Abstract
Seeds are one of the most important food sources, providing humans and animals with essential nutrients. These nutrients include carbohydrates, lipids, proteins, vitamins and minerals. Carbohydrates are one of the main energy sources for both plant and animal cells and play a fundamental role in seed development, human nutrition and the food industry. Many studies have focused on the molecular pathways that control carbohydrate flow during seed development in monocot and dicot species. For this reason, an overview of seed biodiversity focused on the multiple metabolic and physiological mechanisms that govern seed carbohydrate storage function in the plant kingdom is required. A large number of mutants affecting carbohydrate metabolism, which display defective seed development, are currently available for many plant species. The physiological, biochemical and biomolecular study of such mutants has led researchers to understand better how metabolism of carbohydrates works in plants and the critical role that these carbohydrates, and especially starch, play during seed development. In this review, we summarize and analyze the newest findings related to carbohydrate metabolism’s effects on seed development, pointing out key regulatory genes and enzymes that influence seed sugar import and metabolism. Our review also aims to provide guidelines for future research in the field and in this way to assist seed quality optimization by targeted genetic engineering and classical breeding programs.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- AGP:
-
ADPG pyrophosphorylase
- ADPG:
-
ADP-glucose
- CW:
-
Cell wall
- DAP:
-
Days after pollination
- DBE:
-
Starch-debranching enzyme
- FRK:
-
Fructokinase
- G1P:
-
Glucose-1-phosphate
- GBSSI:
-
Granule-bound starch synthase I
- GWD:
-
Glucan, water dikinases
- PK:
-
Piruvate kinase
- SBE:
-
Starch-branching enzymes
- SS:
-
Starch synthase
- SuSy:
-
Sucrose synthase
- SUT:
-
SUC transporters
- UDPG:
-
UDP-glucose
References
Adhikari ND, Bates PD, Browse J (2016) WRINKLED1 rescues feedback inhibition of fatty acid synthesis in hydroxylase-expressing seeds. Plant Physiol 171:179–191. https://doi.org/10.1104/pp.15.01906
Akande TO, Odunsi AA, Olabode OS, Ojediran TK (2012) Physical and nutrient characterisation of raw and processed castor (Ricinus communis L.) seeds in Nigeria department of animal nutrition and biotechnology, Department of Crop Production System. World J Agric Sci 8:89–95
Ambrose MJ, Wang TL, Cook SK, Hedley CL (1987) An analysis of seed development in Pisum sativum: IV. Cotyledon cell populations in vivo and in vitro. J Exp Bot 38:1909–1920. https://doi.org/10.1093/jxb/38.11.1909
An D, Kim H, Ju S et al (2017) Expression of camelina WRINKLED1 isoforms rescue the seed phenotype of the Arabidopsis wri1 mutant and increase the triacylglycerol content in tobacco leaves. Front Plant Sci 8:34. https://doi.org/10.3389/fpls.2017.00034
Andersen MN (2002) Soluble invertase expression is an early target of drought stress during the critical, abortion-sensitive phase of young ovary development in maize. Plant Physiol 130:591–604. https://doi.org/10.1104/pp.005637
Andre C, Froehlich JE, Moll MR, Benning C (2007) A heteromeric plastidic pyruvate kinase complex involved in seed oil biosynthesis in Arabidopsis. Plant Cell 19:2006–2022. https://doi.org/10.1105/tpc.106.048629
Andriotis VME, Pike MJ, Kular B et al (2010) Starch turnover in developing oilseed embryos. New Phytol 187:791–804. https://doi.org/10.1111/j.1469-8137.2010.03311.x
Andriotis VME, Pike MJ, Schwarz SL et al (2012) Altered starch turnover in the maternal plant has major effects on arabidopsis fruit growth and seed composition. Plant Physiol 160:1175–1186. https://doi.org/10.1104/pp.112.205062
Angeles-Núñez JG, Tiessen A (2010) Arabidopsis sucrose synthase 2 and 3 modulate metabolic homeostasis and direct carbon towards starch synthesis in developing seeds. Planta 232:701–718. https://doi.org/10.1007/s00425-010-1207-9
Angeles-Núñez JG, Tiessen A (2011) Mutation of the transcription factor LEAFY COTYLEDON 2 alters the chemical composition of Arabidopsis seeds, decreasing oil and protein content, while maintaining high levels of starch and sucrose in mature seeds. J Plant Physiol 168:1891–1900. https://doi.org/10.1016/j.jplph.2011.05.003
Angeles-Núñez JG, Tiessen A (2012) Regulation of AtSUS2 and AtSUS3 by glucose and the transcription factor LEC2 in different tissues and at different stages of Arabidopsis seed development. Plant Mol Biol 78:377–392. https://doi.org/10.1007/s11103-011-9871-0
Aoki N, Whitfeld P, Hoeren F et al (2002) Three sucrose transporter genes are expressed in the developing grain of hexaploid wheat. Plant Mol Biol 50:453–462. https://doi.org/10.1023/A:1019846832163
Auger B, Marnet N, Gautier V et al (2010) A detailed survey of seed coat flavonoids in developing seeds of Brassica napus L. J Agric Food Chem 58:6246–6256. https://doi.org/10.1021/jf903619v
Bahaji A, Li J, Ovecka M et al (2011) Arabidopsis thaliana mutants lacking ADP-glucose pyrophosphorylase accumulate starch and wild-type ADP-glucose content: further evidence for the occurrence of important sources, other than ADP-glucose pyrophosphorylase, of ADP-glucose linked to leaf starch biosynthesis. Plant Cell Physiol 52:1162–1176. https://doi.org/10.1093/pcp/pcr067
Bahaji A, Baroja-Fernández E, Ricarte-Bermejo A et al (2015) Characterization of multiple SPS knockout mutants reveals redundant functions of the four Arabidopsis sucrose phosphate synthase isoforms in plant viability, and strongly indicates that enhanced respiration and accelerated starch turnover can alleviate the blockage of sucrose biosynthesis. Plant Sci 238:135–147. https://doi.org/10.1016/j.plantsci.2015.06.009
Bala M, Nag TN, Kumar S et al (2011) Proximate composition and fatty acid profile of Pongamia pinnata, a potential biodiesel crop. J Am Oil Chem Soc 88:559–562. https://doi.org/10.1007/s11746-010-1699-2
Baroja-Fernández E, Muñoz FJ, Saikusa T et al (2003) Sucrose synthase catalyzes the de novo production of ADP-glucose linked to starch biosynthesis in heterotrophic tissues of plants. Plant Cell Physiol 44:500–509. https://doi.org/10.1093/pcp/pcg062
