1932

Abstract

In angiosperms, double fertilization triggers the concomitant development of two closely juxtaposed tissues, the embryo and the endosperm. Successful seed development and germination require constant interactions between these tissues, which occur across their common interface. The embryo–endosperm interface is a complex and poorly understood compound apoplast comprising components derived from both tissues, across which nutrients transit to fuel embryo development. Interface properties, which affect molecular diffusion and thus communication, are themselves dynamically regulated by molecular and physical dialogues between the embryo and endosperm. We review the current understanding of embryo–endosperm interactions, with a focus on the structure, properties, and function of their shared interface. Concentrating on , but with reference to other species, we aim to situate recent findings within the broader context of seed physiology, developmental biology, and genetic factors such as parental conflicts over resource allocation.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-102820-091838
2022-05-20
2024-05-11
Loading full text...

Full text loading...

/deliver/fulltext/arplant/73/1/annurev-arplant-102820-091838.html?itemId=/content/journals/10.1146/annurev-arplant-102820-091838&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Aguirre M, Kiegle E, Leo G, Ezquer I 2018. Carbohydrate reserves and seed development: an overview. Plant Reprod 31:3263–90
    [Google Scholar]
  2. 2.
    Allorent G, Osorio S, Vu JL, Falconet D, Jouhet J et al. 2015. Adjustments of embryonic photosynthetic activity modulate seed fitness in Arabidopsis thaliana. New Phytol 205:2707–19
    [Google Scholar]
  3. 3.
    Babu Y, Musielak T, Henschen A, Bayer M. 2013. Suspensor length determines developmental progression of the embryo in Arabidopsis. Plant Physiol 162:31448–58
    [Google Scholar]
  4. 4.
    Barber KG. 1909. Comparative histology of fruits and seeds of certain species of Cucurbitaceae. Bot. Gaz. 47:4263–310
    [Google Scholar]
  5. 5.
    Baroux C, Spillane C, Grossniklaus U. 2002. Evolutionary origins of the endosperm in flowering plants. Genome Biol 3:9reviews1026.1
    [Google Scholar]
  6. 6.
    Batista RA, Figueiredo DD, Santos-González J, Köhler C. 2019. Auxin regulates endosperm cellularization in Arabidopsis. Genes Dev 33:7/8466–76
    [Google Scholar]
  7. 7.
    Baud S, Wuillème S, Lemoine R, Kronenberger J, Caboche M et al. 2005. The AtSUC5 sucrose transporter specifically expressed in the endosperm is involved in early seed development in Arabidopsis. Plant J 43:6824–36
    [Google Scholar]
  8. 8.
    Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W 2009. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323:59201485–88
    [Google Scholar]
  9. 9.
    Berhin A, de Bellis D, Franke RB, Buono RA, Nowack MK, Nawrath C. 2019. The root cap cuticle: a cell wall structure for seedling establishment and lateral root formation. Cell 176:61367–78.e8
    [Google Scholar]
  10. 10.
    Besnard J, Zhao C, Avice J-C, Vitha S, Hyodo A et al. 2018. Arabidopsis UMAMIT24 and 25 are amino acid exporters involved in seed loading. J. Exp. Bot. 69:215221–32
    [Google Scholar]
  11. 11.
    Bethke PC, Libourel IGL, Aoyama N, Chung Y-Y, Still DW, Jones RL. 2007. The Arabidopsis aleurone layer responds to nitric oxide, gibberellin, and abscisic acid and is sufficient and necessary for seed dormancy. Plant Physiol 143:31173–88
    [Google Scholar]
  12. 12.
    Bethke PC, Lonsdale JE, Fath A, Jones RJ 1999. Hormonally regulated programmed cell death in barley aleurone cells. Plant Cell 11:61033–46
    [Google Scholar]
  13. 13.
    Bewley JD. 1997. Seed germination and dormancy. Plant Cell 9:71055–66
    [Google Scholar]
  14. 14.
    Blanvillain R, Young B, Cai Y, Hecht V, Varoquaux F et al. 2011. The Arabidopsis peptide kiss of death is an inducer of programmed cell death. EMBO J 30:61173–83
    [Google Scholar]
  15. 15.
    Borisjuk L, Rolletschek H. 2009. The oxygen status of the developing seed. New Phytol 182:117–30
    [Google Scholar]
  16. 16.
    Borisjuk L, Rolletschek H, Wobus U, Weber H 2003. Differentiation of legume cotyledons as related to metabolic gradients and assimilate transport into seeds. J. Exp. Bot. 54:382503–12
    [Google Scholar]
  17. 17.
    Borisjuk L, Walenta S, Rolletschek H, Mueller-Klieser W, Wobus U, Weber H 2002. Spatial analysis of plant metabolism: Sucrose imaging within Vicia faba cotyledons reveals specific developmental patterns. Plant J 29:4521–30
    [Google Scholar]
  18. 18.
    Borisjuk L, Wang TL, Rolletschek H, Wobus U, Weber H 2002. A pea seed mutant affected in the differentiation of the embryonic epidermis is impaired in embryo growth and seed maturation. Development 129:71595–607
    [Google Scholar]
  19. 19.
    Briggs CL. 1993. Endosperm development in Solanum nigrum L. formation of the zone of separation and secretion. Ann. Bot. 72:4303–13
    [Google Scholar]
  20. 20.
    Briggs CL. 1996. An ultrastructural study of the embryo/endosperm interface in the developing seeds of Solanum nigrum L. zygote to mid torpedo stage. Ann. Bot. 78:3295–304
    [Google Scholar]
  21. 21.
