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

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 ?-carotene. In this study, ?-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 ?g/g DW, 15- to 20-fold increases relative to roots from nontransgenic plants. Approximately 85%-90% of these carotenoids accumulated as all-trans-?-carotene, the most nutritionally efficacious carotenoid. ?-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 ?-carotene-enhanced storage roots. Most significantly, an inverse correlation was observed between ?-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 ?-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.

SUBMITTER: Beyene G

PROVIDER: S-EPMC5978869 | biostudies-literature | 2018 Jun

REPOSITORIES: biostudies-literature

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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 G Solomon Felix R FR Chauhan Raj D RD Gaitán-Solis Eliana E Narayanan Narayanan N Gehan Jackson J Siritunga Dimuth D Stevens Robyn L RL Jifon John J Van Eck Joyce J Linsler Edward E Gehan Malia M Ilyas Muhammad M Fregene Martin M Sayre Richard T RT Anderson Paul P Taylor Nigel J NJ Cahoon Edgar B EB

Plant biotechnology journal 20171227 6

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 caro ...[more]

PMID: 29193665

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Project description:BackgroundCassava (Manihot esculenta Crantz) efficiently accumulates starch in its storage roots. However, how photosynthates are transported from the leaves to the phloem (especially how they are unloaded into parenchymal cells of storage roots) remains unclear.ResultsHere, we investigated the sucrose unloading pattern and its impact on cassava storage root development using microstructural and physiological analyses, namely, carboxyfluorescein (CF) and C14 isotope tracing. The expression profiling of genes involved in symplastic and apoplastic transport was performed, which included enzyme activity, protein gel blot analysis, and transcriptome sequencing analyses. These finding showed that carbohydrates are transported mainly in the form of sucrose, and more than 54.6% was present in the stem phloem. Sucrose was predominantly unloaded symplastically from the phloem into storage roots; in addition, there was a shift from apoplastic to symplastic unloading accompanied by the onset of root swelling. Statistical data on the microstructures indicated an enrichment of plasmodesmata within sieve, companion, and parenchyma cells in the developing storage roots of a cultivar but not in a wild ancestor. Tracing tests with CF verified the existence of a symplastic channel, and [14C] Suc demonstrated that sucrose could rapidly diffuse into root parenchyma cells from phloem cells. The relatively high expression of genes encoding sucrose synthase and associated proteins appeared in the middle and late stages of storage roots but not in primary fibrous roots, or secondary fibrous roots. The inverse expression pattern of sucrose transporters, cell wall acid invertase, and soluble acid invertase in these corresponding organs supported the presence of a symplastic sucrose unloading pathway. The transcription profile of genes involved in symplastic unloading and their significantly positive correlation with the starch yield at the population level confirmed that symplastic sucrose transport is vitally important in the development of cassava storage roots.ConclusionsIn this study, we revealed that the cassava storage root phloem sucrose unloading pattern was predominantly a symplastic unloading pattern. This pattern is essential for efficient starch accumulation in high-yielding varieties compared with low-yielding wild ancestors.

Project description:Cassava (Manihot esculenta Crantz) is an essential stable food crop in Sub-Saharan Africa commonly consumed amongst the low-income communities in Africa. Though cassava roots and leaf have vast economic and commercial benefits, it produces cyanogenic glycosides, which are toxic and most often responsible for the bitter taste of some cassava cultivars. The study evaluates the cassava roots and leaves' cyanogenic potential and dry matter content of the Genetic Gain Assessment trial grown in a different environment. It establishes the association between the cyanogenic potential (CNP) and the roots and leaves dry matter (DM). Genetic Gain Assessment (GGA) cassava genotypes (N = 400) selected for the Uniform Yield Trial (UYT) breeding stage were planted under IVS (Dry season in Inland Valley Hydromorphic area) and Upland (rain-fed conditions) in two locations of IITA Research Farms, namely; Ibadan (IVS and Upland) and Mokwa (Upland) in Nigeria. The CNP content of cassava leaves in IVS, Mokwa, and Upland ranged from 3.39 to 272.16 mg/100 g, 4.28 to 228.72 mg/100 g, and 13.13 to 127.39 mg/100 g, respectively. However, the respective CNP range in root samples across IVS, Mokwa, and Upland was 0.76-76.31 mg/100 g, 0.94-136.53 mg/100 g, and 2.37-47.11 mg/100 g. Also, the mean ± SD of DM content of leaves were 27.97 ± 3.01%, 28.81 ± 4.01%, and 13.65 ± 3.69%, respectively, in IVS, Mokwa, and Upland, while the root samples had mean ± SD of DM content of 38.09 ± 4.80%, 32.69 ± ,5.93% and 24.63 ± 5.07% respectively. Furthermore, location and genotype had a highly significant effect (p < 0.001) on the CNP and DM of roots and leaves. Also, linear regressions were established between CNP and DM of root and leaf with regression equation; DM-Root = 1.1999*DM-Leaf (r = 0.956) and CNP-Root = 0.29006*CNP-Leaf (r = 0.54). The relationship between the DM (root and leaf) and CNP (root and leaf) could serve as a valuable "inter-prediction" tool for these parameters.

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

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

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