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

Kim Fooyontphanich,Chatchawan Jantasuriyarat,Stéphane Dussert,Thierry Joët,Jean-Luc Verdeil,Julien Serret,Myriam Collin,Peerapat Roongsattham,Sithichoke Tangphatsornruang,Philippe Amblard,Fabienne Morcillo,Timothy J Tranbarger

doi:10.1186/s12870-021-02874-1

Abstract

BackgroundFruit 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.ResultsCombining 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.ConclusionsThe 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.

Highlights

Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ)
In the current study we used a multi-scale transcriptome analysis to compare the ripe fruit AZ, pedicel, and immature fruit AZ treated with ethylene, AZ during natural abscission and AZ of non-shedding fruit samples, to identify a robust list of core genes and processes that function in the AZ during fleshy fruit abscission of this monocot
The major objectives of the current study were to identify AZ specific expression related to the timing of oil palm ripe fruit abscission, in order to screen for genes that function in the AZ, and compare to candidates identified from dicot organ abscission models

Summary

Introduction

Fruit abscission depends on cell separation that occurs within specialized cell layers that constitute an abscission zone (AZ). Fruit that shed prematurely before seeds are fully developed, or too late during seasonal climate changes can jeopardize reproductive success of wild species. Fruit detachment mechanisms have been a target of domestication, and a well-known domestication example is the non-abscising jointless mutant, which has been used to develop non-shedding tomato fruit cultivars [1]. This is the case with cereals (rice, barley wheat, etc.) for which domestication has allowed the selection of varieties with non-shedding grains. Interactions between multiple signalling pathways that integrate the environment and the overall developmental and physiological status of the plant are necessary for fruit abscission to occur [4,5,6,7,8,9]

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