    Brown RC, Lemmon BE, Nguyen H, Olsen O-A. 1999. Development of endosperm in Arabidopsis thaliana. Sex. Plant Reprod. 12:132–42
    [Google Scholar]
  22. 22.
    Cannon MC, Terneus K, Hall Q, Tan L, Wang Y et al. 2008. Self-assembly of the plant cell wall requires an extensin scaffold. PNAS 105:62226–31
    [Google Scholar]
  23. 23.
    Carrera-Castaño G, Calleja-Cabrera J, Pernas M, Gómez L, Oñate-Sánchez L. 2020. An updated overview on the regulation of seed germination. Plants 9:6703
    [Google Scholar]
  24. 24.
    Chahtane H, Kim W, Lopez-Molina L 2017. Primary seed dormancy: a temporally multilayered riddle waiting to be unlocked. J. Exp. Bot. 68:4857–69
    [Google Scholar]
  25. 25.
    Chen J, Lausser A, Dresselhaus T. 2014. Hormonal responses during early embryogenesis in maize. Biochem. Soc. Trans. 42:2325–31
    [Google Scholar]
  26. 26.
    Chen L-Q, Lin IW, Qu X-Q, Sosso D, McFarlane HE et al. 2015. A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. Plant Cell 27:3607–19
    [Google Scholar]
  27. 27.
    Chen M, Lin J-Y, Wu X, Apuya NR, Henry KF et al. 2021. Comparative analysis of embryo proper and suspensor transcriptomes in plant embryos with different morphologies. PNAS 118:6e2024704118
    [Google Scholar]
  28. 28.
    Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X et al. 2003. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes Dev 17:81043–54
    [Google Scholar]
  29. 29.
    Corona-Carrillo JI, Flores-Ponce M, Chávez-Nájera G, Díaz-Pontones DM 2014. Peroxidase activity in scutella of maize in association with anatomical changes during germination and grain storage. SpringerPlus 3:399
    [Google Scholar]
  30. 30.
    Costa LM, Marshall E, Tesfaye M, Silverstein KAT, Mori M et al. 2014. Central cell–derived peptides regulate early embryo patterning in flowering plants. Science 344:6180168–72
    [Google Scholar]
  31. 31.
    Creff A, Brocard L, Joubès J, Taconnat L, Doll NM et al. 2019. A stress-response-related inter-compartmental signalling pathway regulates embryonic cuticle integrity in Arabidopsis. PLOS Genet 15:4e1007847
    [Google Scholar]
  32. 32.
    Cubría-Radío M, Nowack MK. 2019. Transcriptional networks orchestrating programmed cell death during plant development. Curr. Top. Dev. Biol. 131:161–84
    [Google Scholar]
  33. 33.
    David LC, Berquin P, Kanno Y, Seo M, Daniel-Vedele F, Ferrario-Méry S. 2016. N availability modulates the role of NPF3.1, a gibberellin transporter, in GA-mediated phenotypes in Arabidopsis. Planta 244:61315–28
    [Google Scholar]
  34. 34.
    De Giorgi J, Fuchs C, Iwasaki M, Kim W, Piskurewicz U et al. 2021. The Arabidopsis mature endosperm promotes seedling cuticle formation via release of sulfated peptides. Dev. Cell 56:223066–81.e5
    [Google Scholar]
  35. 35.
    De Jong TJ, Van Dijk H, Klinkhamer PGL. 2005. Hamilton's rule, imprinting and parent-offspring conflict over seed mass in partially selfing plants. J. Evol. Biol. 18:3676–82
    [Google Scholar]
  36. 36.
    Dekkers BJW, Pearce S, van Bolderen-Veldkamp RP, Marshall A, Widera P et al. 2013. Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol 163:1205–15
    [Google Scholar]
  37. 37.
    Delude C, Moussu S, Joubès J, Ingram G, Domergue F. 2016. Plant surface lipids and epidermis development. Subcell. Biochem. 86:287–313
    [Google Scholar]
  38. 38.
    Denay G, Creff A, Moussu S, Wagnon P, Thévenin J et al. 2014. Endosperm breakdown in Arabidopsis requires heterodimers of the basic helix-loop-helix proteins ZHOUPI and INDUCER OF CBP EXPRESSION 1. Development 141:61222–27
    [Google Scholar]
  39. 39.
    Diboll AG. 1968. Fine structural development of the megagametophyte of Zea mays following fertilization. Am. J. Bot. 55:7797–806
    [Google Scholar]
  40. 40.
    Doblas VG, Smakowska-Luzan E, Fujita S, Alassimone J, Barberon M et al. 2017. Root diffusion barrier control by a vasculature-derived peptide binding to the SGN3 receptor. Science 355:6322280–84
    [Google Scholar]
  41. 41.
    Doll NM, Bovio S, Gaiti A, Marsollier A-C, Chamot S et al. 2020. The endosperm-derived embryo sheath is an anti-adhesive structure that facilitates cotyledon emergence during germination in Arabidopsis. Curr. Biol. 30:5909–15.e4
    [Google Scholar]
  42. 42.
    Doll NM, Depège-Fargeix N, Rogowsky PM, Widiez T. 2017. Signaling in early maize kernel development. Mol. Plant 10:3375–88
    [Google Scholar]
  43. 43.
