Seed Development and Differentiation: A Role for Metabolic Regulation

Abstract

During seed growth, the filial organs, Vicia embryos and barley endosperm, differentiate into highly specialized storage tissues. Differentiation is evident on structural and morphological levels and is reflected by the spatial distribution of metabolites. In Vicia embryos, glucose is spatially correlated to mitotic activity whereas elongating and starch accumulating cells contain high levels of sucrose. Seed development is also regulated by phytohormones. In pea seeds, GA-deficiency stops seed growth before maturation. In Arabidopsis seeds, ABA regulates differentiation and inhibits cell division activity. The ABA pathway, in turn, is linked to sugar responses. In young Vicia embryos, invertases in maternal tissues control both concentration and composition of sugars. Embryonic and endospermal transfer cell formation represents an early differentiation step. Establishing an epidermis-localised sucrose uptake system renders the embryo independent from maternal control. cDNA array analysis in barley seeds revealed a massive transcriptional re-programming of gene expression during the transition stage, when gene clusters related to transport and energy metabolism are highly transcribed. Sucrose represents a signal for differentiation and up-regulates storage-associated gene expression. Sucrose signalling involves protein phosphorylation. Sucrose non-fermenting-1-related protein kinases are apparently induced in response to high cellular sucrose, and could act as mediators of sucrose-specific signals. Energy metabolism changes during seed development. In Vicia embryos metabolic responses upon hypoxia and low energy charge levels are characteristic for young undifferentiated stages when energy demand and respiration are high. During the transition stage, the embryo becomes adapted to low energy availability and metabolism becomes energetically more economic and tightly controlled. These adaptations are embedded in the embryo's differentiation program and coupled with photoheterotrophic metabolism. In Vicia cotyledons, ATP content increases in a development-dependent pattern and is associated with the greening process. The main role of seed photosynthesis is to increase internal O₂ contents and to control biosynthetic fluxes by improving energy supply.

Legume and barley seed development - cell differentiation - metabolic gradients - metabolite imaging - sugar transport - transfer cells - energy metabolism.

References

• 1 Ambrose M. J., Wang T. L., Cook S. K., Hedley C. L.. An analysis of seed development in Pisum sativum L. IV. Cotyledon cell population in vitro and in vivo. .  J. Exp. Bot.. (1987);  38 1909-1920
• 2 Andersen M. N., Asch F., Wu Y., Jensen C. H., Naested H., Mogensen V. O., Koch. K. E.. Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize.  Plant Physiol.. (2002);  130 591-604
• 3 Asano T., Kunieda N., Omura Y., Ibe H., Kawasaki T., Takano M., Sato M., Furuhashi H., Mujin T., Takaiwa F., Wu C. Y., Tada Y., Satozawa T., Sakamoto M., Shimada H.. Rice SPK, a calmodulin-like domain protein kinase, is required for storage product accumulation during seed development: phosphorylation of sucrose synthase is a possible factor.  Plant Cell. (2002);  14 619-628
• 4 Asokanthan P., Johnson R. W., Griffith M., Krol M.. The photosynthetic potential of canola embryos.  Physiol Plant.. (1997);  101 353-360
• 5 Banerji D., Rauf A.. Comparative growth and biochemical studies on seed development. 3. Chlorophyll development and Hill activity in developing seeds of Pisum sativum and Vicia faba. .  Plant Biochem. J.. (1979);  6 31-35
