Hostname: page-component-cd9895bd7-gxg78 Total loading time: 0 Render date: 2024-12-27T09:47:48.029Z Has data issue: false hasContentIssue false

Seed coat formation: its evolution and regulation

Published online by Cambridge University Press:  09 December 2019

Angel J. Matilla*
Affiliation:
Department of Functional Biology, Life Campus, Faculty of Pharmacy, University of Santiago de Compostela (USC), 15782-Santiago de Compostela, Spain
*
Author for correspondence: Angel J. Matilla, E-mail: angeljesus.matilla@usc.es

Abstract

In higher plants, the seed precursor (ovule primordia) is composed of three parts: funiculus, nucellus and chalaza, generating the latter one (II) or two (OI and II) protective maternal integuments (seed coat, SC). The appearance of a viable seed requires the coordinate growth and development of the preceding three compartments. Integuments are essentials for seed life as they nourish, protect and facilitate seed dispersion. Endosperm and integument growth and development are tightly coupled. Gymnosperm and angiosperm ovules are commonly unitegmic and bitegmic, respectively. Unusually, ategmy and threetegmy (OI, II and aril) also exist. The expression of the INO, ATS and ETT genes, involved in integument development, seems to have demonstrated that the fusion of OI and II leads to the appearance of unitegmy in higher plants. Likewise, INO expression also manifests the conservation of OI during evolution. The molecular control of SC development is constituted by a signalling network with still a multitude of gaps. The fertilization-independent development of the ovule is repressed by the FERTILIZATION INDEPENDENT SEED (FIS), a Polycomb-Repressive-Complex-2 (PRC2). Both endosperm and SC development are tightly linked to PRC2 function. As in many other developmental processes, auxin plays an essential role during ovule and SC development. Auxin transport from the endosperm to the integuments is regulated by AGL62 (AGAMOUS-LIKE 62), the encoding gene of which is specifically expressed in the endosperm to suppress its cellularization. In the absence of AGL62 (i.e. agl62 mutants), auxin remains trapped in the endosperm and the SC fails to develop (i.e. seed abortion). This update shows that auxin biosynthesis, transport and signalling play a predominant role and seem to be absolutely required in the pathway(s) that lead to SC formation, most likely not as a unique hormonal component.

Type
Review Paper
Copyright
Copyright © Cambridge University Press 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Arnault, G, Vialette, ACM, Andres-Robin, A, Fogliani, B, Gâteblé, G and Scutt, CP (2018) Evidence for the extensive conservation of mechanisms of ovule integument development since the most recent common ancestor of living Angiosperms. Frontiers in Plant Science 9, 1352.CrossRefGoogle ScholarPubMed
Aw, SJ, Hamamura, Y, Chen, Z, Schnittger, A and Berger, F (2010) Sperm entry is sufficient to trigger division of the central cell but the paternal genome is required for endosperm development in Arabidopsis. Development 137, 26832690.CrossRefGoogle ScholarPubMed
Bao, F, Azhakanandam, S and Franks, RG (2010) SEUSS and SEUSS-LIKE transcriptional adaptors regulate floral and embryonic development in Arabidopsis. Plant Physiology 152, 821836.CrossRefGoogle ScholarPubMed
Bastos-Lima, N, Trindade, FG, da Cunha, M, Oliveira, AEA, Topping, J, Lindsey, K and Fernandes, KVS (2015) Programmed cell death during development of cowpea (Vigna unguiculata (L.) Walp.) SC. Plant, Cell and Environment 38, 718728.CrossRefGoogle Scholar