    Doll NM, Just J, Brunaud V, Caïus J, Grimault A et al. 2020. Transcriptomics at maize embryo/endosperm interfaces identifies a transcriptionally distinct endosperm subdomain adjacent to the embryo scutellum. Plant Cell 32:4833–52
    [Google Scholar]
  44. 44.
    Doll NM, Royek S, Fujita S, Okuda S, Chamot S et al. 2020. A two-way molecular dialogue between embryo and endosperm is required for seed development. Science 367:6476431–35
    [Google Scholar]
  45. 45.
    Dou M, Zhang Y, Yang S, Feng X 2018. Identification of ZHOUPI orthologs in rice involved in endosperm development and cuticle formation. Front. Plant Sci. 9:00223
    [Google Scholar]
  46. 46.
    Dute RR, Peterson CM, Rushing AE. 1989. Ultrastructural changes of the egg apparatus associated with fertilization and proembryo development of soybean, Glycine max (Fabaceae). Ann. Bot. 64:2123–35
    [Google Scholar]
  47. 47.
    Dutta S, Bradford KJ, Nevins DJ. 1994. Cell-wall autohydrolysis in isolated endosperms of lettuce (Lactuca sativa L.). Plant Physiol 104:2623–28
    [Google Scholar]
  48. 48.
    Dutta S, Bradford KJ, Nevins DJ. 1997. Endo-β-mannanase activity present in cell wall extracts of lettuce endosperm prior to radicle emergence. Plant Physiol 113:1155–61
    [Google Scholar]
  49. 49.
    Erdmann RM, Hoffmann A, Walter H-K, Wagenknecht H-A, Groß-Hardt R, Gehring M. 2017. Molecular movement in the Arabidopsis thaliana female gametophyte. Plant Reprod 30:3141–46
    [Google Scholar]
  50. 50.
    Feng F, Qi W, Lv Y, Yan S, Xu L et al. 2018. OPAQUE11 is a central hub of the regulatory network for maize endosperm development and nutrient metabolism. Plant Cell 30:2375–96
    [Google Scholar]
  51. 51.
    Figueiredo DD, Batista RA, Roszak PJ, Hennig L, Köhler C 2016. Auxin production in the endosperm drives seed coat development in Arabidopsis. eLife 5:e20542
    [Google Scholar]
  52. 52.
    Figueiredo DD, Batista RA, Roszak PJ, Köhler C. 2015. Auxin production couples endosperm development to fertilization. Nat. Plants 1:15184
    [Google Scholar]
  53. 53.
    Figueiredo DD, Köhler C. 2018. Auxin: a molecular trigger of seed development. Genes Dev 32:7/8479–90
    [Google Scholar]
  54. 54.
    Finch-Savage WE, Leubner-Metzger G. 2006. Seed dormancy and the control of germination. New Phytol 171:3501–23
    [Google Scholar]
  55. 55.
    Fiume E, Guyon V, Remoué C, Magnani E, Miquel M et al. 2016. TWS1, a novel small protein, regulates various aspects of seed and plant development. Plant Physiol 172:31732–45
    [Google Scholar]
  56. 56.
    Forestan C, Meda S, Varotto S 2010. ZmPIN1-mediated auxin transport is related to cellular differentiation during maize embryogenesis and endosperm development. Plant Physiol 152:31373–90
    [Google Scholar]
  57. 57.
    Forestan C, Varotto S. 2012. The role of PIN auxin efflux carriers in polar auxin transport and accumulation and their effect on shaping maize development. Mol. Plant 5:4787–98
    [Google Scholar]
  58. 58.
    Fourquin C, Beauzamy L, Chamot S, Creff A, Goodrich J et al. 2016. Mechanical stress mediated by both endosperm softening and embryo growth underlies endosperm elimination in Arabidopsis seeds. Development 143:183300–5
    [Google Scholar]
  59. 59.
    Friedman WE, Ryerson KC. 2009. Reconstructing the ancestral female gametophyte of angiosperms: insights from Amborella and other ancient lineages of flowering plants. Am. J. Bot. 96:1129–43
    [Google Scholar]
  60. 60.
    Friml J, Vieten A, Sauer M, Weijers D, Schwarz H et al. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:6963147–53
    [Google Scholar]
  61. 61.
    Gao Z, Daneva A, Salanenka Y, Van Durme M, Huysmans M et al. 2018. KIRA1 and ORESARA1 terminate flower receptivity by promoting cell death in the stigma of Arabidopsis. Nat. Plants 4:6365–75
    [Google Scholar]
  62. 62.
    Garcia D, Fitz Gerald JN, 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 17:152–60
    [Google Scholar]
  63. 63.
    Gehring M, Satyaki PR. 2017. Endosperm and imprinting, inextricably linked. Plant Physiol 173:1143–54
    [Google Scholar]
  64. 64.
    Grimault A, Gendrot G, Chamot S, Widiez T, Rabillé H et al. 2015. ZmZHOUPI, an endosperm-specific basic helix-loop-helix transcription factor involved in maize seed development. Plant J 84:3574–86
    [Google Scholar]
  65. 65.
    Grossniklaus U, Spillane C, Page DR, Köhler C 2001. Genomic imprinting and seed development: endosperm formation with and without sex. Curr. Opin. Plant Biol. 4:121–27
    [Google Scholar]
  66. 66.
    Grossniklaus U, Vielle-Calzada JP, Hoeppner MA, Gagliano WB. 1998. Maternal control of embryogenesis by MEDEA, a Polycomb group gene in Arabidopsis. Science 280:5362446–50
    [Google Scholar]
  67. 67.
