Disruption of endosperm development is a major cause of hybrid seed inviability between Mimulus guttatus and Mimulus nudatus

New Phytologist

Volumn 210, Issue 3, 2016, Pages 1107-1120

  Oneal, Elen ^a   Willis, John H ^a   Franks, Robert G ^b  

^a DUKE UNIVERSITY   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

Endosperm; Hybrid inviability; Mimulus guttatus (monkeyflower); Pollen pistil interactions; Postzygotic isolation; Seed development

Indexed keywords

DEVELOPMENT FAILURE; DICOTYLEDON; ECOLOGICAL MODELING; EMBRYONIC DEVELOPMENT; ENDEMIC SPECIES; FORMATION MECHANISM; GERMINATION; HYBRIDIZATION; PLANT-POLLINATOR INTERACTION; REPRODUCTIVE ISOLATION; REPRODUCTIVE SUCCESS; VICARIANCE;

MAGNOLIOPHYTA; MIMULUS (ANGIOSPERM); MIMULUS GUTTATUS; MIMULUS NUDATUS;

CROSS BREEDING; EMBRYOLOGY; ENDOSPERM; FRUIT; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; HYBRIDIZATION; MIMULUS; PHENOTYPE; POLLEN TUBE; SELF FERTILIZATION; STAINING; SYMPATRY;

CROSSES, GENETIC; ENDOSPERM; FRUIT; GERMINATION; HYBRIDIZATION, GENETIC; MIMULUS; PHENOTYPE; POLLEN TUBE; SELF-FERTILIZATION; STAINING AND LABELING; SYMPATRY;

EID: 84971602941     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.13842     Document Type: Article

References (70)

