Abstract
Cell fate, development timing and occurrence of reproductive versus apomictic development in gymnosperms are shown to be influenced by culture conditions in vitro. In this study, female parthenogenetic apomixis (fPA), androsporogenetic parthenogenesis (mAP) and progenesis were demonstrated using embryonal initials of Araucaria angustifolia in scaled-up cell suspensions passing through a single-cell bottleneck in darkness and in an artificial sporangium (AS). Expression was based on defined nutrition, hormones and feedforward-adaptive feedback process controls at 23–25 °C and in darkness. In fPA, the nucleus of an embryonal initial undergoes endomitosis and amitosis, forming a diploid egg-equivalent and an apoptotic ventral canal nucleus in a transdifferentiated archegonial tube. Discharge of egg-equivalent cells as parthenospores and their dispersal into the aqueous culture medium were followed by free-nuclear conifer-type proembryogenesis. This replaced the plesiomorphic and central features of proembryogenesis in Araucariaceae. Protoplasmic fusions of embryonal initials were used to reconstruct heterokaryotic expressions of fPA in multiwell plates. In mAP, restitutional meiosis (automixis) was responsible for androsporogenesis and the discharge of monads, dyads, tetrads and polyads. In a display of progenesis, reproductive development was brought to an earlier ontogenetic stage and expressed by embryonal initials. Colchicine increased polyploidy, but androspore formation became aberrant and fragmented. Aberrant automixis led to the formation of chromosomal bouquets, which contributed to genomic silencing in embryonal initials, cytomixis and the formation of pycnotic micronucleated cells. Dispersal of female and male parthenospores displayed heteromorphic asexual heterospory in an aqueous environment.
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References
Albrecht-Buehler G (1992) The simulation of microgravity conditions on the ground. Am Soc Grav Space Biol Bull 5(2):3–10
Allen GS (1942) Parthenocarpy, parthenogenesis, and self-sterility of Douglas-fir. J Forestry 40:642–644
Andrulis ED, Neiman AM, Zappula DC, Sternglanz R (1998) Perinuclear localization of chromatin facilitates transcriptional silencing. Nature 394:592–595
Astarita LV, Guerra MP (2000) Conditioning of the culture medium by suspension cells and formation of somatic embryos in Araucaria angustifolia (Coniferae). In Vitro Cell Dev Biol Plant 36:194–200
Bell PR (1994) Apomictic features revealed in a conifer. Int J Plant Sci 155:621–622
Bell PR (1996) Have necrohormones a role in embryogenesis? Acta Societatis Botanicorum Poloniae 65:1–2
Bhatnagar SP, Moitra A (1996) Gymnosperms. New Age International Ltd, New Delhi
Biswas C, Johri BM (1997) The gymnosperms. Springer, New York
Bold HC, Alexopoulos CJ, Delevoryas T (1980) Morphology of plants and fungi, 4th edn. Harper & Row, New York
Burlingame LL (1915) The morphology of Araucaria brasiliensis. III. Fertilization, the embryo and the seed. Bot Gaz 59:1–30
Campbell RA, Durzan DJ (1979) Laser activation of phytochrome-controlled germination in Pinus banksiana. Can J For Res 9:522–524
Chalupa V, Durzan DJ, Vithayasai C (1976) Growth and metabolism of cells and tissue of jack pine (Pinus banksiana). 2. The quantitative analysis of the growth of callus from hypocotyls and radicals. Can J Bot 54:446–455
Cowan CR, Cande WZ (2002) Meiotic telomere clustering is inhibited by colchicine but does not require cytoplasmic microtubules. J Cell Sci 115:3747–3756
Cowan CR, Cowan PM, Cande WZ (2001) The polar arrangement of telomeres in interphase and meiosis. Rabl organization and the bouquet. Plant Physiol 125:532–538
Crow JF (1991) Was Wright right? Science 253:977
Cyr DR (1999) Cryopreservation of embryogenic cultures of conifers and its application to clonal forestry. In: Jain SM, Gupta PK, Newton RJ (eds) Somatic embryogenesis in woody plants, vol 4, pp 239–261
Davis HT (1962) Introduction to nonlinear differential and integral equations. Dover Publications, New York
Dawkins R (1982) The extended phenotype. The gene as a unit of selection. WH Freeman & Co, San Francisco
De Meeûs T, Prugnolle F, Agnew F (2007) Asexual reproduction: genetics and evolutionary aspects. Cell Mol Life Sci 64:1355–1372