    Haig D, Westoby M. 1989. Parent-specific gene expression and the triploid endosperm. Am. Nat. 134:1147–55
    [Google Scholar]
  68. 68.
    Hammes UZ, Nielsen E, Honaas LA, Taylor CG, Schachtman DP. 2006. AtCAT6, a sink-tissue-localized transporter for essential amino acids in Arabidopsis. Plant J 48:3414–26
    [Google Scholar]
  69. 69.
    Han Y-Z, Huang B-Q, Zee S-Y, Yuan M. 2000. Symplastic communication between the central cell and the egg apparatus cells in the embryo sac of Torenia fournieri Lind. before and during fertilization. Planta 211:1158–62
    [Google Scholar]
  70. 70.
    Hauvermale AL, Steber CM. 2020. GA signaling is essential for the embryo-to-seedling transition during Arabidopsis seed germination, a ghost story. Plant Signal. Behav. 15:11705028
    [Google Scholar]
  71. 71.
    Hehenberger E, Kradolfer D, Köhler C. 2012. Endosperm cellularization defines an important developmental transition for embryo development. Development 139:112031–39
    [Google Scholar]
  72. 72.
    Hsieh T-F, Shin J, Uzawa R, Silva P, Cohen S et al. 2011. Regulation of imprinted gene expression in Arabidopsis endosperm. PNAS 108:51755–62
    [Google Scholar]
  73. 73.
    Huang B-Q, Russell SD. 1992. Female germ unit: organization, isolation, and function. Int. Rev. Cytol. 140:233–93
    [Google Scholar]
  74. 74.
    Ibarra CA, Feng X, Schoft VK, Hsieh T-F, Uzawa R et al. 2012. Active DNA demethylation in plant companion cells reinforces transposon methylation in gametes. Science 337:61001360–64
    [Google Scholar]
  75. 75.
    Iglesias-Fernández R, Barrero-Sicilia C, Carrillo-Barral N, Oñate-Sánchez L, Carbonero P. 2013. Arabidopsis thaliana bZIP44: a transcription factor affecting seed germination and expression of the mannanase-encoding gene AtMAN7. Plant J 74:5767–80
    [Google Scholar]
  76. 76.
    Iglesias-Fernández R, Rodríguez-Gacio MC, Barrero-Sicilia C, Carbonero P, Matilla A 2011. Three endo-β-mannanase genes expressed in the micropylar endosperm and in the radicle influence germination of Arabidopsis thaliana seeds. Planta 233:125–36
    [Google Scholar]
  77. 77.
    Ingensiep HW. 2004. The history of the plant embryo. Terminology and visualization from ancient until modern times. Hist. Philos. Life Sci. 26:3/4309–31
    [Google Scholar]
  78. 78.
    Ingram G, Nawrath C. 2017. The roles of the cuticle in plant development: organ adhesions and beyond. J. Exp. Bot. 68:195307–21
    [Google Scholar]
  79. 79.
    Iwasaki M, Penfield S, Lopez-Molina L. 2022. Parental and environmental control of seed dormancy in Arabidopsis thaliana. Annu. Rev. Plant Biol. 73:35578
    [Google Scholar]
  80. 80.
    Jane W-N. 1997. Ultrastructure of the maturing egg apparatus in Arundo formosana Hack. (Poaceae). Int. J. Plant Sci. 158:6713–26
    [Google Scholar]
  81. 81.
    Javelle M, Vernoud V, Rogowsky PM, Ingram GC. 2011. Epidermis: the formation and functions of a fundamental plant tissue. New Phytol 189:117–39
    [Google Scholar]
  82. 82.
    Johansson M, Walles B. 1993. Functional anatomy of the ovule in broad bean, Vicia faba L. II. Ultrastructural development up to early embryogenesis. Int. J. Plant Sci. 154:4535–49
    [Google Scholar]
  83. 83.
    Kanaoka MM, Pillitteri LJ, Fujii H, Yoshida Y, Bogenschutz NL et al. 2008. SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to Arabidopsis stomatal differentiation. Plant Cell 20:71775–85
    [Google Scholar]
  84. 84.
    Kang I-H, Steffen JG, Portereiko MF, Lloyd A, Drews GN 2008. The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20:3635–47
    [Google Scholar]
  85. 85.
    Kang J, Yim S, Choi H, Kim A, Lee KP et al. 2015. Abscisic acid transporters cooperate to control seed germination. Nat. Commun. 6:8113
    [Google Scholar]
  86. 86.
    Kanno Y, Oikawa T, Chiba Y, Ishimaru Y, Shimizu T et al. 2016. AtSWEET13 and AtSWEET14 regulate gibberellin-mediated physiological processes. Nat. Commun. 7:13245
    [Google Scholar]
  87. 87.
    Kawashima T, Goldberg RB. 2010. The suspensor: not just suspending the embryo. Trends Plant Sci 15:123–30
    [Google Scholar]
  88. 88.
    Kazaz S, Barthole G, Domergue F, Ettaki H, To A et al. 2020. Differential activation of partially redundant Δ9 stearoyl-ACP desaturase genes is critical for omega-9 monounsaturated fatty acid biosynthesis during seed development in Arabidopsis. Plant Cell 32:113613–37
    [Google Scholar]
  89. 89.
    Kiyosue T, Ohad N, Yadegari R, Hannon M, Dinneny J et al. 1999. Control of fertilization-independent endosperm development by the MEDEA Polycomb gene in Arabidopsis. PNAS 96:74186–91
    [Google Scholar]
  90. 90.