• 6 Bonnemain J. L., Bourquin S., Renault S., Offler C., Fisher D. G.. Transfer cells: structure and physiology. Bonnemain, J. L., Delrot, S., Lucas, W. J., and Dainty, J., eds. Phloem Transport and Assimilate Compartmentation. Nantes, France; Quest Editions (1991): 178-186
• 7 Borisjuk L., Weber H., Panitz R., Manteuffel R., Wobus U.. Embryogenesis of Vicia faba L.: Histodifferentiation in relation to starch and storage protein synthesis.  J. Plant Physiol.. (1995);  147 203-218
• 8 Borisjuk L., Walenta S., Weber H., Mueller-Klieser W., Wobus U.. High resolution histographical mapping of glucose concentration in developing cotyledons of V. faba in relation to mitotic activity and starch accumulation: glucose as a possible developmental trigger.  Plant J.. (1998);  15 583-591
• 9 Borisjuk L., Walenta S., Rolletschek H., Mueller-Klieser W., Wobus U., Weber H.. Spatial analysis of plant development: Sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns.  Plant J.. (2002 a);  29 521-530
• 10 Borisjuk L., Wang T., Rolletschek H., Wobus U., Weber H.. A pea seed mutant affected in the differentiation of the embryonic epidermis leads to deregulated seed maturation and impaired embryo growth.  Development. (2002 b);  129 1595-1607
• 11 Borisjuk L., Rolletschek H., Weber H., Wobus U., Weber H.. Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds.  J. Exp. Biol.. (2003 a);  54 503-512
• 12 Borisjuk L., Rolletschek H., Walenta S., Panitz P., Wobus U., Weber H.. Energy status and its control on embryogenesis of legumes: ATP distribution within Vicia faba embryos is developmentally regulated and correlated with photosynthetic capacity.  Plant J.. (2003 b);  36 318-329
• 13 Brocard-Gifford I. M., Lynch T. J., Finkelstein R. R.. Regulatory networks in seeds integrating developmental, abscisic acid, sugar, and light signaling.  Plant Physiol.. (2003);  131 78-92
• 14 Cheng W. H., Chourey P. S.. Genetic evidence that invertase-mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize.  Theor. Appl. Gen.. (1999);  98 485-495
• 15 Cheng W. H., Talliercio E. W., Chourey P. S.. The Miniature1 seed locus of maize encodes a cell wall invertase required for normal development of endosperm and maternal cells in the pedicel.  Plant Cell. (1996);  8 971-983
• 16 Corke F. M. K., Hedley C. L., Wang T. L.. An analysis of seed development in Pisum sativum XI. Cellular development and the position of storage protein in immature embryos grown in vivo and in vitro. .  Protoplasma. (1990);  155 127-135
• 17 Eastmond P., Kolacna L., Rawsthorne S.. Photosynthesis by developing embryos of oilseed rape.  J. Exp. Bot.. (1996);  47 1763-1769
• 18 Eastmond P., Rawsthorne S.. Comparison of the metabolic properties of plastids isolated from developing leaves or embryos of Brassica napus. .  J. Exp. Bot.. (1998);  49 1105-1111
• 19 Eastmond P. J., Dijken A. J., Spielmann M., Kerr A., Tissier A. F., Dickinson H. G., Jones J. D., Smeekens S. C., Graham I. A.. Trehalose-6-P synthase1 which catalyses the first step in trehalose synthesis is essential for Arabidopsis embryo maturation.  Plant J.. (2002);  29 225-235
• 20 Emes M. J., Bowsher C. G., Hedley C., Burrell M. M., Scrase-Field E. S. F., Tetlow I. J.. Starch synthesis and carbon partitioning in developing endosperm.  J. Exp. Bot.. (2003);  54 569-575
• 21 Felker F. C., Shannon J. C.. Movement of ¹⁴C ^- labeled assimilates into kernels of Zea mays. An anatomical examination and microautoradiographic study of assimilate transfer.  Plant Physiol.. (1980);  65 864-870