Barthet VJ, Daun JK (2011) Seed morphology, composition, and quality. In: Daun JK, Michael Eskin NA, Hickling D (eds) Canola: chemistry, production, processing, and utilization. Elsevier, Amsterdam, pp 119–162
Baud S, Graham IA (2006) A spatiotemporal analysis of enzymatic activities associated with carbon metabolism in wild-type and mutant embryos of Arabidopsis using in situ histochemistry. Plant J 46:155–169. https://doi.org/10.1111/j.1365-313X.2006.02682.x
Baud S, Boutin JP, Miquel M et al (2002) An integrated overview of seed development in Arabidopsis thaliana ecotype WS. Plant Physiol Biochem 40:151–160. https://doi.org/10.1016/S0981-9428(01)01350-X
Baud S, Wuillème S, Lemoine R et al (2005) The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J 43:824–836. https://doi.org/10.1111/j.1365-313X.2005.02496.x
Baud S, Mendoza MS, To A et al (2007) WRINKLED1 specifies the regulatory action of LEAFY COTYLEDON2 towards fatty acid metabolism during seed maturation in Arabidopsis. Plant J 50:825–838. https://doi.org/10.1111/j.1365-313X.2007.03092.x
Baud S, Dubreucq B, Miquel M et al (2008) Storage reserve accumulation in arabidopsis: metabolic and developmental control of seed filling. Arab B 6:e0113. https://doi.org/10.1199/tab.0113
Baud S, Wuillème S, To A et al (2009) Role of WRINKLED1 in the transcriptional regulation of glycolytic and fatty acid biosynthetic genes in Arabidopsis. Plant J 60:933–947. https://doi.org/10.1111/j.1365-313X.2009.04011.x
Beloshapka A, Buff P, Fahey G, Swanson K (2016) Compositional analysis of whole grains, processed grains, grain co-products, and other carbohydrate sources with applicability to pet animal nutrition. Foods 5:23. https://doi.org/10.3390/foods5020023
Bentsink L, Koornneef M (2008) Seed dormancy and germination. Arab B 6:e0119. https://doi.org/10.1199/tab.0119
Bergareche D, Royo J, Muñiz LM, Hueros G (2018) Cell wall invertase activity regulates the expression of the transfer cell-specific transcription factor ZmMRP-1. Planta 247:429–442. https://doi.org/10.1007/s00425-017-2800-y
Berger F (2003) Endosperm: the crossroad of seed development. Curr Opin Plant Biol 6:42–50. https://doi.org/10.1016/S1369526602000043
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy, 3rd edn. Springer, New York
Bhattacharyya M, Martin C, Smith A (1993) The importance of starch biosynthesis in the wrinkled seed shape character of peas studied by Mendel. Plant Mol Biol 22:525–531. https://doi.org/10.1007/BF00015981
Bihmidine S, Hunter CT, Johns CE et al (2013) Regulation of assimilate import into sink organs: update on molecular drivers of sink strength. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00177
Bihmidine S, Julius BT, Dweikat I, Braun DM (2016) Tonoplast sugar transporters (SbTSTs) putatively control sucrose accumulation in sweet sorghum stems. Plant Signal Behav 11:e1117721. https://doi.org/10.1080/15592324.2015.1117721
Boehlein SK, Shaw JR, Stewart JD et al (2015) Enhancing the heat stability and kinetic parameters of the maize endosperm ADP-glucose pyrophosphorylase using iterative saturation mutagenesis. Arch Biochem Biophys 568:28–37. https://doi.org/10.1016/J.ABB.2015.01.008
Borisjuk L, Walenta S, Weber H et al (1998) High-resolution histographical mapping of glucose concentrations in developing cotyledons of Vicia faba in relation to mitotic activity and storage processes: glucose as a possible developmental trigger. Plant J 15:583–591. https://doi.org/10.1046/j.1365-313X.1998.00214.x
Borisjuk L, Wang TL, Rolletschek H et al (2002) A pea seed mutant affected in the differentiation of the embryonic epidermis is impaired in embryo growth and seed maturation. Development 129:1595–1607
Bowsher CG, Scrase-Field EFAL, Esposito S et al (2007) Characterization of ADP-glucose transport across the cereal endosperm amyloplast envelope. J Exp Bot 58:1321–1332. https://doi.org/10.1093/jxb/erl297
Boyer L, Roussel X, Courseaux A et al (2016) Expression of Escherichia coli glycogen branching enzyme in an Arabidopsis mutant devoid of endogenous starch branching enzymes induces the synthesis of starch-like polyglucans. Plant, Cell Environ 39:1432–1447. https://doi.org/10.1111/pce.12702
Brandt R, Mascher M, Thiel J (2018) Laser capture microdissection-based RNA-Seq of barley grain tissues. Methods Protoc 1723:397–409. https://doi.org/10.1007/978-1-4939-7558-7_23
Chateigner-Boutin A-L, Ordaz-Ortiz JJ, Alvarado C et al (2016) Developing pericarp of maize: a model to study arabinoxylan synthesis and feruloylation. Front Plant Sci 7:1476. https://doi.org/10.3389/fpls.2016.01476
Chen G, Deng W, Peng F et al (2013) Brassica napus TT16 homologs with different genomic origins and expression levels encode proteins that regulate a broad range of endothelium-associated genes at the transcriptional level. Plant J 74:663–677. https://doi.org/10.1111/tpj.12151
Chen H-Y, Huh J-H, Yu Y-C et al (2015a) The Arabidopsis vacuolar sugar transporter SWEET2 limits carbon sequestration from roots and restricts Pythium infection. Plant J 83:1046–1058. https://doi.org/10.1111/tpj.12948
Chen L-Q, Lin IW, Qu X-Q et al (2015b) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the arabidopsis embryo. Plant Cell 27:607–619. https://doi.org/10.1105/tpc.114.134585
Cheng WH, Chourey PS (1999) Genetic evidence that invertase-mediated release of hexoses is critical for appropriate carbon partitioning and normal seed development in maize. Theor Appl Genet 98:485–495. https://doi.org/10.1007/s001220051096
Cheng W, Taliercio E, Chourey P (1996) 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 8:971–983. https://doi.org/10.1105/tpc.8.6.971
Chia TYP, Pike MJ, Rawsthorne S (2005) Storage oil breakdown during embryo development of Brassica napus (L.). J Exp Bot 56:1285–1296. https://doi.org/10.1093/jxb/eri129
Chourey PS, Taliercio EW, Carlson SJ, Ruan YL (1998) Genetic evidence that the two isozymes of sucrose synthase present in developing maize endosperm are critical, one for cell wall integrity and the other for starch biosynthesis. Mol Gen Genet 259:88–96. https://doi.org/10.1007/s004380050792
Chourey PS, Li QB, Cevallos-Cevallos J (2012) Pleiotropy and its dissection through a metabolic gene Miniature1 (Mn1) that encodes a cell wall invertase in developing seeds of maize. Plant Sci 184:45–53. https://doi.org/10.1016/j.plantsci.2011.12.011