    Köhler C, Hennig L, Bouveret R, Gheyselinck J, Grossniklaus U, Gruissem W 2003. Arabidopsis MSI1 is a component of the MEA/FIE Polycomb group complex and required for seed development. EMBO J 22:184804–14
    [Google Scholar]
  91. 91.
    Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T et al. 2008. RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiol 147:41924–35
    [Google Scholar]
  92. 92.
    Kourmpetli S, Drea S. 2014. The fruit, the whole fruit, and everything about the fruit. J. Exp. Bot. 65:164491–503
    [Google Scholar]
  93. 93.
    Kozieradzka-Kiszkurno M, Majcher D, Brzezicka E, Rojek J, Wróbel-Marek J, Kurczyńska E. 2020. Development of embryo suspensors for five genera of Crassulaceae with special emphasis on plasmodesmata distribution and ultrastructure. Plants 9:3320
    [Google Scholar]
  94. 94.
    Kozieradzka-Kiszkurno M, Płachno BJ. 2012. Are there symplastic connections between the endosperm and embryo in some angiosperms? A lesson from the Crassulaceae family. Protoplasma 249:41081–89
    [Google Scholar]
  95. 95.
    Kozieradzka-Kiszkurno M, Płachno BJ, Bohdanowicz J. 2012. New data about the suspensor of succulent angiosperms: ultrastructure and cytochemical study of the embryo-suspensor of Sempervivum arachnoideum L. and Jovibarba sobolifera (Sims) Opiz. Protoplasma 249:3613–24
    [Google Scholar]
  96. 96.
    Kradolfer D, Hennig L, Köhler C. 2013. Increased maternal genome dosage bypasses the requirement of the FIS polycomb repressive complex 2 in Arabidopsis seed development. PLOS Genet 9:1e1003163
    [Google Scholar]
  97. 97.
    Kranz E, von Wiegen P, Lörz H. 1995. Early cytological events after induction of cell division in egg cells and zygote development following in vitro fertilization with angiosperm gametes. Plant J 8:19–23
    [Google Scholar]
  98. 98.
    La Rocca N, Manzotti PS, Cavaiuolo M, Barbante A, Dalla Vecchia F et al. 2015. The maize fused leaves1 (fdl1) gene controls organ separation in the embryo and seedling shoot and promotes coleoptile opening. J. Exp. Bot. 66:195753–67
    [Google Scholar]
  99. 99.
    Lafon-Placette C. 2020. Endosperm genome dosage, hybrid seed failure, and parental imprinting: sexual selection as an alternative to parental conflict. Am. J. Bot. 107:117–19
    [Google Scholar]
  100. 100.
    Lafon-Placette C, Köhler C. 2016. Endosperm-based postzygotic hybridization barriers: developmental mechanisms and evolutionary drivers. Mol. Ecol. 25:112620–29
    [Google Scholar]
  101. 101.
    Lamport DTA, Kieliszewski MJ, Chen Y, Cannon MC 2011. Role of the extensin superfamily in primary cell wall architecture. Plant Physiol 156:111–19
    [Google Scholar]
  102. 102.
    Lee B, Henderson DA, Zhu J-K. 2005. The Arabidopsis cold-responsive transcriptome and its regulation by ICE1. Plant Cell 17:113155–75
    [Google Scholar]
  103. 103.
    Lee KJD, Dekkers BJW, Steinbrecher T, Walsh CT, Bacic A et al. 2012. Distinct cell wall architectures in seed endosperms in representatives of the Brassicaceae and Solanaceae. Plant Physiol 160:31551–66
    [Google Scholar]
  104. 104.
    Lee KP, Piskurewicz U, Turecková V, Strnad M, Lopez-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. PNAS 107:4419108–13
    [Google Scholar]
  105. 105.
    Linkies A, Graeber K, Knight C, Leubner-Metzger G. 2010. The evolution of seeds. New Phytol 186:4817–31
    [Google Scholar]
  106. 106.
    Luo M, Bilodeau P, Dennis ES, Peacock WJ, Chaudhury A. 2000. Expression and parent-of-origin effects for FIS2, MEA, and FIE in the endosperm and embryo of developing Arabidopsis seeds. PNAS 97:1910637–42
    [Google Scholar]
  107. 107.
    Luo M, Dennis ES, Berger F, Peacock WJ, Chaudhury A. 2005. MINISEED3 (MINI3), a WRKY family gene, and HAIKU2 (IKU2), a leucine-rich repeat (LRR) KINASE gene, are regulators of seed size in Arabidopsis. PNAS 102:4817531–36
    [Google Scholar]
  108. 108.
    MacGregor DR, Zhang N, Iwasaki M, Chen M, Dave A et al. 2019. ICE1 and ZOU determine the depth of primary seed dormancy in Arabidopsis independently of their role in endosperm development. Plant J 98:2277–90
    [Google Scholar]
  109. 109.
    Maheshwari P. 1950. An Introduction to the Embryology of Angiosperms New York: McGraw-Hill
  110. 110.
    Malivert A, Hamant O, Ingram G. 2018. The contribution of mechanosensing to epidermal cell fate specification. Curr. Opin. Genet. Dev. 51:52–58
    [Google Scholar]
  111. 111.
    Mansfield SG, Briarty LG. 1991. Early embryogenesis in Arabidopsis thaliana. II. The developing embryo. Can. J. Bot. 69:3461–76
    [Google Scholar]
  112. 112.