Batista, RA, Figueiredo, DD, Santos-González, J and Köhler, C (2019) Auxin regulates endosperm cellularization in Arabidopsis. Genes & Development 33, 111.CrossRefGoogle ScholarPubMed
Baxter, IR, Young, JC, Armstrong, G, Foster, N, Bogenschutz, N, Cordova, T, Peer, WA, Haze, SP, Murphy, AS and Harper, JF (2005) A plasma membrane H+-ATPase is required for the formation of proanthocyanidins in the seed coat endothelium of Arabidopsis thaliana. Proceeding of the National Academic of Sciences of the USA 102, 26492654.CrossRefGoogle ScholarPubMed
Beeckman, T, De Rycke, R, Viane, R and Inze, D (2000) Histological study of seed coat development in Arabidopsis thaliana. Journal of Plant Research 113, 139148.CrossRefGoogle Scholar
Bentsink, L and Koornneef, M (2008) Seed dormancy and germination. Arabidopsis Book 6, e0119.CrossRefGoogle ScholarPubMed
Berger, F, Grini, PE and Schnittger, A (2006) Endosperm: an integrator of seed growth and development. Current Opinion of Plant Biology 9, 664670.CrossRefGoogle ScholarPubMed
Braybrook, SA and Peaucelle, A (2013) Mechano-chemical aspects of organ formation in Arabidopsis thaliana: the relationship between auxin and pectin. PLoS One 8, e57813.CrossRefGoogle ScholarPubMed
Brown, RH, Nickrent, DL and Gasser, Ch.S (2010) Expression of ovule and teguments-associated genes in reduced ovules of Santalales. Evolution and Development 12, 231240.CrossRefGoogle ScholarPubMed
Brunoud, G, Wells, DM, Oliva, M, Larrieu, A, Mirabet, V, Burrow, AH, Beeckman, T, Kepinski, S, Traas, J, Bennett, MJ and Vernoux, T (2012) A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482, 103106.CrossRefGoogle ScholarPubMed
Carrillo-Barral, N, Matilla, AJ, Rodríguez-Gacio, MC and Iglesias-Fernández, R (2018) Mannans and endo-β-mannanase transcripts are located in different seed compartments during Brassicaceae germination. Planta 243, 649661.CrossRefGoogle Scholar
Coen, O, Fiume, E, Xu, W, De Vos, D, Lu, J, Pechoux, C, Lepiniec, L and Magnani, E (2017) Developmental patterning of the sub-epidermal integument cell layer in Arabidopsis seeds. Development 144, 14901497.CrossRefGoogle ScholarPubMed
Coen, O and Magnani, E (2018) Seed coat thickness in the evolution of angiosperms. Cellular and Molecular Life Sciences 75, 25092518.CrossRefGoogle ScholarPubMed
Colombo, L, R. Battaglia, R and Kater, MM (2008) Arabidopsis ovule development and its evolutionary conservation. Trends in Plant Science 13, 444450.CrossRefGoogle ScholarPubMed
Creff, A, Brocard, L and Ingram, G (2015) A mechanically sensitive cell layer regulates the physical properties of the Arabidopsis seed coat. Nature Communications 6, 6382.CrossRefGoogle ScholarPubMed
Chahtane, H, Kim, W and López-Molina, L (2017) Primary seed dormancy: a temporally multilayered riddle waiting to be unlocked. Journal of Experimental Botany 68, 857869.Google ScholarPubMed
Chen, J, Lausser, A and Dresselhaus, T (2014) Hormonal responses during early embryogenesis in maize. Biochemical Society Transactions 42, 325331.CrossRefGoogle ScholarPubMed
Chen, LQ, Lin, IWN, Qu, XQ, Sosso, D, McFarlane, HE, Londono, A, Samuels, AL and Frommer, WB (2015). A cascade of sequentially expressed sucrose transporters in the SC and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27, 607619.CrossRefGoogle Scholar
Debeaujon, I, Léon-Kloosterziel, KM and Koornneef, M (2000) Influence of the testa on seed dormancy, germination, and longevity in Arabidopsis. Plant Physiology 122, 403413.CrossRefGoogle ScholarPubMed
Debeaujon, I, Lepiniec, L, Pourcel, L and Routaboul, J-M (2007) Seed coat development and dormancy, pp. 2549 in Bradford, KJ and Nonogaki, H (eds), Annual Plant Reviews Volume 27: Seed Development, Dormancy and Germination. New York, USA: Blackwell Publishing Ltd.CrossRefGoogle Scholar