1. Arekal GD. 1965. Embryology of Mimulus ringens. Botanical Gazette 1965: 58-66.
2. Beldade P, Koops K, Brakefield PM. 2002. Developmental constraints versus flexibility in morphological evolution. Nature 416: 844-847.
3. Bharathan G. 1999. Endosperm development in angiosperms: a phylogenetic analysis. Biodiversity, Taxonomy, and Ecology 1999: 167-180.
4. Birchler JA. 1993. Dosage analysis of maize endosperm development. Annual Review of Genetics 27: 181-204.
5. Birchler JA. 2014. Interploidy hybridization barrier of endosperm as a dosage interaction. Frontiers in Plant Science 5: 1-4.
6. Birchler JA, Veitia RA. 2010. The gene balance hypothesis: implications for gene regulation, quantitative traits and evolution. New Phytologist 186: 54-62.
7. Boavida LC, Silva JP, Feijó JA. 2001. Sexual reproduction in the cork oak (Quercus suber L). II. Crossing intra-and interspecific barriers. Sexual Plant Reproduction 14: 143-152.
8. Bonner JT. 1988. The evolution of complexity. Princeton, NJ, USA: Princeton University Press.
9. Brandvain Y, Haig D. 2005. Divergent mating systems and parental conflict as a barrier to hybridization in flowering plants. American Naturalist 166: 330-338.
10. Brink RA, Cooper DC. 1947. The endosperm in seed development. Botanical Review 13: 479-541.
11. Burkart-Waco D, Ngo K, Dilkes B, Josefsson C, Comai L. 2013. Early disruption of maternal-zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. Plant Cell Online 25: 2037-2055.
12. Campbell DR, Alarcon R, Wu CA. 2003. Reproductive isolation and hybrid pollen disadvantage in Ipomopsis. Journal of Evolutionary Biology 16: 536-540.
13. Casson S, Spencer M, Walker K, Lindsey K. 2005. Laser capture microdissection for the analysis of gene expression during embryogenesis of Arabidopsis. Plant Journal 42: 111-123.
14. Cooley AM, Willis JH. 2009. Genetic divergence causes parallel evolution of flower color in Chilean Mimulus. New Phytologist 183: 729-739.
15. Costa CB, Costa JA, de Queiroz LP, Borba EL. 2013. Self-compatible sympatric Chamaecrista (Leguminosae-Caesalpinioideae) species present different interspecific isolation mechanisms depending on their phylogenetic proximity. Plant Systematics and Evolution 299: 699-711.
16. Costa LM, Gutierrez-Marcos JF, Dickinson HG. 2004. More than a yolk: the short life and complex times of the plant endosperm. Trends in Plant Science 9: 507-514.
17. Del Toro-De León G, García-Aguilar M, Gillmor CS. 2014. Non-equivalent contributions of maternal and paternal genomes to early plant embryogenesis. Nature 514: 624-627.
18. Deshpande SS, Cheryan M, Salunkhe DK, Luh BS. 1986. Tannin analysis of food products. Critical Reviews in Food Science & Nutrition 24: 401-449.
19. Dowrick GJ, Brandram SN. 1970. Abnormalities of endosperm development in Lilium hybrids. Euphytica 19: 433-442.
20. Erilova A, Brownfield L, Exner V, Rosa M, Twell D, Scheid OM, Hennig L, Köhler C. 2009. Imprinting of the Polycomb Group gene MEDEA srves as a ploidy sensor in Arabidopsis. PLoS Genetics 5: e1000663.
21. Fishman L, Aagaard J, Tuthill JC. 2008. Toward the evolutionary genomics of gametophytic divergence: patterns of transmission ratio distortion in monkeyflower (Mimulus) hybrids reveal a complex genetic basis for conspecific pollen precedence. Evolution 62: 2958-2970.
22. Floyd SK, Friedman WE. 2000. Evolution of endosperm developmental patterns among basal flowering plants. International Journal of Plant Sciences 161: S57-S81.
23. Friedman WE. 2001. Comparative embryology of basal angiosperms. Current Opinion in Plant Biology 4: 14-20.
24. Friedman WE, Madrid EN, Williams JH. 2008. Origin of the fittest and survival of the fittest: relating female gametophyte development to endosperm genetics. International Journal of Plant Sciences 169: 79-92.
25. Fu XL, Lu YG, Liu XD, Li JQ. 2009. Crossability barriers in the interspecific hybridization between Oryza sativa and O. meyeriana. Journal of Integrative Plant Biology 51: 21-28.
26. Galbraith DW, Harkins KR, Knapp S. 1991. Systemic endopolyploidy in Arabidopsis thaliana. Plant Physiology 96: 985-989.
27. Galen C, Newport MEA. 1988. Pollination quality, seed set, and flower traits in Polemonium viscosum: complementary effects of variation in flower scent and size. American Journal of Botany 75: 900-905.
28. Gardner M, Macnair M. 2000. Factors affecting the co-existence of the serpentine endemic Mimulus nudatus Curran and its presumed progenitor, Mimulus guttatus Fischer ex DC. Biological Journal of the Linnean Society 69: 443-459.
29. Gillmor CS, Silva-Ortega CO, Willmann MR, Buendía-Monreal M, Poethig RS. 2014. The Arabidopsis Mediator CDK8 module genes CCT (MED12) and GCT (MED13) are global regulators of developmental phase transitions. Development 141: 4580-4589.
30. Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J. 2000. Microarray analysis of developing Arabidopsis seeds. Plant Physiology 124: 1570-1581.
31. Guignard L. 1899. Sur les anthérozoides et la double copulation sexuelle chez les végétaux angiospermes. Comptes Rendus de l'Academie des Sciences de Paris 128: 864-871.
32. Haig D. 2013. Kin conflict in seed development: an interdependent but fractious collective. Annual Review of Cell and Developmental Biology 29: 189-211.
33. Haig D, 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 B: Biological Sciences 333: 1-13.
34. Hehenberger E, Kradolfer D, Köhler C. 2012. Endosperm cellularization defines an important developmental transition for embryo development. Development 139: 2031-2039.