• 22 Fernie A. R., Tiessen A., Stitt M., Willmitzer L., Geigenberger P.. Altered metabolic fluxes from shifts in metabolite levels in sucrose phosphorylase expressing potato tubers.  Plant Cell Environ.. (2002);  25 1219-1232
• 23 Finkelstein R., Gampala S. S. L., Rock D. C.. Abscisic acid signaling in seeds and seedlings.  Plant Cell. (2002);  14 (Suppl.) S15-S45
• 24 Flinn A. M.. Carbon dioxide fixation in developing seeds. Hebblethwaite, P. D., Heath, M. C., and Dawkins, T. C. K., eds. The Pea Crop: A Basis for Impovement. London; Butterworths (1985): 349-358
• 25 Geigenberger P., Stitt M.. Sucrose synthase catalyses a readily reversible reaction in vivo in developing potato tubers and other plant tissues.  Planta. (1993);  189 329-339
• 26 Geigenberger P.. Regulation of sucrose to starch conversion in growing potato tubers.  J. Exp. Bot.. (2003);  54 457-565
• 27 Gibson S. I.. Sugar and phytohormone response pathway: navigating a signalling network.  J. Exp. Bot.. (2004);  55 253-264
• 28 Giroux M. J., Boyer C., Feix G., Hannah L. C.. Coordinated transcriptional regulation of storage protein genes in maize endosperm.  Plant Physiol.. (1994);  106 713-722
• 29 Golombek S., Heim U., Horstmann C., Wobus U., Weber H.. PEP-carboxylase in developing seeds of Vicia faba. Gene expression and metabolic regulation.  Planta. (1999);  208 66-72
• 31 Gomez E., Royo J., Thompson R., Hueros G.. Establishment of cereal endosperm expression domains: Identification and properties of a mize transfer cell-specific transcription factor, ZmMRP-1.  Plant Cell. (2002);  14 599-610
• 30 Gomez-Cadenas A., Verhey S. D., Holappa D. L., Shen Q., Ho T. H. D., Walker-Simmons M. K.. An abscisic-acid induced protein kinase, PKABA1, mediates abscisic acid-suppressed gene expression in barley aleurone layers.  PNAS. (1999);  96 1767-1772
• 32 Halford N. G., Paul M. J.. Carbon metabolite signalling.  Plant Biotech. J.. (2003);  1 381-398
• 33 Halford N. G., Hey S., Jhurreea D., Laurie S., McKibbin R. S., Paul M., Zhang Y.. Metabolic signalling and carbon partitioning: role of Snf1-related protein kinase.  J. Ex. Bot.. (2003);  54 467-475
• 34 Harrington G. N., Franceschi V. R., Offler C. E., Patrick J. W., Tegeder M., Frommer W. B., Harper J. F., Hitz W. D.. Cell specific expression of three genes involved in plasma membrane sucrose transport in developing Vicia faba seed.  Protoplasma. (1997);  197 160-173
• 35 Harvey D. M., Hedley C. L., Keely R.. Photosynthetic and respiratory studies during pod and seed development in Pisum sativum L.  Annals of Bot.. (1976);  40 993-1001
• 36 Hedley C. L., Harvey D. M., Keely R. J.. The role of PEP-carboxylase during seed development in P. sativum. .  Nature. (1975);  258 352-354
• 37 Heim U., Weber H., Bäumlein H., Wobus U.. A sucrose-synthase gene of Vicia faba: Expression pattern in developing seeds in relation to starch synthesis and metabolic regulation.  Planta. (1993);  191 394-401
• 38 Hill L. M., Morley-Smith E. R., Rawsthorne S.. Metabolism of sugars in the endosperm of developing seeds of oilseed rape.  Plant Physiol,. (2003);  131 228-236
• 39 Johnson R. W., Asokanthan P. S., Griffith M.. Water and sucrose regulate canola embryo development.  Physiol. Plant.. (1997);  101 361-366
• 40 Koch K. E.. Carbohydrate-modulated gene expression in plants.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. (1996);  47 509-540
• 41 Kuang A., Crispi M., Musgrave M. E.. Control of seed development in Arabidopsis thaliana by atmospheric oxygen.  Plant, Cell Environ.. (1998);  21 71-78
