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How much influence does the paternal parent have on seed germination?

Published online by Cambridge University Press:  10 January 2019

Jerry M. Baskin
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA
Carol C. Baskin*
Affiliation:
Department of Biology, University of Kentucky, Lexington, KY 40506-0225, USA Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY 40546-0312, USA
*
Author for correspondence: Carol C. Baskin, Email: [email protected]

Abstract

It is well documented that the mother plant has much more influence than the father on seed dormancy/germination, especially of the F1 offspring, primarily by providing all material (maternally derived tissue) to the diaspore coat(s); by maternal environmental effects and provisioning of nutrient resources, mRNA transcripts, protein, the hormone abscisic acid and nitrate to the seed during its development; and by determining progeny environment via dispersal and phenology. There is some evidence that the paternal influence on seed dormancy/germination of the offspring (seeds) can be mediated through multiple paternity (including mate number and diversity), non-nuclear (cytoplasmic) and nuclear (genotypic) inheritance and paternal environmental effects. Our primary aim was to determine via a literature review the influence (or not) of the paternal parent on seed germination. Altogether, 37 of 59 studies (62.7%) indicated a positive influence of the father on seed germination, although not all of them were statistically significant. In general, however, results of studies reported in the literature do not offer strong support for the paternal parent having a major role in seed germination (or seed size) of his F1 offspring.

Type
Review Paper
Copyright
Copyright © Cambridge University Press 2019 

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References

Alboresi, A, Gestin, C, Leydecker, M-T, Bedu, M, Meyer, C and Truong, H-N (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant, Cell and Environment 28, 500512.Google Scholar
Andersson, S (1990) Paternal effects on seed size in a population of Crepis tectorum (Asteraceae). Oikos 59, 38.Google Scholar
Andersson, S, Månsby, E and Prentice, HC (2008) Paternal effects on seed germination: a barrier to the genetic assimilation of an endemic plant taxon? Journal of Evolutionary Biology 21, 14081417.Google Scholar
Antonovics, J and Schmitt, J (1986) Paternal and maternal effects on propagule size in Anthoxanthum odoratum. Oecologia 69, 277282.Google Scholar
Ashman, T-L, Knight, TM, Steets, JA, Amarasekare, P, Burd, M, Campbell, DR, Dudash, MR, Johnston, MO, Mazer, SJ, Mitchell, RJ, Morgan, MT and Wilson, WG (2004) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85, 24082421.Google Scholar
Augspurger, CK, Franson, SE and Cushman, KC (2017) Wind dispersal is predicted by tree, not diaspore, traits in comparisons of neotropical species. Functional Ecology 31, 808820.Google Scholar
Azhagiri, AE and Maliga, P (2007) Exceptional paternal inheritance of plastids in Arabidopsis suggests that low frequency leakage of plastids via pollen may be universal in plants. The Plant Journal 52, 817823.Google Scholar
Baskin, JM and Baskin, CC (2018) Pollen limitation and its effect on seed germination. Seed Science Research. https://doi.org/10.1017/S0960258518000272Google Scholar
Battle, JP and Whittington, WJ (1971) Genetic variability in time to germination of sugar- beet clusters. Journal of Agriculture Science, Cambridge 76, 2732.Google Scholar
Bernasconi, G (2003) Seed paternity in flowering plants: an evolutionary perspective. Perspectives in Plant Ecology, Evolution and Systematics 6, 149158.Google Scholar
Bertin, RI (1986) Consequences of mixed pollinations in Campsis radicans. Oecologia 70, 15.Google Scholar
