Completing the cycle: Maternal effects as the missing link in plant life histories

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 364, Issue 1520, 2009, Pages 1059-1074

  Donohue, Kathleen ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Demography; Flowering time; Germination; Life cycle; Phenology; Phytochrome

Indexed keywords

DEMOGRAPHY; ENVIRONMENTAL IMPACT; FLOWERING; GENE EXPRESSION; GENETIC VARIATION; GERMINATION; GROWTH RATE; LIFE CYCLE; LIFE HISTORY TRAIT; MATERNAL EFFECT; NATURAL SELECTION; PHENOLOGY; POPULATION GROWTH; PROTEIN;

ANIMAL; ARABIDOPSIS; ENVIRONMENT; FEMALE; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; LIFE CYCLE; MATERNAL BEHAVIOR; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; PLANT SEED; REPRODUCTION; REVIEW; SEASON;

ANIMALS; ARABIDOPSIS; ENVIRONMENT; FEMALE; GERMINATION; LIFE CYCLE STAGES; MATERNAL BEHAVIOR; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; REPRODUCTION; SEASONS; SEEDS;

EID: 65649145495     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2008.0291     Document Type: Article

References (119)

1. Alboresi, A., Gestin, C., Leydecker, M. T., Bedu, M., Meyer, C. & Truong, H. N. 2005 Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ. 28, 500-512. (doi:10.1111/j.1365-3040.2005.01292. x)
2. Ali-Rachedi, A., Bouinot, D., Wagner, M.-H., Bonnet, M., Sotta, B., Grappin, P. & Jullien, M. 2004 Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana. Planta 219, 479-488. (doi:10.1007/s00425-004-1251-4)
3. Almoguera, C. & Jordano, J. 1992 Developmental and environmental concurrent expression of sunflower dry-seed-stored low-molecular-weight heat-shock protein and Lea mRNAs. Plant Mol. Biol. 19, 781-792. (doi:10.1007/BF00027074)
4. Alonso-Blanco, C., Bentsink, L., Hanhart, C. J., Blankestijn-de Vries, H. & Koornneef, M. 2003 Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164, 711-729.
5. Bailly, C. 2004 Active oxygen species and antioxidants in seed biology. Seed Sci. Res. 14, 93-107. (doi:10.1079/SSR2004159)
6. Baskin, J. M. & Baskin, C. C. 1972 Ecological life cycle and physiological ecology of seed germination of Arabidopsis thaliana. Can. J. Bot. 50, 353-360. (doi:10.1139/b72-049)
7. Baskin, J. M. & Baskin, C. C. 1983 Seasonal changes in the germination responses of buried seeds of Arabidopsis thaliana and ecological interpretation. Bot. Gaz. 144, 540-543. (doi:10.1086/337408)
8. Baskin, C. C. & Baskin, J. M. 1998 Seeds: ecology, biogeography and evolution of dormancy and germination. San Diego, CA: Academic Press.
9. Bentsink, L., Jowett, J., Hanhart, C. J. & Koornneef, M. 2006 Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc. Natl Acad. Sci. USA 105, 17 042-17 047. (doi:10.1073/pnas.0607877103)
10. Bewley, J. D. 1997a Breaking down the walls - a role for endo-b-mannanase in release from seed dormancy? Trends Plant Sci. 2, 464-469. (doi:10.1016/S1360-1385(97)01147-3)
11. Bewley, J. D. 1997b Seed germination and dormancy. Plant Cell 9, 1055-1066. (doi:10.1105/tpc.9.7.1055)
12. Biere, A. 1991 Parental effects in Lychnis flos cuculi: I. Seed size, germination and seedling performance in a controlled environment. J. Evol. Biol. 4, 447-465. (doi:10.1046/j.1420-9101.1991.4030447.x)
13. Botto, J. R., Sanchez, R. A. & Casal, J. J. 1995 Role of phytochrome B in the induction of seed germination by light in Arabidopsis thaliana. J. Plant Physiol. 146, 307-312.