Derkacheva, M and Henning, L (2014) Variations on a theme: polycomb group proteins in plants. Journal of Experimental Botany 65, 27692784.CrossRefGoogle ScholarPubMed
Domínguez, F and Cejudo, FJ (2014) Programmed cell death (PCD): an essential process of cereal seed development and germination. Frontiers in Plant Science 5, 366.Google ScholarPubMed
Dorcey, E, Urbez, C, Blázquez, MA, Carbonell, J and Perez-Amador, MA (2009) Fertilization-dependent auxin response in ovules triggers fruit development through the modulation of gibberellin metabolism in Arabidopsis. Plant Journal 58, 318332.CrossRefGoogle ScholarPubMed
Doughty, J, Aljabri, M and Scott, RJ (2014) Flavonoids and the regulation of seed size in Arabidopsis. Biochemistry Society Transactions 42, 364369.CrossRefGoogle ScholarPubMed
Doyle, JA (2006) Seed ferns and the origin of angiosperms. Journal of the Torrey Botanical Society 133, 169209.CrossRefGoogle Scholar
Doyle, JA, Manchester, SR, and Sauquet, H (2008) A seed related to Myristicaceae in the early Eocene of southern England. Systematic Botany 33, 636646.CrossRefGoogle Scholar
Endress, PK (2011a) Angiosperm ovules: diversity, development, evolution. Annals of Botany 107, 14651489.CrossRefGoogle Scholar
Endress, PK (2011b) Evolutionary diversification of the flowers in angiosperms. American Journal of Botany 98, 370396.CrossRefGoogle Scholar
Figueiredo, DD and Köhler, C (2014) Signalling events regulating seed coat development. Biochemical Society Translational 42, 358363.CrossRefGoogle ScholarPubMed
Figueiredo, DD, Batista, RA, Roszak, PJ and Köhler, C (2015) Auxin production couples endosperm development to fertilization. Nature Plants 1, 15184.CrossRefGoogle Scholar
Figueiredo, DD, Batista, RA, Roszak, PJ, Henning, L and Köhler, C (2016) Auxin production in the endosperm drives SC development in Arabidopsis. eLife 5, e20542.CrossRefGoogle Scholar
Figueiredo, DD and Köhler, C (2018) Auxin: a molecular trigger of seed development. Genes and Development 32, 479490.CrossRefGoogle ScholarPubMed
Figueiredo, DD, Batista, RA, Santos-González, J and Köhler, C (2019) Auxin regulates endosperm cellularization in Arabidopsis. Genes and Development 33, 466476.Google Scholar
Galbiati, F, Roy, DS, Simonini, S, Cucinotta, M, Ceccato, L, Cuesta, C, Simaskova, M, Benkova, E, Kamiuchi, Y, Aida, M, Weijers, D, Rudiger, S, Masiero, S and Colombo, L (2013) An integrative model of the control of ovule primordial formation. Plant Journal 76, 446455.CrossRefGoogle Scholar
Francoz, E, Lepiniec, L and North, HM (2018) Seed coats as an alternative molecular factory: thinking outside the box. Plant Reproduction 31, 327342.CrossRefGoogle ScholarPubMed
Friis, EM, Crane, PR and Pedersen, KR (2011) Early Flowers and Angiosperm Evolution. Cambridge, UK: Cambridge University Press.CrossRefGoogle Scholar
García, D, Saingery, V, Chambrier, P, Mayer, U, Jürgens, G and Berger, F (2003) Arabidopsis haiku mutants reveal new controls of seed size by endosperm. Plant Physiology 131, 16611670.CrossRefGoogle ScholarPubMed
García, D, Fitz Gerald, JN 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, 5260.CrossRefGoogle ScholarPubMed
Gasser, CS and Skinner, DK (2019) Development and evolution of the unique ovules of flowering plants. Current Topic Development Biology 131, 373399.CrossRefGoogle ScholarPubMed
Gehring, M (2013) Genomic imprinting: insights from plants. Annual Review of Genetics 47, 187208.CrossRefGoogle ScholarPubMed
