Amphicarpy in Trifolium argentinense: morphological characterisation, seed production, reproductive behaviour and life strategy
Ionara Fatima Conterato A , Maria Teresa Schifino-Wittmann B D , Divanilde Guerra C and Miguel Dall’Agnol BA Fundação Estadual de Pesquisa Agropecuária, Caixa Postal 18, 97300-000, São Gabriel, Rio Grande do Sul, Brazil.
B Departamento de Plantas Forrageiras e Agrometeorologia, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Caixa Postal 15100, 91501-970, Porto Alegre, Rio Grande do Sul, Brazil.
C Departamento de Horticultura e Silvicultura, Faculdade de Agronomia, Universidade Federal do Rio Grande do Sul, Caixa Postal 15100, 91501-970, Porto Alegre, Rio Grande do Sul, Brazil.
D Corresponding author. Email: mtschif@ufrgs.br
Australian Journal of Botany 61(2) 119-127 https://doi.org/10.1071/BT12321
Submitted: 30 October 2012 Accepted: 31 January 2013 Published: 7 March 2013
Abstract
Trifolium argentinense Speg. is an amphicarpic species that occurs naturally in native pastures of Rio Grande do Sul, southern Brazil. Amphicarpy is a rare mode of reproduction in which aerial and subterranean seeds are produced by the same individual. In the present paper, we compare morphology, anther number, pollen viability, seed production and mode of reproduction of T. argentinense flowers, and comment on the life strategy of the species. Plants grown from aerial seeds and from the regrowth of storage roots of aerial plants had longer stolons and a larger plant diameter than did those grown from subterranean plants. Plants grown from seeds were also taller than plants grown from storage roots. More resources were allocated to subterranean reproduction in plants of subterranean origin than in those of aerial origin. Aerial flowers produced more seeds, presented more anthers and produced more pollen grains than did the subterranean ones. T. argentinense is a versatile species, self- and cross-pollinated, consistent with the values of high polymorphism information content. T. argentinense adopts the ‘pessimistic strategy’ (early allocation of energy to large subterranean propagules), common in amphicarpic species when growing in disturbed habitats, such as the native pastures of Rio Grande do Sul, where intense grazing and trampling, as well as long seasonal dry spells, may periodically destroy the aerial plants, thus assuring survival by germination of subterranean seeds and regrowth of storage roots.
Additional keywords: mode of reproduction, ecology, Leguminosae, pastures.
References
Auld JR, Casas RR (2012) The correlated evolution of dispersal and mating-system traits. Evolutionary Ecology.| The correlated evolution of dispersal and mating-system traits.Crossref | GoogleScholarGoogle Scholar |
Becker LCM, Schifino-Wittmann MT, Paim NR, Riboldi J (1987) Observations on the mode of reproduction of Trifolium riograndense Burkart (Leguminosae). Ciencia e Cultura 39, 304–306.
BRASIL (2009) ‘Regras para análise de sementes.’ (Ministério da Agricultura, Pecuária e Abastecimento, Secretaria de Defesa Agropecuária ACS: Brazil)
Burkart A (1952) ‘Las leguminosas argentinas silvestres y cultivadas.’ (Acme Agency: Buenos Aires)
Burkart A (1987) ‘Flora ilustrada de Entre Rios.’ (Colección Científica del INTA: Buenos Aires)
Bystricky M, Schultze-Kraft R, Peters M (2010) Studies on the pollination biology of the tropical forage legume shrub Cratylia argentea. Tropical Grasslands 44, 246–252.
