Abstract
Amborella trichopoda is the sole living angiosperm species belonging to the sister lineage of all other extant flowering plants. In the last decade, the species has been the focus of many phylogenetic, genomic and reproductive biology studies, bringing new highlights regarding the evolution of flowering plants. However, little attention has been paid to in situ A. trichopoda populations, particularly to their fruiting cycle. In this study, an A. trichopoda population was observed during three annual flowering cycles. Individuals and branches were labeled in order to monitor the fruiting cycle precisely, from the flowering stage until the abscission of the fruit. Fruit exocarp was green during the first 9 months following flowering, turned red when the next flowering started a year later then remained on the branch during another year, between fruit ripping and abscission. Presence of fruits with two stages of maturity on shrubs was always noticed. Germination tests showed that seeds acquired their germination capacity 1 year after flowering, when fruits changed color. A. trichopoda’s fruiting cycle is a long process overlapping two annual flowering periods. These results introduce a new model for flowering and fruiting cycles. The availability of mature seeds on shrubs for more than 1 year is likely to maximize opportunities to be dispersed, thus promoting the survival of this basal angiosperm.
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References
Amborella Genome Project (2013) The Amborella genome and the evolution of flowering plants. Science 342:1241089
Armitage FB, Burley J (1980) Pinus kesiya Royle ex Gordon (syn. P. khasya Royle; P. insularis Endlicher). Tropical forestry, Commonwealth Forestry Institute, Oxford
Bailey IW, Swamy BGI (1948) Amborella trichopoda Baill., a new morphological type of vesselless dicotyledon. J Arnold Arbor 29:245–253
Bailly Y, Bernut L, Brinon H, Brinon M, Fort A, Lauri PE, Omniwack L (1986) Etude de la germination et de la conservation des semences d’essences forestières d’intérêt économique. Rapport final de convention. ORSTOM, Nouméa, p 297
Balouet JC, Olson S (1989) Fossil birds from late Quaternary deposits in New Caledonia. Smithson Contrib Zool, vol 469. Smithsonian Institution Press, Washington DC, pp 1–38
Baskin CC, Baskin JM (1998) Seeds: ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego
Bergthorsson U, Richardson AO, Young GJ, Goertzen LR, Palmer JD (2004) Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc Natl Acad Sci USA 101:17747–17752
Bobrov AVF, Endress PK, Melikian AP, Romanov MS, Sorokin AN, Palmarola Bejerano A (2005) Fruit structure of Amborella trichopoda (Amborellaceae). Bot J Lin Soc 148:265–274
Buzgo M, Soltis PS, Soltis DE (2004) Floral developmental morphology of Amborella trichopoda (Amborellaceae). Int J Plant Sci 165:925–947
Carlquist SJ (1974) Island biology. Columbia University Press, New York
Endress PK (2001) The flowers in extant basal angiosperms and inferences on ancestral flowers. Int J Plant Sci 162:1111–1140
Endress PK (2010) The evolution of floral biology in basal angiosperms. Philos Trans R Soc Lond B Biol Sci 365:411–421
Endress PK, Igersheim A (2000) The reproductive structures of the basal angiosperm Amborella trichopoda (Amborellaceae). Int J Plant Sci 161:S237–S248
Evans J (1982) Plantation forestry in the tropics. Clarendon Press, Oxford
Feild TS, Arens NC (2005) Form, function and environments of the early angiosperms: merging extant phylogeny and ecophysiology with fossils. New Phytol 166:383–408
Feild TS, Arens NC (2007) The ecophysiology of early angiosperms. Plant Cell Environ 30:291–309
Feild TS, Zweiniecki MA, Brodribb T, Jaffre T, Donoghue MJ, Holbrook NM (2000) Structure and function of tracheary elements in Amborella trichopoda. Int J Plant Sci 161:705–712