Gerrienne, P, Meyer-Berthaud, B, Fairon-Demaret, M, Streel, M and Steemans, P (2004) Runcaria, a middle devonian seed plant precursor. Science 306, 856858.CrossRefGoogle ScholarPubMed
González, A, Brown, M, Hatlestad, G, Akhavan, N, Smith, T, Hembd, A, Moore, J, Montes, D, Mosley, T, Resendez, J, Nguyen, H, Wilson, L, Campbell, A, Sudarshan, D and Lloyd, A (2016) TTG2 controls the developmental regulation of seed coat tannins in Arabidopsis by regulating vacuolar transport steps in the proanthocyanidin pathway. Development Biology 419, 5463.CrossRefGoogle ScholarPubMed
Graeber, K, Nakabayashi, K, Miatton, E, Leubner-Metzger, G and Soppe, WJJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell & Environment 35, 17691786.CrossRefGoogle ScholarPubMed
Gross-Hardt, R, Lenhard, M and Laux, T (2002) WUSCHEL signaling functions in interregional communication during Arabidopsis ovule development. Genes and Development 16, 1129 1138.CrossRefGoogle ScholarPubMed
Grossniklaus, U and Paro, R (2014) Transcriptional silencing by Polycomb-Group proteins. Cold Spring Harbour Perspectives in Biology 6, a019331.CrossRefGoogle ScholarPubMed
Hands, P, Rabiger, DS and Koltunov, A (2016) Mechanisms of endosperm initiation. Plant Reproduction 29, 215225.CrossRefGoogle ScholarPubMed
Harada, JJ and Pelletier, J (2012) Genome-wide analyses of gene activity during seed development. Seed Science Research 22, S15S22.CrossRefGoogle Scholar
Hatorangan, MR, Laenen, B, Steige, KA, Slotte, T and Kohler, C (2016) Rapid evolution of genomic imprinting in two species of the Brassicaceae. Plant Cell 28, 18151827.CrossRefGoogle ScholarPubMed
Haughn, G and Chaudhury, A (2005) Genetic analysis of SC development in Arabidopsis. Trends in Plant Science 10, 472477.CrossRefGoogle ScholarPubMed
Hehenberger, E, Kradolfer, D and Köhler, C (2012) Endosperm cellularization defines an important developmental transition for embryo development. Development 139, 20312039.CrossRefGoogle ScholarPubMed
Holdsworth, MJ, Bentsink, L and Soppe, WJJ (2008) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytology 179, 3354.CrossRefGoogle ScholarPubMed
Huang, J, DeBowles, D, Esfandiari, E, Dean, G, Carpita, NC and Haughn, GW (2011) The Arabidopsis transcription factor LUH/MUM1 is required for extrusion of SC mucilage. Plant Physiology 156, 491502.CrossRefGoogle Scholar
Ingram, GC (2010) Family life at close quarters: communication and constraint in angiosperm seed development. Protoplasma 247, 195214.CrossRefGoogle ScholarPubMed
Jaramillo, MA and Kramer, EM (2007) The role of developmental genetics in understanding homology and morphological evolution in plants. International Journal of Plant Science 168, 6172.CrossRefGoogle Scholar
Jia, L, Wu, Q, Ye, N, Liu, R, Shi, L, Xu, W, Zhi, H, Rahman, AN, Xia, Y and Zhang, J (2012) Proanthocyanidins inhibit seed germination by maintaining a high level of abscisic acid in Arabidopsis thaliana. Journal of Integrative Plant Biology 54, 663673.CrossRefGoogle ScholarPubMed
Johnson, CS, Kolewski, B and Smyth, DR (2002) TRANSPARENT TESTA GLABRA2, a trichome and seed coat development gene of Arabidopsis, encodes a WRKY transcription factor. Plant Cell 14, 13591375.CrossRefGoogle ScholarPubMed
Kang, I-H, Steffen, JG, Portereiko, MF, Lloyd, A and Drews, GN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20, 635647.CrossRefGoogle ScholarPubMed
Kelley, DR, Arreola, A, Gallagher, TL and Gasser, CS (2012) ETTIN (ARF3) physically interacts with KANADI proteins to form a functional complex essential for integument development and polarity determination in Arabidopsis. Development 139, 11051109.CrossRefGoogle Scholar