Cheplick GP (1987) The ecology of amphicarpic plants. Trends in Ecology & Evolution 2, 97–101.
| The ecology of amphicarpic plants.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3M7gvFGmsg%3D%3D&md5=83188af20f45dca7ee3f55b701c832c7CAS |
Cheplick GP (1994) Life history evolution in amphicarpic plants. Plant Species Biology 9, 119–131.
| Life history evolution in amphicarpic plants.Crossref | GoogleScholarGoogle Scholar |
Cheplick GP, Quinn JA (1982) Amphicarpum purshii and the pessimistic strategy in amphicarpic annuals with subterranean fruit. Oecologia 52, 327–332.
| Amphicarpum purshii and the pessimistic strategy in amphicarpic annuals with subterranean fruit.Crossref | GoogleScholarGoogle Scholar |
Cheplick GP, Quinn JA (1987) The role of seed depth, litter, and fire in the seedling establishment of amphicarpic peanutgrass (Amphicarpum purshii). Oecologia 73, 459–464.
| The role of seed depth, litter, and fire in the seedling establishment of amphicarpic peanutgrass (Amphicarpum purshii).Crossref | GoogleScholarGoogle Scholar |
Conterato IF (2009) Caracterização de populações de Trifolium polymorphum Poir., T. argentinense Speg. e T. riograndense Burkart nativas do Rio Grande do Sul: número cromossômico, morfologia e anficarpia. PhD Thesis, Universidade Federal do Rio Grande do Sul, Porto Alegre, Rio Grande do Sul, Brazil.
Conterato IF, Schifino-Wittmann MT, Agnol MD (2010) Seed dimorphism, chromosome number and karyotype of the amphicarpic species Trifolium argentinense Speg. Genetic Resources and Crop Evolution 57, 727–731.
| Seed dimorphism, chromosome number and karyotype of the amphicarpic species Trifolium argentinense Speg.Crossref | GoogleScholarGoogle Scholar |
Dalla Rizza M, Real R, Reyno R, Quesenberry KH (2005) Use of cross-species amplification markers for pollen-mediated gene flow determination in Trifolium polymorphum Poiret. In ‘Molecular breeding for the genetic improvement of forage crops and turf. Proceeding of the 20th International Grassland Congress’, Aberystwyth, Wales, July 2005. (Ed. MO Humpheys) pp. 194.
Dalla Rizza M, Real D, Reyno R, Porro V, Burgueno J, Errico E, Quesenberry KH (2007) Genetic diversity and ADN content of three South American and three eurasiatic Trifolium species. Genetics and Molecular Biology 30, 1118–1124.
| Genetic diversity and ADN content of three South American and three eurasiatic Trifolium species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFKrtbs%3D&md5=c135f5a267cfc30c7e64fbba70c6b570CAS |
Dias PMB, Julier B, Sampoux JP, Barre P, Dall’Agno LM (2008) Genetic diversity in red clover (Trifolium pratense L.) revealed by morphological and microsatellite (SSR) markers. Euphytica 160, 189–205.
| Genetic diversity in red clover (Trifolium pratense L.) revealed by morphological and microsatellite (SSR) markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1SgsrY%3D&md5=9f68d28769bfc1ae026a52433ce15e20CAS |
Doyle JJ, Doyle JL (1987) Isolation of plant DNA from fresh tissue. Focus 12, 13–15.
Kappel A (1967) ‘Os trevos: espécies do gênero Trifolium.’ (Secretaria da Agricultura do Rio Grande do Sul: Porto Alegre, Brazil)
Kaul V, Koul AK, Sharma MC (2000) The underground flower. Current Science 78, 39–44.
Kaul V, Sharma N, Koul AK (2002) Reproductive effort and sex allocation strategy in Commelina benghalensis L., a common monsoon weed. Biological Journal of the Linnean Society, London 140, 403–413.
Le Corff J, Horvitz CC (2005) Population growth versus population spread of ant-dispersed neotropical herb with a mixed reproductive strategy. Ecological Modelling 188, 41–51.
| Population growth versus population spread of ant-dispersed neotropical herb with a mixed reproductive strategy.Crossref | GoogleScholarGoogle Scholar |
Lev-Yadun S (2000) Why are undergrownd flowering and fruiting more common in Israel than anywhere else in the world? Current Science 79, 289
Liang ZC, Yang JI, Rao GY (2007) Development of microsatellite markers in an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae). Molecular Ecology 7, 863–865.
| Development of microsatellite markers in an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1ertLjO&md5=c1c485e62f7e94c589a0da14404e1a63CAS |
Nikolic N, Kraft RS, Rodriguez I (2005) ‘Amphicarpy in perrenials: Centrosema rotundifolium.’ Tropentag 2005, The Global Food and Prooduct Chain: Dynamics, Innovations, Conflicts, Strategies, Sttutgart, Germany. Section: Biodiversity and Land Rehabilitation in the Tropics and Subtropics. Available at http://www.tropentag.de/2005/abstracts/posters/391.pdf [verified 11 September 2012].
