Metabolic profiles of six African cultivars of cassava (Manihot esculenta Crantz) highlight bottlenecks of root yield.
K battery
carbon fixation
cassava
chlorogenic acid
enzyme activity
nitrogen metabolism
photosynthesis
root yield
source/sink limitation
starch synthesis
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
16
10
2019
revised:
10
12
2019
accepted:
02
01
2020
pubmed:
18
1
2020
medline:
11
2
2021
entrez:
18
1
2020
Statut:
ppublish
Résumé
Cassava is an important staple crop in sub-Saharan Africa, due to its high productivity even on nutrient poor soils. The metabolic characteristics underlying this high productivity are poorly understood including the mode of photosynthesis, reasons for the high rate of photosynthesis, the extent of source/sink limitation, the impact of environment, and the extent of variation between cultivars. Six commercial African cassava cultivars were grown in a greenhouse in Erlangen, Germany, and in the field in Ibadan, Nigeria. Source leaves, sink leaves, stems and storage roots were harvested during storage root bulking and analyzed for sugars, organic acids, amino acids, phosphorylated intermediates, minerals, starch, protein, activities of enzymes in central metabolism and yield traits. High ratios of RuBisCO:phosphoenolpyruvate carboxylase activity support a C
Substances chimiques
Ribulose-Bisphosphate Carboxylase
EC 4.1.1.39
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1202-1219Subventions
Organisme : Bill & Melinda Gates Foundation
ID : OPP1113365
Pays : United States
Informations de copyright
© 2020 The Authors The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Angelov, M.N., Sun, J., Byrd, G.T., Brown, R.H. and Black, C.C. (1993) Novel characteristics of cassava, Manihot esculenta Crantz, a reputed C3-C4 intermediate photosynthesis species. Photosynth. Res. 38, 61-72.
Armengaud, P., Sulpice, R., Miller, A.J., Stitt, M., Amtmann, A. and Gibon, Y. (2009) Multilevel analysis of primary metabolism provides new insights into the role of potassium nutrition for glycolysis and nitrogen assimilation in Arabidopsis roots. Plant Physiol. 150, 772-785.
Arrivault, S., Obata, T., Szecowka, M., Mengin, V., Guenther, M., Hoehne, M., Fernie, A.R. and Stitt, M. (2017) Metabolite pools and carbon flow during C4 photosynthesis in maize: 13CO2 labeling kinetics and cell type fractionation. J. Exp. Bot. 68, 283-298.
Arrivault, S., Moraes, T.A., Obata, T. et al. (2019) Metabolite profiles reveal inter-specific variation in operation of the calvin-benson cycle in both C4 and C3 plants. J. Exp. Bot. 70(6), 1843-1858. https://doi.org/10.1093/jxb/erz051
Benard, C., Bernillon, S., Biais, B. et al. (2015) Metabolomic profiling in tomato reveals diel compositional changes in fruit affected by source-sink relationships. J. Exp. Bot. 66, 3391-3404.
Bradford, M.M. (1976) Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 72, 248-254.
Bull, S.E., Seung, D., Chanez, C. et al. (2018) Accelerated ex situ breeding of GBSS- and PTST1-edited cassava for modified starch. Sci. Adv. 4, eaat6086.
Burnett, A.C., Rogers, A., Rees, M. and Osborne, C.P. (2016) Carbon source-sink limitations differ between two species with contrasting growth strategies. Plant Cell Environ. 39, 2460-2472.
Byju, G. and Anand, M.H. (2009) Differential response of short- and long-duration cassava cultivars to applied mineral nitrogen. J. Plant Nutr. Soil Sci. 172, 572-576.
Calatayud, P.A., Baron, C.H., Velasquez, H., Arroyave, J.A. and Lamaze, T. (2002) Wild manihot species do not possess C4 photosynthesis. Ann. Bot. 89, 125-127.
Chetty, C.C., Rossin, C.B., Gruissem, W., Vanderschuren, H. and Rey, M.E. (2013) Empowering biotechnology in southern Africa: establishment of a robust transformation platform for the production of transgenic industry-preferred cassava. New Biotechnol. 30, 136-143.
