Physical, metabolic and developmental functions of the seed coat

Frontiers in Plant Science

Volumn 5, Issue OCT, 2014, Pages

  Radchuk, Volodymyr ^a   Borisjuk, Ljudmilla ^a  

^a LEIBNIZ INSTITUTE OF PLANT GENETICS AND CROP PLANT RESEARCH IPK   (Germany)

Author keywords

Maternal filial interface; Nutrients supply; PCD; Seed development; Seed photosynthesis

Indexed keywords

EID: 84907982010     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2014.00510     Document Type: Article

References (248)

1. Abirached-Darmency, M., Abdel-gawwad, M. R., Conejero, G., Verdeil, J. L., and Thompson, R. (2005). In situ expression of two storage protein genes in relation to histo-differentiation at mid-embryogenesis in Medicago truncatula and Pisum sativum seeds. J. Exp. Bot. 56, 2019–2028. doi:10.1093/jxb/eri200
2. Adamski, N. M., Anastasiou, E., Eriksson, S., O’Neill, C. M., and Lenhard, M. (2009). Local maternal control of seed size by KLUH/CYP78A5-dependent growth signaling. Proc. Natl. Acad. Sci. U.S.A. 106, 20115–20120. doi:10.1073/pnas.0907024106
3. Albert, S., Delseny, M., and Devic, M. (1997). BANYULS, a novel negative regulator of flavonoid biosynthesis in the Arabidopsis seed coat. Plant J. 11, 289–299. doi:10.1046/j.1365-313X.1997.11020289.x
4. Andriunas, F. A., Zhang, H. M., Weber, H., McCurdy, D. W., Offler, C. E., and Patrick, J. W. (2011). Glucose and ethylene signalling pathways converge to regulate trans-differentiation of epidermal transfer cells in Vicia narbonensis cotyledons. Plant J. 68, 987–998. doi:10.1111/j.1365-313X.2011.04749.x
5. Andriunas, F. A., Zhang, H. M., Xia, X., Offler, C. E., McCurdy, D. W., and Patrick, J. W. (2012). Reactive oxygen species form part of a regulatory pathway initiating trans-differentiation of epidermal transfer cells in Vicia faba cotyledons. J. Exp. Bot. 63, 3617–3630. doi:10.1093/jxb/ers029
6. Andriunas, F. A., Zhang, H. M., Xia, X., Patrick, J. W., and Offler, C. E. (2013). Intersection of transfer cells with phloem biology–broad evolutionary trends, function, and induction. Front. Plant Sci. 4:221. doi:10.3389/fpls.2013. 00221
7. Aoki, N., Hirose, T., and Furbank, R.T. (2012). “Sucrose transport in higher plants:from source to sink,” in Photosynthesis:Plastid Biology, Energy Conversion, and Carbon Assimilation, eds J. J. Eaton-Rye, B. C. Tripathy, and T. D. Sharkey (Dordrecht:Springer), 703–729.
8. 2 to differences in grain mass in durum wheat. Plant Cell Environ. 16, 383–392. doi:10.1111/j.1365-3040.1993.tb00884.x
9. Arsovski, A. A., Haughn, G. W., and Western, T. L. (2010). Seed coat mucilage cells of Arabidopsis thaliana as a model for plant cell wall research. Plant Signal. Behav. 5, 796–801. doi:10.4161/psb.5.7.11773
10. Ashikari, M., Wu, J., Yano, M., Sasaki, T., and Yoshimura, A. (1999). Rice gibberellin-insensive dwarf mutant gene Dwarf 1 encodes the α-subunit of GTP-binding protein. Proc. Natl. Acad. Sci. U.S.A. 96, 10284–10289. doi:10.1073/pnas.96.18.10284
11. Auger, B., Marnet, N., Gautier, V., Maia-Grondard, A., Leprince, F., Renard, M., et al. (2010). A detailed survey of seed coat flavonoids in developing seeds of Brassica napus L. J. Agric. Food Chem. 26, 6246–6256. doi:10.1021/jf903619v
12. Bailly, C., and Kranner, I. (2011). Analyses of reactive oxygen species and antiox-idants in relation to seed longevity and germination. Methods Mol. Biol. 773, 343–367. doi:10.1007/978-1-61779-231-1_20
13. Barrero, C., Royo, J., Grijota-Martinez, C., Faye, C., Paul, W., Sanz, S., et al. (2009). The promoter of ZmMRP-1, a maize transfer cell-specific transcriptional activator, is induced at solute exchange surfaces and responds to transport demands. Planta 229, 235–247. doi:10.1007/s00425-008-0823-0
14. Bassoi, M. C., and Flintham, J. (2005). Relationship between grain colour and preharvest sprouting-resistance in wheat. Pesqui. Agropecu. Bras. 40, 981–988. doi:10.1590/S0100-204X2005001000006
15. Beresniewicz, M. M., Taylor, A. G., Goffinet, M. C., and Terhune, B. T. (1995). Characterization and location of a semipermeable layer in seed coats of leek and onion (Liliaceae), tomato and pepper (Solanaceae). Seed Sci. Technol. 23, 123–134.
16. Bernhardt, C., Zhao, M., Gonzalez, A., Lloyd, A., and Schiefelbein, J. (2005). The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development 132, 291–298. doi:10.1242/dev.01565
17. Bethke, P. C., Libourel, I. G. L., Aoyama, N., Chung, Y. Y., Still, D. W., and Jones, R. L. (2007). The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol. 143, 1173–1188. doi:10.1104/pp.106.093435
18. Bewley, J. D., and Black, M.(1994). Seeds. NewYork:Plenum Press. doi:10.1007/978-1-4899-1002-8
19. Bewley, J. D., Bradford, K., Hilhorst, H., and Nonogaki, H. (2013). Seeds:Physiology of Development, Germination and Dormancy. New York:Springer. doi:10.1007/978-1-4614-4693-4
20. Bihmidine, S., Hunter, C. T, Johns, C. E., Koch, K. E., and Braun, D. M. (2013). Regulation of assimilate import into sink organs:update on molecular drivers of sink strength. Front. Plant Sci. 4:177. doi:10.3389/fpls.2013. 00177
21. Black, M. H., and Halmer, P. (2006). The Encyclopedia of Seeds:Science, Technology and Uses. Wallingford:CABI.
22. Bohinc, T., Ban, S. G., Ban, D., and Trdan, S. (2012). Glucosinolates in plant protection strategies:a review. Arch. Biol. Sci. 64, 821–828. doi:10.2298/ABS1203821B
23. Borisjuk, L., Neuberger, T., Schwender, J., Heinzel, N., Sunderhaus, S., Fuchs, J., et al. (2013). Seed architecture shapes embryo metabolism in oilseed rape. Plant Cell 25, 1625–1640. doi:10.1105/tpc.113.111740
24. Borisjuk, L., Nguyen, T. H., Neuberger, T., Rutten, T., Tschiersch, H., Claus, B., et al. (2005). Gradients of lipid storage, photosynthesis and plastid differentiation in developing soybean seeds. New Phytol. 167, 761–776. doi:10.1111/j.1469-8137.2005.01474.x
25. Borisjuk, L., and Rolletschek, H. (2009). The oxygen status of the developing seed. New Phytol. 182, 17–30. doi:10.1111/j.1469-8137.2008.02752.x
26. Borisjuk, L., Rolletschek, H., and Neuberger, T. (2012). Surveying the plant’s world by magnetic resonance imaging. Plant J. 70, 129–146. doi:10.1111/j.1365-313X.2012.04927.x
27. Borisjuk, L., Walenta, S., Weber, H., Mueller-Klieser, W., and Wobus, U. (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. doi:10.1046/j.1365-313X.1998.00214.x
28. Borisjuk, L., Wang, T. L., Rolletschek, H., Wobus, U., and Weber, H. (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.