Porto A (1954) História das missões orientais do Uruguai. (Livraria Selbach: Porto Alegre, Brazil)
Real D, Dalla Rizza M, Reyno R, Quesenberry KH (2007) Breeding system of the aerial flowers in an amphicarpic clover species: Trifolium polymorphum. Crop Science 47, 1401–1406.
| Breeding system of the aerial flowers in an amphicarpic clover species: Trifolium polymorphum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsF2rtLs%3D&md5=d4f8ad80ded3d7a8c30c3d3d3285483aCAS |
Schultze-Kraft R, Schmidt A, Hohn H (1997) Amphicarpic legumes for tropical pasture persistence. In ‘Proceedings of the XVIII international grassland congress’, Winnipeg and Saskatoon, Canada, 8–19 June 1997. pp. 13–14. Available at http://www.internationalgrasslands.org/files/igc/publications/1997/1-01-013.pdf [verified September 2012].
Simioni C, Schifino-Wittmann MT, Dall’Agnol M, Guerra D (2004) Selection for increasing 2n gametes production in red clover. Crop Breeding and Applied Biotechnology 4, 477–483.
Speroni G, Izaguirre P (2003) Características biológicas de la leguminosa nativa promissora forrajera Trifolium polymorphum Poir. (Fabaceae, Faboideae). Agrociencia 7, 68–76.
Speroni G, Izaguirre P, Bernardello G (2010) Sobre las causas ontogenéticas de la productividad diferencial de semillas en la especie anficárpica Trifolium polymorphum (Leguminosae). Boletín de la Sociedad Argentina de Botánica 45, 57–72.
Tedesco SB, Dall Agnol M, Schifino-Wittmann MT (1998) Observações sobre modo de reprodução em Adesmia latifolia Spreng. Vog. Ciência Rural 28, 141–142.
| Observações sobre modo de reprodução em Adesmia latifolia Spreng. Vog.Crossref | GoogleScholarGoogle Scholar |
Tedesco SB, Dall Agnol M, Schifino-Wittmann MT, Valls JFM (2000) Mode of reproduction of Brazilian species of Adesmia (Leguminosae). Genetics and Molecular Biology 23, 475–478.
| Mode of reproduction of Brazilian species of Adesmia (Leguminosae).Crossref | GoogleScholarGoogle Scholar |
Trapp EJ, Hendrix SD (1988) Consequences of a mixed reproductive system in the hog peanut, Amphicarpaea bracteata (Fabaceae). Oecologia 75, 285–290.
| Consequences of a mixed reproductive system in the hog peanut, Amphicarpaea bracteata (Fabaceae).Crossref | GoogleScholarGoogle Scholar |
Weiss PW (1980) Germination, reproductive and interference in the amphicarpic annual Emex spinosa (L.) Campb. Oecologia 45, 244–251.
| Germination, reproductive and interference in the amphicarpic annual Emex spinosa (L.) Campb.Crossref | GoogleScholarGoogle Scholar |
Zeide B (1978) Reproductive behavior of plants in time. American Naturalist 112, 636–639.
| Reproductive behavior of plants in time.Crossref | GoogleScholarGoogle Scholar |
Zhang Y, Yang J, Rao GY (2005) Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers. Biochemical Systematics and Ecology 33, 1246–1257.
| Genetic diversity of an amphicarpic species, Amphicarpaea edgeworthii Benth. (Leguminosae) based on RAPD markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1aqu7%2FI&md5=cd586a059e963a506b818f9d203bb738CAS |