Cock, J.H., Riano, N.M., El-Sharkawy, M.A., Yamel, L.F. and Bastidas, G. (1987) C3-C 4 intermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz): II. Initial products of(14)CO2 fixation. Photosynth. Res. 12, 237-241.
Couturier, J., Doidy, J., Guinet, F., Wipf, D., Blaudez, D. and Chalot, M. (2010) Glutamine, arginine and the amino acid transporter Pt-CAT11 play important roles during senescence in poplar. Ann. Bot. 105, 1159-1169.
Crozet, P., Margalha, L., Confraria, A., Rodrigues, A., Martinho, C., Adamo, M., Elias, C.A. and Baena-Gonzalez, E. (2014) Mechanisms of regulation of SNF1/AMPK/SnRK1 protein kinases. Front. Plant Sci. 5, 190.
De Souza, A.P. and Long, S.P. (2018) Toward improving photosynthesis in cassava: characterizing photosynthetic limitations in four current African cultivars. Food Energy Secur. 7, e00130.
De Souza, A.P., Massenburg, L.N., Jaiswal, D., Cheng, S., Shekar, R. and Long, S.P. (2017) Rooting for cassava: insights into photosynthesis and associated physiology as a route to improve yield potential. New Phytol. 213, 50-65.
De Souza, A.P., Wang, Y., Orr, D.J., Carmo-Silva, E. and Long, S.P. (2019) Photosynthesis across African cassava germplasm is limited by Rubisco and mesophyll conductance at steady state, but by stomatal conductance in fluctuating light. New Phytol, https://doi.org/10.1111/nph.16142.
Debast, S., Nunes-Nesi, A., Hajirezaei, M.R., Hofmann, J., Sonnewald, U., Fernie, A.R. and Bornke, F. (2011) Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol. 156, 1754-1771.
van Dongen, J.T., Schurr, U., Pfister, M. and Geigenberger, P. (2003) Phloem metabolism and function have to cope with low internal oxygen. Plant Physiol. 131, 1529-1543.
El-Sharkawy, M.A. (2004) Cassava biology and physiology. Plant Mol. Biol. 56, 481-501.
El-Sharkawy, M. (2012) Stress-tolerant cassava: the role of integrative ecophysiology-breeding research in crop improvement. Open J. Soil Sci. 02, 162-186.
El-Sharkawy, M.A. and Cock, J.H. (1987) C3-C4 intermediate photosynthetic characteristics of cassava (Manihot esculenta Crantz): I. Gas exchange. Photosynth. Res. 12, 219-235.
El-Sharkawy, M.A. and De Tafur, S.M. (2010) Comparative photosynthesis, growth, productivity, and nutrient use efficiency among tall-and short-stemmed rain-fed cassava cultivars. Photosynthetica, 48, 173-188.
Evers, D., Lefevre, I., Legay, S., Lamoureux, D., Hausman, J.F., Rosales, R.O., Marca, L.R., Hoffmann, L., Bonierbale, M. and Schafleitner, R. (2010) Identification of drought-responsive compounds in potato through a combined transcriptomic and targeted metabolite approach. J. Exp. Bot. 61, 2327-2343.
Fermont, A.M., van Asten, P.J.A., Tittonell, P.A., van Wijk, M.T. and Giller, K.E. (2009) Closing the cassava yield gap: an analysis from small-holder farms in East Africa. Field Crops Res. 112, 24-36.
Fernie, A.R., Tauberger, E., Lytovchenko, A., Roessner, U., Willmitzer, L. and Trethewey, R.N. (2002) Antisense repression of cytosolic phosphoglucomutase in potato (Solanum tuberosum) results in severe growth retardation, reduction in tuber number and altered carbon metabolism. Planta, 214, 510-520.
Figueroa, C.M. and Lunn, J.E. (2016) A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol. 172, 7-27.
Fudge, J., Mangel, N., Gruissem, W., Vanderschuren, H. and Fitzpatrick, T.B. (2017) Rationalising vitamin B6 biofortification in crop plants. Curr. Opin. Biotechnol. 44, 130-137.
Gajdanowicz, P., Michard, E., Sandmann, M. et al. (2011) Potassium (K+) gradients serve as a mobile energy source in plant vascular tissues. Proc. Natl Acad. Sci. USA, 108, 864-869.