    Marinos NG. 1970. Embryogenesis of the pea (Pisum sativum) I. The cytological environment of the developing embryo. Protoplasma 70:3261–79
    [Google Scholar]
  113. 113.
    Marsollier A-C, Ingram G. 2018. Getting physical: invasive growth events during plant development. Curr. Opin. Plant Biol. 46:8–17
    [Google Scholar]
  114. 114.
    Martínez-Andújar C, Pluskota WE, Bassel GW, Asahina M, Pupel P et al. 2012. Mechanisms of hormonal regulation of endosperm cap-specific gene expression in tomato seeds. Plant J 71:4575–86
    [Google Scholar]
  115. 115.
    Matilla AJ. 2019. Seed coat formation: its evolution and regulation. Seed Sci. Res. 29:4215–26
    [Google Scholar]
  116. 116.
    Miray R, Kazaz S, To A, Baud S. 2021. Molecular control of oil metabolism in the endosperm of seeds. Int. J. Mol. Sci. 22:41621
    [Google Scholar]
  117. 117.
    Mogensen HL, Suthar HK. 1979. Ultrastructure of the egg apparatus of Nicotiana tabacum (Solanaceae) before and after fertilization. Bot. Gaz. 140:2168–79
    [Google Scholar]
  118. 118.
    Morley-Smith ER, Pike MJ, Findlay K, Köckenberger W, Hill LM et al. 2008. The transport of sugars to developing embryos is not via the bulk endosperm in oilseed rape seeds. Plant Physiol 147:42121–30
    [Google Scholar]
  119. 119.
    Moussu S, Doll NM, Chamot S, Brocard L, Creff A et al. 2017. ZHOUPI and KERBEROS mediate embryo/endosperm separation by promoting the formation of an extracuticular sheath at the embryo surface. Plant Cell 29:71642–56
    [Google Scholar]
  120. 120.
    Moussu S, San-Bento R, Galletti R, Creff A, Farcot E, Ingram G 2013. Embryonic cuticle establishment: the great (apoplastic) divide. Plant Signal. Behav. 8:12e27491
    [Google Scholar]
  121. 121.
    Müller B, Fastner A, Karmann J, Mansch V, Hoffmann T et al. 2015. Amino acid export in developing Arabidopsis seeds depends on UmamiT facilitators. Curr. Biol. 25:233126–31
    [Google Scholar]
  122. 122.
    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 47:7864–77
    [Google Scholar]
  123. 123.
    Nakayama T, Shinohara H, Tanaka M, Baba K, Ogawa-Ohnishi M, Matsubayashi Y. 2017. A peptide hormone required for Casparian strip diffusion barrier formation in Arabidopsis roots. Science 355:6322284–86
    [Google Scholar]
  124. 124.
    Olsen O-A. 2004. Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:Suppl.S214–27
    [Google Scholar]
  125. 125.
    Opsahl-Ferstad HG, Le Deunff E, Dumas C, Rogowsky PM 1997. ZmEsr, a novel endosperm-specific gene expressed in a restricted region around the maize embryo. Plant J 12:1235–46
    [Google Scholar]
  126. 126.
    Otegui M, Staehelin LA. 2000. Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 12:6933–47
    [Google Scholar]
  127. 127.
    Penfield S, Rylott EL, Gilday AD, Graham S, Larson TR, Graham IA. 2004. Reserve mobilization in the Arabidopsis endosperm fuels hypocotyl elongation in the dark, is independent of abscisic acid, and requires PHOSPHOENOLPYRUVATE CARBOXYKINASE1. Plant Cell 16:102705–18
    [Google Scholar]
  128. 128.
    Pommerrenig B, Popko J, Heilmann M, Schulmeister S, Dietel K et al. 2013. SUCROSE TRANSPORTER 5 supplies Arabidopsis embryos with biotin and affects triacylglycerol accumulation. Plant J 73:3392–404
    [Google Scholar]
  129. 129.
    Povilus RA, Diggle PK, Friedman WE. 2018. Evidence for parent-of-origin effects and interparental conflict in seeds of an ancient flowering plant lineage. Proc. Biol. Sci. 285:187220172491
    [Google Scholar]
  130. 130.
    Raghavan V. 2003. Some reflections on double fertilization, from its discovery to the present. New Phytol 159:3565–83
    [Google Scholar]
  131. 131.
    Robert HS, Park C, Guitérrez CL, Wójcikowska B, Pěnčík A et al. 2018. Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants 4:8548–53
    [Google Scholar]
  132. 132.
    Rolletschek H, Weber H, 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 132:31196–206
    [Google Scholar]
  133. 133.
    Russell S. 1993. The egg cell: development and role in fertilization and early embryogenesis. Plant Cell 5:101349–59
    [Google Scholar]
  134. 134.
    Sabelli PA. 2012. Replicate and die for your own good: endoreduplication and cell death in the cereal endosperm. J. Cereal Sci. 56:19–20
    [Google Scholar]
  135. 135.
    San-Bento R, Farcot E, Galletti R, Creff A, Ingram G 2014. Epidermal identity is maintained by cell-cell communication via a universally active feedback loop in Arabidopsis thaliana. Plant J 77:146–58
    [Google Scholar]
  136. 136.
    Sánchez-Montesino R, Bouza-Morcillo L, Marquez J, Ghita M, Duran-Nebreda S et al. 2019. A regulatory module controlling GA-mediated endosperm cell expansion is critical for seed germination in Arabidopsis. Mol. Plant 12:171–85
    [Google Scholar]
  137. 137.