Bertin, RI (1990) Parental success following mixed pollinations of Campsis radicans. The American Midland Naturalist 124, 153163.Google Scholar
Bertin, RI, Barnes, C and Guttmann, SI (1989) Self sterility and cryptic self-fertility in Campsis radicans (Bignoniaceae). Botanical Gazette 150, 397403.Google Scholar
Biere, A (1991a) Parental effects in Lychnis flos-cuculi. I: Seed size, germination and seedling performance in a controlled environment. Journal of Evolutionary Biology 3, 447465.Google Scholar
Biere, A (1991b) Parental effects on Lychnis flos-cuculi. II: Selection on time of emergence and seedling performance in the field. Journal of Evolutionary Biology 3, 467486.Google Scholar
Bookman, SS (1984) Evidence for selective fruit abortion in Asclepias. Evolution 38, 7286.Google Scholar
Brown, AHD, Grant, JE and Pullen, R (1986) Outcrossing and paternity in Glycine argyrea by paired fruit analysis. Biological Journal of the Linnean Society 29, 283294.Google Scholar
Burd, M (1994) Bateman's principle and plant reproduction: the role of pollen limitation in fruit and seed set. The Botanical Review 60, 83139.Google Scholar
Burgess, KS and Husband, BC (2004) Maternal and paternal contributions to the fitness of hybrids between red and white mulberry (Morus, Moraceae). American Journal of Botany 91, 18021808.Google Scholar
Byers, DL, Platenkamp, GA and Shaw, RG (1997) Variation in seed characters in Nemophila menziesii: evidence of a genetic bases for maternal effect. Evolution 51, 14451456.Google Scholar
Campbell, DR (1998) Multiple paternity in fruits of Ipomopsis aggregata (Polemoniaceae). American Journal of Botany 85, 10221027.Google Scholar
Cook, SA (1962) Genetic system, variation, and adaptation in Eschscholzia californica. Evolution 16, 278299.Google Scholar
Corriveau, JL and Coleman, AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. American Journal of Botany 75, 14431458.Google Scholar
Costa, LM, Yuan, J, Rouster, J, Wyatt, P, Dickinson, H and Gutierrez-Marcos, JF (2012) Maternal control of nutrient allocation in plant seeds by genomic imprinting. Current Biology 22, 160165.Google Scholar
Crean, AJ, Dwyer, JM and Marshall, DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring fitness. Ecology 94, 25752582.Google Scholar
de Jong, TJ, Hermans, CM and van der Veen-van Wijk, K(C)AM (2011) Paternal effects on seed mass in Arabidopsis thaliana. Plant Biology 13 (suppl. 1), 7177.Google Scholar
de Jong, TJ and Scott, RJ (2007) Parental conflict does not necessarily lead to the evolution of imprinting. Trends in Plant Science 12, 439443.Google Scholar
Diggle, PK, Abrahamson, NJ, Baker, RL, Barnes, MG, Koontz, TL, Lay, CR, Medeiros, JS, Murgel, JL, Shaner, MGM, Simpson, HL, Wu, CC and Marshall, DL (2010) Dynamics of maternal and paternal effects on embryo and seed development in wild radish (Raphanus sativus) Annals of Botany 106, 309319.Google Scholar
Donohue, K (1999) Seed dispersal as a maternally influenced character: mechanistic basis of maternal effects and selection on maternal characters in an annual plant. The American Naturalist 154, 674689.Google Scholar
Donohue, K (2009) Completing the cycle: maternal effects as missing links in plant life histories. Philosophical Transactions of the Royal Society B 364, 10591074.Google Scholar
Dudash, MR and Ritland, K (1991) Multiple paternity and self-fertilization in relation to floral age in Mimulus guttatus (Scrophulariaceae). American Journal of Botany 78, 17461753.Google Scholar
Ellstrand, NC (1984) Multiple paternity within the fruits of the wild radish, Raphanus sativus. The American Naturalist 123, 819828.Google Scholar
Ellstrand, NC and Marshall, DL (1986) Patterns of multiple paternity in populations of Raphanus sativus. Evolution 40, 837842.Google Scholar