Cimini S, Locato V, Vergauwen R et al (2015) Fructan biosynthesis and degradation as part of plant metabolism controlling sugar fluxes during durum wheat kernel maturation. Front Plant Sci 6:89. https://doi.org/10.3389/fpls.2015.00089
Collard BC, Mackill DJ (2008) Marker-assisted selection: an approach for precision plant breeding in the twenty-first century. Philos Trans R Soc B Biol Sci 363:557–572. https://doi.org/10.1098/rstb.2007.2170
Colleoni C, Dauvill D, Mouille G et al (1999) Biochemical characterization of the chlamydomonas reinhardtii alpha-1,4 glucanotransferase supports a direct function in amylopectin biosynthesis. Plant Physiol 120:1005–1014
Costa LM, Marshall E, Tesfaye M et al (2014) Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 344(6180):168–172. https://doi.org/10.1126/science.1243005
Craig J, Barratt P, Tatge H et al (1999) Mutations at the rug4 locus alter the carbon and nitrogen metabolism of pea plants through an effect on sucrose synthase. Plant J 17:353–362. https://doi.org/10.1046/j.1365-313X.1999.00382.x
Creff A, Brocard L, Ingram G (2015) A mechanically sensitive cell layer regulates the physical properties of the Arabidopsis seed coat. Nat Commun 6:1–8. https://doi.org/10.1038/ncomms7382
Crofts N, Abe K, Aihara S et al (2012) Lack of starch synthase IIIa and high expression of granule-bound starch synthase I synergistically increase the apparent amylose content in rice endosperm. Plant Sci 193–194:62–69. https://doi.org/10.1016/j.plantsci.2012.05.006
Dam S, Laursen BS, Ornfelt JH et al (2009) The proteome of seed development in the model legume Lotus japonicus. Plant Physiol 149:1325–1340. https://doi.org/10.1104/pp.108.133405
Dante RA, Larkins BA, Sabelli PA (2014) Cell cycle control and seed development. Front Plant Sci 5:493. https://doi.org/10.3389/fpls.2014.00493
Dasgupta K, Khadilkar AS, Sulpice R et al (2014) Expression of sucrose transporter cDNAs specifically in companion cells enhances phloem loading and long-distance transport of sucrose but leads to an inhibition of growth and the perception of a phosphate limitation. Plant Physiol 165:715–731. https://doi.org/10.1104/pp.114.238410
Dauvillée D, Chochois V, Steup M et al (2006) Plastidial phosphorylase is required for normal starch synthesis in Chlamydomonas reinhardtii. Plant J 48:274–285. https://doi.org/10.1111/j.1365-313X.2006.02870.x
De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20(11):591–597. https://doi.org/10.1016/j.tree.2005.07.008
Dinges JR, Colleoni C, Myers AM, James MG (2001) Molecular structure of three mutations at the maize sugary1 locus and their allele-specific phenotypic effects. Plant Physiol 125:1406–1418
Djemel N, Guedon D, Lechevalier A et al (2005) Development and composition of the seeds of nine genotypes of the Medicago truncatula species complex. Plant Physiol Biochem 43:557–566. https://doi.org/10.1016/j.plaphy.2005.04.005
Doughty J, Aljabri M, Scott RJ (2014) Flavonoids and the regulation of seed size in Arabidopsis. Biochem Soc Trans 42:364–369. https://doi.org/10.1042/BST20140040
Draper J (1997) Salicylate, superoxide synthesis and cell suicide in plant defence. Trends Plant Sci 2:162–165. https://doi.org/10.1016/S1360-1385(97)85222-3
Durand M, Mainson D, Porcheron B et al (2017) Carbon source–sink relationship in Arabidopsis thaliana: the role of sucrose transporters. Planta 247:1–25. https://doi.org/10.1007/s00425-017-2807-4
Ehlers K, Bhide AS, Tekleyohans DG et al (2016) The MADS box genes ABS, SHP1, and SHP2 are essential for the coordination of cell divisions in ovule and seed coat development and for endosperm formation in Arabidopsis thaliana. PLoS ONE 11:e0165075. https://doi.org/10.1371/journal.pone.0165075
Ekop AS (2007) Determination of chemical composition of Gnetum africanum (AFANG) seeds. Pakistan J Nutr 6:40–43. https://doi.org/10.3923/pjn.2007.40.43
Etchells JP, Moore L, Jiang WZ et al (2012) A role for BELLRINGER in cell wall development is supported by loss-of-function phenotypes. BMC Plant Biol 12:1. https://doi.org/10.1186/1471-2229-12-212
Faix B, Radchuk V, Nerlich A et al (2012) Barley grains, deficient in cytosolic small subunit of ADP-glucose pyrophosphorylase, reveal coordinate adjustment of C:N metabolism mediated by an overlapping metabolic-hormonal control. Plant J 69:1077–1093. https://doi.org/10.1111/j.1365-313X.2011.04857.x
Fallahi H, Scofield GN, Badger MR et al (2008) Localization of sucrose synthase in developing seed and siliques of Arabidopsis thaliana reveals diverse roles for SUS during development. J Exp Bot 59:3283–3295. https://doi.org/10.1093/jxb/ern180
Fatihi A, Zbierzak AM, Dormann P (2013) Alterations in seed development gene expression affect size and oil content of Arabidopsis seeds. Plant Physiol 163:973–985. https://doi.org/10.1104/pp.113.226761
Fatland BL (2005) Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell Online 17:182–203. https://doi.org/10.1105/tpc.104.026211
Fiume E, Fletcher JC (2012) Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 24:1000–1012. https://doi.org/10.1105/tpc.111.094839
Fouquet R, Martin F, Fajardo DS et al (2011) Maize rough endosperm3 encodes an RNA splicing factor required for endosperm cell differentiation and has a nonautonomous effect on embryo development. Plant Cell 23:4280–4297. https://doi.org/10.1105/tpc.111.092163
Fu F-F, Xue H-W (2010) Coexpression analysis identifies rice starch Regulator1, a Rice AP2/EREBP family transcription factor, as a novel rice starch biosynthesis regulator. Plant Physiol 154:927–938. https://doi.org/10.1104/pp.110.159517
Fujita N, Yoshida M, Kondo T et al (2007) Characterization of SSIIIa-deficient mutants of rice: the function of SSIIIa and pleiotropic effects by SSIIIa deficiency in the rice endosperm. Plant Physiol 144:2009–2023. https://doi.org/10.1104/pp.107.102533
Fujita N, Satoh R, Hayashi A et al (2011) Starch biosynthesis in rice endosperm requires the presence of either starch synthase I or IIIa. J Exp Bot 62:4819–4831. https://doi.org/10.1093/jxb/err125
Fulton DC, Stettler M, Mettler T et al (2008) AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active β-amylases in Arabidopsis chloroplasts. Plant Cell Online 20:1040–1058. https://doi.org/10.1105/tpc.107.056507
