Embryogenesis and plant regeneration of the perennial pasture and medicinal legume Bituminaria bituminosa (L.) C.H. Stirton
M. Pazos-Navarro A , J. S. Croser B , M. Castello B , P. Ramankutty C , K. Heel D , D. Real B C E , D. J. Walker A , E. Correal A and M. Dabauza A FA Instituto Murciano de Investigación y Desarrollo Agrario y Alimentario (IMIDA), C/Mayor s/n, 30150-La Alberca, Murcia, Spain.
B Centre for Plant Genetics and Breeding, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
C School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
D Centre for Microscopy, Characterisation and Analysis, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.
E Department of Agriculture and Food, Western Australia, South Perth, WA 6151, Australia.
F Corresponding author. Email: mercedes.dabauza@carm.es
Crop and Pasture Science 65(9) 934-943 https://doi.org/10.1071/CP14083
Submitted: 17 March 2014 Accepted: 19 June 2014 Published: 15 August 2014
Abstract
Bituminaria bituminosa (common name tedera) is a drought-tolerant perennial pasture species of agronomic and pharmaceutical interest for Mediterranean climates. Considering the importance of this legume, in vitro experiments were conducted to develop protocols for plant regeneration from embryogenic calli of leaves, petioles and anthers to efficiently exploit and maintain selected important clones from the tedera breeding program. The type of explant was a key factor in the frequency of embryogenesis and the number of embryos per callus. For plant regeneration from cultured anthers, appropriate anther physiological state (uninucleate stage of microsporogenesis), stress treatments (electroporation, 25 Ω, 25 µF, 1500 V) and culture conditions were determined. A robust flow-cytometry method was developed to analyse the ploidy status of callus, in vitro shoots and in vivo acclimatised plants derived from anther and leaf explants.
Additional keywords: androgenesis, flow cytometry, forage, furanocoumarins, haploid, somatic embryos.
References
Ahmad M, Fautrer AG, McNeil V, Hill GD, Burrit DJ (1997) In vitro propagation of Lens species and their F1 interspecific hybrids. Plant Cell, Tissue and Organ Culture 47, 169–176.| In vitro propagation of Lens species and their F1 interspecific hybrids.Crossref | GoogleScholarGoogle Scholar |
Baskaran P, Jayabalan N (2009) In vitro propagation of Psoralea corylifolia L. by somatic embryogenesis in cell suspension culture. Acta Physiologiae Plantarum 31, 1119–1127.
| In vitro propagation of Psoralea corylifolia L. by somatic embryogenesis in cell suspension culture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlSqs77J&md5=3120db130af00f92e9c9f6598b5aa5a7CAS |
Blaydes DF (1966) Interaction of kinetin and various inhibitors in the growth of soybean tissue. Physiologia Plantarum 19, 748–753.
| Interaction of kinetin and various inhibitors in the growth of soybean tissue.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF28XkvVGhsb0%3D&md5=50163edd8704308fb52e14b9ff6e9989CAS |
Chand S, Sahrawat AK (2002) Somatic embryogenesis and plant regeneration from segments of Psoralea corylifolia L., an endangered medicinally important plant. In vitro Cell and Developmental Biology–Plant 38, 33–38.
| Somatic embryogenesis and plant regeneration from segments of Psoralea corylifolia L., an endangered medicinally important plant.Crossref | GoogleScholarGoogle Scholar |
Cousin A, Heel K, Cowling WA, Nelson MN (2009) An efficient high-throughput flow cytometric method for estimating DNA ploidy level in plants. Cytometry 75A, 1015–1019.
| An efficient high-throughput flow cytometric method for estimating DNA ploidy level in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkt1yktA%3D%3D&md5=85d3f740d1cdb9264b8e1333cfe3ef4aCAS |
Croser JS, Lülsdorf MM, Lülsdorf MA, Clarke HJ, Bayliss KL, Mallikarjuna N, Siddique KHM (2006) Towards doubled haploid production in the Fabaceae: progress, constraints, and opportunities. Critical Reviews in Plant Sciences 25, 139–157.
| Towards doubled haploid production in the Fabaceae: progress, constraints, and opportunities.Crossref | GoogleScholarGoogle Scholar |
Croser JS, Lulsdorf MM, Grewal RK, Usher KM, Siddique KHM (2011) Isolated microspore culture of chickpea (Cicer arietinum L.): induction of androgensis and cytological analysis of early haploid divisions. In Vitro Cellular and Developmental Biology – Plant 47, 357–368.
