From Accumulation to Degradation: Reprogramming Polyamine Metabolism Facilitates Dark-Induced Senescence in Barley Leaf Cells

Abstract

The aim of this study was to analyze whether polyamine (PA) metabolism is involved in dark-induced Hordeum vulgare L. ‘Nagrad’ leaf senescence. In the cell, the titer of PAs is relatively constant and is carefully controlled. Senescence-dependent increases in the titer of the free PAs putrescine, spermidine, and spermine occurred when the process was induced, accompanied by the formation of putrescine conjugates. The addition of the anti-senescing agent cytokinin, which delays senescence, to dark-incubated leaves slowed the senescence-dependent PA accumulation. A feature of the senescence process was initial accumulation of PAs at the beginning of the process and their subsequent decrease during the later stages. Indeed, the process was accompanied by both enhanced expression of PA biosynthesis and catabolism genes and an increase in the activity of enzymes involved in the two metabolic pathways. To confirm whether the capacity of the plant to control senescence might be linked to PA, chlorophyll fluorescence parameters, and leaf nitrogen status in senescing barley leaves were measured after PA catabolism inhibition and exogenously applied γ-aminobutyric acid (GABA). The results obtained by blocking putrescine oxidation showed that the senescence process was accelerated. However, when the inhibitor was applied together with GABA, senescence continued without disruption. On the other hand, inhibition of spermidine and spermine oxidation delayed the process. It could be concluded that in dark-induced leaf senescence, the initial accumulation of PAs leads to facilitating their catabolism. Putrescine supports senescence through GABA production and spermidine/spermine supports senescence-dependent degradation processes, is verified by H2O2 generation.

Putrescine catabolism via DAO contributes to proline and GABA accumulation in roots of lupine seedlings growing under salt stress

“…The involvement of DAO-mediated Put oxidation process in GABA production has been recently suggested by Sobieszczuk-Nowicka et al [43]. Microarray-based profiling of glutamate decarboxylase gene expression has shown that in senescing barley leaves GABA, synthesis from glutamate is gradually suppressed.…”

“…Microarray-based profiling of glutamate decarboxylase gene expression has shown that in senescing barley leaves GABA, synthesis from glutamate is gradually suppressed. Put oxidation then becomes an alternative source of GABA to the tricarboxylic acid cycle and also for some as yet undefined signaling pathways [43]. This GABA pool could be involved indirectly in the synthesis of Glu and further synthesis of Pro from Glu [16,39].…”

Polyamine catabolism adds fuel to leaf senescence

“…More information is becoming available on how PA metabolism is linked to physiological changes that ultimately lead to cell death and the nature of changes in the level of the free, conjugated or bound form of PAs. Processes interlinked with the increase or decrease in PA titer during senescence and the ability of plants to control senescence in relation to their capacity to metabolize PAs are slowly being unearthed (Sobieszczuk-Nowicka et al 2015, 2016; Sequera-Mutiozabal et al 2016). Recent studies on leaf senescence in a monocotyledonous crop plant, barley, demonstrate an important issue in relation to the crop yield and impact on sustainability of agricultural crops.…”

“…PA titer in plant cells is highly regulated (Cogen 1998; Moschou et al 2008; 2012; Angelini et al 2010; Moschou and Roubelakis-Angelakis 2013; and references therein). Transformations between individual PAs may essentially contribute to darkness-induced responses, and this was highlighted in barley leaf senescence (Sobieszczuk-Nowicka et al 2016). The question arises: “Is the increase in free PA titer at the beginning of senescence a part of a signalling mechanism that leads the cell to its death.” PA accumulation upon senescence is linked to up-regulation of PA biosynthesis gene and consequently to increase in the corresponding enzymatic activities.…”

“…Senescence is sensitive to hormonal perturbation, particularly to cytokinins (Lim et al 2007). Kinetin (KIN) treatment delays PA accumulation and it has been implied that some senescence-related signals blocked by KIN influence PA synthesis (Sobieszczuk-Nowicka et al 2016). It remains to be established if PA accumulation induced at the beginning of the senescence process has any reactive oxygen species-scavenging (ROS) function (Radyukina et al 2009; Legocka et al 2015).…”