29. Brar, G., and Thies, W. (1977). Contribution of leaves, stem, siliques and seeds to dry-matter accumulation in ripening seeds of rapeseed, Brassica napus L. Z. Pflanzenphysiol. 82, 1–13. doi:10.1016/S0044-328X(77)80128-1
30. Braun, D. M. (2012). SWEET! The pathway is complete. Science 335, 173–174. doi:10.1126/science.1216828
31. Brooker, N. L., Lagalle, C. D., Zlatanic, A., Javni, I., and Petrovic, Z. (2007). Soy polyol formulations as novel seed treatments for the management of soil-borne diseases of soybean. Commun. Agric. Appl. Biol. Sci. 72, 35–43.
32. Caley, C. Y., Duffus, C. M., and Jeffcoat, B. (1990). Photosynthesis in the pericarp of developing wheat grains. J. Exp. Bot. 41, 303–307. doi:10.1093/jxb/41.3.303
33. Carvalho, A. O., and Gomes, V. M. (2009). Plant defensins–prospects for the biological functions and biotechnological properties. Peptides 30, 1007–1020. doi:10.1016/j.peptides.2009.01.018
34. Challis, R. J., Hepworth, J., Mouchel, C., Waites, R., and Leyser, O. (2013). A role for MORE AXILLARY GROWTH1 (MAX1) in evolutionary diversity in strigolactone signaling upstream of MAX2. Plant Physiol. 161, 1885–1902. doi:10.1104/pp.112.211383
35. Chang, S. H., Lu, L. S., Wang, N. N., and Chang, Y. Y. (2008). Negative feedback regulation of system-1 ethylene production by the tomato 1-aminocyclopropane-1-carboxylate synthase 6 gene promoter. Plant Sci. 175, 149–160. doi:10.1016/j.plantsci.2007.11.004
36. Chaudhury, A. M., Koltunow, A., Payne, T., Luo, M., Tucker, M. R., Ming, L., et al. (2001). Control of early seed development. Annu. Rev. Cell Dev. Biol. 17, 677–699. doi:10.1146/annurev.cellbio.17.1.677
37. Cheng, W. H., Taliercio, E. W., and Chourey, P. S. (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. doi:10.1105/tpc.8.6.971
38. Chichkova, N. V., Shaw, J., Galiullina, R. A., Drury, G. E., Tuzhikov, A. I., Kim, S. H., et al. (2010). Phytaspase, a relocalisable cell death promoting plant protease with caspase specificity. EMBO J. 29, 1149–1161. doi:10.1038/emboj.2010.1
39. Cho, J. N., Ryu, J. Y., Jeong, Y. M., Park, J., Song, J. J., Amasino, R. M., et al. (2012). Control of seed germination by light-induced histone arginine demethylation activity. Dev. Cell 22, 736–748. doi:10.1016/j.devcel.2012.01.024
40. Choi, Y., Gehring, M., Johnson, L., Hannon, M., Harada, J. J., Goldberg, R. B., et al. (2002). DEMETER, a DNA glycosylase domain protein, is required for endosperm gene imprinting and seed viability in Arabidopsis. Cell 110, 33–42. doi:10.1016/S0092-8674(02)00807-3
41. Chourey, P. S., Li, Q., and Cevallos-Cevallos, J. (2011). Pleiotropy and its limited dissection through a metabolic gene Miniature1 (Mn1) that encodes a cell wall invertase in developing seeds of maize. Plant Sci. 184, 45–53. doi:10.1016/j.plantsci.2011.12.011
42. Cloetens, P., Mache, R., Schlenker, M., and Lerbs-Mache, S. (2006). Quantitative phase tomography of Arabidopsis seeds reveals intercellular void network. Proc. Natl. Acad. Sci. U.S.A. 103, 14626–14630. doi:10.1073/pnas.0603490103
43. Cochrane, M. P., and Duffus, C. M. (1979). Morphology and ultrastructure of immature cereal grains in relation to transport. Ann. Bot. 44, 67–77.
44. Costa, L. M., Gutierrez-Marcos, J. F., Brutnell, T. P., Greenland, A. J., and Dickinson, H. G. (2003). The globby1-1 (glo1-1) mutation disrupts nuclear and cell division in the developing maize seed causing alterations in endosperm cell fate and tissue differentiation. Development 130, 5009–5017. doi:10.1242/dev.00692
45. Costa, L. M., Yuan, J., Rouster, J., Paul, W., Dickinson, H., and Gutierrez-Marcos, J. F. (2012). Maternal control of nutrient allocation in plant seeds by genomic imprinting. Curr. Biol. 22, 160–165. doi:10.1016/j.cub.2011.11.059
46. Dean, G., Cao, Y., Xiang, D., Provart, N. J., Ramsay, L., Ahad, A., et al. (2011). Analysis of gene expression patterns during seed coat development in Arabidopsis. Mol. Plant 4, 1074–1091. doi:10.1093/mp/ssr040
47. Debeaujon, I., Léon-Kloosterziel, K. M., and Koornneef, M. (2000). Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiol. 122, 403–414. doi:10.1104/pp.122.2.403
48. Dermastia, M., Kladnik, A., Koce, J. D., and Chourey, P. S. (2009). A cellular study of teosinte Zea mays subsp. Parviglumis (Poaceae) caryopsis development showing several processes conserved in maize. Am. J. Bot. 96, 1798–1807. doi:10.3732/ajb.0900059
49. Dibley, S. J., Zhou, Y., Andriunas, F. A., Talbot, M. J., Offler, C. E., Patrick, J. W., et al. (2009). Early gene expression programs accompanying trans-differentiation of epidermal cells of Vicia faba cotyledons into transfer cells. New Phytol. 182, 863–877. doi:10.1111/j.1469-8137.2009.02822.x
50. Domínguez, F., Moreno, J., and Cejudo, F. J. (2001). The nucellus degenerates by a process of programmed cell death during the early stages of wheat grain development. Planta 213, 352–360. doi:10.1007/s004250000517
51. Duffus, C. M., and Rosie, R. (1973). Some enzyme-activities associated with chlorophyll containing layers of immature barley pericarp. Planta 114, 219–226. doi:10.1007/BF00389037
52. Efe, L., Mustafayev, A. S., and Killi, F. (2010). Agronomic, fiber and seed quality of naturally colored cotton in east Mediterranean region of Turkey. Pak. J. Bot. 42, 3865–3873.
53. Fang, W., Wang, Z., Cui, R., Li, J., and Li, Y. (2012). Maternal control of seed size by EOD3/CYP78A6 in Arabidopsis thaliana. Plant J. 70, 929–939. doi:10.1111/j.1365-313X.2012.04907.x
54. Figueiredo, D. D., and Köhler, C. (2014). Signalling events regulating seed coat development. Biochem. Soc. Trans. 42, 358–363. doi:10.1042/BST20130221
55. Finch-Savage, W. E., and Leubner-Metzger, G. (2006). Seed dormancy and the control of germination. New Phytol. 171, 501–523. doi:10.1111/j.1469-8137.2006.01787.x
56. Fisher, D. B., and Cash-Clark, C. E. (2000). Sieve tube unloading and post-phloem transport of fluorescent tracers and proteins injected into sieve tubes via severed aphid stylets. Plant Physiol. 123, 125–138. doi:10.1104/pp.123.1.125
57. Flematti, G. R., Waters, M. T., Scaffidi, A., Merritt, D. J., Ghisalberti, E. L., Dixon, K. W., et al. (2013). Karrikin and cyanohydrin smoke signals provide clues to new endogenous plant signalling compounds. Mol. Plant 6, 29–37. doi:10.1093/mp/sss132
58. Flinn, A. M. (1985). “Carbon dioxide fixation in developing seeds,” in The Pea Crop:A Basis for Improvement, eds P. D. Hebblethwaite, M. C. Heath, and T. C. K. Dawkins (London:Butterworths), 349–358.