• 42 Léon P., Sheen J.. Sugar and hormone connections.  Trends Plant Sci.. (2003);  8 110-116
• 43 Liu Y., Bergervoet J. H. W., Ric De Vos C. H., Hilhorst H. W. M., Kraak H. L., Karssen C. M., Bino R. J.. Nuclear replication activities during imbibition of abscisic acid- and gibberellin-deficient tomato seeds.  Planta. (1994);  194 368-373
• 97 Man A. L., Purcell P. C., Hannappel U., Halford N. G.. Potato SNF1-related protein kinase: molecular cloning, expression analysis and peptide kinase activity measurements.  Plant Mol. Biol.. (1997);  34 31-43
• 44 Möhlmann T., Scheibe R., Neuhaus H. E.. Interaction between starch synthesis and fatty-acid synthesis in isolated cauliflower-bud amyloplasts.  Planta. (1994);  194 492-497
• 46 Neubohn B., Gubatz S., Wobus U., Weber H.. Sugar levels altered by ectopic expression of a yest-derived invertase affects cellular differentiation of developing cotyledons on V. narbonensis. .  Planta. (2000);  211 325-334
• 45 Neuhaus H. E., Emes M. J.. Nonphotosynthetic metabolism in plastids.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. (2000);  51 111-140
• 47 Offler C. E., Liet E., Sutton E. G.. Transfer cell induction in cotyledons of V. faba. .  Protoplasma. (1997);  200 51-64
• 48 Patrick J. W., Offler C. E.. Post-sieve element transport of sucrose in developing seeds.  Aus. J. Plant Physiol.. (1995);  22 681-702
• 49 Patrick J. W., Offler C. E.. Compartmentation of transport and transfer events in developing seeds.  J. Exp. Bot.. (2001);  52 551-564
• 50 Porterfield D. M., Kuang A., Smith P. J. S., Crispi M. L., Musgrave M. E.. Oxygen-depleted zones inside reproductive structures of Brassicaceae: implications for oxygen control of seed development.  Can. J. Bot.. (1999);  77 1439-1446
• 51 Purcell P. C., Smith A. M., Halford M. G.. Antisense expression of a sucrose non-fermenting 1 related protein kinase sequence in potato results in decreased expression of sucrose synthase in zubers and loss of sucrose-inducibility of sucrose synthase transcripts in leaves.  Plant J.. (1998);  14 195-202
• 52 Quebedeaux B., Hardy R. W. F.. Reproductive growth and dry matter production of Glycine max (L.) Merr. in response to oxygen concentration.  Plant Physiol.. (1975);  55 102-107
• 53 Quick P. W., Scheibe R., Neuhaus H. E.. Induction of a hexose-phosphate translocator activity in spinach chloroplasts.  Planta. (1995);  194 193-199
• 54 Raices M., Ulloa R. M., MacIntosh G. C., Crespi M., Tellez-Inon M. T.. StCPDK1 is expressed in potato stolon tips and is induced by high sucrose concentrations.  J. Exp. Bot.. (2003);  54 2589-2591
• 55 Raz V., Bergervoet J., Koorneef M.. Sequential steps for developmental arrest in Arabidopsis seeds.  Development. (2001);  128 243-252
• 56 Rolletschek H., Borisjuk L., Koschorreck M., Wobus U., Weber H.. Legume embryos develop in a hypoxic environment.  J. Exp. Bot.. (2002);  53 1099-1107
• 57 Rolletschek H., Weber H., Borisjuk L.. Energy status and its control on embryogenesis of legumes: Embryo photosynthesis contributes to oxygen supply and is coupled to biosynthetic fluxes.  Plant Physiol.. (2003);  132 1196-1206
• 58 Rolletschek H., Borisjuk L., Radchuk R., Miranda M., Heim U., Wobus U., Weber H.. Seed-specific over-expression of phosphoenolpyruvate carboxylase in Vicia improves carbon economy and increases storage protein content.  Plant Biotech. J.. (2004 a);  in press
• 96 Rolletschek H., Weschke W., Weber H., Wobus U., Borisjuk L.. Energy state and its control on seed development: starch accumulation is associated with high ATP and steep oxygen gradients within barley grains.  J. Exp. Bot.. (2004 b);  in press