    Sangduen N, Kreitner GL, Sorensen EL. 1983. Light and electron microscopy of embryo development in perennial and annual Medicago species. Can. J. Bot. 61:3837–49
    [Google Scholar]
  138. 138.
    Satyaki PRV, Gehring M. 2019. Paternally acting canonical RNA-directed DNA methylation pathway genes sensitize Arabidopsis endosperm to paternal genome dosage. Plant Cell 31:71563–78
    [Google Scholar]
  139. 139.
    Schel JHN, van Lammeren AAM, Kieft H. 1985. Ultrastructural analysis of embryo-endosperm interactions in developing maize seeds (Zea mays L.). Proceedings of the 8th International Symposium on Sexual Reproduction in Seed Plants, Ferns and Mosses MTM Willemse, JL van Went 171 Wageningen, Neth: Pudoc
    [Google Scholar]
  140. 140.
    Scheler C, Weitbrecht K, Pearce SP, Hampstead A, Büttner-Mainik A et al. 2015. Promotion of testa rupture during garden cress germination involves seed compartment–specific expression and activity of pectin methylesterases. Plant Physiol 167:1200–15
    [Google Scholar]
  141. 141.
    Schmid M, Simpson D, Gietl C. 1999. Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. PNAS 96:2414159–64
    [Google Scholar]
  142. 142.
    Schulz P, Jensen WA. 1971. Capsella embryogenesis: the chalazal proliferating tissue. J. Cell Sci. 8:1201–27
    [Google Scholar]
  143. 143.
    Sechet J, Frey A, Effroy-Cuzzi D, Berger A, Perreau F et al. 2016. Xyloglucan metabolism differentially impacts the cell wall characteristics of the endosperm and embryo during Arabidopsis seed germination. Plant Physiol 170:31367–80
    [Google Scholar]
  144. 144.
    Sela A, Piskurewicz U, Megies C, Mène-Saffrané L, Finazzi G, Lopez-Molina L. 2020. Embryonic photosynthesis affects post-germination plant growth. Plant Physiol 182:42166–81
    [Google Scholar]
  145. 145.
    Shigeyama T, Watanabe A, Tokuchi K, Toh S, Sakurai N et al. 2016. α-Xylosidase plays essential roles in xyloglucan remodelling, maintenance of cell wall integrity, and seed germination in Arabidopsis thaliana. J. Exp. Bot. 67:195615–29
    [Google Scholar]
  146. 146.
    Sørensen MB, Mayer U, Lukowitz W, Robert H, Chambrier P et al. 2002. Cellularisation in the endosperm of Arabidopsis thaliana is coupled to mitosis and shares multiple components with cytokinesis. Development 129:245567–76
    [Google Scholar]
  147. 147.
    Stadler R, Lauterbach C, 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 Physiol 139:2701–12
    [Google Scholar]
  148. 148.
    Steffen JG, Kang I-H, Portereiko MF, Lloyd A, Drews GN 2008. AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol 148:1259–68
    [Google Scholar]
  149. 149.
    Steinbrecher T, Leubner-Metzger G. 2017. The biomechanics of seed germination. J. Exp. Bot. 68:4765–83
    [Google Scholar]
  150. 150.
    Stępiński D, Kwiatkowska M, Wojtczak A, Domínguez E, Heredia A, Popłońska K. 2017. Cutinsomes as building-blocks of Arabidopsis thaliana embryo cuticle. Physiol. Plant. 161:4560–67
    [Google Scholar]
  151. 151.
    Szczuka E, Szczuka A. 2003. Cuticle fluorescence during embryogenesis of Arabidopsisthaliana [L.] Heynh. Acta Biol. Cracov. Ser. Bot. 45:163–67
    [Google Scholar]
  152. 152.
    Tal I, Zhang Y, Jørgensen ME, Pisanty O, Barbosa ICR et al. 2016. The Arabidopsis NPF3 protein is a GA transporter. Nat. Commun. 7:11486
    [Google Scholar]
  153. 153.
    Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M et al. 2001. A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development 128:234681–89
    [Google Scholar]
  154. 154.
    Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T et al. 2007. Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development 134:91643–52
    [Google Scholar]
  155. 155.
    Tegeder M, Masclaux-Daubresse C. 2018. Source and sink mechanisms of nitrogen transport and use. New Phytol 217:135–53
    [Google Scholar]
  156. 156.
    Tegeder M, Offler CE, Frommer WB, Patrick JW. 2000. Amino acid transporters are localized to transfer cells of developing pea seeds. Plant Physiol 122:2319–26
    [Google Scholar]
  157. 157.
    Tekleyohans DG, Mao Y, Kägi C, Stierhof Y-D, Groß-Hardt R. 2017. Polyspermy barriers: a plant perspective. Curr. Opin. Plant Biol. 35:131–37
    [Google Scholar]
  158. 158.
    Troncoso-Ponce MA, Barthole G, Tremblais G, To A, Miquel M et al. 2016. Transcriptional activation of two Δ9 palmitoyl-ACP desaturase genes by MYB115 and MYB118 is critical for biosynthesis of Ω7 monounsaturated fatty acids in the endosperm of Arabidopsis seeds. Plant Cell 28:102666–82
    [Google Scholar]
  159. 159.
    Tsuwamoto R, Fukuoka H, Takahata Y. 2008. GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J 54:130–42
    [Google Scholar]
  160. 160.