Geigenberger, P., Stitt, M. and Fernie, A.R. (2004) Metabolic control analysis and regulation of the conversion of sucrose to starch in growing potato tubers. Plant, Cell Environ. 27, 655-673.
Giaquinta, R. (1980) Mechanism and control of phloem loading of sucrose. Ber. Deut. Bot. Ges. 93, 187-201.
Gibon, Y., Blaesing, O.E., Hannemann, J., Carillo, P., Hohne, M., Hendriks, J.H., Palacios, N., Cross, J., Selbig, J. and Stitt, M. (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. Plant Cell, 16, 3304-3325.
Gleadow, R.M. and Moller, B.L. (2014) Cyanogenic glycosides: synthesis, physiology, and phenotypic plasticity. Annu. Rev. Plant Biol. 65, 155-185.
Henkes, S., Sonnewald, U., Badur, R., Flachmann, R. and Stitt, M. (2001) A small decrease of plastid transketolase activity in antisense tobacco transformants has dramatic effects on photosynthesis and phenylpropanoid metabolism. Plant Cell, 13, 535-551.
Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kamper, J., Sonnewald, U. and Voll, L.M. (2010a) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.
Horst, R.J., Doehlemann, G., Wahl, R., Hofmann, J., Schmiedl, A., Kahmann, R., Kämper, J., Sonnewald, U. and Voll, L.M. (2010b) Ustilago maydis infection strongly alters organic nitrogen allocation in maize and stimulates productivity of systemic source leaves. Plant Physiol. 152, 293-308.
Howeler, R., Lutaladio, N. and Thomas, G. (2013) Save and Grow: Cassava. A Guide to Sustainable Production Intensification. Rome, Italy: Food and Agriculture Organization of the United Nations.
Ihemere, U., Arias-Garzon, D., Lawrence, S. and Sayre, R. (2006) Genetic modification of cassava for enhanced starch production. Plant Biotechnol. J. 4, 453-465.
Jonik, C., Sonnewald, U., Hajirezaei, M.R., Flugge, U.I. and Ludewig, F. (2012) Simultaneous boosting of source and sink capacities doubles tuber starch yield of potato plants. Plant Biotechnol. J. 10, 1088-1098.
Jorgensen, K., Bak, S., Busk, P.K., Sorensen, C., Olsen, C.E., Puonti-Kaerlas, J. and Moller, B.L. (2005) Cassava plants with a depleted cyanogenic glucoside content in leaves and tubers. Distribution of cyanogenic glucosides, their site of synthesis and transport, and blockage of the biosynthesis by RNA interference technology. Plant Physiol. 139, 363-374.
Jung, B., Ludewig, F., Schulz, A. et al. (2015) Identification of the transporter responsible for sucrose accumulation in sugar beet taproots. Nat. Plants, 1, 14001.
Klaumann, S., Nickolaus, S.D., Furst, S.H., Starck, S., Schneider, S., Neuhaus, H.E. and Trentmann, O. (2011) The tonoplast copper transporter COPT5 acts as an exporter and is required for interorgan allocation of copper in Arabidopsis thaliana. New Phytol. 192, 393-404.
Kopka, J., Schauer, N., Krueger, S. et al. (2005) GMD@CSB.DB: the Golm metabolome database. Bioinformatics, 21, 1635-1638.
Latif, S. and Muller, J. (2015) Potential of cassava leaves in human nutrition: a review. Trends Food Sci. Technol. 44, 147-158.
Leyva, R., Constan-Aguilar, C., Blasco, B., Sanchez-Rodriguez, E., Romero, L., Soriano, T. and Ruiz, J.M. (2014) Effects of climatic control on tomato yield and nutritional quality in Mediterranean screenhouse. J. Sci. Food Agric. 94, 63-70.
Li, K.T., Moulin, M., Mangel, N., Albersen, M., Verhoeven-Duif, N.M., Ma, Q., Zhang, P., Fitzpatrick, T.B., Gruissem, W. and Vanderschuren, H. (2015) Increased bioavailable vitamin B6 in field-grown transgenic cassava for dietary sufficiency. Nat. Biotechnol. 33, 1029-1032.
Lisec, J., Schauer, N., Kopka, J., Willmitzer, L. and Fernie, A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat. Protoc. 1, 387-396.
