Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch

Plant Biotechnol J. 2018 Jun;16(6):1186-1200. doi: 10.1111/pbi.12862. Epub 2017 Dec 27.

Abstract

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.

Keywords: cassava; dry matter; fatty acid; provitamin A; starch; β-carotene.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Abscisic Acid / metabolism
  • Biofortification*
  • Carbohydrate Metabolism*
  • Carotenoids / metabolism*
  • Food Storage
  • Geranylgeranyl-Diphosphate Geranylgeranyltransferase / genetics
  • Manihot / chemistry*
  • Manihot / genetics
  • Manihot / metabolism
  • Plant Roots / chemistry*
  • Plants, Genetically Modified
  • Solanum tuberosum / chemistry
  • Starch / biosynthesis
  • Transferases / genetics

Substances

  • Carotenoids
  • Abscisic Acid
  • Starch
  • Transferases
  • deoxyxylulose-5-phosphate synthase
  • Geranylgeranyl-Diphosphate Geranylgeranyltransferase

Associated data

  • GENBANK/JN374901
  • GENBANK/JN374902