59. Flintham, J. E. (2000). Different genetic components control coat-imposed and embryo-imposed dormancy in wheat. Seed Sci. Res. 10, 43–50. doi:10.1017/S0960258500000052
60. Forestan, C., Meda, S., and Varotto, S. (2010). ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiol. 152, 1373–1390. doi:10.1104/pp.109. 150193
61. Frommer, W. B., Davidson, M. W., and Campbell, R. E. (2009). Genetically encoded biosensors based on engineered fluorescent proteins. Chem. Soc. Rev. 38, 2833–2841. doi:10.1039/b907749a
62. Fujisawa, Y., Kato, T., Ohki, S., Ishikawa, A., Kitano, H., Sasaki, T., et al. (1999). Suppression of the heterotrimeric G protein causes abnormal morphology, including dwarfism, in rice. Proc. Natl. Acad. Sci. U.S.A. 96, 7575–7580. doi:10.1073/pnas.96.13.7575
63. Fuller, D. Q., and Allaby, R. (2009). Seed dispersal and crop domestication:shattering, germination and seasonality in evolution under cultivation. Ann. Plant Rev. 38, 238–295. doi:10.1002/9781444314557.ch7
64. Gao, X., Hu, C. H., Li, H. Z., Yao, Y. J., Meng, M., Dong, J., et al. (2013). Factors affecting pre-harvest sprouting resistance in wheat (Triticum aestivum L.):a review. J. Anim. Plant Sci. 23, 556–565.
65. Garcia, D., Fitz Gerald, J. N., and Berger, F. (2005). Maternal control of integument cell elongation and zygotic control of endosperm growth are coordinated to determine seed size in Arabidopsis. Plant Cell 17, 52–60. doi:10.1105/tpc.104.027136
66. Gattolin, S., Sorieul, M., and Frigerio, L. (2010). Mapping of tonoplast intrinsic proteins in maturing and germinating Arabidopsis seeds reveals dual localization of embryonic TIPs to the tonoplast and plasma membrane. Mol. Plant 4, 180–189. doi:10.1093/mp/ssq051
67. Gehring, M., Bubb, K. L., and Henikoff, S. (2009). Extensive demethylation of repetitive elements during seed development underlies gene imprinting. Science 324, 1447–1451. doi:10.1126/science.1171609
68. Geisler, M., and Sack, F. D. (2002). Variable timing of developmental progression in the stomatal pathway in Arabidopsis cotyledons. New Phytol. 153, 469–476. doi:10.1046/j.0028-646X.2001.00332.x
69. Gergerich, R. C., and Dolja, V. V. (2006). Introduction to plant viruses, the invisible foe. Plant Heal. Instruct. doi:10.1094/PHI-I-2006-0414-01
70. Gifford, R. M., and Bremner, P. M. (1981). Accumulation and conversion of sugars by developing wheat grains. 2. Light requirement for kernels cultured in vitro. Aust. J. Plant Physiol. 8, 631–640. doi:10.1071/PP9810631
71. Gnaiger, E., Méndez, G., and Hand, S. C. (2000). High phosphorylation efficiency and depression of uncoupled respiration in mitochondria under hypoxia. Proc. Natl. Acad. Sci. U.S.A. 97, 11080–11085. doi:10.1073/pnas.97.20.11080
72. Goffman, F., Ruckle, M., Ohlrogge, J., and Shachar-Hill, Y. (2004). Carbon dioxide concentrations are very high in developing oilseeds. Plant Physiol. Biochem. 42, 703–708. doi:10.1016/j.plaphy.2004.07.003
73. Golombek, S., Heim, U., Horstmann, C., Wobus, U., and Weber, H. (1998). Phosphoenolpyruvate carboxylase in developing seeds of Vicia faba L.:gene expression and metabolic regulation. Planta 208, 66–72. doi:10.1007/s0042500 50535
74. Gómez, E., Royo, J., Guo, Y., Thompson, R., and Hueros, G. (2002). Establishment of cereal endosperm expression domains:identification and properties of a maize transfer cell-specific transcription factor, ZmMRP-1. Plant Cell 14, 599–610. doi:10.1105/tpc.010365
75. Gómez, E., Royo, J., Muñiz, L. M., Sellam, O., Paul, W., Gerentes, D., et al. (2009). The maize transcription factor myb-related protein-1 is a key regulator of the differentiation of transfer cells. Plant Cell 21, 2022–2035. doi:10.1105/tpc.108.065409
76. Gonzalez, A., Zhao, M., Leavitt, J. M., and Lloyd, A. M. (2008). Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J. 53, 814–827. doi:10.1111/j.1365-313X.2007.03373.x
77. Graeber, K., Nakabayashi, K., Miatton, E., Leubner-Metzger, G., and Soppe, W. J. (2012). Molecular mechanisms of seed dormancy. Plant Cell Environ. 35, 1769–1786. doi:10.1111/j.1365-3040.2012.02542.x
78. Greenway, H., and Gibbs, J. (2003). Mechanisms of anoxia tolerance in plants. II. Energy requirements for maintenance and energy distribution to essential processes. Funct. Plant Biol. 30, 999–1036. doi:10.1071/PP98096
79. Greenwood, J. S., Helm, M., and Gietl, C. (2005). Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Rici-nus seed development. Proc. Natl. Acad. Sci. U.S.A. 102, 2238–2243. doi:10.1073/pnas.0409429102
80. Gutiérrez-Marcos, J. F., Costa, L. M., and Evans, M. M. (2006). Maternal gametophytic baseless1 is required for development of the central cell and early endosperm patterning in maize (Zea mays). Genetics 174, 317–329. doi:10.1534/genetics.106.059709
81. Gutiérrez-Marcos, J. F., Dal Prà, M., Giulini, A., Costa, L. M., Gavazzi, G., Cordelier, S., et al. (2007). Empty pericarp4 encodes a mitochondrion-targeted pentatri-copeptide repeat protein necessary for seed development and plant growth in maize. Plant Cell 19, 196–210. doi:10.1105/tpc.105.039594
82. Hanks, J. N., Snyder, A. K., Graham, M. A., Shah, R. K., Blaylock, L. A., Harrison, M. J., et al. (2005). Defensin gene family in Medicago truncatula:structure, expression and induction by signal molecules. Plant Mol. Biol. 58, 385–399. doi:10.1007/s11103-005-5567-7
83. Hara-Nishimura, I., Hatsugai, N., Nakaune, S., Kuroyanagi, M., and Nishimura, M. (2005). Vacuolar processing enzyme:an executor of plant cell death. Curr. Opin. Plant Biol. 8, 404–408. doi:10.1016/j.pbi.2005.05.016
84. Harrington, G. N., Nussbaumer, Y., Wang, X. D., Tegeder, M., Franceschi, V. R., and Frommer, W. B. (1997). Spatial and temporal expression of sucrose transport related genes in developing cotyledons of Vicia faba. Protoplasma 200, 35–50. doi:10.1007/BF01280733
85. Harvey, D. M., Hedley, C. L., and Keely, R. (1976). Photosynthetic and respiratory studies during pod and seed development in Pisum sativum L. Ann. Bot. 40, 993–1001.
86. Haughn, G., and Chaudhury, A. (2005). Genetic analysis of seed coat development in Arabidopsis. Trends Plant Sci. 10, 472–477. doi:10.1016/j.tplants.2005. 08.005
87. Haughn, G. W., and Western, T. L. (2012). Arabidopsis seed coat mucilage is a specialized cell wall that can be used as a model for genetic analysis of plant cell wall structure and function. Front. Plant Sci. 3:64. doi:10.3389/fpls.2012. 00064
88. Haydon, M. J., Mielczarek, O., Robertson, F. C., Hubbard, K. E., and Webb, A. A. (2013). Photosynthetic entrainment of the Arabidopsis thaliana circadian clock. Nature 502, 689–692. doi:10.1038/nature12603
89. Hendry, G. A. F. (1993). Oxygen, free radical processes and seed longevity. Seed Sci. Res. 3, 141–153. doi:10.1017/S0960258500001720
90. Huang, R., Jiang, L., Zheng, J., Wang, T., Wang, H., Huang, Y., et al. (2013). Genetic bases of rice grain shape:so many genes, so little known. Trends Plant Sci. 18, 218–226. doi:10.1016/j.tplants.2012.11.001
91. Iglesias-Fernández, R., Matilla, A. J., Pulgar, I., and Torre, F. (2007). Ripe fruits of Sisymbrium officinale L. contain heterogeneous endospermic seeds with different germination rates. Seed Sci. Biotechnol. 1, 18–24.