Khan, D, Millar, JL, Girard, IJ and Belmonte, MF (2014). Transcriptional circuitry underlying SC development in Arabidopsis. Plant Science 219, 5160.CrossRefGoogle ScholarPubMed
Köhler, C and Makarevich, G (2006) Epigenetic mechanisms governing seed development in plants. EMBO Reports 7, 12231227.CrossRefGoogle ScholarPubMed
Köhler, C and Kradolfer, D (2011) Epigenetic mechanisms in the endosperm and their consequences for the evolution of flowering plants. Biochimica et Biophysica Acta 1809, 438443.CrossRefGoogle ScholarPubMed
Krishnan, S and Dayanandan, P (2003) Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). Journal of Bioscience 28, 455469.CrossRefGoogle Scholar
Lafon-Placette, C and Köhler, C (2014). Embryo and endosperm, partners in seed development. Current Opinion in Plant Biology 17, 6469.CrossRefGoogle ScholarPubMed
Larsson, E, Vivian-Smith, A, Offringa, R and Sundberg, E (2017) Auxin homeostasis in Arabidopsis ovules is anther-dependent at maturation and changes dynamically upon fertilization. Frontiers in Plant Science 8, 1735.CrossRefGoogle ScholarPubMed
Laugesen, A, Westergaard Højfeldt, J and Helin, K (2019) Molecular mechanisms directing PRC2 recruitment and H3K27 methylation. Molecular Cell 74, 818.CrossRefGoogle ScholarPubMed
Lee, KP, Piskurewicz, U, Tureckova, V, Strnad, M and López-Molina, L (2010). A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proceedings of the National Academy of Sciences of the USA 107, 1910819113.CrossRefGoogle ScholarPubMed
Lepiniec, L, Debeaujon, I, Routaboul, JM, Baudry, A, Pourcel, L, Nesi, N and Caboche, M (2006) Genetics and biochemistry of seed flavonoids. Annual Review of Plant Biology 57, 405430.CrossRefGoogle ScholarPubMed
Li, N and Li, Y (2015) Maternal control of seed size in plants. Journal of Experimental Botany 66, 10871097.CrossRefGoogle ScholarPubMed
Liao, CY, Smet, W, Brunoud, G, Yoshida, S, Vernoux, T and Weijers, D (2015) Reporters for sensitive and quantitative measurement of auxin response. Nature Methods 12, 207210.CrossRefGoogle ScholarPubMed
Linkies, A, Müller, K, Morris, K, Turecková, V, Wenk, M, Cadman, CS, Corbineau, F, Strnad, M, Lynn, JR, Finch-Savage, WE and Leubner-Metzger, G (2009) Ethylene interacts with abscisic acid to regulate endosperm rupture during germination: a comparative approach using Lepidium sativum and Arabidopsis thaliana. Plant Cell 21, 38033822.CrossRefGoogle ScholarPubMed
Linkies, A, Graeber, K, Knight, Ch and Leubner-Metzger, G (2010) The evolution of seeds. New Phytologist 186, 817831.CrossRefGoogle ScholarPubMed
Liu, X, Zhang, H, Zhao, Y, Feng, Z, Li, Q, Yang, HQ, Luan, S, Li, J and He, ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceeding National Academic Sciences of the USA 110, 1548515490.CrossRefGoogle ScholarPubMed
Locascio, A, Roig-Villanova, I, Bernardi, J and Varotto, S (2014) Current perspectives on the hormonal control of seed development in Arabidopsis and maize: a focus on auxin. Frontiers in Plant Sciences 5, 412.Google ScholarPubMed
Lora, J, Hormaza, JI, Herrero, M and Gasser, CS (2011) Seedless fruits and the disruption of a conserved genetic pathway in angiosperm ovule development. Proceedings of the National Academy of Sciences of the USA 108, 54615465.CrossRefGoogle ScholarPubMed
Lora, J, Hormaza, JI and Herrero, M (2015) Transition from two to one integument in Prunus species: expression pattern of INNER NO OUTER (INO), ABERRANT TESTA SHAPE (ATS) and ETTIN (ETT). New Phytologist 208, 584595.CrossRefGoogle Scholar
Lu, J and Magnani, E (2018) Seed tissue and nutrient partitioning, a case for the nucellus. Plant Reproduction 31, 309317.CrossRefGoogle ScholarPubMed