Gómez LD, Baud S, Graham IA (2005) The role of trehalose-6-phosphate synthase in Arabidopsis embryo development. Biochem Soc Trans 33:280–282. https://doi.org/10.1042/BST0330280
Gómez LD, Baud S, Gilday A et al (2006) Delayed embryo development in the ARABIDOPSIS TREHALOSE-6-PHOSPHATE SYNTHASE 1 mutant is associated with altered cell wall structure, decreased cell division and starch accumulation. Plant J 46:69–84. https://doi.org/10.1111/j.1365-313X.2006.02662.x
Griffiths JS, Šola K, Kushwaha R et al (2015) Unidirectional movement of cellulose synthase complexes in Arabidopsis seed coat epidermal cells deposit cellulose involved in mucilage extrusion, adherence, and ray formation. Plant Physiol 168(2):502–520. https://doi.org/10.1104/pp.15.00478
Griffiths CA, Paul MJ, Foyer CH (2016) Metabolite transport and associated sugar signalling systems underpinning source/sink interactions. Biochim Biophys Acta Bioenerg 1857:1715–1725. https://doi.org/10.1016/j.bbabio.2016.07.007
Guillon F, Larré C, Petipas F et al (2012) A comprehensive overview of grain development in Brachypodium distachyon variety Bd21. J Exp Bot 63:739–755. https://doi.org/10.1093/jxb/err298
Guo X, Duan X, Wu Y et al (2018) Genetic engineering of maize (Zea mays L.) with improved grain nutrients. J Agric Food Chem. https://doi.org/10.1021/acs.jafc.7b05390
Habib HM, Ibrahim WH (2009) Nutritional quality evaluation of eighteen date pit varieties. Int J Food Sci Nutr 60:99–111. https://doi.org/10.1080/09637480802314639
Hannah LC, Shaw JR, Giroux MJ et al (2001) Maize genes encoding the small subunit of ADP-glucose pyrophosphorylase. Plant Physiol 127:173–183. https://doi.org/10.1104/pp.127.1.173
Hashida Y, Hirose T, Okamura M et al (2016) A reduction of sucrose phosphate synthase (SPS) activity affects sucrose/starch ratio in leaves but does not inhibit normal plant growth in rice. Plant Sci 253:40–49. https://doi.org/10.1016/J.PLANTSCI.2016.08.017
Hedhly A, Vogler H, Schmid MW et al (2016) Starch turnover and metabolism during flower and early embryo development. Plant Physiol 172:2388–2402. https://doi.org/10.1104/pp.16.00916
Hehenberger E, Kradolfer D, Kohler C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139:2031–2039. https://doi.org/10.1242/dev.077057
Herbers K, Sonnewald U (1998) Molecular determinants of sink strength. Curr Opin Plant Biol 1:207–216. https://doi.org/10.1016/S1369-5266(98)80106-4
Herchi W, Al Hujaili AD, Sakouhi F et al (2014) Flaxseed hull: chemical composition and antioxidant activity during development. J Oleo Sci 63:681–689. https://doi.org/10.5650/jos.ess14006
Hills MJ (2004) Control of storage-product synthesis in seeds. Curr Opin Plant Biol 7:302–308. https://doi.org/10.1016/j.pbi.2004.03.003
Högy P, Fangmeier A (2008) Effects of elevated atmospheric CO2 on grain quality of wheat. J Cereal Sci 48:580–591. https://doi.org/10.1016/j.jcs.2008.01.006
Hua S, Yu H, Zhang Y et al (2012) Variation of carbohydrates and macronutrients during the flowering stage in canola (Brasscia napus L.) plants with contrasting seed oil content. Aust J Crop Sci 6:1275–1282
Huang B, Hennen-Bierwagen TA, Myers AM (2014) Functions of multiple genes encoding ADP-glucose pyrophosphorylase subunits in maize endosperm, embryo, and leaf. Plant Physiol 164:596–611. https://doi.org/10.1104/pp.113.231605
Huang J, Schols HA, van Soest JJG et al (2007) Physicochemical properties and amylopectin chain profiles of cowpea, chickpea and yellow pea starches. Food Chem 101:1338–1345. https://doi.org/10.1016/j.foodchem.2006.03.039
Huang X, Zhao Y, Wei X et al (2012) Genome-wide association study of flowering time and grain yield traits in a worldwide collection of rice germplasm. Nat Genet 44:32–39. https://doi.org/10.1038/ng.1018
Ingram GC (2010) Family life at close quarters: communication and constraint in angiosperm seed development. Protoplasma 247:195–214. https://doi.org/10.1007/s00709-010-0184-y
Itoh K, Ozaki H, Okada K et al (2003) Introduction of Wx transgene into rice wx mutants leads to both high- and low-amylose rice. Plant Cell Physiol 44:473–480. https://doi.org/10.1093/pcp/pcg068
James MG, Robertson DS, Myers AM et al (2015) Characterization of the maize gene sugary1, a determinant of starch composition in kernels. Plant Cell 7:417–429
Jaynes TA, Nelson OE (1971) Invertase activity in normal and mutant maize endosperms during development. Plant Physiol 47:623–628
Jofuku KD, Omidyar PK, Gee Z, Okamuro JK (2005) Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc Natl Acad Sci 102:3117–3122. https://doi.org/10.1073/pnas.0409893102
Khan S, Anwar S, Kuai J et al (2018) Alteration in yield and oil quality traits of winter rapeseed by lodging at different planting density and nitrogen rates. Sci Rep 8:634. https://doi.org/10.1038/s41598-017-18734-8
Kim Y, Keogh JB, Clifton PM (2017) Benefits of nut consumption on insulin resistance and cardiovascular risk factors: multiple potential mechanisms of actions. Nutrients 9:1271. https://doi.org/10.3390/nu9111271
Kirchberger S, Leroch M, Huynen MA et al (2007) Molecular and biochemical analysis of the plastidic ADP-glucose transporter (ZmBT1) from Zea mays. J Biol Chem 282:22481–22491. https://doi.org/10.1074/jbc.M702484200
Kok S, Ong-Abdullah M, Ee GC, Namasivayam P (2011) Comparison of nutrient composition in kernel of tenera and clonal materials of oil palm (Elaeis guineensis Jacq.). Food Chem 129:1343–1347. https://doi.org/10.1016/J.FOODCHEM.2011.05.023
Kondou Y, Nakazawa M, Kawashima M et al (2008) RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147:1924–1935. https://doi.org/10.1104/pp.108.118364
Kunieda T, Shimada T, Kondo M et al (2013) Spatiotemporal secretion of PEROXIDASE36 is required for seed coat mucilage extrusion in arabidopsis. Plant Cell 25:1355–1367. https://doi.org/10.1105/tpc.113.110072
Kunz H-H, Zamani-Nour S, Häusler RE et al (2014) Loss of cytosolic phosphoglucose isomerase affects carbohydrate metabolism in leaves and is essential for fertility of Arabidopsis. Plant Physiol 166:753–765. https://doi.org/10.1104/pp.114.241091
Kurai T, Wakayama M, Abiko T et al (2011) Introduction of the ZmDof1 gene into rice enhances carbon and nitrogen assimilation under low-nitrogen conditions. Plant Biotechnol J 9:826–837. https://doi.org/10.1111/j.1467-7652.2011.00592.x