Etterson, JR and Galloway, LF (2002) The influence of light on paternal plants in Campanula americana (Campanulaceae): pollen characteristics and offspring traits. American Journal of Botany 89, 18991906.Google Scholar
Fenster, CB (1991) Effect of male pollen donor and female seed parent on allocation of resources to developing seeds and fruit in Chamaecrista fasciculata (Leguminosae). American Journal of Botany 78, 1323.Google Scholar
Finkelstein, RR, Gampala, SSL and Rock, CD (2002) Abscisic acid signaling in seeds and seedlings. The Plant Cell 14 (suppl.), S15S45.Google Scholar
Fischer, M, Hock, M and Paschke, M (2003) Low genetic variation reduces cross-compatibility and offspring fitness in populations of a narrow endemic plant with a self-incompatibility system. Conservation Genetics 4, 325336.Google Scholar
Frey, A, Godin, B, Bonnet, M, Sotta, B and Marion-Poll, A (2004) Maternal synthesis of abscisic acid controls seed development and yield in Nicotiana plumbaginifolia. Planta 218, 958964.Google Scholar
Galloway, LF (2001a). The effect of maternal and paternal environments on seed characters of the herbaceous plant Campanula americana (Campanulaceae). American Journal of Botany 88, 832840.Google Scholar
Galloway, LF (2001b) Parental environmental effects on life history in the herbaceous plant Campanula americana. Ecology 82, 27812789.Google Scholar
Garbutt, K and Witcombe, JR (1986) The inheritance of seed dormancy in Sinapis arvensis L. Heredity 56, 2531.Google Scholar
Gehring, M (2013) Genomic imprinting: insights from plants. Annual Review of Genetics 47, 187208.Google Scholar
Girard, J (1990) Study of the inheritance of seed primary dormancy and the ability to enter secondary dormancy in Petunia: influence of temperature, light and gibberellic acid on dormancy. Plant, Cell and Environment 13, 827832.Google Scholar
Godwin, J, Raviv, B and Grafi, G (2017) Dead pericarps and dry fruits function as long-term storage for active hydrolytic enzymes and other substances that affect germination and microbial growth. Plants 6, 64. doi: 10.3390/plants6040064Google Scholar
Good-Avila, SV and Stephenson, AG (2003) Parental effects in a partially self-incompatible herb Campanula rapunculoides L. (Campanulaceae): influence of variation in the strength of self-incompatibility on seed set and progeny performance. The American Naturalist 161, 615630.Google Scholar
Grossniklaus, U, Vielle-Calzada, J-P, Hoeppner, MA and Gagliano, WB (1998) Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science 280, 446450.Google Scholar
Haig, D and Westoby, M (1989) Parent-specific gene expression and the triploid endosperm. The American Naturalist 134, 147155.Google Scholar
Haig, D and Westoby, M (1991) Genomic imprinting in endosperm: its effect on seed development in crosses between species, and between different ploidies of the same species, and its implications for the evolution of apomixis. Philosophical Transactions of the Royal Society of London B 222, 113.Google Scholar
Helenurm, K and Schaal, B (1996) Genetics and maternal effects on offspring fitness in Lupinus texensis. American Journal of Botany 83, 15961608.Google Scholar
Herman, JJ and Sultan, SE (2011) Adaptive transgenerational plasticity in plants: case studies, mechanisms, and implications for natural populations. Frontiers in Plant Science 2 (article 102), 110.Google Scholar
Himes, SL and Wyatt, R (2005) Costs and benefits of self-sterility in Asclepias exaltata (Apocynaceae). Journal of the Torrey Botanical Society 132, 2432.Google Scholar
Holland, JN, Chamberlain, SA, Waguespack, AM and Kinyo, AS (2009) Effects of pollen load and donor diversity on seed and fruit mass in the columnar cactus Pachycereus schottii (Cactaceae). International Journal of Plant Sciences 170, 467475.Google Scholar