• 59 Rook F., Corke F., Card R., Munz G., Smith C., Bevan M. W.. Impaired sucrose-induction mutants reveal the modulation of sugar-induced starch biosynthetic gene expression by abscisic signalling.  Plant J.. (2001);  26 421-433
• 60 Ross H. A., Davies H. V.. Purification and characterization of sucrose synthase from the cotyledons of Vicia faba L.  Plant Physiol.. (1992);  100 1008-1013
• 61 Ruuska S. A., Girke T., Benning C., Ohlrogge J. B.. Contrapunctal networks of gene expression during Arabidopsis seed filling.  Plant Cell. (2002);  14 1191-1206
• 62 Saito G. Y., Chang Y. C., Walling L. L., Thompson W. W.. A correlation in plastid development and cytoplasmic ultrastructure with nuclear gene expression during seed ripening in soybean.  New Phytol.. (1989);  113 459-469
• 63 Silva M. P., Ricardo C. P. P.. β-fructosidases and in vitro dedifferentiation-redifferentiation of carrot cells.  Phytochem.. (1992);  31 1507-1511
• 64 Simcox P. D., Garland W., Deluca V., Canvin D. T., Dennis D. T.. Respiratory pathways and fat synthesis in the developing castor oil seed.  Can. J. Bot.. (1979);  57 1008-1014
• 65 Smeekens S.. Sugar-induced signal transduction.  Ann. Rev. Plant Physiol. Plant Mol. Biol.. (2000);  51 49-81
• 66 Sreenivasulu N., Altschmied L., Radchuk V., Gubatz S., Wobus U., Weschke W.. Transcript profiling and deduced changes of metabolic pathways in maternal and filial tissues of developing barley grains.  Plant J.. (2004);  37 539-553
• 67 Stitt M.. Nitrate regulation of metabolism and growth.  Current Opinion Plant Biol.. (1999);  2 178-186
• 68 Sturm A.. Invertases. Primary structure, functions, and roles in plant development and sucrose partitioning.  Plant Physiol.. (1999);  121 1-7
• 69 Sturm A., Tang G. Q.. The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning.  Trends Plant Sci.. (1999);  4 401-407
• 70 Swain S. M., Ross J. J., Reid J. B., Kamiya Y.. Gibberellins and pea seed development. Expression of the lhi, ls and le5839 mutations.  Planta. (1995);  195 426-433
• 71 Tegeder M., Wang X. D., Frommer W. B., Offler E. O., Patrick J. W.. Sucrose transport into developing seeds of Pisum sativum. .  Plant J.. (1999);  18 151-161
• 72 Tegeder M., Offler C. E., Frommer W. B., Patrick J. W.. Amino acid transporters are localized to transfer cells of developing pea seeds.  Plant Physiol.. (2000);  122 319-326
• 74 Thompson R. D., Hueros G., Becker H. A., Maitz M.. Development and functions of seed transfer cells.  Plant Sci.. (2001);  160 775-783
• 77 Tiessen A., Hendriks J. H. M., Stitt M., Branscheid A., Gibon Y., Farre E. M., Geigenberger P.. 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. (2002);  14 2191-2213
• 73 Tiessen A., Prescha K., Branscheid A., Palacios N., McKibban R., Halford N., Geigenberger P.. Evidence that SNF1-related kinase and hexokinase are involved in separate sugar-signalling pathways modulating pst-translational redox activation of ADP-glucose pyrophosphorylase in potato tubers.  Plant J.. (2003);  35 490-500
• 75 Trethewey R. N., Geigenberger P., Hajirezaei M., Sonnewald U., Stitt M., Riesmeier J., Willmitzer L.. Combined expression of glucokinase and invertase in potato tubers leads to a dramatic reduction in starch accumulation and a stimulation of glycolysis.  Plant J.. (1998);  15 109-118
• 76 Trethewey R. N., Fernie A. R., Bachmann A., Fleischer-Notter H., Geigenberger P., Riesmeier J., Willmitzer L.. Expression of a bacterial sucrose phosphorylase in potato tubers results in a glucose-independent induction of glycolysis.  Plant Cell Environ.. (2001);  24 357-365