Luo, M, Dennis, ES, Berger, F, Peacock, WJ and Chaudhury, A (2005) MINNISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. Proceedings of the National Academic Sciences of the USA 102, 1753117536.CrossRefGoogle Scholar
Luo, M, Platten, D, Chaudhury, A, Peacock, WJ and Dennis, ES (2009) Expression, imprinting, and evolution of rice homologs of the Polycomb Group genes. Molecular Plant 2, 711723.CrossRefGoogle ScholarPubMed
Ma, X, Guo, J, Han, X and Yang, G (2015) Grevillea (Proteaceae) seed coats contain inhibitors for seed germination. Australian Journal of Botany 63, 566571.CrossRefGoogle Scholar
Matilla, AJ (2019) Programmed cell death in seeds: an adaptive mechanism required for life. doi: 10.5772/intchopen.86833CrossRefGoogle Scholar
McAbee, JM, Kuzoff, RK, Charles, S and Gasser, CG (2005) Mechanisms of derived unitegmy among Impatiens species. Plant Cell 17, 16741684.CrossRefGoogle ScholarPubMed
McAbee, JM, Hill, TA, Skinner, DJ, Izhaki, A, Hauser, BA, Meister, RJ, Venugopala Reddy, G, Meyerowitz, EM, Bowman, JL and Gasser, CS (2006) ABERRANT TESTA SHAPE encodes a KANADI family member, linking polarity determination to separation and growth of Arabidopsis ovule integuments. Plant Journal 46, 522531.CrossRefGoogle ScholarPubMed
Mizzotti, C, Mendes, MA, Caporali, E, Schnittger, A, Kater, MM, Battaglia, R and Colombo, L (2012) The MADs box genes SEEDSTICK and ARABIDOPSIS Bsister play a maternal role in fertilization and seed development. Plant Journal 70, 409420.CrossRefGoogle ScholarPubMed
Mizzotti, C, Ezquer, I, Paolo, D, Rueda-Romero, P, Guerra, RF, Battaglia, R, Rogachev, I, Aharoni, A, Kater, MM, Caporali, E and Colombo, L (2014) SEEDSTICK is a master regulator of development and metabolism in the Arabidopsis seed coat. PLOS Genetics 10, e1004856.CrossRefGoogle ScholarPubMed
Nonogaki, H (2019) ABA responses during seed development and germination, in Marion-Poll, A and Seo, M (eds), Abscisic Acid in Plants. Advances in Botanical Research Vol. 92. New York, USA: Academic Press.Google Scholar
Obroucheva, NV (2013) Aquaporins in seeds. Seed Science Research 23, 213216.CrossRefGoogle Scholar
Olsen, OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16, S214S227.CrossRefGoogle ScholarPubMed
Orozco-Arroyo, G, Paolo, D, Ezquer, I and Colombo, L (2015) Networks controlling seed size in Arabidopsis. Plant Reproduction 28, 1732.CrossRefGoogle ScholarPubMed
Pagnussat, GC, Alandete-Saez, M, Bowman, JL and Sundaresan, V (2009) Auxin-dependent patterning and gamete specification in the Arabidopsis female gametophyte. Science 324, 16841689.CrossRefGoogle ScholarPubMed
Panoli, A, Martin, MV, Alandete-Saez, M, Simon, M, Neff, C, Swarup, R, Bellido, A, Yuan, L, Pagnussat, GC and Sundaresan, V (2015) Auxin import and local auxin biosynthesis are required for mitotic divisions, cell expansion and cell specification during female gametophyte development in Arabidopsis thaliana. PLoS One 10, e0126164.CrossRefGoogle ScholarPubMed
Patrick, JW and Offler, Ch.E (2001) Compartmentation of transport and transfer events in developing seeds. Journal of Experimental Botany 52, 551564.CrossRefGoogle ScholarPubMed
Radchuk, V and Borisjuk, L (2014) Physical, metabolic and developmental functions of SC. Frontiers of Plant Science 5, 510.CrossRefGoogle Scholar
Reinheimer, R and Kellogg, EA (2009) Evolution of AGL6-like MADS box genes in grasses (Poaceae): ovule expression is ancient and palea expression is new. Plant Cell 21, 25912605.CrossRefGoogle Scholar
Robert, HS, Park, Ch, Gutièrrez, CL, Wójcikowska, B, Pěnčík, A, Ondřej Novák, O, Junyi Chen, J, Grunewald, W, Dresselhaus, T, Friml, J and Laux, T (2018) Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nature Plants 4, 548553.CrossRefGoogle ScholarPubMed
