In the unconventional climacteric fig (Ficus carica) fruit, pollinated and parthenocarpic fruit of the same genotype exhibit different ripening characteristics. Integrative comparative analyses of tissue-specific transcript and of hormone levels during fruit repining from pollinated vs. parthenocarpic fig fruit were employed to unravel the similarities and differences in their regulatory processes during fruit repining. Assembling tissue-specific transcripts into 147,000 transcripts with 53,000 annotated genes provided new insights into the spatial distribution of many classes of regulatory and structural genes, including those related to color, taste and aroma, storage, protein degradation, seeds and embryos, chlorophyll, and hormones. Comparison of the pollinated and parthenocarpic tissues during fruit ripening showed differential gene expression, especially in the fruit inflorescence. The distinct physiological green phase II and ripening phase III differed significantly in their gene-transcript patterns in both pulp and inflorescence tissues. Gas chromatographic analysis of whole fruits enabled the first determination of ripening-related hormone levels from pollinated and non-pollinated figs. Ethylene and auxin both increased during fruit ripening, irrespective of pollination, whereas no production of active gibberellins or cytokinins was found in parthenocarpic or pollinated ripening fruit. Tissue-specific transcriptome revealed apparent different metabolic gene patterns for ethylene, auxin and ABA in pollinated vs. parthenocarpic fruit, mostly in the fruit inflorescence. Our results demonstrate that the production of abscisic acid (ABA), non-active ABA–GE conjugate and non-active indoleacetic acid (IAA)–Asp conjugate in pollinated fruits is much higher than in parthenocarpic fruits. We suggest that fruit ripening is coordinated by the reproductive part of the syconium and the differences in ABA production between pollinated and parthenocarpic fig fruit might be the key to their different ripening characteristics.
The common fig bears a unique closed inflorescence structure, the syconium, composed of small individual drupelets that develop from the ovaries enclosed in the succulent vegetative-originated receptacle. The fig ripening process is traditionally classified as climacteric; however, recent studies have suggested distinct mechanisms in its reproductive and non-reproductive parts. We analyzed ABA and ethylene production, and expression of ABA-metabolism, ethylene-biosynthesis, MADS-box, NAC and ethylene-response factor genes in the inflorescence and receptacle of on-tree ABA-, ethephon-, fluridone- and NDGA-treated fruit. Exogenous ABA and ethephon accelerated fruit ripening and softening, whereas fluridone and NDGA had the opposite effect, delaying endogenous ABA and ethylene production compared to controls. Expression of ABA-biosynthesis genes FcNCED2 and FcABA2, ethylene-biosynthesis genes FcACS4, FcACOL and FcACO2, FcMADS8, 14, 15, FcNAC1, 2, 5, and FcERF9006 was upregulated by exogenous ABA and ethephon. NDGA downregulated FcNCED2 and FcABA2, whereas fluridone downregulated FcABA2; both downregulated ethylene-related genes. This demonstrates the key role of ABA in ripening regulation by promoting ethylene production as in climacteric tomato, especially in the inflorescence. However, increasing accumulation of endogenous ABA until full ripeness and significantly low expression of ethylene-biosynthesis genes in the receptacle suggests non-climacteric, ABA-dependent ripening in the vegetative-originated succulent receptacle fruit part.
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