35. Hsieh TF, Shin J, Uzawa R, Silva P, Cohen S, Bauer MJ, Hashimoto M, Kirkbride RC, Harada JJ, Zilberman D et al. 2011. Regulation of imprinted gene expression in Arabidopsis endosperm. Proceedings of the National Academy of Sciences, USA 108: 1755-1762.
36. Johnston SA, Hanneman RE. 1982. Manipulations of endosperm balance number overcome crossing barriers between diploid Solanum species. Science 217: 446-448.
37. Josefsson C, Dilkes B, Comai L. 2006. Parent-dependent loss of gene silencing during interspecies hybridization. Current Biology 16: 1322-1328.
38. Kearns CA, Inouye DW. 1993. Techniques for pollination biologists. Colorado, CO, USA: University Press of Colorado.
39. Köhler C, Hennig L, Spillane C, Stephane P, Gruissem W, Grossniklaus U. 2003. The Polycomb-group protein MEDEA regulates seed development by controlling expression of the MADS-box gene PHERES1. Genes and Development 17: 1540-1553.
40. Köhler C, Mittelsten Scheid O, Erilova A. 2010. The impact of the triploid block on the origin and evolution of polyploid plants. Trends in Genetics 26: 142-148.
41. Köhler C, Wolff P, Spillane C. 2012. Epigenetic mechanisms underlying genomic imprinting in plants. Annual Review of Plant Biology 63: 331-352.
42. 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 Genetics 9: e1003163.
43. Lester RN, Kang JH. 1998. Embryo and endosperm function and failure in Solanum species and hybrids. Annals of Botany 82: 445-453.
44. Linkies A, Graeber K, Knight C, Leubner-Metzger G. 2010. The evolution of seeds. New Phytologist 186: 817-831.
45. Lowry DB, Hall MC, Salt DE, Willis JH. 2009. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytologist 183: 776-788.
46. Lowry DB, Willis JH. 2010. A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biology 8: e1000500.
47. Martin NH, Willis JH. 2010. Geographical variation in postzygotic isolation and its genetic basis within and between two Mimulus species. Philosophical Transactions of the Royal Society B: Biological Sciences 365: 2469-2478.
48. Nawaschin SG. 1898. Resultate einer Revision der Befruchtungs- vorgänge bei Lilium martagon und Fritillaria tenella. Bulletin de l'Academie des Sciences de Saint Petersbourg 9: 377-382.
49. Nguyen H, Brown RC, Lemmon BE. 2000. The specialized chalazal endosperm in Arabidopsis thaliana and Lepidium virginicum (Brassicaceae). Protoplasma 212: 99-110.
50. Oneal E, Lowry DB, Wright KM, Zhu Z, Willis JH. 2014. Divergent population structure and climate associations of a chromosomal inversion polymorphism across the Mimulus guttatus species complex. Molecular Ecology 23: 2844-2860.
51. Pal M, Pandey RM, Khoshoo TN. 1972. Evolution and improvement of cultivated amaranths. Journal of Heredity 73: 353-356.
52. Płachno BJ, Światek P, Sas-Nowosielska H, Kozieradzka-Kiszkurno M. 2013. Organisation of the endosperm and endosperm-placenta syncytia in bladderworts (Utricularia, Lentibulariaceae) with emphasis on the microtubule arrangement. Protoplasma 250: 863-873.
53. Raghavan V. 1997. Molecular embryology of flowering plants. Cambridge, UK: Cambridge University Press, 328.
54. Ramsey J, Bradshaw HD, Schemske DW. 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evolution 57: 1520-1534.
55. Rebernig CA, Lafon-Placette C, Hatorangan MR, Slotte T, Köhler C. 2015. Non-reciprocal interspecies hybridization barriers in the Capsella genus are established in the endosperm. PLoS Genetics 11: e1005295.
56. Reyes JC, Grossniklaus U. 2003. Diverse functions of Polycomb group proteins during plant development. Seminars in Cell and Developmental Biology 14: 77-84.
57. Ritland C, Ritland K. 1989. Variation of sex allocation among eight taxa of the Mimulus guttatus species complex (Scrophulariaceae). American Journal of Botany 1989: 1731-1739.
58. Roszak P, Köhler C. 2011. Polycomb group proteins are required to couple seed coat initiation to fertilization. Proceedings of the National Academy of Sciences, USA 108: 20826-20831.
59. Running M 2007. Nuclear staining of plants for confocal microscopy. Cold Spring Harbor Protocols 2007: pdb-prot4685.
60. Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671-675.
61. Scott RJ, Spielman M, Bailey J, Dickinson HG. 1998. Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125: 3329-3341.
62. Searcy KB, Macnair MR. 1990. Differential seed production in Mimulus guttatus in response to increasing concentrations of copper in the pistil by pollen from copper tolerant and sensitive sources. Evolution 1990: 1424-1435.
63. Smith JM, Burian R, Kauffman S, Alberch P, Campbell J, Goodwin B, Lande R, Raup D, Wolpert L. 1985. Developmental constraints and evolution: a perspective from the Mountain Lake conference on development and evolution. Quarterly Review of Biology 60: 265-287.
64. Tiffin P, Olson S, Moyle LC. 2001. Asymmetrical crossing barriers in angiosperms. Proceedings of the Royal Society of London B: Biological Sciences 268: 861-867.
65. Vickery RK. 1966. Speciation and isolation in section Simiolus of the genus Mimulus. Taxon 15: 55-63.
66. Vickery RK. 1978. Case studies in the evolution of species complexes in Mimulus. Evolutionary Biology 11: 405-507.
67. Williams JH. 2009. Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase. American Journal of Botany 96: 144-165.
68. Wright KM, Lloyd D, Lowry DB, Macnair MR, Willis JH. 2013. Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLoS Biology 11: e1001497.
69. Wu CA, Lowry DB, Cooley AM, Wright KM, Lee YW, Willis JH. 2007. Mimulus is an emerging model system for the integration of ecological and genomic studies. Heredity 100: 220-230.
70. Yuan YW, Sagawa JM, Frost L, Vela JP, Bradshaw HD. 2014. Transcriptional control of floral anthocyanin pigmentation in monkeyflowers (Mimulus). New Phytologist 204: 1013-1027.