Lafon-Placette C, Köhler C (2014) Embryo and endosperm, partners in seed development. Curr Opin Plant Biol 17:64–69. https://doi.org/10.1016/j.pbi.2013.11.008
Lalonde S, Wipf D, Frommer WB (2004) Transport mechanisms for organic forms of carbon and nitrogen between source and sink. Annu Rev Plant Biol 55:341–372. https://doi.org/10.1146/annurev.arplant.55.031903.141758
Lee SK, Hwang SK, Han M et al (2007) Identification of the ADP-glucose pyrophosphorylase isoforms essential for starch synthesis in the leaf and seed endosperm of rice (Oryza sativa L.). Plant Mol Biol 65:531–546. https://doi.org/10.1007/s11103-007-9153-z
Lee KJD, Dekkers BJW, Steinbrecher T et al (2012) Distinct cell wall architectures in seed endosperms in representatives of the Brassicaceae and Solanaceae. Plant Physiol 160:1551–1566. https://doi.org/10.1104/pp.112.203661
Lee Y, Choi MS, Lee G et al (2017) Sugary endosperm is modulated by starch branching enzyme IIa in rice (Oryza sativa L.). Rice 10:33. https://doi.org/10.1186/s12284-017-0172-3
Li N, Li Y (2015) Maternal control of seed size in plants. J Exp Bot 66:1087–1097. https://doi.org/10.1093/jxb/eru549
Li J, Baroja-Fernández E, Bahaji A et al (2013) Enhancing sucrose synthase activity results in increased levels of starch and adp-glucose in maize (Zea mays l.) seed endosperms. Plant Cell Physiol 54:282–294. https://doi.org/10.1093/pcp/pcs180
Li JY, Wang J, Zeigler RS (2014) The 3,000 rice genomes project: new opportunities and challenges for future rice research. Gigascience 3:8. https://doi.org/10.1186/2047-217X-3-8
Li G, Pan J, Cui K et al (2017a) Limitation of unloading in the developing grains is a possible cause responsible for low stem non-structural carbohydrate translocation and poor grain yield formation in rice through verification of recombinant inbred lines. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01369
Li S, Wei X, Ren Y et al (2017b) OsBT1 encodes an ADP-glucose transporter involved in starch synthesis and compound granule formation in rice endosperm. Sci Rep 7:40124. https://doi.org/10.1038/srep40124
Lin Q, Huang B, Zhang M et al (2012) Functional interactions between starch synthase III and isoamylase-type starch-debranching enzyme in maize endosperm. Plant Physiol 158:679–692. https://doi.org/10.1104/pp.111.189704
Liu J, Huang J, Guo H et al (2017) The conserved and unique genetic architecture of kernel size and weight in maize and rice. Plant Physiol 175:774–785. https://doi.org/10.1104/pp.17.00708
Locascio A, Roig-Villanova I, Bernardi J, Varotto S (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Front Plant Sci 5:1–22. https://doi.org/10.3389/fpls.2014.00412
Lonien J, Schwender J (2009) Analysis of metabolic flux phenotypes for two Arabidopsis mutants with severe impairment in seed storage lipid synthesis. Plant Physiol 151:1617–1634. https://doi.org/10.1104/pp.109.144121
Luo M, Dennis ES, Berger F et al (2005) MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proc Natl Acad Sci 102:17531–17536. https://doi.org/10.1073/pnas.0508418102
Ma W, Kong Q, Mantyla JJ et al (2016) 14-3-3 protein mediates plant seed oil biosynthesis through interaction with AtWRI1. Plant J 88:228–235. https://doi.org/10.1111/tpj.13244
Malinova I, Kunz HH, Alseekh S et al (2014) Reduction of the cytosolic phosphoglucomutase in Arabidopsis reveals impact on plant growth, seed and root development, and carbohydrate partitioning. PLoS ONE 9:e112468. https://doi.org/10.1371/journal.pone.0112468
Matsushima R, Maekawa M, Kusano M et al (2014) Amyloplast-localized SUBSTANDARD STARCH GRAIN4 protein influences the size of starch grains in rice endosperm. Plant Physiol 164:623–636. https://doi.org/10.1104/pp.113.229591
McDonald R, Wang HL, Patrick JW, Offler CE (1995) The cellular pathway of sucrose transport in developing cotyledons of Vicia faba L. and Phaseolus vulgaris L.: a physiological assessment. Planta 196:659–667. https://doi.org/10.1007/BF00197329
Melkus G, Rolletschek H, Fuchs J et al (2011) Dynamic 13C/1H NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnol J 9:1022–1037. https://doi.org/10.1111/j.1467-7652.2011.00618.x
Mendel G (1865) Versuche uber Pflanzen-Hybriden. Verh. Naturforsch. Ver Brunn 4:3–47
Meng L-S, Wang Y-B, Loake GJ, Jiang J-H (2016) Seed embryo development is regulated via an AN3-MINI3 gene cascade. Front Plant Sci 7:1073. https://doi.org/10.3389/fpls.2016.01645
Mentzen WI, Peng J, Ransom N et al (2008) Articulation of three core metabolic processes in Arabidopsis: fatty acid biosynthesis, leucine catabolism and starch metabolism. BMC Plant Biol 8:76. https://doi.org/10.1186/1471-2229-8-76
Morley-Smith ER, Pike MJ, Findlay K et al (2008) The transport of sugars to developing embryos is not via the bulk endosperm in oilseed rape seeds. Plant Physiol 147:2121–2130. https://doi.org/10.1104/pp.108.124644
Mudgil D, Barak S, Khatkar BS (2014) Guar gum: processing, properties and food applications—a review. J Food Sci Technol 51:409–418. https://doi.org/10.1007/s13197-011-0522-x
Müller K, Tintelnot S, Leubner-Metzger G (2006) Endosperm-limited Brassicaceae seed germination: Abscisic acid inhibits embryo-induced endosperm weakening of Lepidium sativum (cress) and endosperm rupture of cress and Arabidopsis thaliana. Plant Cell Physiol 47:864–877. https://doi.org/10.1093/pcp/pcj059
Musa A, Birinyauri UA, Muhammad C, Umar A (2012) Proximate composition and mineral analysis of Nymphaea lotus seeds. Afr J Food Sci Technol 3(7):1–5
Nakamura Y (2002) Towards a better understanding of the metabolic system for amylopectin biosynthesis in plants: rice endosperm as a model tissue. Plant Cell Physiol 43:718–725. https://doi.org/10.1093/pcp/pcf091
Nakamura Y, Ono M, Sawada T et al (2017) Characterization of the functional interactions of plastidial starch phosphorylase and starch branching enzymes from rice endosperm during reserve starch biosynthesis. Plant Sci 264:83–95. https://doi.org/10.1016/j.plantsci.2017.09.002
Nehdi IA, Sbihi HM, Tan CP et al (2018) Chemical composition of date palm (Phoenix dactylifera L.) seed oil from six Saudi Arabian cultivars. J Food Sci. https://doi.org/10.1111/1750-3841.14033