Feild TS, Brodribb T, Jaffre T, Holbrook NM (2001) Acclimation of leaf anatomy, photosynthetic light use, and xylem hydraulics to light in Amborella trichopoda (Amborellaceae). Int J Plant Sci 162:999–1008
Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ (2004) Dark and disturbed: a new image of early angiopserm ecology. Paleobiology 30:82–107
Floyd SK, Friedman WE (2001) Developmental evolution of endosperm in basal angiosperms: evidence from Amborella (Amborellaceae), Nuphar (Nymphaeaceae), and Illicium (Illiciaceae). Plant Syst Evol 228:153–169
Fogliani B, Klein N, Gâteble G, Scutt CP (2010) Seed biology and germination of the basal angiosperm Amborella trichopoda. In: Pendleton SMR, Schultz B (eds) Seed ecology III. The European Plant Science Organisation, Salt Lake City, Utah, pp 51–52
Forbis TA, Floyd SK, de Queiroz A (2002) The evolution of embryo size in angiosperms and other seed plants: implications for the evolution of seed dormancy. Evolution 56:2112–2125
Friedman WE (2001) Comparative embryology of basal angiosperms. Curr Opin Plant Biol 4:14–20
Friedman WE, Bachelier JB (2013) Seed development in Trimenia (Trimeniaceae) and its bearing on the evolution of embryo-nourishing strategies in early flowering plant lineages. Am J Bot 100:906–915
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 96:129–143
Goremykin VV, Nikiforova SV, Biggs PJ, Zhong B, Delange P, Martin W, Woetzel S, Atherton RA, McLenachan PA, Lockhart PJ (2013) The evolutionary root of flowering plants. Syst Biol 62:50–61
Grandcolas P, Nattier R, Trewick S (2014) Relict species: a relict concept? Trends Ecol Evol 29:655–663
Howe HF, Smallwood J (1982) Ecology of seed dispersal. Ann Rev Ecol Syst 13:201–228
Jérémie J (1982) Amborellacées. In: Aubréville ALJF (ed) Flore de la Nouvelle Calédonie. Muséum National d’Histoire Naturelle, Paris, pp 157–160
Lupia R, Lidgard S, Crane PR (1999) Comparing palynological abundance and diversity: implications for biotic replacement during the Cretaceous angiosperm radiation. Paleobiology 25:305–340
Mathews S, Donoghue MJ (1999) The root of angiosperm phylogeny inferred from duplicate phytochrome genes. Science 286:947–950
Moore MJ, Bell CD, Soltis PS, Soltis DE (2007) Using plastid genome-scale data to resolve enigmatic relationships among basal angiosperms. Proc Natl Acad Sci USA 104:19363–19368
Morat P, Mac Kee HS (1977) Quelques précisions sur le Trimenia neocaledonica Bak. F. et la famille des Triméniacées en Nouvelle-Calédonie. Adansonia 17:205–2013
Norton SA (1980) Reproductive ecology of Pseudowintera (Winteraceae). M.S. thesis. Victoria University of Wellington, New Zealand
Oginuma K, Jaffre T, Tobe H (2000) The karyotype analysis of somatic chromosomes in Amborella trichopoda (Amborellaceae). J Plant Res 113:281–283
Pascal M, Barré N, Garine-Wichatitsky D, Lorvelec O, Frétey T, Brescia F, Jourdan H (2006) Les peuplements néo-calédoniens de vertébrés : invasions, disparitions. In: IRD (ed) Les espèces envahissantes dans l’archipel néo-calédonien = Invasive species in the New Caledonian archipelago (Expertise Collégiale), Paris, p 259
Pelletier B (2006) Geology of the New Caledonia region and its implication for the study of the New Caledonian biodiversity. In: Pairy C. RdFB (ed) Forum Biodiversité des écosystèmes corallines, Nouméa, pp 17–30
Pillon Y (2009) Récolte d’échantillons d’Amborella trichopoda. Institut de Recherche pour le Développement, pp 1–12
Pillon Y (2012) Time and tempo of diversification in the flora of New Caledonia. Bot J Lin Soc 170:288–298
Poncet V, Munoz F, Munzinger J, Pillon Y, Gomez C, Couderc M, Tranchant-Dubreuil C, Hamon S, de Kochko A (2013) Phylogeography and niche modelling of the relict plant Amborella trichopoda (Amborellaceae) reveal multiple Pleistocene refugia in New Caledonia. Mol Ecol 22:6163–6178
