Transcriptome Analysis of Pistacia vera Inflorescence Buds in Bearing and Non-Bearing Shoots Reveals the Molecular Mechanism Causing Premature Flower Bud Abscission

Abstract

The alteration of heavy (“ON/bearing”) and light (“OFF/non-bearing”) yield in pistachio (Pistacia vera L.) has been reported to result from the abscission of inflorescence buds on high yielding trees during the summer, but the regulatory mechanisms involved in this bud abscission remain unclear. The analysis provides insights into the transcript changes between inflorescence buds on bearing and non-bearing shoots, that we indicated as “ON” and “OFF”, and shed light on the molecular mechanisms causing premature inflorescence bud abscission in the pistachio cultivar “Bianca” which can be related to the alternate bearing behavior. In this study, a transcriptome analysis was performed in inflorescence buds of “ON” and “OFF” shoots. A total of 14,330 differentially expressed genes (DEGs), most of which are involved in sugar metabolism, plant hormone pathways, secondary metabolism and oxidative stress pathway, were identified. Our results shed light on the molecular mechanisms underlying inflorescence bud abscission in pistachio and we proposed a hypothetical model behind the molecular mechanism causing this abscission in “ON” shoots. Results highlighted how changes in genes expressed in nutrient pathways (carbohydrates and mineral elements) in pistachio “ON” vs. “OFF” inflorescence buds triggers a cascade of events involving trehalose-6-phosphate and target of rapamycin (TOR) signaling, SnRK1 complex, hormones, polyamines and ROS which end, through programmed cell death and autophagy phenomena, with the abscission of inflorescence buds. This is the first study reporting gene expression profiling of the fate of “ON” and “OFF” inflorescence buds associated with the alternate bearing in the pistachio.

Transcriptomic Analysis of the Pistacia vera (L.) Fruits Enable the Identification of Genes and Hormone-Related Gene Linked to Inflorescence Bud Abscission

“…At the same time, some studies proved that hormone concentrations are also involved in inflorescence bud abscission [ 6 ]. Auxin, Cytokinin, and polyamines may significantly affect the abscission of pistachio flower buds [ 10 , 11 ].…”

“…In pistachio, a recent experiment of high-throughput RNA-Seq analysis has been performed by Benny et al (2020) [ 11 ] on inflorescence buds of “ON” and “OFF” trees of the Italian cultivar Bianca and provided insight into the mechanism leading to the premature inflorescence bud abscission [ 11 ]. From this study, it is evident that the lack of resources (primarily carbohydrates) triggers a cascade of events that lead to the fall of the buds of the loaded “ON” branches starting around the third week of June [ 11 ], indicating a source-sink competition. Inflorescence bud abscission can be considered a “within shoot phenomenon” interconnected to the crop load on the one-year-old growth.…”

“…In this study, the inflorescence buds of “ON” branches in June and July showed an intense starch degradation due to the up-regulation of ALPHA-AMYLASE 3 , over-expression of genes involved in the biosynthetic pathways of raffinose and of the MIOX gene, which are activated in conditions of limited energy reserves and stress. Changes in carbohydrate levels affected the trehalose-6-phosphate, which was found down-regulated [ 11 ], involved in the genetic control of sucrose levels and sink development [ 17 ]. The SnRK1 gene key regulator of the plant energy balance and involved in the stress signaling network, which includes the TOR kinase [ 18 ], was given as active.…”

“…The SnRK1 gene key regulator of the plant energy balance and involved in the stress signaling network, which includes the TOR kinase [ 18 ], was given as active. The auxin-mediated TOR gene, which regulates translation, transcription, cell growth and proliferation, differentiation, and autophagy [ 19 ] was also affected, confirming its involvement in various signal responses, including nutrient availability, stress, and hormones [ 11 , 20 ]. At the hormonal level, the genes involved in the biosynthetic pathways of auxins were down-regulated, and the polyamines (PA), including spermidine, were down-regulated.…”

Profile of Semiquinone Radicals, Phytohormones and Sugars in Pistacia vera L. cv. Kirmizi Development

“…Transcriptome analysis of P. vera L. cv. Bianca inflorescence buds in bearing and non-bearing shoots was carried out by Benny et al [21], revealing differentially expressed genes, most of which being involved in sugar metabolism, plant hormone pathways, secondary metabolism and oxidative stress pathways.…”