Niittylä T, Messerli G, Trevisan M et al (2004) A previously unknown maltose transporter essential for starch degradation in leaves. Science 303:87–89. https://doi.org/10.1126/science.1091811
Nishinari K, Takemasa M, Zhang H, Takahashi R (2007) Storage plant polysaccharides: Xyloglucans, Galactomannans, Glucomannans. In: Kamerling JP (ed) Comprehensive glycoscience: from chemistry to systems biology, 1st edn. Elsevier, Amsterdam, pp 613–652
Nonogaki H, Gee OH, Bradford KJ (2000) A germination-specific endo-β-mannanase gene is expressed in the micropylar endosperm cap of tomato seeds. Plant Physiol 123:1235–1246. https://doi.org/10.1104/pp.123.4.1235
Nyström L, Lampi A-M, Andersson AAM, Kamal-Eldin A, Gebruers K, Courtin CM et al (2008) Phytochemicals and dietary fiber components in rye varieties in the healthgrain diversity screen. J Agric Food Chem 56(21):9758–9766. https://doi.org/10.1021/jf801065r
Ohto M-AA, Fischer RL, Goldberg RB et al (2005) Control of seed mass by APETALA2. Proc Natl Acad Sci USA 102:3123–3128. https://doi.org/10.1073/pnas.0409858102
Onda Y, Mochida K (2016) Exploring genetic diversity in plants using high-throughput sequencing techniques. Curr Genomics 17:356–365. https://doi.org/10.2174/1389202917999160304160040
Orozco-Arroyo G, Paolo D, Ezquer I, Colombo L (2015) Networks controlling seed size in Arabidopsis. Plant Reprod 28:17–32. https://doi.org/10.1007/s00497-015-0255-5
Patron NJ (2004) The lys5 mutations of barley reveal the nature and importance of plastidial ADP-Glc transporters for starch synthesis in cereal endosperm. Plant Physiol 135:2088–2097. https://doi.org/10.1104/pp.104.045203
Paul MJ, Oszvald M, Jesus C et al (2017) Increasing crop yield and resilience with trehalose 6-phosphate: targeting a feast–famine mechanism in cereals for better source–sink optimization. J Exp Bot 68:4455–4462. https://doi.org/10.1093/jxb/erx083
Peng C, Wang Y, Liu F et al (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77:917–930. https://doi.org/10.1111/tpj.12444
Perdomo FA, Acosta-Osorio AA, Herrera G et al (2013) Physicochemical characterization of seven Mexican Ricinus communis L. seeds & oil contents. Biomass Bioenerg 48:17–24. https://doi.org/10.1016/j.biombioe.2012.10.020
Periappuram C, Steinhauer L, Barton DL et al (2000) The plastidic phosphoglucomutase from arabidopsis. a reversible enzyme reaction with an important role in metabolic control. Plant Physiol 122:1193–1200. https://doi.org/10.1104/pp.122.4.1193
Pfister B, Zeeman SC (2016) Formation of starch in plant cells. Cell Mol Life Sci 73:2781–2807. https://doi.org/10.1007/s00018-016-2250-x
Pirone C, Gurrieri L, Gaiba I et al (2017) The analysis of the different functions of starch-phosphorylating enzymes during the development of Arabidopsis thaliana plants discloses an unexpected role for the cytosolic isoform GWD2. Physiol Plant 160:447–457. https://doi.org/10.1111/ppl.12564
Pommerrenig B, Popko J, Heilmann M et al (2013) SUCROSE TRANSPORTER 5 supplies Arabidopsis embryos with biotin and affects triacylglycerol accumulation. Plant J 73:392–404. https://doi.org/10.1111/tpj.12037
Poschet G, Hannich B, Raab S et al (2011) A novel Arabidopsis vacuolar glucose exporter is involved in cellular sugar homeostasis and affects the composition of seed storage compounds. Plant Physiol 157:1664–1676. https://doi.org/10.1104/pp.111.186825
Pouvreau B, Baud S, Vernoud V et al (2011) Duplicate maize Wrinkled1 transcription factors activate target genes involved in seed oil biosynthesis. Plant Physiol 156:674–686. https://doi.org/10.1104/pp.111.173641
Rachwa-Rosiak D, Nebesny E, Budryn G (2015) Chickpeas—composition, nutritional value, health benefits, application to bread and snacks: a review. Crit Rev Food Sci Nutr 55:1137–1145. https://doi.org/10.1080/10408398.2012.687418
Radchuk V (2006) Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell Online 18:1652–1666. https://doi.org/10.1105/tpc.106.041335
Radchuk V, Borisjuk L (2014) Physical, metabolic and developmental functions of the seed coat. Front Plant Sci 5:510. https://doi.org/10.3389/fpls.2014.00510
Reidel EJ, Turgeon R, Cheng L (2008) A maltose transporter from apple is expressed in source and sink tissues and complements the Arabidopsis maltose export-defective mutant. Plant Cell Physiol 49:1607–1613. https://doi.org/10.1093/pcp/pcn134
Ritchie RJ, Fieuw-Makaroff S, Patrick JW (2003) Sugar retrieval by coats of developing seeds of Phaseolus vulgaris L. and Vicia faba L. Plant Cell Physiol 44:163–172. https://doi.org/10.1093/pcp/pcg022
Rolletschek H (2005) Ectopic expression of an amino acid transporter (VfAAP1) in seeds of vicia narbonensis and pea increases storage proteins. Plant Physiol 137:1236–1249. https://doi.org/10.1104/pp.104.056523
Rolletschek H, Grafahrend-Belau E, Munz E et al (2015) Metabolic architecture of the cereal grain and its relevance to maximize carbon use efficiency. Plant Physiol 169:1698–1713. https://doi.org/10.1104/pp.15.00981
Ruan Y-L, Chourey PS (2006) Carbon partitioning in developing seeds. In: Basra AS (ed) Handbook of seed science and technology. Food Products Press, New York, pp 125–152
Ruan YL, Llewellyn DJ, Liu Q et al (2008) Expression of sucrose synthase in the developing endosperm is essential for early seed development in cotton. Funct Plant Biol 35:382–393. https://doi.org/10.1071/FP08017
Ruuska S, Girke T (2002) Contrapuntal networks of gene expression during Arabidopsis seed filling. Plant Cell 14:1191–1206. https://doi.org/10.1105/tpc.000877.teins
Satoh H (2003) Starch-branching enzyme I-deficient mutation specifically affects the structure and properties of starch in rice endosperm. Plant Physiol 133:1111–1121. https://doi.org/10.1104/pp.103.021527
Satoh H, Shibahara K, Tokunaga T et al (2008) Mutation of the plastidial α-glucan phosphorylase gene in rice affects the synthesis and structure of starch in the endosperm. Plant Cell Online 20:1833–1849. https://doi.org/10.1105/tpc.107.054007
Scott RJ, Spielman M, Bailey J, Dickinson HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341
Scott PT, Pregelj L, Chen N et al (2008) Pongamia pinnata: an untapped resource for the biofuels industry of the future. BioEnergy Res 1:2–11. https://doi.org/10.1007/s12155-008-9003-0
