Abstract
BackgroundCytokinins are known to play an important role in fruit set and early fruit growth, but their involvement in later stages of fruit development is less well understood. Recent reports of greatly increased cytokinin concentrations in the flesh of ripening kiwifruit (Actinidia deliciosa (A. Chev.) C.F. Liang & A.R. Ferguson) and grapes (Vitis vinifera L.) have suggested that these hormones are implicated in the control of ripening-related processes.ResultsA similar pattern of isopentenyladenine (iP) accumulation was observed in the ripening fruit of several grapevine cultivars, strawberry (Fragaria ananassa Duch.) and tomato (Solanum lycopersicum Mill.), suggesting a common, ripening-related role for this cytokinin. Significant differences in maximal iP concentrations between grapevine cultivars and between fruit species might reflect varying degrees of relevance or functional adaptations of this hormone in the ripening process. Grapevine orthologues of five Arabidopsis (Arabidopsis thaliana L.) gene families involved in cytokinin metabolism and signalling were identified and analysed for their expression in developing grape berries and a range of other grapevine tissues. Members of each gene family were characterised by distinct expression profiles during berry development and in different grapevine organs, suggesting a complex regulation of cellular cytokinin activities throughout the plant. The post-veraison-specific expression of a set of biosynthesis, activation, perception and signalling genes together with a lack of expression of degradation-related genes during the ripening phase were indicative of a local control of berry iP concentrations leading to the observed accumulation of iP in ripening grapes.ConclusionsThe transcriptional analysis of grapevine genes involved in cytokinin production, degradation and response has provided a possible explanation for the ripening-associated accumulation of iP in grapes and other fruit. The pre- and post-veraison-specific expression of different members from each of five gene families suggests a highly complex and finely-tuned regulation of cytokinin concentrations and response to different cytokinin species at particular stages of fruit development. The same complexity and specialisation is also reflected in the distinct expression profiles of cytokinin-related genes in other grapevine organs.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0611-5) contains supplementary material, which is available to authorized users.
Highlights
Cytokinins are known to play an important role in fruit set and early fruit growth, but their involvement in later stages of fruit development is less well understood
In order to evaluate if the ripening-associated accumulation of iP is a common occurrence in grapes, berries from three different grapevine cultivars, sampled from 2 weeks post flowering to commercial harvest after 15–17 wpf, were analysed for their iP content (Fig. 1)
From the few examples where iP has been quantified throughout the development of fleshy fruit, grapes ([38]; this study) were shown to accumulate up to 100-fold more iP during the ripening phase than tomato, strawberry and kiwifruit [21, 37] and no increase in iP concentration was detected during the transition from pink to red raspberries [22]. iP concentrations in tomato, strawberry and kiwifruit fall into a similar range to what has been published for Arabidopsis seedlings [80, 81], maize roots, leaves and kernels [82], young ‘Microtom’ tomato ovaries [83], rice inflorescence meristem [14] and various soybean (Glycine max (L.) Merr.) tissues [84], whereas the iP quantities detected in grape berries are unprecedented
Summary
Cytokinins are known to play an important role in fruit set and early fruit growth, but their involvement in later stages of fruit development is less well understood. The four most abundant cytokinins found in plants, trans-zeatin (tZ), N6-(Δ2-isopentenyl)-adenine (iP), cis-zeatin (cZ), and dihydrozeatin, differ in the stereo-isomeric position, hydroxylation and saturation of the isoprenoid side chain [1], but little is known about the physiological relevance of these side chain differences [2] Apart from their well-described role in regulating cell division and differentiation [3], cytokinins are involved in a range of processes essential to plant survival, such as leaf senescence [4, 5], control of shoot-to-root balance [6, 7], nutritional signalling [8, 9], stress tolerance [10] and nodulation [11, 12]. In the case of kiwifruit, the main contributor to this increase was tZ, whereas iP was found to be the main cytokinin species accumulating in ripening grapes
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