Aluminum induces rapidly mitochondria-dependent programmed cell death in Al-sensitive peanut root tips

Abstract

BackgroundAlthough many studies suggested that aluminum (Al) induced programmed cell death (PCD) in plants, the mechanism of Al-induced PCD and its effects in Al tolerance is limited. This study was to investigate the mechanism and type of Al induced PCD and the relationship between PCD and Al tolerance.ResultsIn this study, two genotypes of peanut 99-1507 (Al tolerant) and ZH2 (Al sensitive) were used to investigate Al-induced PCD. Peanut root growth inhibition induced by AlCl3 was concentration and time-dependent in two peanut varieties. AlCl3 at 100 μM could induce rapidly peanut root tip PCD involved in DNA cleavage, typical apoptotic chromatin condensation staining with DAPI, apoptosis related gene Hrs203j expression and cytochrome C (Cyt c) release from mitochondria to cytosol. Caspase3-like protease was activated by Al; it was higher in ZH2 than in 99-1507. Al increased the opening of mitochondrial permeability transition pore (MPTP), decreased inner membrane potential (ΔΨm) of mitochondria. Compared with the control, Al stress increased O2•- and H2O2 production in mitochondria. Reactive oxygen species (ROS) burst was produced at Al treatment for 4 h.ConclusionsAl-induced PCD is earlier and faster in Al-sensitive peanut cultivar than in Al-tolerant cultivar. There is a negative relationship between PCD and Al resistance. Mitochondria- dependence PCD was induced by Al and ROS was involved in this process. The mechanism can be explained by the model of acceleration of senescence under Al stress.Electronic supplementary materialThe online version of this article (doi:10.1186/s40529-014-0067-1) contains supplementary material, which is available to authorized users.

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“…This was agreed with the findings of [1] on peanut and [12] and [23] on in vitro wheat plants. Accumulation of Al occurred at root meristems and as a result inhibition of root elongation was the first sign of Al toxicity [7,36,39].…”

“…Aluminium (Al) is the most abundant metal in the earth's crust [1], comprising about 7% of its mass [2,3]. Hence, the potential for soils to be Al toxic is considerable.…”

“…Hence, the potential for soils to be Al toxic is considerable. In acidic soil, Al could exist as Al 3+ , Al(OH) + and Al(OH) 2+ which are deteriorate to plants [1,4]. Many plant species are sensitive to Al even at micromolar concentration, thus, Al toxicity is a major factor restricting plant production on acidic soils [1,4,5,6,7], currently destroying more than 40% of agricultural land around the world [8,9,10].…”

“…[12] reported that the roots of in vitro wheat plants were found to exhibit reduced root growth, accumulating more Al 3+ and reactive oxygen species. Aluminium accumulation was found chiefly in the root apex (epidermis cell and cortex) [1]. [13] observed that the elongation of roots exposed to Al 3+ was inhibited within an hour(s).…”

“…Many Al tolerant plants exclude Al from roots by excretion of organic acids such as citrate, malate or oxalate from the roots that chelate Al [6,7,25,26,27,28], excretion of ion H + [17,29,30], excretion of phosphate that precipitate Al [31], excretion of mucilage [32,33] and protein [34] that bind Al. On the other hand, internal mechanisms of Al tolerance include reduction of accumulation of lipid peroxides through a higher proline and carbohydrate content related to osmoregulation and membrane stabilization [35], internal Al detoxification by organic acid anions and enhanced scavenging of free oxygen radicals, [7], protection of root apices by development of root border cells [36], acceleration of senescence of root tips [1], programed cell death under Al stress [1,37] immobilization of Al at cell wall [17], as well as selective permeability of the plasma membrane as a barrier to movement of Al into the cytosol [38].…”