Deal RB, Henikoff S (2010) A chromatin thermostat. Nature 463:887–888
Delevoryas T (1980) Polyploidy in gymnosperms. In: Lewis WH (ed) Polyploidy. Biological relevance. Plenum Press, NY, pp 215–218
Dogra PD (1966) Observations on Abies pindrow with a discussion on the question of occurrence of apomixis in gymnosperms. Silvae Genetica 15:11–20
Dogra PD (1978) Morphology, development and nomenclature of conifer embryo. Phytomorphology 28:307–322
Doyle J (1963) Proembryogeny in Pinus in relation to that in other conifers—a survey. Proc Roy Irish Acad 62B:181–216
Durzan DJ (1968) Nitrogen metabolism of Picea glauca. I. Seasonal changes of free amino acids in buds, shoot apices and leaves, and the metabolism of uniformly labeled 14C-l-arginine by buds during the onset of dormancy. Can J Bot 46:909–919
Durzan DJ (1969) Nitrogen metabolism of Picea glauca. IV. Metabolism of uniformly labeled 14C-l-arginine, [carbamyl-14C]-L-citrulline, and [1,2,3,4–14C]-γ-guanidinobutyric acid during diurnal changes in the soluble and protein nitrogen associated with the onset of expansion of spruce buds. Can J Biochem 47:771–783
Durzan DJ (1973) Nitrogen metabolism of Picea glauca. V. metabolism of uniformly labeled 14C-l-proline and 14C-l-glutamine by dormant buds in late fall. Can J Bot 51:359–369
Durzan DJ (1980) Progress and promise in forest genetics. In: Paper science and technology: the cutting edge, 50th anniversary, May 8–10, 1979, Institute of Paper Chemistry, Appleton, pp 31–60
Durzan DJ (1983a) Metabolism of tritiated water during imbibition and germination of jack pine seeds. Can J For Res 13:1204–1218
Durzan DJ (1983b) The fate of carbon during the assimilation of carbamoyl phosphate in white spruce seedlings as revealed by [14C]-carbamoyl phosphate, [14C]-cyanate, and [14C]-bicarbonate labeling patterns. Physiol Plant 59:233–241
Durzan DJ (1996a) Protein ubiquitination in diploid parthenotes of Norway spruce. Intl J Plant Sci 157:17–26
Durzan DJ (1996b) Protein ubiquitination in diploid parthenotes of Norway spruce. Int J Plant Sci 157:17–26
Durzan DJ (2008) Monozygotic cleavage polyembryogenesis. Cytol Genetics 42:159–173 (English and Russian versions)
Durzan DJ (2010) Salmine and the homeotic integrity of early embryos of Norway spruce. Cytol Genetics 44:67–78
Durzan DJ (2011) Parthenogenetic apomixis and androsporogenesis in a Douglas-fir artificial sporangium. Sex Plant Reprod 24:283–296
Durzan DJ, Bourgon G (1976) Growth and metabolism of cells and tissue of jack pine (Pinus banksiana). 7. Observations on cytoplasmic streaming and effects of l-glutamine and its analogues on subcellular activities. Can J Bot 54:507–517
Durzan DJ, Chalupa V (1976a) Growth and metabolism of cells and tissue of jack pine (Pinus banksiana). 3. Growth of cells in liquid suspension cultures in light and darkness. Can J Bot 54:456–467
Durzan DJ, Chalupa V (1976b) Growth and metabolism of cells and tissue of jack pine (Pinus banksiana). 6. Free nitrogenous compounds in cell suspension cultures of jack pine as affected by light and darkness. Can J Bot 54:496–506
Durzan DJ, Pedroso MC (2002) Nitric oxide and reactive nitrogen oxide species in plants. Biotechnol Genet Eng Rev 19:293–337
Durzan DJ, Mia AJ, Wang BSP (1971) Effects of tritiated water on the metabolism and germination of jack pine seeds. Can J Bot 49:2139–2149
Durzan DJ, Campbell RA, Wilson A (1979) Inhibition of female cone production in white spruce by red light treatment during night under field conditions. Environ Exp Bot 19:133–144
Durzan DJ, Jokinen K, Guerra MP, Santerre A, Chalupa V, Havel L (1994) Latent diploid parthenogenesis and parthenote cleavage in egg-equivalents of Norway spruce. Int J Plant Sci 155:677–688
Dyer AF (1979) Investigating chromosomes. Edward Arnold, London
Eames AE (1913) The morphology of Agathis australis. Ann Bot (London) 27:1–38
Eigen M, Schuster P (1979) The hypercycle: a principle of natural self-organization. Springer, Berlin
Friedman WE (1992) Double fertilization in non flowering seed plants and its relevance to the origin of flowering plants. Int Rev Cytol 140:319–355
Garcês H, Durzan DJ, Pedroso MC (2001) Mechanical stress elicits nitric oxide formation and DNA fragmentation in Arabidopsis thaliana. Ann Bot 87:567–574
