Diversity for morphological traits, flowering time and leaf isoflavone content among ecotypes of Trifolium subterraneum L. subsp. yanninicum and their relationships with site of origin
Gereltsetseg Enkhbat
A B * , Phillip G. H. Nichols A , Kevin J. Foster A , Megan H. Ryan A , Yoshiaki Inukai B and William Erskine A
+ Author Affiliations
- Author Affiliations
A UWA School of Agriculture and Environment and Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
B Graduate School of Bioagricultural Science at Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Japan.
Crop & Pasture Science 72(12) 1022-1033 https://doi.org/10.1071/CP21226
Submitted: 29 March 2021 Accepted: 13 July 2021 Published: 1 December 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution 4.0 International License (CC BY)
Abstract
Trifolium subterraneum L. subsp. yanninicum is a pasture legume that is widely grown in medium and high rainfall areas of southern Australia and shows waterlogging tolerance. This study investigated diversity within subsp. yanninicum corresponding to eco-geographic variables, which may help to identify adapted parents with new traits for genetic improvement. Diversity for 10 morphological traits, flowering time and leaf isoflavone content was investigated using 108 ecotypes derived from wild Mediterranean populations and 10 cultivars, grown as spaced plants. Among the ecotypes, the range of flowering time was 94–149 days after sowing, and contents of formononetin, genistein and biochanin A were 0.05–1.38%, 0.73–2.33% and 0.15–2.10% of dry matter, respectively. Leaf markings also varied considerably. Leaf size and petiole length were correlated at each growth stage. Later flowering genotypes had larger leaves, longer petioles, longer internodes and thicker stems at flowering, but smaller leaves and shorter petioles at both 63 and 88 days after sowing. Contents of genistein and biochanin A were unrelated, but both were negatively associated with formononetin. Flowering time had a weak positive influence on genistein and biochanin A, but a weak negative influence on formononetin. All traits among the ecotypes (except stem diameter and leaf mark crescent size) were significantly correlated with at least one of 22 eco-geographic variables from their collection sites. Precipitation and altitude were more influential than temperature. The study found sufficient diversity to broaden the narrow genetic base of current subsp. yanninicum cultivars; however, other agronomically important traits also need to be considered. Further diversity may result from targeted collection, particularly in areas not represented in annual legume genebanks.
Keywords: eco-geographic variables, genetic resources, genotypic diversity, leaf marks, morphological traits, oestrogenic compounds, pasture legume, subterranean clover.
References
Abdi AI, Nichols PGH, Kaur P, Wintle BJ, Erskine W (2020) Morphological diversity within a core collection of subterranean clover (Trifolium subterraneum L.): lessons in pasture adaptation from the wild. PloS One 15, e0223699| Morphological diversity within a core collection of subterranean clover (Trifolium subterraneum L.): lessons in pasture adaptation from the wild.Crossref | GoogleScholarGoogle Scholar | 31914457PubMed |
Aitken Y, Drake FR (1941) Studies on the varieties of subterranean clover. Proceedings of the Royal Society of Victoria 53, 342–393.
Bennett SJ (2000) Genetic variation of five species of Trifolium L. from south-west Turkey. Genetic Resources and Crop Evolution 47, 81–91.
| Genetic variation of five species of Trifolium L. from south-west Turkey.Crossref | GoogleScholarGoogle Scholar |
Bennett SJ, Bullitta S (2003) Ecogeographical analysis of the distribution of six Trifolium species in Sardinia. Biodiversity and Conservation 12, 1455–1466.
| Ecogeographical analysis of the distribution of six Trifolium species in Sardinia.Crossref | GoogleScholarGoogle Scholar |
Bennetts HW, Uuderwood EJ, Shier FL (1946) A specific breeding problem of sheep on subterranean clover pastures in Western Australia. Australian Veterinary Journal 22, 2–12.
| A specific breeding problem of sheep on subterranean clover pastures in Western Australia.Crossref | GoogleScholarGoogle Scholar | 21028682PubMed |
Black JN (1960) The significance of petiole length, leaf area, and light interception in competition between strains of subterrranean clover (Trifolium subterraneum L.) grown in swards. Australian Journal of Agricultural Research 11, 277–291.