92. Ingouff, M., Jullien, P. E., and Berger, F. (2006). The female gametophyte and the endosperm control cell proliferation and differentiation of the seed coat in Arabidopsis. Plant Cell 18, 3491–3501. doi:10.1105/tpc.106.047266
93. Ingram, G. C. (2010). Family life at close quarters:communication and constraint in angiosperm seed development. Protoplasma 247, 195–214. doi:10.1007/s00709-010-0184-y
94. Izawa, Y., Takayanagi, Y., Inaba, N., Abe, Y., Minami, M., Fujisawa, Y., et al. (2010). Function and expression pattern of the alpha subunit of the heterotrimeric G protein in rice. Plant Cell Physiol. 51, 271–281. doi:10.1093/pcp/pcp186
95. Jahnke, S., Menzel, M. I., Van Dusschoten, D., Roeb, G. W., Bühler, J., Minwuyelet, S., et al. (2009). Combined MRI–PET dissects dynamic changes in plant structures and functions. Plant J. 59, 634–644. doi:10.1111/j.1365-313X.2009.03888.x
96. Jofuku, K. D., Omidyar, P. K., Gee, Z., and Okamuro, J. K. (2005). Control of seed mass and seed yield by the floral homeotic gene APETALA2. Proc. Natl. Acad. Sci. U.S.A. 102, 3117–3122. doi:10.1073/pnas.0409893102
97. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323–329. doi:10.1038/nature05286
98. Julián, I., Gandullo, J., Santos-Silva, L. K., Diaz, I., and Martinez, M. (2013). Phylo-genetically distant barley legumains have a role in both seed and vegetative tissues. J. Exp. Bot. 64, 2929–2941. doi:10.1093/jxb/ert132
99. Kang, B. H., Xiong, Y., Williams, D. S., Pozueta-Romero, D., and Chourey, P. S. (2009). Miniature1-encoded cell wall invertase is essential for assembly and function of wall-ingrowth in the maize endosperm transfer cell. Plant Physiol. 151, 1366–1376. doi:10.1104/pp.109.142331
100. Kathage, J., and Qaim, M. (2012). Economic impacts and impact dynamics of Bt (Bacillus thuringiensis) cotton in India. Proc. Natl. Acad. Sci. U.S.A. 109, 11652–11656. doi:10.1073/pnas.1203647109
101. Kelley, D. R., and Gasser, C. S. (2009). Ovule development:genetic trends and evolutionary considerations. Sex. Plant Reprod. 22, 229–234. doi:10.1007/s00497-009-0107-2
102. Khan, D., Millar, J. L., Girard, I. J., and Belmonte, M. F. (2014). Transcriptional circuitry underlying seed coat development in Arabidopsis. Plant Sci. 219–220, 51–60. doi:10.1016/j.plantsci.2014.01.004
103. Kimmel, L. B., and Day, M. P. (2001). New life for an old fiber:attributes and advantages of naturally colored cotton. AATCC Rev. 1, 32–36.
104. Kladnik, A., Chamusco, K., Dermastia, M., and Chourey, P. (2004). Evidence of programmed cell death in post-phloem transport cells of the maternal pedicel tissue in developing caryopsis of maize. Plant Physiol. 136, 3572–3581. doi:10.1104/pp.104.045195
105. Koch, K. (2004). Sucrose metabolism:regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr. Opin. Plant Biol. 7, 235–246. doi:10.1016/j.pbi.2004.03.014
106. Kovalchuk, N., Li, M., Wittek, F., Reid, N., Singh, R., Shirley, N., et al. (2010). Defensin promoters as potential tools for engineering disease resistance in cereal grains. Plant Biotechnol. J. 8, 47–64. doi:10.1111/j.1467-7652.2009.00465.x
107. Kranner, I., Beckett, R. P., Minibayeva, F. V., and Seal, C. E. (2010). What is stress? Concepts, definitions and applications in seed science. New Phytol. 188, 655–673. doi:10.1111/j.1469-8137.2010.03461.x
108. Krishnan, S., and Dayanandan, P. (2003). Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). J. Biosci. 28, 455–469. doi:10.1007/BF02705120
109. Kunieda, K., Mitsuda, N., Ohme-Takagi, M., Takeda, S., Aida, M., Tasaka, M., et al. (2008). NAC family proteins NARS1/NAC2 and NARS2/NAM in the outer integument regulate embryogenesis in Arabidopsis. Plant Cell 20, 2631–2642. doi:10.1105/tpc.108.060160
110. Ladwig, F., Stahl, M., Ludewig, U., Hirner, A. A., Hammes, U. Z., Stadler, R., et al. (2012). Siliques are Red1 from Arabidopsis acts as a bidirectional amino acid transporter that is crucial for the amino acid homeostasis of siliques. Plant Physiol. 158, 1643–1655. doi:10.1104/pp.111.192583
111. Lafon-Placette, C., and Köhler, C. (2014). Embryo and endosperm, partners in seed development. Curr. Opin. Plant Biol. 17, 64–69. doi:10.1016/j.pbi.2013. 11.008
112. Lanning, F. C., and Eleuterius, L. N. (1992). Silica and ash in seeds of cultivated grains and native plants. Ann. Bot. 69, 151–160.
113. Lattanzio, V., Lattanzio, V. M. T., and Cardinali, A. (2006). “Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects,” in Phytochemistry:Advances in Research, ed. F. Imperato (Trivandrum:Research Signpost), 23–67.
114. Lay, F. T., and Anderson, M. A. (2005). Defensins–components of the innate immune system in plants. Curr. Protein Pept. Sci. 6, 85–101. doi:10.2174/1389203053027575
115. Lee, J. J., Woodward, A. W., and Chen, Z. J. (2007). Gene expression changes and early events in cotton fibre development. Ann. Bot. 100, 1391–1401. doi:10.1093/aob/mcm232
116. Lepiniec, L., Debeaujon, I., Routaboul, J. M., Baudry, A., Pourcel, L., Nesi, N., et al. (2006). Genetics and biochemistry of seed flavonoids. Annu. Rev. Plant Biol. 57, 405–430. doi:10.1146/annurev.arplant.57.032905.105252
117. Li, Q., and Li, L. (2014). Uniquitin-mediated control of seed size in plant. Front. Plant Sci. 5:332. doi:10.3389/fpls.2014.00332
118. Li, Q., Li, L., Yang, X., Warburton, M. L., Bai, G., Dai, J., et al. (2010). Relationship, evolutionary fate and function of two maize co-orthologs of rice GW2 associated with kernel size and weight. BMC Plant Biol. 10:143. doi:10.1186/1471-2229-10-143
119. Li, S. F., Milliken, O. N., Pham, H., Seyit, R., Napoli, R., Preston, J., et al. (2009). The Arabidopsis MYB5 transcription factor regulates mucilage synthesis, seed coat development, and trichome morphogenesis. Plant Cell 21, 72–89. doi:10.1105/tpc.108.063503
120. Li, Y., Zheng, L., Corke, F., Smith, C., and Bevan, M. W. (2008). Control of final seed and organ size by the DA1 gene family in Arabidopsis thaliana. Genes Dev. 22, 1331–1336. doi:10.1101/gad.463608
121. Linnestad, C., Doan, D. N., Brown, R. C., Lemmon, B. E., Meyer, D. J., Jung, R., et al. (1998). Nucellain, a barley homolog of the dicot vacuolar-processing protease, is localized in nucellar cell walls. Plant Physiol. 118, 1169–1180. doi:10.1104/pp.118.4.1169
122. Liu, Q., Llewellyn, D. J., Singh, S. P., and Green, A. G. (2012). “Cotton seed development:opportunities to add value to a byproduct of fiber production,” in Flowering and fruiting in cotton, eds D. M. Oosterhuis and J. T. Cothren (Cordova:The Cotton Foundation Press), 131–162.
