Metabolic diversity in sweet potato (Ipomoea batatas, Lam.) leaves and storage roots

Abstract

Sweet potato (Ipomoea batatas, Lam.) is an important root vegetable in developing countries. After its domestication in Neotropical America, human migration led to the distribution of the sweet potato plant throughout the world. Both leaf and storage root are high in compounds of nutritional value. Yet, the storage roots are of particular value due to their significant content of provitamin A (β-carotene). The breeding effort for elite sweet potato lines led to the reduction of genetic diversity and the potential to improve other traits. The focus of the present study was to assess the metabolic diversity of 27 sweet potato cultivars including landraces and improved varieties. A metabolite profiling approach was optimised for sweet potato leaf and storage root tissue and 130 metabolites identified with three different analysis platforms. The data highlighted a lack of correlation between storage root phenotype and leaf metabolism. Furthermore, the metabolic diversity of storage roots was based on the secondary metabolism, including phenylpropanoids and carotenoids. Three cultivars of three different flesh colouration (yellow, orange and purple) showed a significant difference of the primary metabolism. This data demonstrates the value of metabolite profiling to breeding programs as a means of identifying differences in phenotypes/chemotypes and characterising parental material for future pre-breeding resources.

References

[1] O’Brien, P. J. The sweet potato: its origin and dispersal. Am. Anthropol. 74, 342-365 (1972).

[2] Roullier, C. et al. Disentangling the origins of cultivated sweet potato (Ipomoea batatas (L.) Lam). PLoS One 8, e62707 (2013).

[3] CIP. Roots and tubers improving the lives of the poor. Annual Report (2015).

[4] Mohanraj, R. & Sivasankar, S. Sweet potato (Ipomoea batatas [L.] Lam)-a valuable medicinal food: a review. J. Med. Food 17, 733-741 (2014).

[5] Shekhar, S., Mishra, D., Buragohain, A. K., Chakraborty, S. & Chakraborty, N. Comparative analysis of phytochemicals and nutrient availability in two contrasting cultivars of sweet potato (Ipomoea batatas L.). Food Chem. 173, 957-965 (2015).

[6] Teow, C. C. et al. Antioxidant activities, phenolic and β-carotene contents of sweet potato genotypes with varying flesh colours. Food Chem. 103, 829-838 (2007).

[7] Woolfe, J. A. Sweet Potato: An Untapped Food Resource (University Press, Cambridge, United Kingdom 1992).

[8] Sun, H., Mu, T., Xi, L., Zhang, M. & Chen, J. Sweet potato (Ipomoea batatas L.) leaves as nutritional and functional foods. Food Chem. 156, 380-389 (2014).

[9] Burri, B. J. Evaluating sweet potato as an intervention food to prevent vitamin A deficiency. Compr. Rev. Food Sci. Food Saf. 10, 118-130 (2011).

[10] Su, W. et al. Genome-wide assessment of population structure and genetic diversity and development of a core germplasm set for sweet potato based on specific length amplified fragment (SLAF) sequencing. PLoS One 12, e0172066 (2017).

[11] Camargo, L. K. P., Mógor, A. F., Resende, J. T. V. & Da-Silva, P. R. Establishment and molecular characterization of a sweet potato germplasm bank of the highlands of Paraná State, Brazil. Genet. Mol. Res. 12, 5574-5588 (2013).

[12] Ahn, Y. O. et al. Exogenous sucrose utilization and starch biosynthesis among sweetpotato cultivars. Carbohydr. Res. 345, 55-60 (2010).

[13] Cervantes-Flores, J. C. et al. Identification of quantitative trait loci for dry-matter, starch, and β-carotene content in sweetpotato. Mol. Breed. 28, 201-216 (2011).

[14] Xie, F. et al. De novo sequencing and a comprehensive analysis of purple sweet potato (Ipomoea batatas L.) transcriptome. Planta 236, 101-113 (2012).

[15] Ojong, P. B. et al. Variation of flavonoid content among sweetpotato accessions. J. Am. Soc. Hortic. Sci. 133, 819-824 (2008).

[16] Cuevas Montilla, E., Hillebrand, S. & Winterhalter, P. Anthocyanins in purple sweet potato (Ipomoea batatas L.) varieties. Fruit. Veg. Cereal Sci. Biotechnol. 5, 19-24 (2011).

[17] Xu, J. et al. Characterisation and stability of anthocyanins in purple-fleshed sweet potato P40. Food Chem. 186, 90-96 (2015).

[18] Bauernfeind, J. C. Carotenoid vitamin A precursors and analogs in foods and feeds. J. Agric. Food Chem. 20, 456-473 (1972).