Honing, JA (1930) Nuclear and plasma in the heredity of the need of light for germination in Nicotiana seeds. Genetics 12, 441468.Google Scholar
House, C, Roth, C, Hunt, J and Kover, PX (2010) Paternal effects in Arabidopsis thaliana indicate that offspring can influence their own size. Proceedings of the Royal Society B 277, 28852893.Google Scholar
Ibarra-Perez, FJ, Ellstrand, NC and Waines, JG (1996) Multiple paternity in common bean (Phaseolus vulgaris L., Fabaceae). American Journal of Botany 83, 749758.Google Scholar
Jacobs, BS and Lesmeister, SA (2012) Maternal environment effects on fitness, fruit morphology and ballistic seed dispersal distance in an annual forb. Functional Ecology 26, 588597.Google Scholar
Jolivet, C and Bernasconi, G (2007) Within/between population crosses reveal genetic basis for siring success in Silene latifolia (Caryophyllaceae). Journal of Evolutionary Biology 20, 13611374.Google Scholar
Kagawa, M, Tani, T and Kachi, N (2011) Maternal and paternal effects on the germination time of non-dormant seeds of a monocarpic perennial species, Aster kantoensis (Compositae). Plant Species Biology 26, 6672.Google Scholar
Kanno, Y, Jikumaru, Y, Hanada, A, Nambara, E, Abrams, SR, Kimiya, Y and Seo, M (2010). Comprehensive hormone profiling in developing Arabidopsis seeds: examination of the site of ABA biosynthesis, ABA transport and hormone interactions. Plant and Cell Physiology 51, 19882001.Google Scholar
Karssen, CM, Brinkhorst-van der Swan, DLC, Breekland, AE and Koornneef, 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, 158165.Google Scholar
Karron, JD and Marshall, DL (1990) Fitness consequences of multiple paternity in wild radish Raphanus sativus. Evolution 44, 260268.Google Scholar
Karron, JD, Mitchell, RJ and Bell, JM (2006) Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits. American Journal of Botany 93, 13061312.Google Scholar
Kasperbauer, MJ (1968) Dark-germination of reciprocal hybrid seed from light-requiring and -indifferent Nicotiana tobacum. Physiologia Plantarum 21, 13081311.Google Scholar
Knight, TM, Steets, JA, Vamosi, JC, Mazer, SJ, Burd, M, Campbell, DR, Dudash, MR, Johnston, MO, Mitchell, RJ and Ashman, T-L (2005) Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics 36, 467497.Google Scholar
Köhler, C, Wolff, P and Spillane, C (2012) Epigenetic mechanisms underlying genomic imprinting in plants. Annual Review of Plant Biology 63, 331352.Google Scholar
Kucera, B, Cohn, MA and Leubner-Metzger, G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281307.Google Scholar
Lacey, EP (1996) Parental effects in Plantago lanceolata L. I.: a growth chamber experiment to examine pre- and postzygotic temperature effects. Evolution 50, 865878.Google Scholar
Lacey, EP and Herr, D (2000) Parental effects in Plantago lanceolata L. III. Measuring parental temperature effects in the field. Evolution 54, 12071217.Google Scholar
Lacey, EP, Smith, S and Case, AL (1997) Parental effects on seed mass:seed coat but not embryo/endosperm effects. American Journal of Botany 84, 16171620.Google Scholar
Landry, CL and Rathcke, BJ (2007) Do inbreeding depression and relative male fitness explain the maintenance of androdioecy in white mangrove, Laguncularia racemosa (Combretaceae)? New Phytologist 176, 891901.Google Scholar
Lankinen, Å and Madjidian, JA (2011) Enhancing pollen competition by delaying stigma receptivity: pollen deposition schedules affect siring ability, paternal diversity, and seed production in Collinsia heterophylla (Plantaginaceae). American Journal of Botany 98, 11911200.Google Scholar
Larson, BMH and Barrett, SCH (2000) A comparative analysis of pollen limitation in flowering plants. Biological Journal of the Linnean Society 69, 503520.Google Scholar