123. Lohaus, G., and Moellers, C. (2000). Phloem transport of amino acids in two Brassica napus L. genotypes and one B. carinata genotype in relation to their seed protein content. Planta 211, 833–840. doi:10.1007/s004250000349
124. Lombardi, L., Casani, S., Ceccarelli, N., Galleschi, L., Picciarelli, P., and Lorenzi, R. (2007). Programmed cell death of the nucellus during Sechium edule Sw. seeddevelopment is associated with activation of caspase-like proteases. J. Exp. Bot. 58, 2949–2958. doi:10.1093/jxb/erm137
125. Lopato, S., Borisjuk, N., Langridge, P., and Hrmova, M. (2014). Endospermtransfer cell-specific genes and proteins:structure, function and applications in biotechnology. Front. Plant Sci. 5:64. doi:10.3389/fpls.2014.00064
126. López-Fernández, M. P., and Maldonado, S. (2013). Programmed cell death during quinoa perisperm development. J. Exp. Bot. 64, 3313–3325. doi:10.1093/jxb/ert170
127. Maitz, M., Santandrea, G., Zhang, Z., Lal, S., Hannah, L. C., Salamini, F., et al. (2000). rgf1, a mutation reducing grain filling in maize through effects on basal endosperm and pedicel development. Plant J. 23, 29–42. doi:10.1046/j.1365-313x.2000.00747.x
128. Méchin, V., Thévenot, C., Le Guilloux, M., Prioul, J. L., and Damerval, C. (2007). Developmental analysis of maize endosperm proteome suggests a pivotal role for pyruvate orthophosphate dikinase. Plant Physiol. 143, 1203–1219. doi:10.1104/pp.106.092148
129. 1H NMR imaging uncovers sugar allocation in the living seed. Plant Biotechnol. J. 9, 1022–1037. doi:10.1111/j.1467-7652.2011.00618.x
130. Melkus, G., Rolletschek, H., Radchuk, R., Fuchs, J., Rutten, T., Wobus, U., et al. (2009). The metabolic role of the legume endosperm:a nonin-vasive imaging study. Plant Physiol. 151, 1139–1154. doi:10.1104/pp.109. 143974
131. Mochizuki, M., Tanaka, R., Grimm, B., Masuda, T., Moulin, M., Smith, A. G., et al. (2009). The cell biology of tetrapyrroles:a life and death struggle. Trends Plant Sci. 15, 488–499. doi:10.1016/j.tplants.2010.05.012
132. Möhlmann, T., and Neuhaus, H. E. (1997). Precursor and effector dependency of lipid synthesis in amyloplasts isolated from developing maize and wheat endosperm. J. Cereal Sci. 26, 161–167. doi:10.1006/jcrs.1997.0116
133. Möhlmann, T., Scheibe, R., and Neuhaus, H. E. (1994). Interaction between fatty-acid and starch synthesis in isolated amyloplasts from cauliflower floral buds. Planta 194, 492–497. doi:10.1007/BF00714461
134. Molina, I., Li-Beisson, Y., Beisson, F., Ohlrogge, J. B., and Pollard, M. (2008). Identification of an Arabidopsis feruloyl-coenzyme A transferase required for suberin synthesis. Plant Physiol. 151, 1317–1328. doi:10.1104/pp.109.144907
135. Monjardino, P., Rocha, S., Tavares, A. C., Fernandes, R., Sampaio, P., Salema, R., et al. (2013). Development of flange and reticulate wall ingrowths in maize (Zea mays L.) endosperm transfer cells. Protoplasma 250, 495–450. doi:10.1007/s00709-012-0432-4
136. Morley-Smith, E. R., Pike, M. J., Findlay, K., Köckenberger, W., Hill, L. M., Smith, A. M., 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. doi:10.1104/pp.108.124644
137. Nakaune, S., Yamada, K., Kondo, M., Kato, T., Tabata, S., Nishimura, M., et al. (2005). Avacuolar processingenzyme,δVPE,isinvolvedinseedcoat formationatthe early stage of seed development. Plant Cell 17, 876–887. doi:10.1105/tpc.104.026872
138. Nayar, S., Sharma, R., Tyagi, A. K., and Kapoor, S. (2013). Functional delineation of rice MADS29 reveals its role in embryo and endosperm development by affecting hormone homeostasis. J. Exp. Bot. 64, 4239–4253. doi:10.1093/jxb/ert231
139. Nelson, D. C., Flematti, G. R., Ghisalberti, E. L., Dixon, K. W., and Smith, S. M. (2012). Regulation of seed germination and seedling growth by chemical signals from burning vegetation. Annu. Rev. Plant Biol. 63, 107–130. doi:10.1146/annurev-arplant-042811-105545
140. Nelson, D. C., Flematti, G. R., Riseborough, J. A., Ghisalberti, E. L., Dixon, K. W., and Smith, S. M. (2010). Karrikins enhance light responses during germination and seedling development in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 107, 7095–7100. doi:10.1073/pnas.0911635107
141. Nutbeam, A. R., and Duffus, C. M. (1978). Oxygen-exchange in pericarp green layer of immature cereal-grains. Plant Physiol. 62, 360–362. doi:10.1104/pp.62.3.360
142. Offler, C. E., McCurdy, D. W., Patrick, J. W., and Talbot, M. J. (2003). Transfer cells:cells specialized for a special purpose. Annu. Rev. Plant Biol. 54, 431–454. doi:10.1146/annurev.arplant.54.031902.134812
143. Offler, C. E., Nerlich, S. M., and Patrick, J. W. (1989). Pathway of photosynthate transfer in the developing seed of Vicia faba L. transfer in relation to seed anatomy. J. Exp. Bot. 40, 769–780. doi:10.1093/jxb/40.7.769
144. Ohto, M. A., Fischer, R. L., Goldberg, R. B., Nakamura, K., and Harada, J. J. (2005). Control of seed mass by APETALA2. Proc. Natl. Acad. Sci. U.S.A. 102, 3123–3128. doi:10.1073/pnas.0409858102
145. Ohto, M. A., Floyd, S. K., Fischer, R. L., Goldberg, R. B., and Harada, J. J. (2009). Effects of APETALA2 on embryo, endosperm, and seed coat development determine seed size in Arabidopsis. Sex. Plant Reprod. 22, 277–289. doi:10.1007/s00497-009-0116-1
146. Okuda, S., Tsutsui, H., Shiina, K., Sprunck, S., Takeuchi, H., Yui, R., et al. (2009). Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature 458, 357–361. doi:10.1038/nature07882
147. Olsen, O. A. (2004). Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16, S214–S227. doi:10.1105/tpc.017111
148. Oparka, K. J., and Gates, P. (1981). Transport of assimilates in the developing caryopsis of rice (Oryza sativa L.). Planta 152, 388–396. doi:10.1007/BF00385354
149. Oparka, K. J., Roberts, A. G., Boevink, P., Santa Cruz, S., Roberts, I., Pradel, K. S., etal. (1999). Simple, but not branched, plasmodesmata allow the nonspecific trafficking of proteins in developing tobacco leaves. Cell 97, 743–754. doi:10.1016/S0092-8674(00)80786-2
150. Panitz, R., Borisjuk, L., Manteuffel, R., and Wobus, U. (1995). Transient expression of storage-protein genes during early embryogenesis of Vicia faba:synthesis and metabolization of vicilin and legumin in the embryo, suspensor and endosperm. Planta 196, 765–774. doi:10.1007/BF01106772
151. Patrick, J. W., Botha, F. C., and Birch, R. G. (2013). Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnol. J. 11, 142–156. doi:10.1111/pbi.12002
152. Patrick, J. W., and Offler, C. E. (1995). Post-sieve element transport of sucrose in developing seeds. Aust. J. Plant Physiol. 22, 681–702. doi:10.1071/PP9950681
153. Patrick, J. W., and Offler, C. E. (2001). Compartmentation of transport and transfer events in developing seeds. J. Exp. Bot. 52, 551–564. doi:10.1093/jexbot/52.356.551
154. Patrick, J. W., Offler, C. E., and Wang, X.-D. (1995). Cellular pathway of photosyn-thate transport in coats of developing seed of Vicia faba L. and Phaseolus vulgaris L. I. Extent of transport through the coat symplast. J. Exp. Bot. 46, 35–47. doi:10.1093/jxb/46.1.35
155. Penfield, S., and King, J. (2009). Towards a systems biology approach to understanding seed dormancy and germination. Proc. Biol. Sci. 276, 3561–3569. doi:10.1098/rspb.2009.0592