Luedemann, A., Strassburg, K., Erban, A. and Kopka, J. (2008) TagFinder for the quantitative analysis of gas chromatography - mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics, 24, 732-737.
Lukuyu, B., Okike, I., Duncan, A., Beveridge, M. and Blummel, M. (2014) Use of Cassava in Livestock and Aquaculture Feeding Programs. ILRI Discussion Paper. Nairobi, Kenya: International Livestock Research Institute.
Lunn, J.E., Delorge, I., Figueroa, C.M., Van Dijck, P. and Stitt, M. (2014) Trehalose metabolism in plants. Plant J. 79, 544-567.
Mengel, K. and Haeder, H.E. (1977) Effect of potassium supply on the rate of phloem sap exudation and the composition of phloem sap of Ricinus communis. Plant Physiol. 59, 282-284.
Minchin, P.E.H. and Thorpe, M.R. (1987) Measurement of unloading and reloading of photoassimilate within the stem of bean. J. Exp. Bot. 38, 211-220.
Nartey, F. (1969) Studies on cassava, Manihot utilissima. II. Biosynthesis of asparagine-14C from 14C-labelled hydrogen cyanide and its relations with cyanogenesis. Physiol. Plant. 22, 1085-1096.
Nielsen, T.H., Krapp, A., Röper-Schwarz, U. and Stitt, M. (1998) The sugar-mediated regulation of genes encoding the small subunit of Rubisco and the regulatory subunit of ADP glucose pyrophosphorylase is modified by phosphate and nitrogen. Plant, Cell Environ. 21, 443-454.
Nordin, A. and Nasholm, T. (1997) Nitrogen storage forms in nine boreal understorey plant species. Oecologia, 110, 487-492.
Pellet, D. and El-Sharkawy, M.A. (1993) Cassava varietal response to phosphorus fertilization. I. Yield, biomass and gas exchange. Field Crop Res. 35, 1-11.
Picmanova, M., Neilson, E.H., Motawia, M.S. et al. (2015) A recycling pathway for cyanogenic glycosides evidenced by the comparative metabolic profiling in three cyanogenic plant species. Biochem. J. 469, 375-389.
Prajapati, K. (2012) The importance of potassium in plant growth - a review. Indian J. Plant Sci. 1, 177-186.
Roessner, U., Wagner, C., Kopka, J., Trethewey, R.N. and Willmitzer, L. (2000) Technical advance: simultaneous analysis of metabolites in potato tuber by gas chromatography-mass spectrometry. Plant J. 23, 131-142.
Roessner-Tunali, U. (2003) Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol. 133, 84-99.
Rosenthal, D.M., Slattery, R.A., Miller, R.E., Grennan, A.K., Cavagnaro, T.R., Fauquet, C.M., Gleadow, R.M. and Ort, D.R. (2012) Cassava about-FACE: greater than expected yield stimulation of cassava (Manihot esculenta) by future CO2 levels. Glob. Change Biol. 18, 2661-2675.
Sayre, R., Beeching, J.R., Cahoon, E.B. et al. (2011) The BioCassava plus program: biofortification of cassava for sub-Saharan Africa. Annu. Rev. Plant Biol. 62, 251-272.
Schauer, N., Zamir, D. and Fernie, A.R. (2005) Metabolic profiling of leaves and fruit of wild species tomato: a survey of the Solanum lycopersicum complex. J. Exp. Bot. 56, 297-307.
Scheible, W.R., Gonzalez-Fontes, A., Lauerer, M., Muller-Rober, B., Caboche, M. and Stitt, M. (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell, 9, 783-798.
Siritunga, D. and Sayre, R. (2004) Engineering cyanogen synthesis and turnover in cassava (Manihot esculenta). Plant Mol. Biol. 56, 661-669.
Smidansky, E.D., Meyer, F.D., Blakeslee, B., Weglarz, T.E., Greene, T.W. and Giroux, M.J. (2007) Expression of a modified ADP-glucose pyrophosphorylase large subunit in wheat seeds stimulates photosynthesis and carbon metabolism. Planta, 225, 965-976.
Sonnewald, U. and Fernie, A.R. (2018) Next-generation strategies for understanding and influencing source-sink relations in crop plants. Curr. Opin. Plant Biol. 43, 63-70.