Lassere, T.B, Carroll, SB and Mulcahy, DL (1996) Effect of pollen competition on offspring quality at varying stages of the life cycle of Silene latifolia Poiret (Caryophyllaceae). Bulletin of the Torrey Botanical Club 123, 175179.Google Scholar
Li, N, Peng, W, Shi, J, Wang, X, Liu, G and Wang, H (2015) The natural variation in seed weight is mainly controlled by maternal genotype in rapeseed (Brassica napus L.). PLoS ONE 10, e0125360.Google Scholar
Lienert, J and Fischer, M (2004) Experimental inbreeding reduced seed production and germination independent of fragmentation of populations of Swertia perennis. Basic and Applied Ecology 5, 4352.Google Scholar
Llaurens, V, Castric, V, Austerlitz, F and Vekemaus, X (2008) High parental diversity in the self-incompatible Arabidopsis halleri despite clonal reproduction and spatially restricted pollen dispersal. Molecular Ecology 17, 15771588.Google Scholar
Lyons, EE (1996) Breeding system evolution in Leavenworthia. II. Genetic and nongenetic parental effects on reproductive success in selfing and more outcrossing populations of Leavenworthia crassa. The American Naturalist 147, 6585.Google Scholar
Marshall, DL (1988) Postpollination effects on seed paternity: mechanisms in addition to microgametophyte competition operate in wild radish. Evolution 42, 12561266.Google Scholar
Marshall, DL (1990) Nonrandom mating in a wild radish, Raphanus sativus. Plant Species Biology 5, 143156.Google Scholar
Marshall, DL (1991) Nonrandom mating in wild radish: variation in pollen donor success and effects of multiple paternity among one- to six-donor pollinations. American Journal of Botany 78, 14041418.Google Scholar
Marshall, DL and Ellstrand, NC (1985) Proximal causes of multiple paternity in wild radish, Raphanus sativus. The American Naturalist 126, 596605.Google Scholar
Marshall, DL and Ellstrand, NC (1986) Sexual selection in Raphanus sativus: experimental data on nonrandom fertilization, maternal choice, and consequences of multiple paternity. The American Naturalist 127, 446461.Google Scholar
Marshall, DL and Evans, AS (2016) Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, Raphanus sativus. American Journal of Botany 103, 553567.Google Scholar
Marshall, DL, Reynolds, J, Abrahamson, NJ, Simpson, HL, Barnes, MG, Medeiros, JS, Walsh, S, Oliveras, DM and Avritt, JJ (2007) Do differences in plant and flower age change mating patterns and later offspring fitness in Raphanus sativus (Brassicaceae)? American Journal of Botany 94, 409418.Google Scholar
Marshall, DL and Whittaker, KL (1989) Effects of pollen donor identity on offspring quality in wild radish, Raphanus sativus. American Journal of Botany 76, 10811088.Google Scholar
Matakiadis, T, Alboresi, A, Jikumaru, Y, Tatematsu, K, Pichon, O, Renou, J-P, Kamiya, Y, Nambara, E and Truong, H-H (2009) The Arabidopsis abscisic acid catabolic gene CYP707A2 plays a key role in nitrate control of seed dormancy. Plant Physiology 149, 949960.Google Scholar
Mazer, SJ (1987a) The quantitative genetics of life history and fitness components of Raphanus raphanistrum L. (Brassicaceae): ecological and evolutionary consequences of seed-weight variation. The American Naturalist 130, 891914.Google Scholar
Mazer, SJ (1987b) Parental effects of seed development and seed yield in Raphanus raphanistrum: implications for natural and sexual selection. Evolution 41, 355371.Google Scholar
Mazer, SJ and Gorchov, DL (1996) Parental effects on progeny phenotype in plants: distinguishing genetic and environmental causes. Evolution 50, 4453.Google Scholar
Mazer, SJ and Schick, CT (1991a) Constancy of population parameters for life history and floral traits in Raphanus sativus L. I. Norms of reaction and the nature of genotypes by environment interactions. Heredity 67, 143156.Google Scholar