14. Bouwmeester, H. J. & Karssen, C. M. 1993 Annual changes in dormancy and germination in seeds of Sisymbrium officinale (L.) Scop. New Phytol. 124, 179-191. (doi:10. 1111/j.1469-8137.1993.tb03808.x)
15. Bove, J., Lucas, P., Godin, B., Oge, L., Jullien, M. & Grappin, P. 2005 Gene expression analysis by cDNA-AFLP highlights a set of new signalling networks and translational control during seed dormancy breaking in Nicotiana plumbaginifolia. Plant Mol. Biol. 57, 593-612. (doi:10. 1007/s 11103-005-0953-8)
16. Boyd, E. W., Dorn, L. A., Weinig, C. & Schmitt, J. 2007 Maternal effects and germination timing mediate the expression of winter and spring annual life histories in Arabidopsis thaliana. Int. J. Plant Sci. 168, 205-214. (doi:10.1086/509587)
17. Brandes, D. & Schrei, J. 1997 Population biology and ecology of Berteroa incana (L.) DC. Braunschweiger Naturkundliche Schriften 5, 441-466.
18. Brown, J. S. & Venable, D. L. 1986 Evolutionary ecology of seed-bank annuals in temporally varying environments. Am. Nat. 127, 31-47. (doi:10.1086/284465)
19. Cadman, C. S., Toorop, P. E., Hilhorst, H. W. M. & Finch-Savage, W E. 2006 Gene expression profiles of Arabidopsis Cvi seeds during cycling through dormant and non-dormant states indicate a common underlying dormancy control mechanism. Plant J. 46, 805-822. (doi:10.1111/j. 1365-313X.2006.02738.X)
20. Carrera, E., Holman, T., Medhurst, A., Dietrich, D., Footitt, S., Theodoulou, F. L. & Holdsworth, M. J. 2008 Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J. 53, 214-224. (doi:10.1111/j.1365-313X.2007.03331.x)
21. Casal, J. J. & Sanchez, R. A. 1998 Phytochromes and seed germination. Seed Sci. Res. 8, 317-329. (doi:10.1017/S0960258500004256)
22. Caswell, H. 2001 Matrix population models: construction, analysis, and interpretation. Sunderland, MA: Sinauer Associates, Inc.
23. Chibani, K., Ali-Rachedi, S., Job, C., Job, D., Jullien, M. & Grappin, P. 2006 Proteomic analysis of seed dormancy in Arabidopsis. Plant Physiol. 142, 1493-1510. (doi:10.1104/pp. 106.087452)
24. Chouard, P. 1960 Vernalization and its relations to dormancy. Annu. Rev. Plant Physiol. 11, 191-237. (doi:10.1146/annurev.pp.11.060160. 001203)
25. Clack, T., Mathews, S. & Sharrock, R. 1994 The phytochrome apoprotein family in Arabidopsis is encoded by five genes: the sequences and expression of PHYD and PHYE. Plant Mol. Biol. 25, 413-427. (doi:10.1007/BF00043870)
26. Coupland, G. 1995 Genetic and environmental control of flowering time in Arabidopsis. Trends Genet. 11, 393-397. (doi:10.1016/S0168- 9525(00)89122-2)
27. Debeaujon, I. & Koornneef, M. 2000 Gibberellin requirement for Arabidopsis seed germination is determined both by test characteristics and embryonic abscisic acid. Plant Physiol. 122, 415-424. (doi:10.1104/pp.122.2.415)
28. Debeaujon, I., Leon-Kloosterzeil, K. M. & 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)
29. Debeaujon, I., Lepiniec, L., Pourcel, L. & Routaboul, J.-M. 2007 Seed coat development and dormancy. In Seed development, dormancy, and germination (eds K. J. Bradford & H. Nonagaki), pp. 25-49. Oxford, UK: Blackwell.