| The significance of petiole length, leaf area, and light interception in competition between strains of subterrranean clover (Trifolium subterraneum L.) grown in swards.Crossref | GoogleScholarGoogle Scholar |
Brightling A (2006) ‘Livestock diseases in Australia: diseases of cattle, sheep, goats and farm dogs’, (CH Jerram & Associates: Mount Waverley, Vic., Australia)
Chapman SC, Chakraborty SM, Dreccer MF, Howden SM (2012) Plant adaptation to climate change-opportunities and priorities in breeding. Crop & Pasture Science 63, 251–268..
| Plant adaptation to climate change-opportunities and priorities in breeding.Crossref | GoogleScholarGoogle Scholar |
Cocks PS (1992) Evolution in sown populations of subterranean clover (Trifolium subterraneum L.) in South Australia. Australian Journal of Agricultural Research 43, 1583–1595.
| Evolution in sown populations of subterranean clover (Trifolium subterraneum L.) in South Australia.Crossref | GoogleScholarGoogle Scholar |
Collins WJ, Cox RI (1984) Oestrogenic activity in forage legumes. In ‘Forage legumes for energy efficient animal production. Proceedings of a trilateral workshop’. Palmerston North, New Zealand. (Eds RF Barnes, PR Ball, RW Brougham, GC Mearten, DJ Minson) (USDA-ARS: Springfield VA, USA)
Craig A (1992) Pasture production of two cultivars of Trifolium subterraneum at Kybybolite, South Australia. Australian Journal of Experimental Agriculture 32, 611–617.
| Pasture production of two cultivars of Trifolium subterraneum at Kybybolite, South Australia.Crossref | GoogleScholarGoogle Scholar |
Davidson JL, Donald CM (1958) The growth of swards of subterranean clover with particular reference to leaf area. Australian Journal of Agricultural Research 9, 53–72.
| The growth of swards of subterranean clover with particular reference to leaf area.Crossref | GoogleScholarGoogle Scholar |
Davies LH (1986) Limitations to livestock production associated with phytoestrogens and bloat. In ‘Temperate pastures: their production, use and management’. (Eds JL Wheeler, CJ Pearson, GE Robards) pp. 446–456. (Australian Wool Corporation/CSIRO Australia: Melbourne, Vic., Australia)
Dear BS, Sandral GA, Peoples MB, Wilson BCD, Taylor JN, Rodham CA (2003) Growth, seed set and nitrogen fixation of 28 annual legume species on 3 Vertosol soils in southern New South Wales. Animal Production Science 43, 1101–1115.
| Growth, seed set and nitrogen fixation of 28 annual legume species on 3 Vertosol soils in southern New South Wales.Crossref | GoogleScholarGoogle Scholar |
Devitt AC, Francis CM (1972) The effect of waterlogging on the mineral nutrient content of ‘Trifolium subterraneum’. Australian Journal of Experimental Agriculture 12, 614
| The effect of waterlogging on the mineral nutrient content of ‘Trifolium subterraneum’.Crossref | GoogleScholarGoogle Scholar |
Ehrman T, Cocks PS (1996) Reproductive patterns in annual legume species on an aridity gradient. Vegetatio 122, 47–59.
| Reproductive patterns in annual legume species on an aridity gradient.Crossref | GoogleScholarGoogle Scholar |
Enkhbat G, Ryan MH, Foster KJ, Nichols PGH, Kotula L, Hamblin A, Inukai Y, Erskine W (2021) Large variation in waterlogging tolerance and recovery among the three subspecies of Trifolium subterranean L. is related to root and shoot responses. Plant and Soil 464, 467–487.
| Large variation in waterlogging tolerance and recovery among the three subspecies of Trifolium subterranean L. is related to root and shoot responses.Crossref | GoogleScholarGoogle Scholar |
Erskine W, Adham Y, Holly L (1989) Geographic distribution of variation in quantitative traits in a world lentil collection. Euphytica 43, 97–103.
| Geographic distribution of variation in quantitative traits in a world lentil collection.Crossref | GoogleScholarGoogle Scholar |
Falconer DS, Mackay TFC (1996) ‘Introduction to quantitative genetics’, 4th edn. (Pearson/Longman: England)
Francis CM (1976) ‘Observations on the ecology of subterranean clover in Greece and Crete: a report based on a seed collection tour 1976’, (Western Australian Department of Agriculture: Perth, WA, Australia)
Francis CM, Devitt AC (1969) The effect of waterlogging on the growth and isoflavone concentration of Trifolium subterraneum L. Australian Journal of Agricultural Research 20, 819–825.