Mazer, SJ and Schick, CT (1991b) Constancy of population parameters for life history and floral traits in Raphanus sativus L. II. Effects of planting density on phenotype and heritability estimates. Evolution 45, 18881907.Google Scholar
Mazer, SJ, Snow, AA and Stanton, ML (1986) Fertilization dynamics and parental effects upon fruit development in Raphanus raphanistrum: consequences for seed size variation. American Journal of Botany 73, 500511.Google Scholar
McCauley, DE and Olson, MS (2008) Do recent findings in plant mitochondrial molecular and population genetics have implications for the study of gynodioecy and cytonuclear conflict? Evolution 62, 10131025.Google Scholar
Meyer, SE and Pendleton, RL (2000) Genetic regulation of seed dormancy in Purshia tridentata (Rosaceae). Annals of Botany 85, 521529.Google Scholar
Mitchell, RJ, Karron, JD, Holmquist, KG and Bell, JM (2005) Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae). American Journal of Botany 92, 885890.Google Scholar
Mogensen, HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. American Journal of Botany 83, 383404.Google Scholar
Moore, T and Haig, D (1991) Genomic imprinting in mammalian development: a parental tug-of-war. Trends in Genetics 7, 4549.Google Scholar
Nakamura, RR and Stanton, ML (1989) Embryo growth and seed size in Raphanus sativus: maternal and paternal effects in vivo and in vitro. Evolution 43, 14351443.Google Scholar
Niesenbaum, RA (1999) The effects of pollen load size and donor diversity on pollen performance, selective abortion, and progeny vigor in Mirabilis jalapa (Nyctaginaceae). American Journal of Botany 86, 261268.Google Scholar
Palmer, TM and Zimmerman, M (1994) Pollen competition and sporophyte fitness in Brassica campestris: does intense pollen competition result in individuals with better pollen? Oikos 69, 8086.Google Scholar
Pannell, JR (2000) The evolution and maintenance of androdioecy. Annual Review of Ecology and Systematics 33, 397425.Google Scholar
Paschke, M, Abs, C and Schmid, B (2002) Effects of population size and pollen diversity on reproductive success and offspring size in the narrow endemic Cochlearia bavarica (Brassicaceae). American Journal of Botany 89, 12501259.Google Scholar
Pasonen, H-L, Pulkkinen, P and Käpylä, M (2001) Do pollen donors with fastest-growing pollen tubes give the best offspring in an anemophilous tree, Betula pendula (Betulaceae)? American Journal of Botany 88, 854860.Google Scholar
Pearl, SA, Welch, ME and McCauley, DE (2009) Mitochondrial heteroplasmy and paternal leakage in natural populations of Silene vulgaris, a gynodioecious plant. Molecular Biology and Evolution 26, 537545.Google Scholar
Pélabon, C, Hennet, L, Bolstad, GH, Albertsen, E, Opedal, ØH, Ekrem, RK and Armbruster, WS (2016) Does stronger pollen competition improve offspring fitness when pollen load does not vary? American Journal of Botany 103, 522531.Google Scholar
Pires, ND (2014) Seed evolution: parental conflicts in a multi-generational household. Biomolecular Concepts 5, 7186.Google Scholar
Pires, ND, Bemer, M, Müller, LM, Baroux, C, Spillane, C and Grossniklaus, U (2016) Quantitative genetics identifies cryptic genetic variation involved in the paternal regulation of seed development. PLoS Genetics 12, e1005806.Google Scholar
Piskurewicz, U, Iwasaki, M, Susaki, D, Megies, C, Kinoshita, T and Lopez-Molina, L (2016) Dormancy-specific imprinting underlies maternal inheritance of seed dormancy in Arabidopsis thaliana. eLife 5, e19573.Google Scholar
Pittman, KE and Levin, DA (1989) Effects of parental identities and environment on components of crossing success in Phlox drummondii. American Journal of Botany 76, 409418.Google Scholar