[19] Gruber, K. Agrobiodiversity: the living library. Nature 544, S8-S10 (2017).

[20] Drapal, M. et al. Identification of metabolites associated with water stress responses in Solanum tuberosum L. clones. Phytochemistry 135, 24-33 (2017).

[21] Price, E. J., Wilkin, P., Sarasan, V. & Fraser, P. D. Metabolite profiling of Dioscorea (yam) species reveals underutilised biodiversity and renewable sources for high-value compounds. Sci. Rep. 6, 29136 (2016).

[22] Rodriguez-Bonilla, L. et al. Assessment of genetic diversity of sweet potato in Puerto Rico. PLoS One 9, e116184 (2015).

[23] Roullier, C., Rossel, G., Tay, D., McKey, D. & Lebot, V. Combining chloroplast and nuclear microsatellites to investigate origin and dispersal of New World sweet potato landraces. Mol. Ecol. 20, 3963-3977 (2011).

[24] Roullier, C., Benoit, L., McKey, D. B. & Lebot, V. Historical collections reveal patterns of diffusion of sweet potato in Oceania obscured by modern plant movements and recombination. Proc. Natl. Acad. Sci. U.S.A. 110, 2205-2210 (2013).

[25] Kyndt, T. et al. The genome of cultivated sweet potato contains Agrobacterium T-DNAs with expressed genes: an example of a naturally transgenic food crop. Proc. Natl. Acad. Sci. U.S.A. 112, 5844-5849 (2015).

[26] Park, S.-C. et al. Enhanced accumulation of carotenoids in sweetpotato plants overexpressing IbOr-Ins gene in purple-fleshed sweetpotato cultivar. Plant Physiol. Biochem. 86, 82-90 (2015).

[27] Li, L., Paolillo, D. J., Parthasarathy, M. V., DiMuzio, E. M. & Garvin, D. F. A novel gene mutation that confers abnormal patterns of β-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J. 26, 59-67 (2001).

[28] Grüneberg, W. J., Mwanga, R., Andrade, M. & Espinoza, J. in Plant Breeding and Farmer Participation (eds S. Ceccarelli, S. et al. ) Ch. 13, 275-322 (FAO, Rome, Italy 2009).

[29] Tumwegamire, S. et al. Evaluation of dry matter, protein, starch, sucrose, β-carotene, iron, zinc, calcium, and magnesium in East African sweetpotato [Ipomoea batatas (L.) Lam] germplasm. HortScience 46, 348-357 (2011).

[30] Cervantes-Flores, J. C. et al. Development of a genetic linkage map and identification of homologous linkage groups in sweetpotato using multiple-dose AFLP markers. Mol. Breed. 21, 511-532 (2008).

[31] Medicine, I. O. Dietary Reference Intakes for Vitamin A, Vitamin K, Arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum, Nickel, Silicon, Vanadium, and Zinc (The National Academies Press, Washington (DC), United States 2001).

[32] Grace, M. H. et al. Phytochemical changes in phenolics, anthocyanins, ascorbic acid, and carotenoids associated with sweetpotato storage and impacts on bioactive properties. Food Chem. 145, 717-724 (2014).

[33] zum Felde, T. et al. In Proc. 15th International Symposium of the International Society for Tropical Root Crops (ISTRC) 27-33 (Lima, Peru, 2009).

[34] Nogueira, M., Mora, L., Enfissi, E. M., Bramley, P. M. & Fraser, P. D. Subchromoplast sequestration of carotenoids affects regulatory mechanisms in tomato lines expressing different carotenoid gene combinations. Plant Cell 25, 4560-4579 (2013).

[35] Fraser, P. D., Pinto, M. E., Holloway, D. E. & Bramley, P. M. Technical advance: application of high-performance liquid chromatography with photodiode array detection to the metabolic profiling of plant isoprenoids. Plant J. 24, 551-558 (2000).

[36] Enfissi, E. M. A. et al. Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit. Plant Cell 22, 1190-1215 (2010).

[37] Shahaf, N. et al. Constructing a mass measurement error surface to improve automatic annotations in liquid chromatography/mass spectrometry based metabolomics. Rapid Commun. Mass Spectrom. 27, 2425-2431 (2013).

[38] Wehrens, R., Bloemberg, T. G. & Eilers, P. H. Fast parametric time warping of peak lists. Bioinformatics 31, 3063-3065 (2015).

[39] Xia, J. and Wishart, D.S. 2016. Using MetaboAnalyst 3.0 for comprehensive metabolomics data analysis. Curr. Protoc. Bioinform. 55: 14.10.1‐ 14.10.91. https://doi.org/10.1002/cpbi.11