Delaitre C, Ochatt SJ, Deleury E (2001) Electroporation modulates the embryogenic responses of aspargus (Asparagus officinalis L.) microspores. Protoplasma 216, 39–46.
| Electroporation modulates the embryogenic responses of aspargus (Asparagus officinalis L.) microspores.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mnos1OlsQ%3D%3D&md5=4674cea4c390dc67bf310aa72da3079dCAS | 11732195PubMed |
Fennell A, Hauptmann R (1992) Electroporation and PEG delivery of DNA into maize microspores. Plant Cell Reports 11, 567–570.
| Electroporation and PEG delivery of DNA into maize microspores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhslSrtA%3D%3D&md5=ee79fdcef7f522551f28a1e2468057deCAS | 24213288PubMed |
Ferrie AMR, Möllers C (2011) Haploids and doubled haploids in Brassica ssp. for genetic and genomic research. Plant Cell, Tissue and Organ Culture 104, 375–386.
| Haploids and doubled haploids in Brassica ssp. for genetic and genomic research.Crossref | GoogleScholarGoogle Scholar |
Fratini R, Ruiz ML (2002) Comparative study of different cytokinins in the induction of morphogenesis in lentil (Lens culinaris Medik). In Vitro Cellular & Developmental Biology. Plant 38, 46–51.
| Comparative study of different cytokinins in the induction of morphogenesis in lentil (Lens culinaris Medik).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmsFahurw%3D&md5=749f732d1df415c7688e17e57799016fCAS |
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Experimental Cell Research 50, 151–158.
| Nutrient requirements of suspension cultures of soybean root cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF1cXktVyqtLw%3D&md5=85eb3727a0052a15fdfe6e8a398d89f2CAS | 5650857PubMed |
Greilhuber J (1988) ‘Self-tanning’—a new and important source of stoichiometric error in cytophotometric determination of nuclear DNA content in plants. Plant Systematics and Evolution 158, 87–96.
| ‘Self-tanning’—a new and important source of stoichiometric error in cytophotometric determination of nuclear DNA content in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXitFynur0%3D&md5=48ad0e5aa8b7820457ab3b3a637c5727CAS |
Grewal R, Lülsdorf M, Croser J, Ochatt S, Vandenberg A, Warkentin T (2009) Doubled haploid production in chickpea (Cicer arietinum L.): role of stress treatments. Plant Cell Reports 28, 1289–1299.
| Doubled haploid production in chickpea (Cicer arietinum L.): role of stress treatments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptFGmtLc%3D&md5=e3dbc42d327f889bf260b43e064493feCAS | 19543732PubMed |
Haydu Z, Vasil IK (1981) Somatic embryogenesis and plant regeneration from leaf tissue and anthers of Penisetum purpureum Schum. Theoretical and Applied Genetics 59, 269–273.
| Somatic embryogenesis and plant regeneration from leaf tissue and anthers of Penisetum purpureum Schum.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2c3gslertg%3D%3D&md5=fe1ab5eb5477b14066a09236a7a9f6f8CAS | 24276510PubMed |
Heinze B, Schmidt J (1995) Monitoring genetic fidelity vs somaclonal variation in Norway spruce (Picea abies) somatic embryogenesis by RAPD analysis. Euphytica 85, 341–345.
| Monitoring genetic fidelity vs somaclonal variation in Norway spruce (Picea abies) somatic embryogenesis by RAPD analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitlGqsA%3D%3D&md5=13dbc0074fafc41a286ebd12671cd5f7CAS |
Innocenti G, Capelleti EM, Caporale G (1991) Furocoumarin contents in the vegetative organs of cultivated Psoralea species. International Journal of Pharmacology 29, 141–146.