Plakhine, D, Tadmore, Y, Ziadne, H and Joel, DM (2012) Maternal tissue is involved in stimulant reception by seeds of the parasitic plant Orobanche. Annals of Botany 109, 979986.Google Scholar
Platenkamp, GAJ and Shaw, RG (1993) Environmental and genetic maternal effects on seed characters in Nemophila menziesii. Evolution 47, 540555.Google Scholar
Povilus, RA, Diggle, PK and Friedman, WE (2018) Evidence for parent-of-origin effects and interparental conflict in seeds of an ancient flowering plant lineage. Proceedings of the Royal Society B 285, 20172491.Google Scholar
Raviv, B, Aghajanyan, L, Granot, G, Makeover, V, Frenkel, O, Gutterman, Y and Grafi, G (2017a) The dead seed coat functions as a long-term storage for active hydrolytic enzymes. PLoS ONE 12, e01811102.Google Scholar
Raviv, B, Granot, G, Chilifa-Caspi, V and Grafi, G (2017b). The dead, hardened floral bracts of dispersal units of wild wheat function as storage for active hydrolases and in enhancing seedling vigor. PLoS ONE 12, e0177537.Google Scholar
Raz, V, Bergervoet, JHW and Koornneef, M (2001) Sequential steps for developmental arrest in Arabidopsis seeds. Development 128, 243252.Google Scholar
Reusch, TBH (2000) Pollination in the marine realm: microsatellites reveal high outcrossing rates and multiple paternity in eelgrass Zostera marina. Heredity 85, 459464.Google Scholar
Richardson, TE and Stephenson, AG (1991) Effects of parentage, prior fruit set and pollen load on fruit and seed production in Campanula americana L. Oecologia 87, 8085.Google Scholar
Richardson, TE and Stephenson, AG (1992) Effect of parentage and size of the pollen load on progeny performance in Campanula americana. Evolution 46, 17311739.Google Scholar
Rideau, M, Monin, J, Dommergues, P and Cornu, A (1976) Estude sur les mécanismes hereditaires de la dormance des akenes de Lactuca sativa L. Comptes rendus hebdomadaires des séances de l'Académie des sciences. Série D, Sciences naturelles 283, 769772.Google Scholar
Riesberg, LH, Philbrick, CT, Pack, PE, Hanson, MA and Fritsch, P (1993) Inbreeding depression in androdioecious populations of Datisca glomerata (Datiscaceae). American Journal of Botany 80, 757762.Google Scholar
Rix, KD, Gracie, AJ, Potts, BM, Brown, PH, Spurr, CJ and Gore, PL (2012) Paternal and maternal effects on the response of seed germination to high temperatures in Eucalyptus globulus. Annals of Forest Science 69, 673679.Google Scholar
Roach, DA and Wulff, RD (1987) Maternal effects in plants. Annual Review of Ecology and Systematics 18, 209235.Google Scholar
Rodrigues, JA and Zilberman, D (2015) Evolution and function of genomic imprinting in plants. Genes and Development 29, 25172531.Google Scholar
Rossiter, MC (1996) Incidence and consequences of inherited environmental effects. Annual Review of Ecology, and Systematics 27, 451476.Google Scholar
Rubio de Casas, R, Willis, CG and Donohue, K (2012) Plant dispersal phenotypes: a seed perspective of maternal habitat selection, pp. 171184 in Clobert, J, Baguette, M, Benton, TG and Bullock, JM (eds), Dispersal Ecology and Evolution. Oxford, Oxford University Press.Google Scholar
Schemske, DW and Pautler, LP (1984) The effects of pollen composition on fitness components in a neotropical herb. Oecologia 62, 3136.Google Scholar
Schlichting, CD and Devlin, B (1992) Pollen and ovule sources affect seed production of Lobelia cardinalis (Lobeliaceae). American Journal of Botany 79, 891898.Google Scholar
Schmid, B and Dolt, C (1994) Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima L. Evolution 48, 15251549.Google Scholar
Schmitt, J and Antonovics, J (1986) Experimental studies on the evolutionary significance of sexual reproduction. III. Maternal and paternal effects during seedling establishment. Evolution 40, 817829.Google Scholar