30. Dobrovolna, J. & Cetl, I. 1966 An increase of germination of dormant seeds by pricking. Arabidopsis Information Service 3, 33.
31. Donohue, K. 2005 Niche construction through phenological plasticity: life history dynamics and ecological consequences. New Phytol. 166, 83-92. (doi:10.1111/j.1469-8137.2005.01357.x)
32. Donohue, K. & Schmitt, J. 1998 Maternal environmental effects: adaptive plasticity? In Maternal effects as adaptations (eds T. A. Mousseau & C. W. Fox), pp. 137-158. Oxford, UK: Oxford University Press.
33. Donohue, K., Dorn, L. A., Griffith, C., Schmitt, J., Kim, E.-S. & Aguilera, A. 2005a Environmental and genetic influences on the germination of Arabidopsis thaliana in the field. Evolution 59, 740-757. (doi:10.1554/04-419)
34. Donohue, K., Dorn, L. A., Griffith, C., Schmitt, J., Kim, E.-S. & Aguilera, A. 2005b The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59, 758-770. (doi:10.1554/04-418)
35. Donohue, K., Heschel, M. S., Chiang, G. C. K., Butler, C. M. & Barua, D. 2007 Phytochrome mediates germination responses to multiple seasonal cues. Plant Cell Environ. 30, 202-212. (doi:10.1111/j.1365-3040.2006. 01619.x)
36. Donohue, K., Heschel, M. S., Butler, C. M., Barua, D., Sharrock, R. A., Whitelam, G. C. & Chiang, G. C. K.
37. 2008Diversification of phytochrome contributions to germination as a function of maternal environment. New Phytol. 177, 367-379.
38. Dubreucq, B., Berger, N., Vincent, E., Boisson, M., Pelletier, G., Caboche, M. & Lepiniec, L. 2003 The Arabidopsis AtEPRl extensin-like gene is specifically expressed in endosperm during seed germination. Plant J. 23, 643-652. (doi:10.1046/j.1365-313x.2000.00829.x)
39. Dure, L. & Waters, L. 1965 Long-lived messenger RNA: evidence from cotton seed germination. Science 147, 410-412. (doi:10.1126/science.147.3656.410)
40. Effmertova, E. 1967 The behaviour of "summer annual", "mixed", and "winter annual" natural populations as compared with early and late races in field conditions. Arabidopsis Information Service 4.
41. Evans, J. & Ratcliffe, D. 1972 Variation in 'after-ripening' of seeds of Arabidopsis thaliana and its ecological significance. Arabidopsis Information Service 9, 3-5.
42. Evans, M. E. K., Fernere, R., Kane, M. J. & Venable, D. L. 2007 Bet hedging via seed banking in desert evening
43. primroses (Oenothera, Onagraceae): demographic evidence from natural populations. Am. Nat. 169, 184-194. (doi:10.1086/510599)
44. Fait, A., Angelovici, R., Less, H., Ohad, I., Urbanczyk-Wochniak, E., Fernie, A. R. & Galili, G. 2006 Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol. 142, 839-854. (doi:10.1104/pp.106.086694)
45. Fenner, M. 1991 The effects of parent environment on seed germinability. Seed Sci. Res. 1, 75-84. (doi:10.1017/S0960258500000696)
46. Finch-Savage, W. E. & Leubner-Metzger, G. 2006 Seed dormancy and the control of germination. New Phytol. 171, 501-523.
47. Finch-Savage, W. E., Cadman, C. S., Toorop, P. E., Lynn, J. R. & Hilhorst, H. W. M. 2007 Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51, 60-78. (doi:10.1111/j.1365-313X.2007.03118.x)
48. Finkelstein, R. 1994 Maternal effects govern variable dominance of two abscisic acid mutations in Arabidopsis thaliana. Plant Physiol. 105, 1203-1208.