Innocenti G, Piovan A, Filippini R, Caniato R, Capelleti EM (1997) Quantitative recovery of furanocoumarins from Psoralea bituminosa. Phytochemical Analysis 8, 84–86.
| Quantitative recovery of furanocoumarins from Psoralea bituminosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXhvFygurc%3D&md5=ce84d0d175b4b1b7a6ddd1d697ae8e5cCAS |
Jardinaud MF, Souvré A, Alibert G (1993) Transient GUS gene expression in Brassica napus electroporated microspores. Plant Science 93, 177–184.
| Transient GUS gene expression in Brassica napus electroporated microspores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXitlOiu74%3D&md5=8f4a27e08abebade70ed9a54227cc8e0CAS |
Jones RAC, Real D, Vincent SJ, Gajda BE, Coutts BA (2012) First report of Alfalfa mosaic virus infecting tedera (Bituminaria bituminosa (L.) C.H. Stirton var. albomarginata and crassiuscula) in Australia. Plant Disease 96, 1384
| First report of Alfalfa mosaic virus infecting tedera (Bituminaria bituminosa (L.) C.H. Stirton var. albomarginata and crassiuscula) in Australia.Crossref | GoogleScholarGoogle Scholar |
Laurain D, Trémouillaux-Guiller J, Chénieux JC (1993) Embryogenesis from microspores of Ginkgo biloba L., a medicinal woody species. Plant Cell Reports 12, 501–505.
Malik KA, Saxena PK (1992) Thidiazuron induces high frequency shoot regeneration in intact seedlings of pea (Pisum sativum), chickpea (Cicer arietinum) and lentil (Lens culinaris). Australian Journal of Plant Physiology 19, 731–740.
| Thidiazuron induces high frequency shoot regeneration in intact seedlings of pea (Pisum sativum), chickpea (Cicer arietinum) and lentil (Lens culinaris).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhs1eis7Y%3D&md5=de1f50a57f62ac5a747a6cc2607e3928CAS |
Maluszynski M, Kasha KJ, Szarejko I (2003) Published doubled haploid protocols in plant species. In ‘Doubled haploid production in crop plants; A manual’. (Eds M Maluszynski, KJ Kasha, BP Forster, I Szarejko) pp. 309–335. (Kluwer Academic Publishers: Dordrecht, The Netherlands)
Martínez S, Correal E, Real D, Ortuño A, del Río JA (2010) Bituminaria bituminosa: a source of furanocoumarins of pharmaceutical interest. In ‘Recent progress in medicinal plants (RPMP). Drug plants I’. (Eds AS Awaad, JN Govil, VK Singh) pp. 307–322. (Studium Press, LLC: Houston, TX, USA)
Maurich T, Pistelli L, Turchi G (2004) Anti-clastogenic activity of two structurally related pterocarpans purified from Bituminaria bituminosa in cultured human lymphocytes. Mutation Research – Genetic Toxicology 561, 75–81.
| Anti-clastogenic activity of two structurally related pterocarpans purified from Bituminaria bituminosa in cultured human lymphocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlsVWit7g%3D&md5=3043268193cd7cc9acf3ead9427cbbb4CAS |
Maurich T, Iorio M, Chimentu D, Turchi G (2006) Erybraedin C and bitucarpin A. Two structurally related pterocarpans purified from Bituminaria bituminosa, induced apoptosis in human colon adenocarcinoma cell lines MMR- and p53-proficient and deficient in a dose, time, and structure dependent fashion. Chemico-Biological Interactions 159, 104–116.
| Erybraedin C and bitucarpin A. Two structurally related pterocarpans purified from Bituminaria bituminosa, induced apoptosis in human colon adenocarcinoma cell lines MMR- and p53-proficient and deficient in a dose, time, and structure dependent fashion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFemsg%3D%3D&md5=0d478e110084c52794ede621d6935f32CAS | 16271357PubMed |
Mishra KP, Joshua DC, Bhatia CR (1987) In vitro electroporation of tobacco pollen. Plant Science 52, 135–139.
| In vitro electroporation of tobacco pollen.Crossref | GoogleScholarGoogle Scholar |
Morison WL (2004) Psoralen ultraviolet A therapy. Photodermatology, Photoimmunology & Photomedicine 20, 315–320.
| Psoralen ultraviolet A therapy.Crossref | GoogleScholarGoogle Scholar |
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
| A revised medium for rapid growth and bio-assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaF3sXksFKm&md5=d0744961b92749d21cd15bb6930dcf02CAS |
Ochatt SJ, Pech C, Grewal R, Conreux C, Lülsdorf M, Jacas L (2009) Abiotic stress enhances androgenesis from isolated microspores of some legume species (Fabaceae). Journal of Plant Physiology 166, 1314–1328.
| Abiotic stress enhances androgenesis from isolated microspores of some legume species (Fabaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpvVylt7s%3D&md5=5bef2588f3be98b5e1191d505b14b671CAS |
Pazos-Navarro M, del Río JA, Ortuño A, Romero-Espinar P, Correal E, Dabauza M (2012) Micropropagation from apical and nodal segments of Bituminaria bituminosa and the furanocoumarin content of propagated plants. The Journal of Horticultural Science & Biotechnology 87, 29–35.