Shahid S, Begum R, Razzaque S et al (2016) Variability in amylose content of Bangladeshi rice cultivars due to unique SNPs in Waxy allele. J Cereal Sci 71:1–9. https://doi.org/10.1016/J.JCS.2016.07.006
Shannon JC, Pien FM, Cao H, Liu KC (1998) Brittle-1, an adenylate translocator, facilitates transfer of extraplastidial synthesized ADP-glucose into amyloplasts of maize endosperms. Plant Physiol 117:1235–1252. https://doi.org/10.1104/pp.117.4.1235
Shen B, Allen WB, Zheng P et al (2010) Expression of ZmLEC1 and ZmWRI1 increases seed oil production in maize. Plant Physiol 153:980–987. https://doi.org/10.1104/pp.110.157537
Shewry PR, Underwood C, Wan Y et al (2009) Storage product synthesis and accumulation in developing grains of wheat. J Cereal Sci 50:106–112. https://doi.org/10.1016/j.jcs.2009.03.009
Solís-Guzmán MG, Argüello-Astorga G, López-Bucio J et al (2017) Arabidopsis thaliana sucrose phosphate synthase (sps) genes are expressed differentially in organs and tissues, and their transcription is regulated by osmotic stress. Gene Expr Patterns 25–26:92–101. https://doi.org/10.1016/j.gep.2017.06.001
Song Y, He L, Wang X-D et al (2017a) Regulation of carbon partitioning in the seed of the model legume Medicago truncatula and Medicago orbicularis: a comparative approach. Front Plant Sci 8:2070. https://doi.org/10.3389/fpls.2017.02070
Song Y, Wang XD, Rose RJ (2017b) Oil body biogenesis and biotechnology in legume seeds. Plant Cell Rep 36:1519–1532. https://doi.org/10.1007/s00299-017-2201-5
Stadler R (2005) Cell-to-cell movement of green fluorescent protein reveals post-phloem transport in the outer integument and identifies symplastic domains in Arabidopsis seeds and embryos. Plant Physiol 139:701–712. https://doi.org/10.1104/pp.105.065607
Stein O, Avin-Wittenberg T, Krahnert I et al (2017) Arabidopsis fructokinases are important for seed oil accumulation and vascular development. Front Plant Sci 7:1–16. https://doi.org/10.3389/fpls.2016.02047
Streb S, Zeeman SC (2014) Replacement of the endogenous starch debranching enzymes ISA1 and ISA2 of arabidopsis with the rice orthologs reveals a degree of functional conservation during starch synthesis. PLoS ONE 9:e92174. https://doi.org/10.1371/journal.pone.0092174
Sullivan TD (1991) Analysis of maize brittle-1 alleles and a defective suppressor-mutator-induced mutable allele. Plant Cell Online 3:1337–1348. https://doi.org/10.1105/tpc.3.12.1337
Sun Y, Jiao G, Liu Z et al (2017) Generation of high-amylose rice through CRISPR/Cas9-mediated targeted mutagenesis of starch branching enzymes. Front Plant Sci 8:298. https://doi.org/10.3389/fpls.2017.00298
Taliercio EW, Kim JY, Mahé A et al (1999) Isolation, characterization and expression analyses of two cell wall invertase genes in maize. J Plant Physiol 155:197–204. https://doi.org/10.1016/S0176-1617(99)80007-8
Tang XJ, Peng C, Zhang J et al (2016) ADP-glucose pyrophosphorylase large subunit 2 is essential for storage substance accumulation and subunit interactions in rice endosperm. Plant Sci 249:70–83. https://doi.org/10.1016/j.plantsci.2016.05.010
Tausz M, Norton RM, Tausz-Posch S et al (2017) Can additional N fertiliser ameliorate the elevated CO2-induced depression in grain and tissue N concentrations of wheat on a high soil N background? J Agron Crop Sci 203:574–583. https://doi.org/10.1111/jac.12209
Tetlow I, Emes M (2017) Starch biosynthesis in the developing endosperms of grasses and cereals. Agronomy 7:81. https://doi.org/10.3390/agronomy7040081
Thiel J, Weier D, Sreenivasulu N et al (2008) Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: a microdissection-based transcriptome study of young barley grains. Plant Physiol 148:1436–1452. https://doi.org/10.1104/pp.108.127001
Turbant A, Fournet F, Lequart M et al (2016) PME58 plays a role in pectin distribution during seed coat mucilage extrusion through homogalacturonan modification. J Exp Bot 67:2177–2190. https://doi.org/10.1093/jxb/erw025
Umemoto T, Aoki N, Lin H et al (2004) Natural variation in rice starch synthase IIa affects enzyme and starch properties. Funct Plant Biol 31:671–684. https://doi.org/10.1071/FP04009
van Bel AJE, Helariutta Y, Thompson GA et al (2013) Phloem: the integrative avenue for resource distribution, signaling, and defense. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00471
Vilhar B (2002) Cytometrical evidence that the loss of seed weight in the miniature1 seed mutant of maize is associated with reduced mitotic activity in the developing endosperm. Plant Physiol 129:23–30. https://doi.org/10.1104/pp.001826
Wan H, Wu L, Yang Y et al (2017) Evolution of sucrose metabolism: the dichotomy of invertases and beyond. Trends Plant Sci 23:163–177. https://doi.org/10.1016/j.tplants.2017.11.001
Wang X (2010) The dawn angiosperms: uncovering the origin of flowering plants. Springer, New York
Wang N, Fisher DB (1994) The use of fluorescent tracers to characterize the post-phloem transport pathway in maternal tissues of developing wheat grains. Plant Physiol 104:17–27
Wang L, Ruan Y-L (2012) New insights into roles of cell wall invertase in early seed development revealed by comprehensive spatial and temporal expression patterns of GhCWIN1 in cotton. Plant Physiol 160:777–787. https://doi.org/10.1104/pp.112.203893
Wang L, Ruan Y-L (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:163. https://doi.org/10.3389/fpls.2013.00163
Wang XD, Harrington G, Patrick JW et al (1995) Cellular pathway of photosynthate transport in coats of developing seed of Vicia faba L. and Phaseolus vulgaris L. II. Principal cellular site(s) of efflux. J Exp Bot 46:49–63. https://doi.org/10.1093/jxb/46.1.49
Wang AY, Kao MH, Yang WH et al (1999) Differentially and developmentally regulated expression of three rice sucrose synthase genes. Plant Cell Physiol 40:800–807. https://doi.org/10.1093/oxfordjournals.pcp.a029608
Wang A, Garcia D, Zhang H et al (2010a) The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63:670–679. https://doi.org/10.1111/j.1365-313X.2010.04271.x
Wang X, Xue L, Sun J, Zuo J (2010b) The Arabidopsis BE1 gene, encoding a putative glycoside hydrolase localized in plastids, plays crucial roles during embryogenesis and carbohydrate metabolism. J Integr Plant Biol 52:273–288. https://doi.org/10.1111/j.1744-7909.2010.00930.x