Steinhauser, M.C., Steinhauser, D., Koehl, K., Carrari, F., Gibon, Y., Fernie, A.R. and Stitt, M. (2010) Enzyme activity profiles during fruit development in tomato cultivars and Solanum pennellii. Plant Physiol. 153, 80-98.
Stitt, M., Muller, C., Matt, P., Gibon, Y., Carillo, P., Morcuende, R., Scheible, W.R. and Krapp, A. (2002) Steps towards an integrated view of nitrogen metabolism. J. Exp. Bot. 53, 959-970.
Stitt, M., Lunn, J. and Usadel, B. (2010) Arabidopsis and primary photosynthetic metabolism - more than the icing on the cake. Plant J. 61, 1067-1091.
Sulpice, R., Tschoep, H., Von Korff, M., Buessis, D., Usadel, B., Hoehne, M., Witucka-Wall, H., Altmann, T., Stitt, M. and Gibon, Y. (2007) Description and applications of a rapid and sensitive non-radioactive microplate-based assay for maximum and initial activity of D-ribulose-1,5-bisphosphate carboxylase/oxygenase. Plant, Cell Environ. 30, 1163-1175.
Sweetlove, L.J., Kossmann, J., Riesmeier, J.W., Trethewey, R.N. and Hill, S.A. (1998) The control of source to sink carbon flux during tuber development in potato. Plant J. 15, 697-706.
Sweetlove, L.J., Nielsen, J. and Fernie, A.R. (2017) Engineering central metabolism - a grand challenge for plant biologists. Plant J. 90, 749-763.
Szecowka, M., Heise, R., Tohge, T. et al. (2013) Metabolic fluxes in an illuminated Arabidopsis rosette. Plant Cell, 25, 694-714.
Tamoi, M., Nagaoka, M., Miyagawa, Y. and Shigeoka, S. (2006) Contribution of fructose-1,6-bisphosphatase and sedoheptulose-1,7-bisphosphatase to the photosynthetic rate and carbon flow in the Calvin cycle in transgenic plants. Plant Cell Physiol. 47, 380-390.
Tiessen, A., Hendriks, J.H., Stitt, M., Branscheid, A., Gibon, Y., Farre, E.M. and Geigenberger, P. (2002) Starch synthesis in potato tubers is regulated by post-translational redox modification of ADP-glucose pyrophosphorylase: a novel regulatory mechanism linking starch synthesis to the sucrose supply. Plant Cell, 14, 2191-2213.
Tohge, T. and Fernie, A.R. (2017) Leveraging natural variance towards enhanced understanding of phytochemical sunscreens. Trends Plant Sci., 22, 308-315.
Trankner, M., Tavakol, E. and Jakli, B. (2018) Functioning of potassium and magnesium in photosynthesis, photosynthate translocation and photoprotection. Physiol. Plant. 163(3), 414-431. https://doi.org/10.1111/ppl.12747.
Wang, L., Czedik-Eysenberg, A., Mertz, R.A. et al. (2014) Comparative analyses of C(4) and C(3) photosynthesis in developing leaves of maize and rice. Nat. Biotechnol. 32, 1158-1165.
White, A.C., Rogers, A., Rees, M. and Osborne, C.P. (2016) How can we make plants grow faster? A source-sink perspective on growth rate. J. Exp. Bot. 67, 31-45.
Zeeman, S.C., Kossmann, J. and Smith, A.M. (2010) Starch: its metabolism, evolution, and biotechnological modification in plants. Annu. Rev. Plant Biol. 61, 209-234.
Zhai, Z., Keereetaweep, J., Liu, H., Feil, R., Lunn, J.E. and Shanklin, J. (2018) Trehalose 6-phosphate positively regulates fatty acid synthesis by stabilizing WRINKLED1. Plant Cell, 30, 2616-2627.
Zhang, Y., Primavesi, L.F., Jhurreea, D., Andralojc, P.J., Mitchell, R.A., Powers, S.J., Schluepmann, H., Delatte, T., Wingler, A. and Paul, M.J. (2009) Inhibition of SNF1-related protein kinase1 activity and regulation of metabolic pathways by trehalose-6-phosphate. Plant Physiol. 149, 1860-1871.