156. Phelps, M. E. (2004). PET:Molecular Imaging and Its Biological Application. New York:Springer.
157. Pignocchi, C., Minns, G. E., Nesi, N., Koumproglou, R., Kitsios, G., Benning, C., et al. (2009). ENDOSPERM DEFECTIVE1 is a novel microtubule-associated protein essential for seed development in Arabidopsis. Plant Cell 21, 90–105. doi:10.1105/tpc.108.061812
158. Quail, P. H. (1997). An emerging molecular map of the phytochrome. Plant Cell Environ. 20, 657–665. doi:10.1046/j.1365-3040.1997.d01-108.x
159. Radchuk, V., Borisjuk, L., Radchuk, R., Steinbiss, H. H., Rolletschek, H., Broeders, S., et al. (2006). Jekyll encodes a novel protein involved in the sexual reproduction of barley. Plant Cell 18, 1652–1666. doi:10.1105/tpc.106.041335
160. Radchuk, V., Kumlehn, J., Rutten, T., Sreenivasulu, N., Radchuk, R., Rolletschek, H., et al. (2012). Fertility in barley flowers depends on Jekyll functions in male and female sporophytes. New Phytol. 194, 142–157. doi:10.1111/j.1469-8137.2011.04032.x
161. Radchuk, V., Weier, D., Radchuk, R., Weschke, W., and Weber, H. (2011). Development of maternal seed tissue in barley is mediated by regulated cell expansion and cell disintegration and coordinated with endosperm growth. J. Exp. Bot. 62, 1217–1227. doi:10.1093/jxb/erq348
162. Radchuk, V. V., Borisjuk, L., Sreenivasulu, N., Merx, K., Mock, H. P., Rolletschek, H., et al. (2009). Spatio-temporal profiling of starch biosynthesis and degradation in the developing barley grain. Plant Physiol. 150, 190–204. doi:10.1104/pp.108.133520
163. Raissig, M. T., Baroux, C., and Grossniklaus, U. (2011). Regulation and flexibility of genomic imprinting during seed development. Plant Cell 23, 16–26. doi:10.1105/tpc.110.081018
164. Rochat, C., Wuillème, S., Boutin, J.-P., and Hedley, C. L. (1995). A mutation at the rb gene, lowering ADPGPPase activity, affects storage product metabolism of pea seed coats. J. Exp. Bot. 46, 415–421. doi:10.1093/jxb/46.4.415
165. Rolletschek, H., Borisjuk, L., Koschorreck, M., Wobus, U., and Weber, H. (2002). Legume embryos develop in a hypoxic environment. J. Exp. Bot. 53, 1099–1107. doi:10.1093/jexbot/53.371.1099
166. Rolletschek, H., Koch, K., Wobus, U., and Borisjuk, L. (2005). Positional cues for the starch/lipid balance in maize kernels and resource partitioning to the embryo. Plant J. 42, 69–83. doi:10.1111/j.1365-313X.2005.02352.x
167. Rolletschek, H., Melkus, G., Grafahrend-Belau, E., Fuchs, J., Heinzel, N., Schreiber, F., et al. (2011). Combined noninvasive imaging and modeling approaches reveal metabolic compartmentation in the barley endosperm. Plant Cell 23, 3041–3054. doi:10.1105/tpc.111.087015
168. Rolletschek, H., Weber, H., and Borisjuk, L. (2003). Energy status and its control on embryogenesis of legumes. Embryo photosynthesis contributes to oxygen supply and is coupled to biosynthetic fluxes. Plant Physiol. 132, 1196–1206. doi:10.1104/pp.102.017376
169. Rolletschek, H., Weschke, W., Weber, H., Wobus, U., and Borisjuk, L. (2004). 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. 55, 1351–1359. doi:10.1093/jxb/erh130
170. Roszak, P., and Köhler, C. (2011). Polycomb group proteins are required to couple seed coat initiation to fertilization. Proc. Natl. Acad. Sci. U.S.A. 108, 20826–20831. doi:10.1073/pnas.1117111108
171. Ruan, Y. L. (2013). Boosting seed development as a new strategy to increase cotton fiber yield and quality. J. Integr. Plant Biol. 55, 572–575. doi:10.1111/jipb.12074
172. Ruan, Y. L., Jin, Y., Yang, Y. J., Li, G. J., and Boyer, J. S. (2010). Sugar input, metabolism, and signaling mediated by invertase:roles in development, yield potential, and response to drought and heat. Mol. Plant 3, 942–955. doi:10.1093/mp/ssq044
173. Ruan, Y. L., and Patrick, J. W. (1995). The cellular pathway of post-phloem sugar-transport in developing tomato fruit. Planta 196, 434–444. doi:10.1007/BF00203641
174. Ruuska, S. A., Schwender, J., and Ohlrogge, J. B. (2004). The capacity of green oilseeds to utilize photosynthesis to drive biosynthetic processes. Plant Physiol. 136, 2700–2709. doi:10.1104/pp.104.047977
175. Saito, G. Y., Chang, Y. C., Walling, L. L., and Thomson, W. W. (1989). A correlation in plastid development and cytoplasmic ultrastructure with nuclear gene-expression during seed ripening in soybean. New Phytol. 113, 459–469. doi:10.1111/j.1469-8137.1989.tb00357.x
176. Sanders, A., Collier, R., Trethewy, A., Gould, G., Sieker, R., and Tegeder, M. (2009). AAP1 regulates import of amino acids into developing Arabidopsis embryos. Plant J. 59, 540–552. doi:10.1111/j.1365-313X.2009.03890.x
177. Sang, T. (2009). Genes and mutations underlying domestication transitions in grasses. Plant Physiol. 149, 63–70. doi:10.1104/pp.108.128827
178. Schiefelbein, J. (2003). Cell-fate specification in the epidermis, a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74–78. doi:10.1016/S136952660200002X
179. Schruff, M. C., Spielman, M., Tiwari, S., Adams, S., Fenby, N., and Scott, R. J. (2006). The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signalling, cell division, and the size of seeds and other organs. Development 133, 251–261. doi:10.1242/dev.02194
180. Schwender, J. (2008). Metabolic flux analysis as a tool in metabolic engineering of plants. Curr. Opin. Biotechnol. 19, 131–137. doi:10.1016/j.copbio.2008.02.006
181. Schwender, J., and Ohlrogge, J. B. (2002). Probing in vivo metabolism by stable isotope labeling of storage lipids and proteins in developing Brassica napus embryos. Plant Physiol. 130, 347–361. doi:10.1104/pp.004275
182. Shen-Miller, J. (2002). Sacred lotus, the long-living fruits of China Antique. Seed Sci. Res. 12, 131–143. doi:10.1079/SSR2002112
183. Sinclair, T. R. (1988). Oxygen and temperature effects on soybean seed coat respiration rates. Plant Physiol. 86, 124–128. doi:10.1104/pp.86.1.124
184. Sinclair, T. R., Ward, J. P., and Randall, C. A. (1987). Soybean seed growth in response to long-term exposures to differing oxygen partial pressures. Plant Physiol. 83, 467–468. doi:10.1104/pp.83.3.467