Scott, RJ, Speilman, M, Bailey, J and Dickinson, HG (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125, 33293341.Google Scholar
Shaw, RG and Byers, DL (1998) Genetics of maternal and paternal effects, pp. 97111 in Mousseau, TA and Fox, CW (eds), Maternal Effects as Adaptations. Oxford, Oxford University Press.Google Scholar
Snow, AA (1990) Effects of pollen-load size and number of donors on sporophyte fitness in wild radish (Raphanus raphanistrum). The American Naturalist 136, 742758.Google Scholar
Snow, AA and Spira, TP (1991a) Pollen vigour and the potential for sexual selection in plants. Nature 352, 796797.Google Scholar
Snow, AA and Spira, TP (1991b) Differential pollen-tube growth rates and nonrandom fertilization in Hibiscus moscheutos (Malvaceae). American Journalof Botany 78, 14191426.Google Scholar
Sork, VL and Schemske, DW (1992) Fitness consequences on mixed-donor pollen loads in the annual legume Chamaecrista fasciculata. American Journal of Botany 79, 508515.Google Scholar
Sosa, VJ and Fleming, TH (1999) Seedling performance in a trioecious cactus, Pachycereus pringlei: effects of maternity and paternity. Plant Systematics and Evolution 218, 145151.Google Scholar
Tamme, R, Götzenberer, L, Zobel, M, Bullock, JM, Hooftman, DAP, Kaasik, A and Pärtel, M (2014) Predicting species’ maximum dispersal distances from simple plant traits. Ecology 95, 505513.Google Scholar
Teixeira, S and Bernasconi, G (2007) High prevalence of multiple paternity within fruits in natural populations of Silene latifolia, as revealed by microsatellite DNA analysis. Molecular Ecology 16, 43704379.Google Scholar
Teixeira, S, Foerster, K and Bernasconi, G (2009) Evidence for inbreeding depression and post-pollination selection against inbreeding in the dioecious plant Silene latifolia. Heredity 102, 101112.Google Scholar
Thomson, FJ, Moles, AT, Auld, TD and Kingsford, RT (2011) Seed dispersal distance is more strongly correlated with plant height than with seed mass. Journal of Ecology 99, 12991307.Google Scholar
Vander Kloet, SP and Tosh, D (1984) Effect of pollen donors on seed production, seed weight, germination and seedling vigor of Vaccinium corymbosum L. The American Midland Naturalist 112, 392396.Google Scholar
Van Zandt, PA and Mopper, S (2004) The effects of maternal salinity and seed environment on germination and growth of Iris hexagona. Evolutionary Ecology Research 6, 813832.Google Scholar
Verdu, M, Montilla, AI and Pannell, JR (2004) Paternal effects on functional gender account for cryptic dioecy in a perennial plant. Proceedings of the Royal Society, London B 271, 20172023.Google Scholar
Vinkenoog, R, Bushell, C, Spielman, M, Adams, S, Dickinson, HG and Scott, RJ (2003) Genomic imprinting and endosperm development in flowering plants. Molecular Biotechnology 25, 149184.Google Scholar
Vu, WT, Chang, PL, Moriuchi, KS and Friesen, ML (2015) Genetic variation of transgenerational plasticity of offspring germination in response to salinity stress and seed transcriptome of Medicago truncatula. BMC Evolutionary Biology 15, 59.Google Scholar
Welch, ME, Darnell, MZ and McCauley, DE (2006) Variable populations within variable populations: quantifying mitochondrial heteroplasmy in natural populations of the gynodioecious plant Silene vulgaris. Genetics 174, 829837.Google Scholar
Wenslaff, TF and Lyrene, PM (2001) Results of multiple pollination in blueberry (Vaccinium elliottii Chapm.). Euphytica 117, 233240.Google Scholar
Yan, A and Chen, Z (2017) The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Reports 36, 689703.Google Scholar
Young, HJ and Stanton, ML (1990) Influence of environmental quality on pollen competition ability in wild radish. Science 248, 16311633.Google Scholar