| The effect of waterlogging on the growth and isoflavone concentration of Trifolium subterraneum L.Crossref | GoogleScholarGoogle Scholar |
Francis CM, Millington AJ (1965) Varietal variation in the isoflavone content of subterranean clover: its estimation by a microtechnique. Australian Journal of Agricultural Research 16, 557
| Varietal variation in the isoflavone content of subterranean clover: its estimation by a microtechnique.Crossref | GoogleScholarGoogle Scholar |
Francis CM, Devitt AC, Steele P (1974) Influence of flooding on the alcohol dehydrogenase activity of roots of Trifolium subterraneum L. Australian Journal of Plant Physiology 1, 9–13.
| Influence of flooding on the alcohol dehydrogenase activity of roots of Trifolium subterraneum L.Crossref | GoogleScholarGoogle Scholar |
Ghamkhar K, Snowball R, Bennett SJ (2007) Ecogeographical studies identify diversity and potential gaps in the largest germplasm collection of bladder clover (Trifolium spumosum L.). Australian Journal of Agricultural Research 58, 728–738.
| Ecogeographical studies identify diversity and potential gaps in the largest germplasm collection of bladder clover (Trifolium spumosum L.).Crossref | GoogleScholarGoogle Scholar |
Ghamkhar K, Isobe S, Nichols PGH, Faithfull T, Ryan MH, Snowball R, Sato S, Appels R (2012) The first genetic maps for subterranean clover (Trifolium subterraneum L.) and comparative genomics with T. pratense L. and Medicago truncatula Gaertn. to identify new molecular markers for breeding. Molecular Breeding 30, 213–226.
| The first genetic maps for subterranean clover (Trifolium subterraneum L.) and comparative genomics with T. pratense L. and Medicago truncatula Gaertn. to identify new molecular markers for breeding.Crossref | GoogleScholarGoogle Scholar |
Ghamkhar K, Nichols PGH, Erskine W, Snowball R, Murillo M, Appels R, Ryan MH (2015) Hotspots and gaps in the world collection of subterranean clover (Trifolium subterraneum L.). Journal of Agricultural Science 153, 1069–1083.
| Hotspots and gaps in the world collection of subterranean clover (Trifolium subterraneum L.).Crossref | GoogleScholarGoogle Scholar |
Gibberd MR, Cocks PS (1997) Effect of waterlogging and soil pH on the micro-distribution of naturalised annual legumes. Australian Journal of Agricultural Research 48, 223–230.
| Effect of waterlogging and soil pH on the micro-distribution of naturalised annual legumes.Crossref | GoogleScholarGoogle Scholar |
Gladstones JS (1967) Naturalized subterranean clover strains in Western Australia: a preliminary agronomic examination. Australian Journal of Agricultural Research 18, 713–731.
| Naturalized subterranean clover strains in Western Australia: a preliminary agronomic examination.Crossref | GoogleScholarGoogle Scholar |
Gladstones JS, Collins WJ (1984) Naturalized subterranean clover strains of Western Australia. Technical Bulletin No. 64. Western Australian Department of Agriculture, Perth, WA, Australia.
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 1965–1978.
| Very high resolution interpolated climate surfaces for global land areas.Crossref | GoogleScholarGoogle Scholar |
Hill MJ (1996) Defining the white clover zone in eastern mainland Australia using a model and a geographic information system. Ecological Modelling 86, 245–252.
| Defining the white clover zone in eastern mainland Australia using a model and a geographic information system.Crossref | GoogleScholarGoogle Scholar |
Hungerford T (1975) ‘Diseases of livestock’, (McGraw-Hill: Sydney, NSW, Australia)
Katznelson JS (1966) Report on seed collection tour in Greece, Yugoslavia and northern Italy. Technical Pamphlet No. 101. Volcani Institute, Israel.
Katznelson J, Morley FHW (1965) A taxonomic revision of sect. Calycomorphum of the genus Trifolium. I. The geocarpic species. Israel Journal of Botany 14, 112–134.
