Fluorescent chlorophyll catabolites in bananas light up blue halos of cell death

Abstract

Breakdown of chlorophyll is a major contributor to the diagnostic color changes in fall leaves, and in ripening apples and pears, where it commonly provides colorless, nonfluorescent tetrapyrroles. In contrast, in ripening bananas (Musa acuminata) chlorophylls fade to give unique fluorescent catabolites (FCCs), causing yellow bananas to glow blue, when observed under UV light. Here, we demonstrate the capacity of the blue fluorescent chlorophyll catabolites to signal symptoms of programmed cell death in a plant. We report on studies of bright blue luminescent rings on the peel of very ripe bananas, which arise as halos around necrotic areas in 'senescence associated' dark spots. These dark spots appear naturally on the peel of ripe bananas and occur in the vicinity of stomata. Wavelength, space, and time resolved fluorescence measurements allowed the luminescent areas to be monitored on whole bananas. Our studies revealed an accumulation of FCCs in luminescent rings, within senescing cells undergoing the transition to dead tissue, as was observable by morphological textural cellular changes. FCCs typically are short lived intermediates of chlorophyll breakdown. In some plants, FCCs are uniquely persistent, as is seen in bananas, and can thus be used as luminescent in vivo markers in tissue undergoing senescence. While FCCs still remain to be tested for their own hypothetical physiological role in plants, they may help fill the demand for specific endogenous molecular reporters in noninvasive assays of plant senescence. Thus, they allow for in vivo studies, which provide insights into critical stages preceding cell death.apoptosis ͉ luminescent marker ͉ tetrapyrrole ͉ fruit ͉ plant senescence

Update on the biochemistry of chlorophyll breakdown

“…Hypermodified FCCs New types of FCCs, termed hypermodified FCCs (hFCCs) were recently identified in ripening banana fruits and in senescent banana and peace lily leaves Moser et al 2008aMoser et al , 2009Kräutler et al 2010). In contrast to the transient occurrence of mFCCs as intermediary catabolites in senescing leaves that are converted to NCCs (see above), hFCCs persist in ripening or senescing tissues.…”

A Role for TIC55 as a Hydroxylase of Phyllobilins, the Products of Chlorophyll Breakdown during Plant Senescence

“…fluorescent chlorophyll catabolites) as the result of nonenzymatic isomerization inside the acidic vacuolar sap (Oberhuber et al, 2003;Christ et al, 2013). Since the first identification of an NCC in senescent leaves of barley (Hordeum vulgare) in 1991 (Kräutler et al, 1991), phyllobilins were found in senescent leaves from more than 20 different angiosperm species (Kräutler, 2016) but are also formed during fruit ripening Moser et al, 2009). Although the principal linear tetrapyrrole backbone of all phyllobilins is identical, they exhibit rather great structural diversity among the investigated species.…”

A novel blue fluorescent chlorophyll catabolite accumulates in senescent leaves of the peace lily and indicates a split path of chlorophyll breakdown

“…Related FCCs were found to accumulate and induce blue luminescence in yellow M. acuminata bananas [12], in senescent sections of peels of overripe bananas [14], and in senescent banana leaves [13] (see SuppMat, Fig. S2).…”

“…[40,41]). 'Persistent' FCCs, the newly discovered blue luminescent plant pigments, are sources of optical signals [12][13][14], and may be useful as natural molecular in-vivo markers and signals of ripening and of programmed cell death. .…”

“…Two of these were identified as FCCs, unstable precursors of NCCs [10,11]. In banana peels (Musa acuminata) and in senescent banana leaves, accumulation of 'persistent' FCCs was discovered recently [12][13][14].…”