Robert, HS (2019) Molecular communication for coordinated seed and fruit development: what can we learn from auxin and sugars? International Journal of Molecular Sciences 20, 939.CrossRefGoogle ScholarPubMed
Rodríguez-Gacio, MC, Iglesias-Fernández, R, Carbonero, P and Matilla, AJ (2012) Softening-up mannan-rich cell walls. Journal of Experimental Botany 63, 39763988.CrossRefGoogle Scholar
Roszak, P and Köhler, C (2011) Polycomb group proteins are required to couple SC initiation to fertilization. Proceedings of the National Academy of Sciences of the USA 108, 2082620831.CrossRefGoogle Scholar
Sánchez-Montesino, R, Bouza-Morcillo, L, Márquez, J, Ghita, M, Durán-Nebreda, S, Gómez, L, Holdsworth, MJ, Bassel, G and Oñate-Sánchez, L (2019) A regulatory module controlling GA- mediated endosperm cell expansion is critical for seed germination in Arabidopsis. Molecular Plant 12, 7185.CrossRefGoogle ScholarPubMed
Schon, MA and Nodine, MD (2017) Widespread contamination of Arabidopsis embryo and endosperm transcriptome data sets. Plant Cell 29, 608617.CrossRefGoogle ScholarPubMed
Schruff, MC, Spielman, M, Tiwari, S, Adams, S, Fenby, N and Scott, RJ (2006) The AUXIN RESPONSE FACTOR 2 gene of Arabidopsis links auxin signaling, cell division, and the size of seeds and other organs. Development 133, 251261.CrossRefGoogle ScholarPubMed
Shah, FA, Ni, J, Chen, J, Wang, Q, Liu, W, Chen, X, Tang, C, Fu, S and Wu, L (2018) Proanthocyanidins in seed coat tegmen and endospermic cap inhibit seed germination in Sapium sebiferum. PeerJ 6, e4690.CrossRefGoogle ScholarPubMed
Sieber, P, Gheyselinck, J, Gross-Hardt, R, Laux, T, Grossniklaus, U and Schneitz, K (2004) Pattern formation during early ovule development in Arabidopsis thaliana. Developmental Biology 273, 321334.CrossRefGoogle ScholarPubMed
Simon, MK, Skinner, DK, Gallagher, TL and Gasser, CS (2017) Integument development in Arabidopsis depends on interaction of YABBY protein INNER NO OUTER with co-activators and co-repressors. Genetics 207, 14891500.Google Scholar
Simonini, S, Deb, J, Moubayidin, L, Stephenson, P, Valluru, M, Freire-Rios, A, Sorefan, K, Weijers, D, Friml, J and Østergaard, L (2016) A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis. Genes and Development 30, 22862296.CrossRefGoogle ScholarPubMed
Skinner, DJ, Brown, RH, Kuzoff, RK and Gasser, CS (2016) Conservation of the role of INNER NO OUTER in development of unitegmic ovules of the Solanaceae despite a divergence in protein function. BMC Plant Biology 16, 143.CrossRefGoogle ScholarPubMed
Skinner, DJ, Hill, TA and Gasser, CS (2004) Regulation of ovule development. The Plant Cell 16, S32S45.CrossRefGoogle ScholarPubMed
Smÿkal, P, Vernoud, V, Blair, MW, Soukup, A and Thompson, RD (2014) The role of the testa during development and in establishment of dormancy of the legume seed. Frontiers in Plant Science 5, 119.Google ScholarPubMed
Smit, ME and Weijers, D (2015) The role of auxin signaling in early embryo pattern formation. Current Opinion in Plant Biology 28, 99105.CrossRefGoogle ScholarPubMed
Souza-Caetano, AP, Basso-Alves, JP, Cortez, PA, Garcia De Brito, VL, Michelangeli, FA, Reginato, M, Goldenberg, R, Carmello-Guerreiro, SM and Pádua Teixeira, SP (2018) Evolution of the outer ovule integument and its systematic significance in Melastomataceae. Botanical Journal of the Linnean Society 186, 224246.CrossRefGoogle Scholar
Stadler, R, Lauterbach, C and Sauer, N (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 Physiology 139, 701712.CrossRefGoogle ScholarPubMed
