provides evidence for their functions during abscission. Our results substantiate the conservation of gene function between dicot dry fruit dehiscence and monocot fleshy fruit abscission. The study also revealed major metabolic transitions occur in the AZ during abscission, including key senescence marker genes and transcriptional regulators, in addition to genes involved in nutrient recycling and reallocation, alternative routes for energy supply and adaptation to oxidative stress. Conclusions The study provides the first reference transcriptome of a monocot fleshy fruit abscission zone and provides insight into the mechanisms underlying abscission by identifying key genes with functional roles and processes, including metabolic transitions, cell wall modifications, signalling, stress adaptations and transcriptional regulation, that occur during ripe fruit abscission of the monocot oil palm. The transcriptome data comprises an original reference and resource useful towards understanding the evolutionary basis of this fundamental plant process.

A Non-Shedding Fruit Elaeis oleifera Palm Reveals Perturbations to Hormone Signaling, ROS Homeostasis, and Hemicellulose Metabolism

“…This study also provides a unique opportunity to compare the molecular basis of ripe fruit abscission of the two species of oil palm, E. guineensis from Africa and E. oleifera from South and Central America. Notably, a total of six DEGs identified in the current study of E. oleifera were common to those found in the previous study of E. guineensis [11]. These DEGs are particularly relevant, given the differences in the criteria used for screening for DEG candidates in the two studies: the use of a non-shedding individual for the E. oleifera study and the use of a large-scale, multifaceted analysis of ripe fruit AZ induced by ethylene with E. guineensis [11].…”

“…To compare E. oleifera fruit abscission with what is known about ripe fruit abscission in E. guineensis, we compared the DEG list identified in the current study with those found in a recent transcriptome study of E. guineensis [11]. In total, there were six DEGs found in common from the two analyses (Table 1).…”

“…For the transcriptome analyses, two palms within the same progeny (Figure 1, TA59D) were selected based on their contrasted AI values and contrasted abscission characters in field conditions: the palm individual 28-7, which sheds its fruit normally (Sd), and palm 26-11, that is the non-shedding oil palm variant (NSd), with which little or no fruit abscission was observed in the field. From undamaged fruit, AZs between the pedicel and the mesocarp were isolated with a scalpel from the base of each fruit and collected as previously described [11]. Three biological replications were sampled from each fruit bunch collected from each individual, for a total of twelve samples, which included three PR and three ripe Sd, as well as three PR and three ripe NSd.…”

“…Furthermore, an ET-dependent decrease in auxin in the AZ leads to the acquisition of ET sensitivity and abscission competence [15,39]. Previous work has shown that ET can accelerate E. guineensis fruit abscission through modulation of gene expression [7,9,11]. In the current study, the NSd variant had reduced amounts of two similar DEGs (LOC105043735 and LOC105053951) for the ERF-1 (Ethylene Response Factor-1) that functions to maintain a balance between cambium-driven growth and adaptation to environmental stress [55].…”

“…While both AZs are located at the boundary area between the mesocarp and the pedicel, the E. guineensis AZ is made up of around 8-10 cells layers with pectin rich cell walls, and the E. oleifera AZ is less distinct; that creates an abrupt transition between the mesocarp and pedicel tissues [6]. While we have previously examined in great detail the ripe fruit abscission processes at the molecular and cellular levels in the multilayer AZ of the African oil palm [7][8][9][10][11], very little is known about the molecular processes of abscission in E. oleifera and how the abscission processes have diverged between these two closely related species separated by millions of years of evolution.…”