Marshall T, Millington A (1967) Flooding tolerance of some Western Australian pasture legumes. Australian Journal of Experimental Agriculture 7, 367–371.
| Flooding tolerance of some Western Australian pasture legumes.Crossref | GoogleScholarGoogle Scholar |
Millington AJ, Francis CM, McKeown NR (1964) Wether bioassay of annual pasture legumes. II. The oestrogenic activity of nine strains of Trifolium subterraneum L. Australian Journal of Agricultural Research 15, 527
Morley FHW, Francis CM (1968) Varietal and environmental variations in isoflavone concentrations in subterranean clover (L.). Australian Journal of Agricultural Research 19, 15–26.
| Varietal and environmental variations in isoflavone concentrations in subterranean clover (L.).Crossref | GoogleScholarGoogle Scholar |
Mousavi-Derazmahalleh M, Bayer PE, Nevado B, Hurgobin B, Filatov D, Kilian A, Kamphuis LG, Singh KB, Berger JD, Hane JK, Edwards D, Erskine W, Nelson MN (2018) Exploring the genetic and adaptive diversity of a pan-Mediterranean crop wild relative: narrow-leafed lupin. Theoretical and Applied Genetics 131, 887–901.
| Exploring the genetic and adaptive diversity of a pan-Mediterranean crop wild relative: narrow-leafed lupin.Crossref | GoogleScholarGoogle Scholar | 29353413PubMed |
Nichols PGH (2013) Development of R&D pre-breeding plans for annual legumes. Report preperad for Meat & Livestock Australia for project P.BE.0028. Available at https://www.mla.com.au/research-and-development/reports/2014/development-of-rd-plans-for-annual-legumes/
Nichols PGH, Collins WJ, Barbetti MJ (1996) Registered cultivars of subterranean clover: their characteristics, origin and identification. Bulletin No. 4327. Agriculture Western Australia, Perth, WA, Australia.
Nichols PGH, Cocks PS, Francis CM (2009) Evolution over 16 years in a bulk-hybrid population of subterranean clover (Trifolium subterraneum L.) at two contrasting sites in south-western Australia. Euphytica 169, 31–48.
| Evolution over 16 years in a bulk-hybrid population of subterranean clover (Trifolium subterraneum L.) at two contrasting sites in south-western Australia.Crossref | GoogleScholarGoogle Scholar |
Nichols PGH, Loi A, Nutt BJ, Evans PM, Craig AD, Pengelly BC, Dear BS, Lloyd DL, Revell CK, Nair RM, Ewing MA, Howieson JG, Auricht GA, Howie JH, Sandral GA, Carr SJ, De Koning CT, Hackney BF, Crocker GJ, Snowball R, Hughes SJ, Hall EJ, Foster KJ, Skinner PW, Barbetti MJ, You MP (2007) New annual and short-lived perennial pasture legumes for Australian agriculture: 15 years of revolution. Field Crops Research 104, 10–23.
| New annual and short-lived perennial pasture legumes for Australian agriculture: 15 years of revolution.Crossref | GoogleScholarGoogle Scholar |
Nichols P, Loi A, Nutt B, Snowball R, Revell C (2010) Domestication of new mediterranean annual pasture legumes. In ‘Sustainable use of genetic diversity in forage and turf breeding’. pp. 137–141. (Springer: Dordrecht, Netherlands)
Nichols PGH, Revell CK, Humphries AW, Howie JH, Hall EJ, Sandral GA, Ghamkhar K, Harris CA (2012) Temperate pasture legumes in Australia – their history, current use, and future prospects. Crop & Pasture Science 63, 691–725.
| Temperate pasture legumes in Australia – their history, current use, and future prospects.Crossref | GoogleScholarGoogle Scholar |
Nichols PGH, Foster KJ, Piano E, Pecetti L, Kaur P, Ghamkhar K, Collins WJ (2013) Genetic improvement of subterranean clover (Trifolium subterraneum L.). 1. Germplasm, traits and future prospects. Crop & Pasture Science 64, 312–346.
| Genetic improvement of subterranean clover (Trifolium subterraneum L.). 1. Germplasm, traits and future prospects.Crossref | GoogleScholarGoogle Scholar |
Oram RN (1989) ‘Register of Australian herbage plant cultivars’, (Australian Herbage Plant Registration Authority, Division of Plant Industry, CSIRO: Melbourne, Vic., Australia)
PBR (2021) Plant Breeders Rights database. IP Australia, Australian Government, Canberra, ACT, Australia. Available at https://www.ipaustralia.gov.au/plant-breeders-rights [Accessed 12 January 2021]
Pecetti L, Piano E (1993) Influence of the environment of origin on early dry matter yield and plant morphology in subterranean clover. In ‘Management of Mediterranean shrublands and related forage resources’. REUR Technical Series 28. pp. 20–23. (FAO: Rome, Italy)
Pecetti L, Piano E (1997) Leaf size variation in subterranean clover (Trifolium subterraneum L. sensu lato. Genetic Resources and Crop Evolution 45, 161–165.
