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

Research output: Contribution to journalArticle

2 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)1186-1200
Number of pages15
JournalPlant Biotechnology Journal
Volume16
Issue number6
DOIs
StatePublished - Jun 2018

Fingerprint

biofortification
Manihot
Carotenoids
carotenes
dry matter content
cassava
Starch
shelf life
Carbon
starch
carbon
carotenoids
xylulose
Provitamins
Biofortification
phosphates
patatin
phytoene synthase
Glucose-1-Phosphate Adenylyltransferase
Manihot esculenta

Keywords

  • cassava
  • dry matter
  • fatty acid
  • provitamin A
  • starch
  • β-carotene

ASJC Scopus subject areas

  • Biotechnology
  • Agronomy and Crop Science
  • Plant Science

Cite this

Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch. / Beyene, Getu; Solomon, Felix R.; Chauhan, Raj D.; Gaitán-Solis, Eliana; Narayanan, Narayanan; Gehan, Jackson; Siritunga, Dimuth; Stevens, Robyn L.; Jifon, John; Van Eck, Joyce; Linsler, Edward; Gehan, Malia; Ilyas, Muhammad; Fregene, Martin; Sayre, Richard T.; Anderson, Paul; Taylor, Nigel J.; Cahoon, Edgar B.

In: Plant Biotechnology Journal, Vol. 16, No. 6, 06.2018, p. 1186-1200.

Research output: Contribution to journalArticle

Beyene, G, Solomon, FR, Chauhan, RD, Gaitán-Solis, E, Narayanan, N, Gehan, J, Siritunga, D, Stevens, RL, Jifon, J, Van Eck, J, Linsler, E, Gehan, M, Ilyas, M, Fregene, M, Sayre, RT, Anderson, P, Taylor, NJ & Cahoon, EB 2018, 'Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch', Plant Biotechnology Journal, vol. 16, no. 6, pp. 1186-1200. https://doi.org/10.1111/pbi.12862
Beyene, Getu ; Solomon, Felix R. ; Chauhan, Raj D. ; Gaitán-Solis, Eliana ; Narayanan, Narayanan ; Gehan, Jackson ; Siritunga, Dimuth ; Stevens, Robyn L. ; Jifon, John ; Van Eck, Joyce ; Linsler, Edward ; Gehan, Malia ; Ilyas, Muhammad ; Fregene, Martin ; Sayre, Richard T. ; Anderson, Paul ; Taylor, Nigel J. ; Cahoon, Edgar B. / Provitamin A biofortification of cassava enhances shelf life but reduces dry matter content of storage roots due to altered carbon partitioning into starch. In: Plant Biotechnology Journal. 2018 ; Vol. 16, No. 6. pp. 1186-1200.
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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.",
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AU - Beyene, Getu

AU - Solomon, Felix R.

AU - Chauhan, Raj D.

AU - Gaitán-Solis, Eliana

AU - Narayanan, Narayanan

AU - Gehan, Jackson

AU - Siritunga, Dimuth

AU - Stevens, Robyn L.

AU - Jifon, John

AU - Van Eck, Joyce

AU - Linsler, Edward

AU - Gehan, Malia

AU - Ilyas, Muhammad

AU - Fregene, Martin

AU - Sayre, Richard T.

AU - Anderson, Paul

AU - Taylor, Nigel J.

AU - Cahoon, Edgar B.

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N2 - 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.

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