49. Finkelstein, R., Reeves, W., Ariizumi, T. & Steber, C. 2008 Molecular aspects of seed dormancy. Annu. Rev. Plant Biol. 59, 387-415. (doi:10.1146/annurev.arplant.59. 032607.092740)
50. Galloway, L. F. 2001a The effect of maternal and paternal environments on seed characters in the herbaceous plant Campanula americana (Campanulaceae). Am. J. Bot. 88, 832-840. (doi:10.2307/2657035)
51. Galloway, L. F. 200 lb Parental environmental effects on life history in the herbaceous plant Campanula americana. Ecology 82, 2781-2789. (doi:10.2307/2679960)
52. Galloway, L. F. & Etterson, J. R. 2007 Transgenerational plasticity is adaptive in the wild. Science 318, 1134-1136. (doi: 10.1126/science.l 148766)
53. Goodrich, J. 1998 Plant development: Medea's maternal instinct. Curr. Biol. 8, R480-R484. (doi:10.1016/S0960-9822(98)70312-4)
54. Goto, N. 1982 The relationship between characteristics of seed coat and dark-germination by gibberellins. Arabidopsis Information Service 19, 29-38.
55. Griffith, C., Kim, E.-S. & Donohue, K. 2004 Life-history variation and adaptation in the historically mobile plant, Arabidopsis thaliana (Brassicaceae), in North America. Am. J. Bot. 91, 837-849. (doi:10.3732/ajb.91.6.837)
56. Gualberti, G., Papi, M., Bellucci, L., Ricci, L., Bouchez, D., Camilleri, C., Costantino, P. & Vittorioso, P. 2002 Mutations in the Dof zinc finger genes DAG2 and DAG1 influence with opposite effects the germination of Arabidopsis seeds. Plant Cell 14, 1253-1263. (doi:10.1105/tpc.010491)
57. Gutterman, Y. 1978 Seed coat permeability as a function of photoperiodical treatments of the mother plants during seed maturation in the desert annual plant: Trigonella arabica, DA. J. Arid Environ. 1, 141-144.
58. Gutterman, Y 1992 Maternal effects on seeds during development. In Seeds: the ecology of regeneration in plant communities (ed. M. Fenner), pp. 59-84. Wallingford, UK: CAB International.
59. Gutterman, Y 1994 Effect of day length during plant development and caryopsis maturation on flowering and germination, in addition to temperature during dry storage and light during wetting, of Schismus arabicus (Poaceae) in the Negev desert, Israel. J. Arid Environ. 33, 439-448. (doi: 10.1006/jare. 1996.0079)
60. Gutterman, Y., Thomas, T. H. & Heydecker, W. 1975 Effect on the progeny of applying different day length and
61. hormone treatments to parent plants of Lactuca scariola. Physiol. Plant. 34, 30-38. (doi:10.1111/j. 1399-3054. 1975.tb01851.x)
62. Hayes, R. G. & Klein, W. H. 1974 Spectral quality influence of light during development of Arabidopsis thaliana plants in regulating seed germination. Plant CellPhysiol. 15, 643-653.
63. Holdsworth, M. J., Finch-Savage, W. E., Grappin, P. & Job, D. 2007 Post-genomics dissection of seed dormancy and germination. Trends Plant Sci. 13, 7-13. (doi:10.1016/j.tplants.2007.11.002)
64. Holdsworth, M. J., Bentsink, L. & Soppe, W. J. J. 2008 Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy, and germination. New Phytol. 179, 33-54. (doi:10.1111/j.1469-8137.2008.02437.x)
65. Hume, L. 1994 Maternal environment effects on plant growth and germination of two strains of Thlaspi arvense L. Int. J. Plant Sci. 155, 180-186. (doi:10.1086/297157)
66. Junttila, O. 1971 Effect of mother plant temperature on seed development and germination in Syringa reflexa Schneid. Meld. Norges Landbruk. Shogsk 50, 1-16.
