A hypothetical model behind the molecular mechanism of alternate behaviour in Pistacia vera L.

Abstract

The alternate bearing behaviour of pistachio (Pistacia vera L.) is strictly related to the premature inflorescence bud abscission on high yielding trees that occur during the summer, and it is the consequence of a regulatory mechanism modulating nutritional stress and embryo survival. A branch has a finite availability of sugars to supply the energy consuming organs (sinks), such as buds and fruits. During a heavy fruit bearing year (“ON”), the competition between the same branch’s sinks trigger a cascade of events mediated by sugar and hormone signaling pathways. In the present work, we propose an updated hypothetical model, carried out from de novo discovery and transcriptome analysis, to better elucidate the fall of inflorescence buds linked to alternate bearing. The model suggests that sugar availability regulates organ development by interacting with nutrient signaling sensors, such as trehalose-6phosphate gene (T6P) and SnRK1 (SUCROSE-NON-FERMENTING-1-RELATED PROTEIN KINASE-1 gene). The “ON” fruits showed an enhancement of the T6P gene and downregulation of SnRK1, which is opposite to the expression pattern in “ON” buds. A system for scavenging ROS is active in the “ON” fruits, mediated by hormone signaling (ABA), the antagonistic T6P and SnRK1 regulatory loop, and the gene expression rate of transcription factors (like WRINKLED1 (WRI1), APETALA2 (AP2), MADS factors). ABA and cytokinin in developing embryos/fruits of “ON” branches reinforce the sink strength presumably by intensifying cell proliferation and gaining more photo-assimilates. Ethylene-responsive genes and transcription factors regulating the expression of genes involved in the allocation of carbon into oil are overexpressed in “ON” fruits. Among the auxin conjugates, IAA was the main and dominant indole detected in this work. It has also been determined that quite a few organs during the less prolific fruiting year (‘OFF-year’) have higher auxin content than in ‘ON-year’ trees. Genes of the secondary metabolism and transcription factors are also involved in tailoring the individual branch’s response to the nutritional stress and sink competition, indicating the semi-autonomy of the branches. Meanwhile, the inflorescence buds in “ON” branches are under energy stress, and the overexpression of SnRK1 inhibits vegetative growth and triggers a ROS mediated programmed cell death which leads to the abscission of inflorescence buds.