185. Singh, D., and Mathur, S. B. (2004). Histopathology of Seed-Borne Infections. Boca Raton:CRC Press.
186. Smidansky, E. D., Clancy, M., Meyer, F. D., Lanning, S. P., Blake, N. K., Talbert, L. E., et al. (2002). Enhanced ADP-glucose pyrophosphorylase activity in wheat endosperm increases seed yield. Proc. Natl. Acad. Sci. U.S.A. 99, 1724–1729. doi:10.1073/pnas.022635299
187. Smirnoff, N. (2010). Tocochromanols:rancid lipids, seed longevity, and beyond. Proc. Natl. Acad. Sci. U.S.A. 107, 17857–17858. doi:10.1073/pnas.1012749107
188. Smith, H.(2000). Phytochromes and light signal perceptionbyplants—an emerging synthesis. Nature 407, 585–591. doi:10.1038/35036500
189. Smýkal, P., Vernoud, V., Blair, M. W., Soukup, A., and Thompson, R. D. (2014). The role of the testa during development and in establishment of dormancy of the legume seed. Front. Plant Sci. 5:351. doi:10.3389/fpls.2014.00351
190. Song, X. J., Huang, W., Shi, M., Zhu, M. Z., and Lin, H. X. (2007). A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nat. Genet. 39, 623–630. doi:10.1038/ng2014
191. Sreenivasulu, N., Borisjuk, L., Junker, B. H., Mock, H. P., Rolletschek, H., Seiffert, U., et al. (2010). Barley grain development toward an integrative view. Int. Rev. Cell Mol. Biol. 281, 49–89. doi:10.1016/S1937-6448(10)81002-0
192. Sreenivasulu, N., Radchuk, V., Strickert, M., Miersch, O., Weschke, W., and Wobus, U. (2006). Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA-regulated maturation in developing barley seeds. Plant J. 47, 310–327. doi:10.1111/j.1365-313X.2006.02789.x
193. Sriram, G., Fulton, D. B., Iyer, V. V., Peterson, J. M., Zhou, R., Westgate, M. E., et al. (2004). Quantification of compartmented metabolic fluxes in developing soybean embryos by employing biosynthetically directed fractional 13C labeling, two-dimensional [13C, 1H] nuclear magnetic resonance, and comprehensive isotopomer balancing. Plant Physiol. 136, 3043–3057. doi:10.1104/pp.104.050625
194. Stadler, R., Lauterbach, C., and Sauer, N. (2005a). 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. doi:10.1104/pp.105.065607
195. Stadler, R., Wright, K. M., Lauterbach, C., Amon, G., Gahrtz, M., Feuerstein, A., et al. (2005b). Expression of GFP-fusions in Arabidopsis companion cells reveals nonspecific protein trafficking into sieve elements and identifies a novel post-phloem domain in roots. Plant J. 41, 319–331. doi:10.1111/j.1365-313X.2004.02298.x
196. Stiff, M. R., and Haigler, H. C. (2012). “Recent advances in cotton development,” in Flowering and Fruiting in Cotton, eds D. M. Oosterhuis and J. T. Cothren (Cordova:The Cotton Foundation Press), 163–190.
197. Stotz, H. U., Thomson, J. G., and Wang, Y. (2009). Plant defensins:defense, development and application. Plant Signal. Behav. 4, 1010–1012. doi:10.4161/psb.4.11.9755
198. Su, Z., Hao, C., Wang, L., Dong, Y., and Zhang, X. (2011). Identification and development of a functional marker of TaGW2 associated with grain weight in bread wheat (Triticum aestivum L.). Theor. Appl. Genet. 122, 211–223. doi:10.1007/s00122-010-1437-z
199. Tegeder, M. (2014). Transporters involved in source to sink partitioning of amino acids and ureides:opportunities for crop improvement. J. Exp. Bot. 65, 1865–1878. doi:10.1093/jxb/eru012
200. Thiel, J. (2014). Development of endosperm transfer cells in barley. Front. Plant Sci. 5:108. doi:10.3389/fpls.2014.00108
201. Thiel, J., Weier, D., Sreenivasulu, N., Strickert, M., Weichert, N., Melzer, M., 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. doi:10.1104/pp.108.127001
202. Thomma, B. P., Cammue, B. P., and Thevissen, K. (2002). Plant defensins. Planta 216, 193–202. doi:10.1007/s00425-002-0902-6
203. Thorne, J. H. (1982). Temperature and oxygen effects on C14-labeled photosynthate unloading and accumulation in developing soybean seeds. Plant Physiol. 69, 48–53. doi:10.1104/pp.69.1.48
204. Tilsner, J., Kassner, N., Struck, C., and Lohaus, G. (2005). Amino acid contents and transport in oilseed rape (Brassica napus L.) under different nitrogen conditions. Planta 221, 328–338. doi:10.1007/s00425-004-1446-8
205. Tschiersch, H., Liebsch, G., Borisjuk, L., Stangelmayer, A., and Rolletschek, H. (2012). An imaging method for oxygen distribution, respiration and photosynthesis at a microscopic level of resolution. New Phytol. 196, 926–936. doi:10.1111/j.1469-8137.2012.04295.x
206. Tsiatsiani, L., Gevaert, K., and Van Breusegem, F. (2012). Natural substrates of plant proteases:how can protease degradomics extend our knowledge? Physiol. Plant. 145, 28–40. doi:10.1111/j.1399-3054.2011.01534.x
207. Ungru, A., Nowack, M. K., Reymond, M., Shirzadi, R., Kumar, M., Biewers, S., et al. (2008). Natural variation in the degree of autonomous endosperm formation reveals independence and constraints of embryo growth during seed development in Arabidopsis thaliana. Genetics 179, 829–841. doi:10.1534/genetics.107.084889
208. van Bel, A. J., Helariutta, Y., Thompson, G. A., Ton, J., Dinant, S., Ding, B., et al. (2013). Phloem:the integrative avenue for resource distribution, signaling, and defense. Front. Plant Sci. 4:471. doi:10.3389/fpls.2013.00471
209. van Dongen, J. T., Ammerlaan, A. M., Wouterlood, M., Van Aelst, A. C., and Borstlap, A. C. (2003). Structure of the developing pea seed coat and the post-phloem transport pathway of nutrients. Ann. Bot. 91, 729–737. doi:10.1093/aob/mcg066
210. van Dongen, J. T., Roeb, G. W., Dautzenberg, M., Froehlich, A., Vigeolas, H., Minchin, P. E. H., etal. (2004). Phloem import and storage metabolism are highly coordinated by the low oxygen concentrations within developing wheat seeds. Plant Physiol. 135, 1809–1821. doi:10.1104/pp.104.040980
211. Verboven, P., Herremans, E., Borisjuk, L., Helfen, L., Ho, Q. T., Tschiersch, H., et al. (2013). Void space inside the developing seed of Brassica napus and the modelling of its function. New Phytol. 199, 936–947. doi:10.1111/nph. 12342
212. Verdier, J., Dessaint, F., Schneider, C., and Abirached-Darmency, M. (2013). A combined histology and transcriptome analysis unravels novel questions on Medicago truncatula seed coat. J. Exp. Bot. 64, 459–470. doi:10.1093/jxb/ers304
213. Verdier, J., Zhao, J., Torres-Jerez, I., Ge, S., Liu, C., He, X., et al. (2012). MtPAR MYB transcription factor acts as an on switch for proanthocyanidin biosynthesis in Medicago truncatula. Proc. Natl. Acad. Sci. U.S.A. 109, 1766–1771. doi:10.1073/pnas.1120916109