67. Junttila, O. 1973 Seed and embryo germination in Syringa vulgaris and 5. reflexa as affected by temperature during seed development. Physiol. Plant. 29, 264-268. (doi:10. 1111/j.1399-3054.1973. tb03103.x)
68. Kalisz, S. 1986 Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae). Evolution 40, 479-491. (doi:10.2307/2408571)
69. Kalisz, S. & McPeek, M. A. 1992 Demography of an age-structured annual: resampled projection matrices, elasticity analyses and seed bank effects. Ecology 73, 1082-1093. (doi:10.2307/1940182)
70. Kalisz, S. & McPeek, M. A. 1993 Extinction dynamics, population growth and seed banks. Oecologia 95, 314-320. (doi:10.1007/ BF00320982)
71. Kalisz, S. & Wardle, G. M. 1994 Life history variation in Campanula americana (Campanulaceae): population differentiation. Am. J. Bot. 81, 521-527. (doi:10.2307/2445725)
72. Karssen, C. M. 1970 The light promoted germination of the seeds of Chenopodium album L. III. Effect of the photoperiod during growth and development of the plants on the dormancy of the produced seeds. Acta Bot. Neerl. 19, 81-94.
73. Karssen, C. M., Brinkhorst-Van der Swan, D. L. C., Breekland, A. E. & Koorneef, M. 1983 Induction of dormancy during seed development by endogenous abscisic acid: studies on abscisic acid deficient genotypes of Arabidopsis thaliana L. (Heynh.). Planta 157, 158-165. (doi:10.1007/BF00393650)
74. Kirkpatrick, M. & Lande, R. 1989 The evolution of maternal characters. Evolution 43, 485-503. (doi:10.2307/2409054)
75. Koornneef, M. & Karssen, C. M. 1994 Seed dormancy and germination. In Arabidopsis (eds C. Somerville & E. Meyerowitz), pp. 313-334. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
76. Kucera, B., Cohn, M. A. & Leubner-Metzger, G. 2005 Plant hormone interactions during seed dormancy release and germination. Seed Sci. Res. 15, 281-307. (doi:10.1079/SSR2005218)
77. Lacey, E. P. 1991 Parental effects on life history traits in plants. In The unity of evolutionary biology (ed. E. C. Dudley), pp. 735-744. Portland, OR: Dioscorides Press.
78. Lacey, E.P. 1996Parental effects in Plantago lanceolataL. L: a growth chamber experiment to examine pre- and post-zygotic temperature effects. Evolution 50, 865-878. (doi:10.2307/2410858)
79. Lacey, E. P. & Pace, R. 1983 Effect of parental flowering and dispersal times on offspring fate in Daucus carota (Apiaceae). Oecologia 60, 274-278. (doi:10.1007/BF00379533)
80. Lee, I. & Amasino, R. M. 1995 Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiol. 108, 157-162.
81. Leon-Kloosterzeil, K. M., Keijzer, C. J. & Koorneef, M. 1994 A seed shape mutant Arabidopsis that is affected in integument development. Plant Cell 6, 385-392. (doi:10. 1105/tpc.6.3.385)
82. Leubner-Metzger, G. 2005 Beta-1, 3-glucanase gene expression in low-hydrated seeds as a mechanism for dormancy release during tobacco after-ripening. Plant J. 41, 133-145. (doi:10.1111/j.1365-313X. 2004.02284.x)
83. Li, Q., Feng, J.-X., Han, P. & Zhu, Y.-X. 2006 Parental RNA is significantly degraded during Arabidopsis seed germination. J. Integr. Plant Biol. 48, 114-120. (doi:10.1111/j.1744-7909.2006.00216.x)
84. Liu, P. P., Koizuka, N., Martin, R. C. & Nonogaki, H. 2005 The BME3 (Blue Mycropylar End 3) GATA zinc finger transcription factor is a positive regulator of Arabidopsis seed germination. Plant J. 44, 960-971. (doi:10.1111/J.1365-313X.2005.02588.x)
85. Masuda, M. & Washitani, I. 1990 A comparative ecology of the seasonal schedules for 'reproduction by seeds' in a moist tall grassland community. Funct. Ecol. 4, 169-182. (doi:10.2307/2389336)
86. Masuda, M. & Washitani, I. 1992 Differentiation of spring emerging and autumn emerging ecotypes in Galium spurium var. echinospermon. Oecologia 89, 42-46. (doi: 10. 1007/BF00319013)
87. Mathews, S. & Sharrock, R. A. 1997 Phytochrome gene diversity. Plant Cell Environ. 20, 666-671. (doi: 10.1046/j.1365-3040.1997. d01-117.x)
88. McCullough, J. M. & Shropshire Jr, W. 1970 Physiological predetermination of germination responses in Arabidopsis thaliana (1.) HEYNH. Plant Cell Physiol. 11, 139-148.