| Leaf size variation in subterranean clover (Trifolium subterraneum L. sensu lato.Crossref | GoogleScholarGoogle Scholar |
Pecetti L, Piano E (2002) Variation of morphological and adaptive traits in subterranean clover populations from Sardinia (Italy). Genetic Resources and Crop Evolution 49, 189–197.
| Variation of morphological and adaptive traits in subterranean clover populations from Sardinia (Italy).Crossref | GoogleScholarGoogle Scholar |
Pecetti L, Carroni AM, Annicchiarico P (2020) Performance and adaptability of subterranean clover pure lines and line mixtures of different complexity across contrasting Mediterranean environments. Field Crops Research 256, 107907
| Performance and adaptability of subterranean clover pure lines and line mixtures of different complexity across contrasting Mediterranean environments.Crossref | GoogleScholarGoogle Scholar |
Piano E (1984) Preliminary observations on the structure and variability of Sardinian populations of subterranean clover. Genetica Agraria 38, 75–90.
Piano E, Spanu F, Pecetti L (1993) Structure and variation of subterranean clover populations from Sicily, Italy. Euphytica 68, 43–51.
| Structure and variation of subterranean clover populations from Sicily, Italy.Crossref | GoogleScholarGoogle Scholar |
Piano E, Pecetti L, Carroni AM (1996) Climatic adaptation in subterranean clover populations. Euphytica 92, 39–44.
| Climatic adaptation in subterranean clover populations.Crossref | GoogleScholarGoogle Scholar |
Porqueddu C, Ates S, Louhaichi M, Kyriazopoulos AP, Moreno G, Pozo A, Ovalle C, Ewing MA, Nichols PGH (2016) Grasslands in ‘Old World’ and ‘New World’ Mediterranean-climate zones: past trends, current status and future research priorities. Grass and Forage Science 71, 1–35.
| Grasslands in ‘Old World’ and ‘New World’ Mediterranean-climate zones: past trends, current status and future research priorities.Crossref | GoogleScholarGoogle Scholar |
Reed KFM, Schroder PM, Eales JW, McDonald RM, Chin JF (1985) Comparative productivity of Trifolium subterraneum and T. yanninicum in south-western Victoria. Australian Journal of Experimental Agriculture 25, 351–361.
| Comparative productivity of Trifolium subterraneum and T. yanninicum in south-western Victoria.Crossref | GoogleScholarGoogle Scholar |
Revell CK, Ewing MA, Nutt BJ (2012) Breeding and farming system opportunities for pasture legumes facing increasing climate variability in the south-west of Western Australia. Crop & Pasture Science 63, 840–847.
| Breeding and farming system opportunities for pasture legumes facing increasing climate variability in the south-west of Western Australia.Crossref | GoogleScholarGoogle Scholar |
Rossiter RC (1959) The influence of maturity grading on total yield and seed production in strains of Trifolium subterraneum L. grown as single plants and in swards. Australian Journal of Agricultural Research 10, 305
| The influence of maturity grading on total yield and seed production in strains of Trifolium subterraneum L. grown as single plants and in swards.Crossref | GoogleScholarGoogle Scholar |
Rosso BS, Pagano EM (2005) Evaluation of introduced and naturalised populations of red clover (Trifolium pratense L.) at Pergamino EEA-INTA, Argentina. Genetic Resources and Crop Evolution 52, 507–511.
| Evaluation of introduced and naturalised populations of red clover (Trifolium pratense L.) at Pergamino EEA-INTA, Argentina.Crossref | GoogleScholarGoogle Scholar |
Tan BH, Collins WJ (1987) Multi-allelic nature of the locus controlling leaf marking in subterranean clover. Australian Journal of Agricultural Research 38, 547–558.
Tucak M, Cupic T, Popovic S, Stjepanovi M, Gantner R, Meglic V (2009) Agronomic evaluation and utilization of red clover (Trifolium pratense L.) germplasm. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 37, 206–210.
| Agronomic evaluation and utilization of red clover (Trifolium pratense L.) germplasm.Crossref | GoogleScholarGoogle Scholar |
Williams R, Evans L, Ludwig L (1964) Estimation of leaf area for clover and lucerne. Australian Journal of Agricultural Research 15, 231–233.
| Estimation of leaf area for clover and lucerne.Crossref | GoogleScholarGoogle Scholar |
Zohary M, Heller D (1984) ‘The genus Trifolium’, (The Israel Academy of Science and Humanities: Jerusalem, Israel)
