Influence of domestication on specialized metabolic pathways in fruit crops

Abstract

Main conclusion

During the process of plant domestication, the selection and traditional breeding for desired characters such as flavor, juiciness and nutritional value of fruits, probably have resulted in gain or loss of specialized metabolites contributing to these traits. Their appearance in fruits is likely due to the acquisition of novel and specialized metabolic pathways and their regulation, driven by systematic molecular evolutionary events facilitated by traditional breeding.

Abstract

Plants change their armory of specialized metabolism to adapt and survive in diverse ecosystems. This may occur through molecular evolutionary events, such as single nucleotide polymorphism, gene duplication and transposition, leading to convergent or divergent evolution of biosynthetic pathways producing such specialized metabolites. Breeding and selection for improved specific and desired traits (fruit size, color, taste, flavor, etc.) in fruit crops through conventional breeding approaches may further alter content and profile of specialized metabolites. Biosynthetic routes of these metabolites have been studied in various plants. Here, we explore the influence of plant domestication and breeding processes on the selection of biosynthetic pathways of favorable specialized metabolites in fruit crops. An orderly clustered arrangement of genes associated with their production is observed in many fruit crops. We further analyzed selection-based acquisition of specialized metabolic pathways comparing first the metabolic profiles and genes involved in their biosynthesis, followed by the genomic organization of such genes between wild and domesticated horticultural crops. Domestication of crop plants favored the acquisition and retention of metabolic pathways that enhanced the fruit value while eliminated those which produced toxic or unfavorable metabolites. Interestingly, unintentional reorganization of complex metabolic pathways by selection and traditional breeding processes has endowed us with flavorful, juicy and nutritionally rich fruits.

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Fig. 1
Fig. 2

modified from Zhou et al. (2016). KEGG database was used to draft the pathway map for the cucurbitacin biosynthetic pathway differentiation in the wild and the domesticated cucurbits (https://www.genome.jp/kegg/). Metabolite structures were drawn using ChemDraw v16.0

Fig. 3
Fig. 4
Fig. 5

modified from Yu et al. (2015). Plant species names: Vvin, Vitis vinifera; Tcac, Theobroma cacao; Slyc, Solanum lycopersicum; Pmum, Prunus mume; Mdom, Malus domestica Borkh.; Fves, Fragaria vesca; Csat, Cucumis sativus; Csin, Citrus sinensis; Clan, Citrullus lanatus; Cpap, Carica papaya. Data for tandem genes and clusters, specifically to the fruit crop plants only, were extracted from the integrated database of “PTGBase” (Yu et al. 2015)

Fig. 6

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Acknowledgements

MSD and PSO are thankful to Council of Scientific and Industrial Research (CSIR, New Delhi) for research fellowship; and MSD acknowledge the Academy of Scientific and Innovative Research (AcSIR), India for enrollment in the Ph.D. program. This research was funded by the CSIR New Delhi, India under the project CSC0133 (FUNHEALTH) to CSIR-National Chemical Laboratory, Pune.

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MSD, BBD and APG conceptualized the idea and subsequently framed the review outline. MSD prepared the figures with inputs from APK, BBD and DS. MSD, BBD, VSG and APG wrote the initial drafts of the manuscript with inputs from DS, APK and PSO. All authors contributed in revising and editing the manuscript drafts; and subsequently approved the final manuscript.

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Correspondence to Bhushan B. Dholakia or Ashok P. Giri.

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Dar, M.S., Dholakia, B.B., Kulkarni, A.P. et al. Influence of domestication on specialized metabolic pathways in fruit crops. Planta 253, 61 (2021). https://doi.org/10.1007/s00425-020-03554-4

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Keywords

  • Aroma
  • Domestication
  • Flavour
  • Fruit crops
  • Gene cluster
  • Specialized metabolites
  • Taste