Giorgetti MR, Vergara M, Evangelista M, Lo Schiavo F, Terzi M, Nuti Ronchi V (1995) On the occurrence of somatic meiosis in embryogenic carrot cells. Mol Gen Genet 246:657–662
Giorgetti L, Castiglione R, Martini G, Geri C, Nuti Ronchi V (2007) Methylated DNA sequence extrusion during plant early meiotic prophase. Caryologia 60:279–289
Gupta PK, Durzan DJ (1987) Somatic embryos from protoplasts of loblolly pine proembryonal cells. Bio/Technology 5:710–712
Gupta PK, Durzan DJ, Finkle B (1987) Somatic polyembryogenesis in embryogenic cell masses of Picea abies (Norway spruce) and Pinus taeda (loblolly pine) after thawing from liquid nitrogen. Can J For Res 17:1130–1134
Haines RJ (1983) Embryo development and anatomy in Araucaria Juss. Aust J Bot 31:125–140
Haines RJ, Prakash N (1980) Proembryo development and suspensor elongation in Araucaria Juss. Aust J Bot 28:511–522
Havel L, Durzan DJ (1996a) Apoptosis in plants. Bot Acta 109:268–277
Havel L, Durzan DJ (1996b) Apoptosis during diploid parthenogenesis and early somatic embryogenesis of Norway spruce. Int J Plant Sci 157:8–16
Hawkins BJ, Sweet GB (1989) Photosynthesis and growth of present New Zealand forest trees relate to ancient climates. Ann Sci For 46(suppl):512s–514s
Hemsley AR (1994) The origin of the land plant sporophyte: an interpolation scenario. Biol Rev 69:263–273
Henderson LJ (1913) The fitness of the environment. Chapter IV. Carbonic acid. MacMillan, New York
Heslop-Harrison JS (2000) Comparative genome organization in plants from sequence to chromosomes. Plant Cell 12:617–635
Higashiyama T, Kuroiwa H, Kawano S, Kuroiwa T (2000) Explosive discharge of pollen tube contents in Torenia fournieri. Plant Physiol 122:11–13
Johansen DA (1950) Plant embryology. Chronica Botanica, Waltham Mass
Kaur D, Bhatnagar SP (1983) Studies in the family Araucariaceae: embryogeny of Agathis robusta C. Moore (FM Bailey). Beitr Biol Pflanzen 58:369–381
Khoshoo TN (1961) Chromosome numbers in gymnosperms. Silvae Genetica 10:1–9
Kiessling W, Simpson C, Foote M (2010) Reefs as cradles of evolution and sources of biodiversity in the Phanerozoic. Science 327:196–198
Kornberg A, Baker TA (1992) DNA replication. WH Freeman, New York
Lewin BJ (1994) Genes V. Oxford University Press, Oxford
Littlewood RK, Munkres KD (1972) Simple and reliable method for replica plating Neurospora crassa. J Bacteriol 110:1017–1021
Magalhaes JR, Monte DC, Durzan DJ (2000) Nitric oxide and ethylene emission in Arabidopsis thaliana. Physiol Mol Biol Plant 6:117–127
Maggs CA, Callow ME (2002) Algal spores. Encyclopedia of life sciences. Nature Publishing Group, London
Mehra PN, Dogra PD (1975) Embryogeny of Pinaceae. 1. Proembryogeny. Proc Indian Natl Sci Acad 41B:486–497
Messerli MA, Robinson KR (2003) Ionic and osmotic disruptions of the lily pollen tube oscillator: testing proposed models. Planta 217:147–157
Mitchell-Olds T (1995) Interval mapping of viability loci causing heterosis in Arabidopsis. Genetics 140:1105–1109
Mogie M (1992) The evolution of asexual reproduction in plants. Chapman and Hall, London
Murray A, Hunt T (1993) The cell cycle. An introduction. WH Freeman, New York
Nagalingum NS, Marshall CR, Quental TB, Rai HS, Little DP, Mathews S (2011) Recent synchronous radiation of a living fossil. Science 334:796–799
Namkoong G, Bishir J (1987) The frequency of lethal alleles in forest tree populations. Evolution 41:1123–1127
Nelson DL, Cox MM (2008) Principles of biochemistry. WH Freeman, New York
Nuti Ronchi V (1995) Mitosis and meiosis in cultured plant cells and their relationship to variant cell types arising in culture. Int Rev Cytol 158:65–140
Orr-Ewing AL (1957a) Possible occurrence of viable unfertilized seeds in Douglas-fir. For Sci 3:243–248
Orr-Ewing AL (1957b) A cytological study of the effects of self-pollination on Pseudotsuga menziesii (Mirb.) Franco. Silvae Genetica 6:179–185
Owens JN, Catalano GL, Morris SJ, Aitken-Christie J (1995) The reproductive biology of Kauri (Agathis australis). III. Proembryogeny and early embryogeny. Int J Plant Sci 156:793–806
Paszkowski J, Grossniklaus U (2011) Selected aspects of transgenerational epigenetic inheritance in plants. Curr Opin Plant Biol 14:195–203
Pedroso MC, Magalhaes JR, Durzan DJ (2000a) A nitric oxide burst precedes apoptosis in an angiosperm and a gymnosperm. J Exp Bot 51:1027–1036