• 78 Vigeolas H., van Dongen J. T., Waldeck P., Hühn D., Geigenberger P.. Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape.  Plant Physiol.. (2003);  133 2048-2060
• 79 Walenta S., Doetsch J., Mueller-Klieser W.. ATP concentrations in multicellular tumor spheroids assessed by single photon imaging and quantitative bioluminescence.  Eur. J. Cell Biol.. (1990);  52 389-393
• 80 Wang T. L., Hedley C. L.. Genetic and developmental analysis of the seed. Casey, R. and Davies, D. R., eds. Peas: Genetics, Molecular Biology and Biotechnology. Cambridge; CAB International (1993): 83-120
• 83 Weber H., Borisjuk L., Heim U., Buchner P., Wobus U.. Seed coat associated invertases of Fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression.  Plant Cell. (1995);  7 1835-1846
• 84 Weber H., Borisjuk L., Wobus U.. Controlling seed development and seed size in Vicia faba: a role for seed coat-associated invertases and carbohydrate state.  Plant J.. (1996 a);  10 823-834
• 85 Weber H., Buchner P., Borisjuk L., Wobus U.. Sucrose metabolism during cotyledon development of Vicia faba L. is controlled by the concerted action of both sucrose-phosphate synthase and sucrose synthase: Expression patterns, metabolic regulation and implications on seed development.  Plant J.. (1996 b);  9 841-850
• 86 Weber H., Borisjuk L., Heim U., Sauer N., Wobus U.. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in Fava bean seeds.  Plant Cell. (1997 a);  9 895-908
• 87 Weber H., Borisjuk L., Wobus U.. Sugar import and metabolism during seed development.  Trends Plant Sci.. (1997 b);  22 169-174
• 88 Weber H., Heim U., Golombek S., Borisjuk L., Wobus U.. Assimilate uptake and the regulation of seed development.  Seed Sci. Res.. (1998 a);  8 331-345
• 89 Weber H., Heim U., Golombek S., Borisjuk L., Manteuffel R., Wobus U.. Expression of a yeast-derived invertase in developing cotyledons of Vicia narbonensis alters the carbohydrate state and affects storage functions.  Plant J.. (1998 b);  16 163-172
• 81 Weschke W., Panitz R., Sauer N., Wang Q., Neubohn B., Weber H., Wobus U.. Sucrose transport into barley seeds: molecular characterisation of two transporters and implications for seed development and starch accumulation.  Plant J.. (2000);  21 455-467
• 82 Weschke W., Panitz R., Gubatz S., Wang Q., Radchuk R., Weber H., Wobus U.. The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development.  Plant J.. (2003);  33 395-411
• 90 Willms J. R., Salon C., Layzell D. B.. Evidence for light-stimulated fatty acid synthesis in soybean fruit.  Plant Physiol.. (1999);  120 1117-1128
• 91 Wobus U., Weber H.. Sugars as signal molecules in plant development.  Biol. Chem.. (1999 a);  380 937-944
• 92 Wobus U., Weber H.. Seed maturation: genetic programmes and control signals.  Current Opinions in Plant Biology, section Growth and Development. (1999 b);  2 33-38
• 93 Yazdi-Samadi B., Rinne R. W., Seif R. D.. Components of developing soybean seeds: oil, protein, starch, organic acids and amino acids.  Agron. J.. (1976);  69 481-486
• 94 Zhang Y., Shewry P. R., Jones H., Barcelo P., Lazzeri P. A., Halford N. G.. Expression of antisense SnRK1 protein kinase sequence causes abnormal pollen development and male sterility in transgenic barley.  Plant J.. (2001);  28 431-442
• 95 Zinselmeier C., Jeong B. R., Boyer J. S.. Starch and the control of kernel number in maize at low water potentials.  Plant Physiol.. (1999);  121 25-36

Section Editor: L. A. C. J. Voesenek