89. Munir, J., Dorn, L., Donohue, K. & Schmitt, J. 2001 The influence of maternal photoperiod on germination requirements in Arabidopsis thaliana. Am. J. Bot. 88, 1240-1249. (doi:10.2307/3558335)
90. Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y & Nambara, E. 2005 Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epige-netic and genetic regulation of transcription on seed. Plant J 41, 697-709. (doi:10.1111/j.1365-313X.2005.02337.x)
91. Neuffer, B. 1990 Ecotype differentiation in Capsella. Vegetatio 89, 165-172. (doi:10.1007/BF00032168)
92. Neuffer, B. & Hurka, H. 1988 Germination behavior in populations of Capsella bursa-pastoris Cruciferae. Plant Syst. Evol. 161, 35-48. (doi:10.1007/BF00936010)
93. Neuffer, B. & Koch, K. 1996 Maternal effects on populations of Capsella bursa-pastoris (L.) Med. from Scandinavia and the Alps: in dependence of seed weight and the germination behavior of the maturation conditions in lowland and mountains. Biol. Zent. Bl. 115, 337-352.
94. Nishimura, N., Kitahata, N., Seki, M., Narusaka, Y., Narusaka, M., Kuromori, T., Asami, T., Shinozaki, K. & Hirayama, T. 2005 Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J. 44, 972-984. (doi:10.1111/j.1365-313X.2005.02589.x)
95. Nordborg, M. & Bergelson, J. 1999 The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. Am. J. Bot. 86, 470-475. (doi: 10.2307/2656807)
96. Papi, M., Sabatini, S., Bouchez, D., Camilleri, C., Costantino, P. & Vittorioso, P. 2000 Identification and disruption of an Arabidopsis zinc finger gene controlling seed germination. Genes Dev. 14, 28-33.
97. Papi, M., Sabatini, S., Altamura, M. M., Hennig, L., Schafer, E., Costantino, P. & Vittorioso, P. 2002 Inactivation of the
98. phloem-specific Dof zinc finger gene DAG1 affects response to light and integrity of the testa of Arabidopsis seeds. Plant Physiol. 128, 411-417. (doi:10.1104/pp. 010488)
99. Penfield, S., Li, Y., Gilday, A. D., Graham, S. & Graham, I. A. 2006 Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18, 1887-1899. (doi: 10.1105/tpc. 106.041277)
100. Platenkamp, G. A. J. & Shaw, R. G. 1993 Environmental and genetic maternal effects on seed characters in Neomophila menziesii. Evolution 47, 540-555. (doi:10.2307/2410070)
101. Pourrat, Y. & Jacques, R. 1978 The influence of photo-periodic conditions received by the mother plant on morphological and physiological characteristics of Cheno-podiumpolyspermum L. seeds. Plant Sci. Lett. 4, 273-279. (doi:10.1016/0304-4211(75)90286-2)
102. Rajjou, L., Gallardo, K., Debeaujon, I., Vandekerckhove, J., Job, C. & Job, D. 2004 The effect of alpha-amanitin on the Arabidopsis seed proteome highlights the distinct roles of stored and neosynthesized mRNAs during germination. Plant Physiol. 134, 1598-1613. (doi:10.1104/pp.103. 036293)
103. Ratcliffe, D. 1965 The geographical and ecological distribution of Arabidopsis and comments on physiological variation. Arabidopsis Information Service IS.
