Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch.
Getu Beyene, Felix R Solomon, Raj D Chauhan, Eliana Gaitán-Solis, Narayanan Narayanan, Jackson Gehan, Dimuth Siritunga, Robyn L Stevens, John Jifon, Joyce Van Eck, Edward Linsler, Malia Gehan, Muhammad Ilyas, Martin Fregene, Richard T Sayre, Paul Anderson, Nigel J Taylor, Edgar B Cahoon
Author Information
Getu Beyene: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Felix R Solomon: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Raj D Chauhan: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Eliana Gaitán-Solis: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Narayanan Narayanan: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Jackson Gehan: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Dimuth Siritunga: Department of Biology, University of Puerto Rico, Mayaguez, Puerto Rico.
Robyn L Stevens: Donald Danforth Plant Science Center, St. Louis, MO, USA.
John Jifon: Department of Horticultural Sciences, Texas A&M AgriLife Research and Extension Center, Weslaco, TX, USA.
Joyce Van Eck: Boyce Thompson Institute, Ithaca, NY, USA.
Edward Linsler: Boyce Thompson Institute, Ithaca, NY, USA.
Malia Gehan: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Muhammad Ilyas: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Martin Fregene: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Richard T Sayre: New Mexico Consortium, Los Alamos National Laboratory, Los Alamos, NM, USA.
Paul Anderson: Donald Danforth Plant Science Center, St. Louis, MO, USA.
Nigel J Taylor: Donald Danforth Plant Science Center, St. Louis, MO, USA. ORCID
Edgar B Cahoon: Donald Danforth Plant Science Center, St. Louis, MO, USA. ORCID
Storage roots of cassava (Manihot esculenta Crantz), a major subsistence crop of sub-Saharan Africa, are calorie rich but deficient in essential micronutrients, including provitamin A β-carotene. In this study, β-carotene concentrations in cassava storage roots were enhanced by co-expression of transgenes for deoxy-d-xylulose-5-phosphate synthase (DXS) and bacterial phytoene synthase (crtB), mediated by the patatin-type 1 promoter. Storage roots harvested from field-grown plants accumulated carotenoids to ≤50 μg/g DW, 15- to 20-fold increases relative to roots from nontransgenic plants. Approximately 85%-90% of these carotenoids accumulated as all-trans-β-carotene, the most nutritionally efficacious carotenoid. β-Carotene-accumulating storage roots displayed delayed onset of postharvest physiological deterioration, a major constraint limiting utilization of cassava products. Large metabolite changes were detected in β-carotene-enhanced storage roots. Most significantly, an inverse correlation was observed between β-carotene and dry matter content, with reductions of 50%-60% of dry matter content in the highest carotenoid-accumulating storage roots of different cultivars. Further analysis confirmed a concomitant reduction in starch content and increased levels of total fatty acids, triacylglycerols, soluble sugars and abscisic acid. Potato engineered to co-express DXS and crtB displayed a similar correlation between β-carotene accumulation, reduced dry matter and starch content and elevated oil and soluble sugars in tubers. Transcriptome analyses revealed a reduced expression of genes involved in starch biosynthesis including ADP-glucose pyrophosphorylase genes in transgenic, carotene-accumulating cassava roots relative to nontransgenic roots. These findings highlight unintended metabolic consequences of provitamin A biofortification of starch-rich organs and point to strategies for redirecting metabolic flux to restore starch production.