    Ueda M, Aichinger E, Gong W, Groot E, Verstraeten I et al. 2017. Transcriptional integration of paternal and maternal factors in the Arabidopsis zygote. Genes Dev 31:6617–27
    [Google Scholar]
  161. 161.
    van Lammeren AAM. 1987. Embryogenesis in Zea mays L.: a structural approach to maize caryopsis development in vivo and in vitro PhD Thesis, Wageningen Univ. Wageningen, Neth:.
    [Google Scholar]
  162. 162.
    Vaughan JG, Whitehouse JM. 1971. Seed structure and the taxonomy of the Cruciferae. Bot. J. Linn. Soc. 64:4383–409
    [Google Scholar]
  163. 163.
    Völz R, von Lyncker L, Baumann N, Dresselhaus T, Sprunck S, Groß-Hardt R. 2012. LACHESIS-dependent egg-cell signaling regulates the development of female gametophytic cells. Development 139:3498–502
    [Google Scholar]
  164. 164.
    Wang A, Garcia D, Zhang H, Feng K, Chaudhury A et al. 2010. The VQ motif protein IKU1 regulates endosperm growth and seed size in Arabidopsis. Plant J 63:4670–79
    [Google Scholar]
  165. 165.
    Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y. 2004. The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J 39:3298–308
    [Google Scholar]
  166. 166.
    Waters A, Creff A, Goodrich J, Ingram G. 2013.. “ What we've got here is failure to communicate”: zou mutants and endosperm cell death in seed development. Plant Signal. Behav. 8:6e24368
    [Google Scholar]
  167. 167.
    Weber H, Borisjuk L, Heim U, Sauer N, Wobus U. 1997. A role for sugar transporters during seed development: molecular characterization of a hexose and a sucrose carrier in fava bean seeds. Plant Cell 9:6895–908
    [Google Scholar]
  168. 168.
    Williams EG, Knox RB, Kaul V, Rouse JL 1984. Post-pollination callose development in ovules of Rhododendron and Ledum (Ericaceae): zygote special wall. J. Cell Sci. 69:127–35
    [Google Scholar]
  169. 169.
    Wróbel-Marek J, Kurczyńska E, Płachno BJ, Kozieradzka-Kiszkurno M. 2017. Identification of symplasmic domains in the embryo and seed of Sedum acre L. (Crassulaceae). Planta 245:3491–505
    [Google Scholar]
  170. 170.
    Wu J-J, Peng X-B, Li W-W, He R, Xin H-P, Sun M-X. 2012. Mitochondrial GCD1 dysfunction reveals reciprocal cell-to-cell signaling during the maturation of Arabidopsis female gametes. Dev. Cell 23:51043–58
    [Google Scholar]
  171. 171.
    Xing Q, Creff A, Waters A, Tanaka H, Goodrich J, Ingram GC. 2013. ZHOUPI controls embryonic cuticle formation via a signalling pathway involving the subtilisin protease ABNORMAL LEAF-SHAPE1 and the receptor kinases GASSHO1 and GASSHO2. Development 140:4770–79
    [Google Scholar]
  172. 172.
    Xiong H, Wang W, Sun M-X 2021. Endosperm development is an autonomously programmed process independent of embryogenesis. Plant Cell 33:41151–60
    [Google Scholar]
  173. 173.
    Xu X, E Z, Zhang D, Yun Q, Zhou Y et al. 2021. OsYUC11-mediated auxin biosynthesis is essential for endosperm development of rice. Plant Physiol 185:3934–50
    [Google Scholar]
  174. 174.
    Yamauchi Y, Ogawa M, Kuwahara A, Hanada A, Kamiya Y, Yamaguchi S. 2004. Activation of gibberellin biosynthesis and response pathways by low temperature during imbibition of Arabidopsis thaliana seeds. Plant Cell 16:2367–78
    [Google Scholar]
  175. 175.
    Yan A, Wu M, Yan L, Hu R, Ali I, Gan Y 2014. AtEXP2 is involved in seed germination and abiotic stress response in Arabidopsis. PLOS ONE 9:1e85208
    [Google Scholar]
  176. 176.
    Yan D, Duermeyer L, Leoveanu C, Nambara E. 2014. The functions of the endosperm during seed germination. Plant Cell Physiol 55:91521–33
    [Google Scholar]
  177. 177.
    Yang S, Johnston N, Talideh E, Mitchell S, Jeffree C et al. 2008. The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development. Development 135:213501–9
    [Google Scholar]
  178. 178.
    Yeats TH, Rose JKC. 2013. The formation and function of plant cuticles. Plant Physiol 163:15–20
    [Google Scholar]
  179. 179.
    Yeung EC. 1980. Embryogeny of Phaseolus: the role of the suspensor. Z. Pflanzenphysiol. 96:117–28
    [Google Scholar]
  180. 180.
    Yeung EC, Meinke D. 1993. Embryogenesis in angiosperms: development of the suspensor. Plant Cell 5:101371–81
    [Google Scholar]
  181. 181.
    Zang J, Huo Y, Liu J, Zhang H, Liu J, Chen H. 2020. Maize YSL2 is required for iron distribution and development in kernels. J. Exp. Bot. 71:195896–910
    [Google Scholar]
  182. 182.
    Zhang Y, Chen B, Xu Z, Shi Z, Chen S et al. 2014. Involvement of reactive oxygen species in endosperm cap weakening and embryo elongation growth during lettuce seed germination. J. Exp. Bot. 65:123189–200
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-102820-091838
Loading
/content/journals/10.1146/annurev-arplant-102820-091838
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error