214. Vermerris, W., and Nicholson, R. (2007). Phenolic Compound Biochemistry. Springer e-Books ISBN 1402051646.
215. Vigeolas, H., Möhlmann, T., Martini, N., Neuhaus, H. E., and Geigenberger, P. (2004). Embryo-specific reduction of ADP-Glc pyrophosphorylase leads to an inhibition of starch synthesis and a delay in oil accumulation in developing seeds of oilseed rape. Plant Physiol. 136, 2676–2686. doi:10.1104/pp.104.046854
216. Vigeolas, H., Van Dongen, J. T., Waldeck, P., Hühn, D., and Geigenberger, P. (2003). Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape. Plant Physiol. 133, 2048–2060. doi:10.1104/pp.103.031963
217. Vinogradova, I. S., and Falaleev, O. V. (2012). Formation of the vascular system of developing bean (Phaseolus limensis L.) seeds according to nuclear magnetic resonance microtomography. Ontogenez 43, 28–38. doi:10.1134/S1062360412010079
218. 2 and buffering of tissue. J. Exp. Bot. 85, 330–337. doi:10.1093/jxb/25.2.330
219. Walker, N. A., Zhang, W. H., Harrington, G., Holdaway, N., and Patrick, J. W. (2000). Effluxes of solutes from developing seed coats of Phaseolus vulgaris L. and Vicia faba L.:locating the effect of turgor in a coupled chemiosmotic system. J. Exp. Bot. 51, 1047–1055. doi:10.1093/jexbot/51.347.1047
220. Wang, E., Wang, J., Zhu, X., Hao, W., Wang, L., Li, Q., et al. (2008). Control of rice grain-filling and yield by a gene with a potential signature of domestication. Nat. Genet. 40, 1370–1374. doi:10.1038/ng.220
221. Wang, N., and Fisher, D. B. (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. doi:10.1104/pp.104.1.17
222. Waters, A. J., Makarevitch, I., Eichten, S. R., Swanson-Wagner, R. A., Yeh, C.-T., Xu, W., et al. (2011). Parent-of-origin effects on gene expression and DNA methylation in the maize endosperm. Plant Cell 23, 4221–4233. doi:10.1105/tpc.111.092668
223. Watson, P. A., and Duffus, C. M. (1988). Carbon-dioxide fixation by detached cereal caryopses. Plant Physiol. 87, 504–509. doi:10.1104/pp.87.2.504
224. Weber, H., Borisjuk, L., and Wobus, U. (1996a). Controlling seed development and seed size in Vicia faba:a role for seed coat-associated invertases and carbohydrate state. Plant J. 10, 823–834. doi:10.1046/j.1365-313X.1996.10050823.x
225. Weber, H., Buchner, P., Borisjuk, L., and Wobus, U. (1996b). 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 for seed development. Plant J. 9, 841–850. doi:10.1046/j.1365-313X.1996.9060841.x
226. Weber, H., Borisjuk, L., and Wobus, U. (2005). Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56, 253–279. doi:10.1146/annurev.arplant.56.032604.144201
227. Weijers, D., van Hamburg, J. P., van Rijn, E., Hooykaas, P. J. J., and Offringa, R. (2003). Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiol. 133, 1882–1892. doi:10.1104/pp.103.030692
228. Welbaum, G. E., and Bradford, K. J. (1990). Water relations of seed development and germination in muskmelon (Cucumis melo L.):IV. Characteristics of the perisperm during seed development. Plant Physiol. 92, 1038–1045. doi:10.1104/pp.92.4.1038
229. Weng, J., Gu, S., Wan, X., Gao, H., Guo, T., Su, N., et al. (2008). Isolation and initial characterization of GW5, a major QTL associated with rice grain width and weight. Cell Res. 18, 1199–1209. doi:10.1038/cr.2008.307
230. Wolf, J. B., and Hager, R. (2006). A maternal-offspring co-adaptation theory for the evolution of genomic imprinting. PLoS Biol. 4:e380. doi:10.1371/jour-nal.pbio.0040380
231. Wolff, P., Weinhofer, I., Seguin, J., Roszak, P., Beisel, C., Donoghue, M. T., et al. (2011). High-resolution analysis of parent-of-origin allelic expression in the Arabidopsis endosperm. PLoS Genet. 7:e1002126. doi:10.1371/journal.pgen. 1002126
232. Wu, B., Andersch, F., Weschke, W., Weber, H., and Becker, J. S. (2013). Diverse accumulation and distribution of nutrient elements in developing wheat grain studied by laser ablation inductively coupled plasma mass spectrometry imaging. Metallomics 5, 1276–1284. doi:10.1039/c3mt00071k
233. Xia, T., Li, N., Dumenil, J., Li, J., Kamenski, A., Bevan, M. W., et al. (2013). The ubiquitin receptor DA1 interacts with the E3 ubiquitin ligase DA2 to regulate seed and organ size in Arabidopsis. Plant Cell 25, 3347–3359. doi:10.1105/tpc.113. 115063
234. Xia, X., Zhang, H. M., Andriunas, F. A., Offler, C. E., and Patrick, J. W. (2012). Extracellular hydrogen peroxide, produced through a respiratory burst oxidase/superoxide dismutase pathway, directs ingrowth wall formation in epidermal transfer cells of Vicia faba cotyledons. Plant Signal. Behav. 7, 1–4. doi:10.4161/psb.21320
235. Xiong, F., Yu, X. R., Zhou, L., Wang, F., and Xiong, A. S. (2013a). Structural and physiological characterization during wheat pericarp development. Plant Cell Rep. 32, 1309–1320. doi:10.1007/s00299-013-1445-y
236. Xiong, Y., McCormack, M., Li, L., Hall, Q., Xiang, C., and Sheen, J. (2013b). Glucose-TOR signalling reprograms the transcriptome and activates meristems. Nature 496, 181–186. doi:10.1038/nature12030
237. Yan, H., Hua, Z., Qian, G., Wang, M., Du, G., and Chen, J. (2009). Analysis of the chemical composition of cotton seed coat by Fourier-transform infrared (FT-IR) microspectroscopy. Cellulose 16, 1099–1107. doi:10.1007/s10570-009-9349-2
238. Yang, C., and Ye, Z. (2013). Trichomes as models for studying plant cell differentiation. Cell. Mol. Life Sci. 70, 1937–1948. doi:10.1007/s00018-012-1147-6
239. Yang, X., Wu, F., Lin, X., Du, X., Chong, K., Gramzow, L., et al. (2012). Live and let die–the B(sister) MADS-box gene OsMADS29 controls the degeneration of cells in maternal tissues during seed development of rice (Oryza sativa). PLoS ONE 7:e51435. doi:10.1371/journal.pone.0051435
240. Yeung, E. C., and Meinke, D. W. (1993). Embryogenesis in angiosperms:development of the suspensor. Plant Cell 5, 1371–1381. doi:10.1105/tpc.5. 10.1371
241. Yin, L. L., and 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. doi:10.1105/tpc.111.094854
242. Yu, C. Y. (2013). Molecular mechanism of manipulating seed coat coloration in oilseed Brassica species. J. Appl. Genet. 54, 135–145. doi:10.1007/s13353-012-0132-y
243. Zhang, M., Zhao, H., Xie, S., Chen, J., Xu, Y., Wang, K., etal. (2011). Extensive, clustered parental imprinting of protein-coding and noncoding RNAs in developing maize endosperm. Proc. Natl. Acad. Sci. U.S.A. 108, 20042-20047. doi:10.1073/pnas.1112186108
244. Zhang, W. H., Zhou, Y., Dibley, K. E., Tyerman, S. D., Furbank, R. T., and Patrick, J. W. (2007). Nutrient loading of developing seeds. Funct. Plant Biol 34, 314-331. doi:10.1071/FP06271
245. Zhang, X., Wang, J., Huang, J., Lan, H., Wang, C, Yin, C, et al. (2012). Rare allele of OsPPKL1 associated with grain length causes extra-large grain and a significant yield increase in rice. Proc. Natl Acad. Sci. U.S.A. 109, 21534-21539. doi:10.1073/pnas.1219776110
246. ;-O-glucoside for proanthocyanidin biosynthesis in Medicago trun-catula and Arabidopsis. Plant Cell 21, 2323-2340. doi:10.1105/tpc.109.067819
247. Zhou, Y, Andriunas, F. A., Offler, C. E., McCurdy, D. W, and Patrick, J. W. (2010). An epidermal-specific ethylene signal cascade regulates trans-differentiation of transfer cells in Vicia faba cotyledons. New Phytol. 185, 931-943. doi:10.1111/j.1469-8137.2009.03136.x
248. Zhou, Z., Wang, L., Li, J., Song, X., and Yang, C. (2009). Study on programmed cell death and dynamic changes of starch accumulation in pericarp cells of Triticum aestivum L. Protoplasma 236,49-58. doi:10.1007/s00709-009-0046-7