Pedroso MC, Magalhaes JR, Durzan DJ (2000b) Nitric oxide induces cell death in Taxus cells. Plant Sci 157:173–181
Rieger R, Michaelis A, Green MM (1976) Glossary of genetics, 4th edn. Springer, Berlin
Rohde E (1923) Der plasmodiale Aufbau des Tier- und Pfllanzenkörpers. Zeitschrift für wissenshaftliche Zoologie 120:325–535
Rose MR, Nusbaum TJ, Chippindale AK (1996) Laboratory evolution: the experimental wonderland and the Cheshire cat syndrome. In: Rose MR, Lauder GV (eds) Adaptation. Academic Press, San Diego, pp 221–241
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459:1071–1078
Saxton WT (1909) Parthenogenesis in Pinus pinaster. Bot Gaz 47:406–409
Schlögl PS, Wendt dos Santos AL, Vieira L, Floh EIS, Guerra MP (2012) Gene expression during early somatic embryogenesis in Brazilian pine (Araucaria angustifolia (Bert) O. Ktze). Plant Cell Tiss Organ Cult 108:173–180
Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork J, Ecker JR (2011) Transgenerational epigenetic instability is a source of novel methylation variants. Science 334:369–373
Seguí-Simarro JM (2010) Androgenesis revisited. Bot Rev 76:377–404
Sharma AK, Sharma A (1980) Chromosome techniques, theory and practice. Frankenham Press Ltd., Norfolk
Singh H (1978) Embryology of gymnosperms. Handbuch der Pflanzenatomie, vol 10, part 2. Gebrüder Borntraeger, Berlin
Society Linnean (1909) Alternation of generations. Meeting of the Linnean Society on February 18th 1909 following a paper by Dr. WH Lang. New Phytol 8:104–116
Somer IF (1988) On a seasonally oscillating growth function. Fishbyte 6:8–11
Sporne KR (1965) The morphology of gymnosperms. Hutchinson University Library, London
Sterling C (1963) Structure of the male gametophyte in gymnosperms. Biol Rev 38:167–203
Steward FC, Mapes MO, Smith J (1958) Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. Am J Bot 45:693–713
Stewart WN, Rothwell GW (1993) Paleobotany and the evolution of plants. Cambridge University Press, Cambridge
Suomalainen E, Saura A, Lokki J (1987) Cytology and evolution in parthenogenesis. CRC Press, Boca Raton
Taylor TN, Taylor EN, Krings M (2009) Paleobotany. The biology and evolution of fossil plants, 2nd edn. Elsevier, Amsterdam
Thomson RB (1927) Evolution of the seed habit in plants. Trans R Soc Can 21:229–272
Thomson RB (1945) Polyembryony. Sexual and asexual embryo initiation and food supply. Trans R Soc Can 34:143–169
Whittle C-A, Johnston MO (2002) Male-driven evolution of mitochondrial and chloroplast DNA sequences in plants. Mol Biol Evol 19:938–942
Wilkins AS, Holliday R (2009) The evolution of meiosis from mitosis. Genetics 181:3–12
Acknowledgments
Miguel Guerra provided cultures of Araucaria and images of early somatic embryos rescued from seeds. Ladi Havel provided the protoplast observations. Frank Ventimiglia at Davis and Theresa Scorano from Nuti Ronchi’s laboratory carried out cytological staining with suspension culture runs in nippled flasks. The late Gaylor Stebbins and Ernest Gifford provided encouragement for this study. The late Prem Dogra offered insights and reprints of his research on conifer parthenogenesis while visiting Davis. The late F.C. Steward and Adrian Srb (Cornell) provided training in expressions of plant cell totipotency in nippled flasks and on the utility of heterokaryotic assays. Studies with tritiated water and nitrogen metabolism in conifers with carbon-14 were supported by the Canadian Forestry Service. Research relating to conifer cell biology at Davis was supported in part by McIntyre-Stennis funds (1990–1994) and by a NASA grant to DJD on tissue engineering in simulated microgravity (NG 9–825) (1996–1998). Comments on a preliminary manuscript were provided by Michael Mogie. The author declares no conflict of interests.
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Durzan, D.J. Female parthenogenetic apomixis and androsporogenetic parthenogenesis in embryonal cells of Araucaria angustifolia: interpolation of progenesis and asexual heterospory in an artificial sporangium. Sex Plant Reprod 25, 227–246 (2012). https://doi.org/10.1007/s00497-012-0189-0
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DOI: https://doi.org/10.1007/s00497-012-0189-0