Wang J, Hu P, Chen Z et al (2017a) Progress in high-amylose cereal crops through inactivation of starch branching enzymes. Front Plant Sci 8:469. https://doi.org/10.3389/fpls.2017.00469
Wang X, Pang Y, Wang C et al (2017b) New candidate genes affecting rice grain appearance and milling quality detected by genome-wide and gene-based association analyses. Front Plant Sci. https://doi.org/10.3389/fpls.2016.01998
Weber H (1995) Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. Plant Cell Online 7:1835–1846. https://doi.org/10.1105/tpc.7.11.1835
Weber H, Borisjuk L, Wobus U (1996) Controlling seed development and seed size in Vicia faba: a role for seed coat-associated invertases and carbohydrate state. Plant J 10(5):823–834. https://doi.org/10.1046/j.1365-313X.1996.10050823.x
Weber H, Borisjuk L, Wobus U (2005) Molecular physiology of legume seed development. Annu Rev Plant Biol 56:253–279. https://doi.org/10.1146/annurev.arplant.56.032604.144201
Wei X, Jiao G, Lin H et al (2017) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59:134–153. https://doi.org/10.1111/jipb.12510
Weichert N, Saalbach I, Weichert H et al (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol 152:698–710. https://doi.org/10.1104/pp.109.150854
Weickert MO, Pfeiffer AF (2018) Impact of dietary fiber consumption on insulin resistance and the prevention of type 2 diabetes. J Nutr 148:7–12. https://doi.org/10.1093/jn/nxx008
Weigelt K, Küster H, Radchuk R et al (2008) Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J 55:909–926. https://doi.org/10.1111/j.1365-313X.2008.03560.x
Weschke W, Panitz R, Gubatz S et al (2003) The role of invertases and hexose transporters in controlling sugar ratios in maternal and filial tissues of barley caryopses during early development. Plant J 33:395–411. https://doi.org/10.1046/j.1365-313X.2003.01633.x
Weselake RJ, Taylor DC, Rahman MH et al (2009) Increasing the flow of carbon into seed oil. Biotechnol Adv 27:866–878. https://doi.org/10.1016/j.biotechadv.2009.07.001
Wobus U, Weber H (1999) Sugars as signal molecules in plant seed development. Biol Chem 380:937–944. https://doi.org/10.1515/BC.1999.116
Wu AC, Ral JP, Morell MK, Gilbert RG (2014) New perspectives on the role of α- and β-amylases in transient starch synthesis. PLoS ONE 9:e100498. https://doi.org/10.1371/journal.pone.0100498
Xiao Q, Wang Y, Du J et al (2017) ZmMYB14 is an important transcription factor involved in the regulation of the activity of the ZmBT1 promoter in starch biosynthesis in maize. FEBS J 284:3079–3099. https://doi.org/10.1111/febs.14179
Xie G, Li Z, Ran Q et al (2017) Over-expression of mutated ZmDA1 or ZmDAR1 gene improves maize kernel yield by enhancing starch synthesis. Plant Biotechnol J 16:234–244. https://doi.org/10.1111/pbi.12763
Xu J-J, Zhang X-F, Xue H-W (2016) Rice aleurone layer specific OsNF-YB1 regulates grain filling and endosperm development by interacting with an ERF transcription factor. J Exp Bot 67(22):6399–6411. https://doi.org/10.1093/jxb/erw409
Xu W, Bobet S, Le Gourrierec J et al (2017) TRANSPARENT TESTA 16 and 15 act through different mechanisms to control proanthocyanidin accumulation in Arabidopsis testa. J Exp Bot 68:2859–2870. https://doi.org/10.1093/jxb/erx151
Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55:1521–1533. https://doi.org/10.1093/pcp/pcu089
Yang S, Johnston N, Talideh E et al (2008) The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development. Development 135:3501–3509. https://doi.org/10.1242/dev.026708
Yin L-L, Xue H-W (2012) The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–1065. https://doi.org/10.1105/tpc.111.094854
Ying R, Rondeau-Mouro C, Barron C et al (2013) Hydration and mechanical properties of arabinoxylans and β-d-glucans films. Carbohydr Polym 96:31–38. https://doi.org/10.1016/J.CARBPOL.2013.03.090
Yu T-S, Zeeman SC, Thorneycroft D et al (2005) alpha-Amylase is not required for breakdown of transitory starch in Arabidopsis leaves. J Biol Chem 280:9773–9779. https://doi.org/10.1074/jbc.M413638200
Zeeman SC, Thorneycroft D, Schupp N, Chapple A, Weck M, Dunstan H et al (2004) Plastidial α-glucan phosphorylase is not required for starch degradation in Arabidopsis leaves but has a role in the tolerance of abiotic stress. Plant Physiol 135(2):849–858. https://doi.org/10.1104/pp.103.032631
Zhang WH, Zhou Y, Dibley KE et al (2007) Review: nutrient loading of developing seeds. Funct Plant Biol 34:314–331. https://doi.org/10.1071/FP06271
Zhang H, Lu Y, Zhao Y, Zhou D-X (2016) OsSRT1 is involved in rice seed development through regulation of starch metabolism gene expression. Plant Sci 248:28–36. https://doi.org/10.1016/J.PLANTSCI.2016.04.004
Zhou X, Yang J, Qu G (2007) Study on synthesis and properties of modified starch binder for foundry. J Mater Process Technol 183:407–411. https://doi.org/10.1016/j.jmatprotec.2006.11.001
Zhou H, Wang L, Liu G et al (2016) Critical roles of soluble starch synthase SSIIIa and granule-bound starch synthase Waxy in synthesizing resistant starch in rice. Proc Natl Acad Sci 113:12844–12849. https://doi.org/10.1073/pnas.1615104113
Zhu F (2018) Triticale: nutritional composition and food uses. Food Chem 241:468–479. https://doi.org/10.1016/j.foodchem.2017.09.009
Acknowledgements
We would like to thank the reviewer for their detailed comments and suggestions for the manuscript. We thank Prof. L. Colombo and Prof. J. Pozueta for scientific support. We also thank M. A. Garin for technical support.
Funding
This work was partially supported by the Università degli Studi di Milano (UNIMI-RTD-A and Piano di sviluppo di ateneo - Biosciences dept. Linea 2-2017-2018 - CUP G43C17000590001 and Linea 2-2016-2017 - CUP G42F16001710005) and the H2020-MSCA-RISE Project (ExpoSeed GA-691109). M. Aguirre acknowledges the Universiteit van Amsterdam (NL AMSTERD01).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by L. Lepiniec, H. North, G. Ingram.
A contribution to the special issue ‘Seed Biology’.
Rights and permissions
About this article
Cite this article
Aguirre, M., Kiegle, E., Leo, G. et al. Carbohydrate reserves and seed development: an overview. Plant Reprod 31, 263–290 (2018). https://doi.org/10.1007/s00497-018-0336-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00497-018-0336-3