Qiu YL, Lee J, Bernasconi-Quadroni F, Soltis DE, Soltis PS, Zanis M, Zimmer EA, Chen Z, Savolainen V, Chase MW (1999) The earliest angiosperms: evidence from mitochondrial, plastid and nuclear genomes. Nature 402:404–407
Rice DW, Alverson AJ, Richardson AO, Young GJ, Sanchez-Puerta MV, Munzinger J, Barry K, Boore JL, Zhang Y, dePamphilis CW, Knox EB, Palmer JD (2013) Horizontal transfer of entire genomes via mitochondrial fusion in the angiosperm Amborella. Science 342:1468–1473
Robbins AMJ (1983) Pinus oocarpa Schiede (mimeo). Seed leaflet No 3. DANIDA Forest Seed Centre, Denmark
Romanov MS, Dilcher DL (2013) Fruit structure in Magnoliaceae s.l. and Archaeanthus and their relationships. Am J Bot 100:1494–1508
Schlessman MA, Vary LB, Munzinger J, Lowry PP (2014) Incidence, correlates, and origins of dioecy in the island flora of New Caledonia. Int J Plant Sci 175:271–286
Singh H (1978) Embryology of gymnosperms. Gebruder Borntraeger, Berlin
Soltis PS, Soltis DE, Chase MW (1999) Angiosperm phylogeny inferred from multiple genes as a tool for comparative biology. Nature 402:402–404
Soltis DE, Albert VA, Leebens-Mack J, Palmer JD, Wing RA, dePamphilis CW, Ma H, Carlson JE, Altman N, Kim S, Wall PK, Zuccolo A, Soltis PS (2008) The Amborella genome: an evolutionary reference for plant biology. Genome Biol 9:402
Soltis PS, Brockington SF, Yoo MJ, Piedrahita A, Latvis M, Moore MJ, Chanderbali AS, Soltis DE (2009) Floral variation and floral genetics in basal angiosperms. Am J Bot 96:110–128
Thien LB, White DA, Larry YY (1983) The reproductive biology of a relict-Illicium floridanum Ellis. Am J Bot 70:719–727
Thien LB, Sage T, Jaffre T, Bernhardt P, Pontieri V, Weston PH, Malloch D, Azuma H, Graham SW, McPherson MA, Rai HS, Sage RF, Dupre JL (2003) The population structure and floral biology of Amborella trichopoda (Amborellaceae). Ann Missouri Bot Gard 90:466–490
Tobe H, Jaffre T, Raven PH (2000) Embryology of Amborella (Amborellaceae): descriptions and polarity of character states. J Plant Res 113:271–280
van Schaik CP, Terborgh JW, Wright SJ (1983) The phenology of tropical forests: adaptive significance and consequences for primary consumers. Ann Rev Ecol Syst 24:353–377
von Balthazar M, Endress PK (1999) Floral bract function, flowering process and breeding systems of Sarcandra and Chloranthus (Chloranthaceae). Plant Syst Evol 218:161–178
Walters GA (1974) Araucaria (Juss.) Araucaria. Seeds of woody plants in the United States, vol 450. Forest Service, USDA, Washington DC
Whitmore TC (1977) A first look at Agathis. Tropical forestry. Commonwealth Forestry Institute, Oxford
Williams JH (2009) Amborella trichopoda (Amborellaceae) and the evolutionary developmental origins of the angiosperm progamic phase. Am J Bot 96:144–165
Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693
Zuccolo A, Bowers JE, Estill JC, Xiong Z, Luo M, Sebastian A, Goicoechea JL, Collura K, Yu Y, Jiao Y, Duarte J, Tang H, Ayyampalayam S, Rounsley S, Kudrna D, Paterson AH, Pires JC, Chanderbali A, Soltis DE, Chamala S, Barbazuk B, Soltis PS, Albert VA, Ma H, Mandoli D, Banks J, Carlson JE, Tomkins J, dePamphilis CW, Wing RA, Leebens-Mack J (2011) A physical map for the Amborella trichopoda genome sheds light on the evolution of angiosperm genome structure. Genome Biol 12:R48
Acknowledgments
The authors thank Josianne Patissou (IRD) for technical help on the field and Gildas Gâtéblé from Institut Agronomique néo-Calédonien (IAC) for hosting germination tests in the IAC greenhouses.
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Fourcade, F., Pouteau, R., Jaffré, T. et al. In situ observations of the basal angiosperm Amborella trichopoda reveal a long fruiting cycle overlapping two annual flowering periods. J Plant Res 128, 821–828 (2015). https://doi.org/10.1007/s10265-015-0744-5
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DOI: https://doi.org/10.1007/s10265-015-0744-5