Steinbrecher, T and Leubner-Metzger, G (2018) Tissue and cellular mechanisms of seeds. Current Opinion in Genetics and Development 51, 110.CrossRefGoogle ScholarPubMed
Sun, Y, Wang, C, Wang, N, Jiang, X, Mao, H, Zhu, C, Wen, F, Wang, X, Lu, Z, Yue, G, Xu, Z-F and Ye, J 2017. Manipulation of Auxin response factor 19 affects seed size in the woody perennial Jatropha curcas. Scientific Reports 7, 40844.CrossRefGoogle Scholar
Tobe, H, Jaffré, T and Raven, PH (2000) Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. Journal of Plant Research 113, 271280.CrossRefGoogle Scholar
Tonosaki, K and Kinoshita, T (2015) Possible roles for polycomb repressive complex 2 in cereal endosperm. Frontiers Plant Science 6, 144.CrossRefGoogle ScholarPubMed
Tsai, AY-L, Kunieda, T, Rogalski, J, Foster, , Ellis, LJ, Ellis, B and Haughn, GW (2017) Identification and characterization of Arabidopsis seed coat mucilage proteins 173, 10591074.CrossRefGoogle Scholar
Urbanova, T and Leubner-Metzger, G (2016) Gibberellins and seed germination, pp. 253284 in Hedden, P and Thomas, SG (eds), The Gibberellins. Annual Plant Reviews Vol. 49. New York, USA: Wiley Blackwell.CrossRefGoogle Scholar
Villanueva, JM, Broadhvest, J, Hauser, BA, Meister, RJ, Schneitz, K and Gasser, CS (1999) INNER NO OUTER regulates abaxial–adaxial patterning in Arabidopsis ovules. Genes and Development 13, 31603169.CrossRefGoogle ScholarPubMed
Vogiatzaki, E, Celia Baroux, C, Jung, J-Y and Poirier, Y (2017) PHO1 exports phosphate from the chalazal SC to the embryo in developing Arabidopsis seeds. Current Biology 27, 28932900.CrossRefGoogle Scholar
Weber, H, Borisjuk, L and Wobus, U (2005) Molecular physiology of legume seed development. Annual Review of Plant Biology 56, 253279.CrossRefGoogle ScholarPubMed
Weijers, D, van Hamburg, JP, van Rijn, E, Hooykaas, PJJ and Offringa, R (2003) Diphtheria toxin-mediated cell ablation reveals interregional communication during Arabidopsis seed development. Plant Physiology 133, 18821892.CrossRefGoogle ScholarPubMed
Western, TL (2012) The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal. Seed Science Research 22, 125.CrossRefGoogle Scholar
Wolff, P, Jiang, H, Wang, G, Santos-González, J and Köhler, C (2015) Paternally expressed imprinted genes establish post-zygotic hybridization barriers in Arabidopsis thaliana. eLife 4, e10074.CrossRefGoogle Scholar
Xu, W, Fiume, E, Coen, O, Pechoux, C, Lepiniec, L and Magnani, E (2016) Endosperm and nucellus develop antagonistically in Arabidopsis seeds. Plant Cell 28, 13431360.CrossRefGoogle ScholarPubMed
Yamada, T, Ito, M and Kato, M (2003) Expression pattern of INNER NO OUTER homologue in Nymphea (water lily family, Nympheaceae). Development Genes and Evolution 213, 510513.CrossRefGoogle Scholar
Yamada, T, Yokota, S, Hirayama, Y, Imaichi, R, Kato, M and Gasser, CS (2011) Ancestral expression patterns and evolutionary diversification of YABBY genes in angiosperms. Plant Journal 67, 2636.CrossRefGoogle ScholarPubMed
Yang, Y (2004) Ontogeny of triovulate cones of Ephedra intermedia and origin of the outer envelope of ovules of Ephedraceae. American Journal of Botany 91, 361368.CrossRefGoogle ScholarPubMed
Zhang, WH, Zhou, YC, Dibley, KE, Tyerman, SD, Furbank, RT and Patrick, JW (2007). Nutrient loading of developing seeds. Functional Plant Biology 34, 314331.CrossRefGoogle Scholar
Zhang, S, Wang, D, Zhang, H, Skaggs, MI, Lloyd, A, Ran, D, An, L, Schumaker, KS, Drews, GN and Yadegari, R (2018) FERTILIZATION-INDEPENDENT SEED-polycomb repressive complex-2 plays a dual role in regulating type I MADS-Box genes in early endosperm development. Plant Physiology 177, 285299.CrossRefGoogle Scholar