104. Raz, V., Bergervoet, J. H. W. & Koornneef, M. 2001 Sequential steps for developmental arrest in Arabidopsis seeds. Development 128, 243-252.
105. Roach, D. A. & Wulff, R. D. 1987 Maternal effects in plants. Annu. Rev. Ecol. Syst. 18, 209-235. (doi: 10.1146/annurev.es.18.110187. 001233)
106. Roberts, H. A. & Boddrell, J. E. 1983 Seed survival and periodicity of seedling emergence in 8 species of Cruciferae. Ann. Appl. Biol. 103, 301-312. (doi:10. 1111/j.1744-7348.1983.tb02768.x)
107. Schmitt, J. 1995 Genotype-environment interaction, parental effects, and the evolution of plant reproductive traits. In Experimental and molecular approaches to plant biosystematics (ed. P. Hoch), pp. 1-16. St Louis, MO: Missouri Botanical Garden.
108. Schmuths, H., Bachmann, K., Weber, W E., Horres, R. & Hoffmann, M. H. 2006 Effects of preconditioning and temperature during germination of 73 natural accessions of Arabidopsis thaliana. Ann. Bot. 97, 623-634. (doi: 10. 1093/aob/mcl012)
109. Sharrock, R. A. & Quail, P. H. 1989 Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Dev. 3, 1745-1757. (doi:10.1101/gad.3.11. 1745)
110. Sills, G. R. & Nienhuis, J. 1995 Maternal phenotypic effects due to soil nutrient levels and sink removal in Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 82, 491-495. (doi:10. 2307/2445696)
111. Simpson, G. G. & Dean, C. 2002 Arabidopsis, the rosetta stone of flowering time? Science 296, 285-289. (doi:10. 1126/science.296.5566.285)
112. Thompson, L. 1994 The spatiotemporal effects of nitrogen and litter on the population dynamics of Arabidopsis thaliana. J. Ecol. 82, 63-68. (doi:10.2307/2261386)
113. Tonsor, S. J., Kalisz, S., Fisher, J. & Holtsford, T. P. 1993 A life-history based study of population genetic structure: seed bank to adults in Plantago lanceolata. Evolution 47, 833-843. (doi:10.2307/2410187)
114. Venable, D. L. 1984 Using intraspecific variation to study the ecological significance and evolution of plant life-histories. In Perspectives in plant population ecology (eds R. Dirzo & J. Sarukhan), pp. 166-187. Sunderland, MA: Sinauer Associates, Inc.
115. Venable, D. L. 1985 The evolutionary ecology of seed heteromorphism. Am. Nat. 126, 577-595. (doi:10.1086/284440)
116. Venable, D. L., Burquez, A., Corral, G., Morales, E. & Espinosa, F. 1987 The ecology of seed heteromorphism in Heterosperma pinnatum in central Mexico. Ecology 68, 65-76. (doi:10.2307/1938805)
117. Weber, H., Borisjuk, L. & Wobus, U. 2005 Molecular physiology of legume seed development. Annu. Rev. Plant Biol. 56, 253-279. (doi:10.1146/annurev.arplant. 56.032604.144201)
118. Wulff, R. D. 1995 Environmental maternal effects on seed quality and germination. In Seed development and germination (eds J. Kigel & G. Galili), pp. 491-505. New York: Dekker.
119. Wulff, R. D., Caceres, C. & Schmitt, J. 1994 Seed and seedling responses to maternal and offspring environments m Plantago lanceolata. Funct. Ecol. 8, 763-769. (doi:10.2307/2390236)