Pazos-Navarro M, Dabauza M, Correal E, Walker DJ, del Río JA, Ortuño A, Méndez P, Santos A, Ríos S, Martínez-Frances V, Real D (2013a) Legumes for grazing and health: the case of Bituminaria bituminosa. In ‘Legumes: Types, nutritional composition and health benefits’. (Eds H Satou, R Nakamura) pp. 1–39. (Nova Science Publishers Inc.: New York)
Pazos-Navarro M, del Río JA, Ortuño A, Romero-Espinar P, Correal E, Dabauza M (2013b) Plant regeneration from different explant types of Bituminaria bituminosa and furanocoumarin content along plant regeneration stages. Plant Growth Regulation 70, 123–129.
| Plant regeneration from different explant types of Bituminaria bituminosa and furanocoumarin content along plant regeneration stages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmvVehsbg%3D&md5=8be390565f3a5c83309db2ca27b8e17bCAS |
Pistelli L, Noccioli C, Appendina G, Bianchi F, Sterner O, Ballero M (2003) Pterocarpans from Bituminaria morisiana and Bituminaria bituminosa. Phytochemistry 64, 595–598.
| Pterocarpans from Bituminaria morisiana and Bituminaria bituminosa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXms1Orsbg%3D&md5=e6e281327c3bbccc9fe41e7263f27433CAS | 12943781PubMed |
Polanco MC, Ruiz ML (1997) Effect of benzylaminopurine on in vitro and in vivo root development in lentil, Lens culinaris Medik. Plant Cell Reports 17, 22–26.
| Effect of benzylaminopurine on in vitro and in vivo root development in lentil, Lens culinaris Medik.Crossref | GoogleScholarGoogle Scholar |
Real D, Verbyla AP (2010) Maximizing genetic gains using a ‘plant’ model in the tedera (Bituminaria bituminosa var. albomarginata and var. crassiuscula) breeding program in Australia. In ‘Options Méditerranéennes: The contribution of grasslands to the conservation of Mediterranean biodiversity, Zaragoza, Spain’. Vol. 92. (Eds C Porqueddu, S Ríos Ruiz) pp. 87–96. (CIHEAM: Paris)
Real D, Correal E, Méndez P, Santos A, Ríos Ruiz S, Sternberg M, Dini-Papanastasi O, Pecetti L, Tava A (2009) Bituminaria bituminosa C.H. Stirton (synonym: Psoralea bituminosa L.). In ‘Grassland species’. (FAO: Rome) Available at: www.fao.org/ag/AGP/AGPC/doc/GBASE/new_species/tedera/bitbit.htm
Real D, Guangdi DL, Clark S, Albersten TO, Hayes RC, Denton MD, D’Antuono MF, Dear BS (2011) Evaluation of perennial forage legumes and herbs in six Mediterranean environments. Chilean Journal of Agricultural Research 71, 357–369.
| Evaluation of perennial forage legumes and herbs in six Mediterranean environments.Crossref | GoogleScholarGoogle Scholar |
Rech EL, Ochatt SJ, Chand PK, Davey MR (1987) Electro-enhancement of division of plant protoplast-derived cells. Protoplasma 141, 169–176.
| Electro-enhancement of division of plant protoplast-derived cells.Crossref | GoogleScholarGoogle Scholar |
Ribalta FM, Croser JS, Ochatt SJ (2012) Flow cytometry enables identification of sporophytic eliciting stress treatments in gametic cells. Journal of Plant Physiology 169, 104–110.
| Flow cytometry enables identification of sporophytic eliciting stress treatments in gametic cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Sgt7vF&md5=a00ed7ef7dcf1b01e593774413f013dfCAS | 22055211PubMed |
Rodrigues LR, Terra TF, Bered F, Bodanese-Zanettini MH (2004) Origin of embryo-like structures in soybean anther culture investigated using SSR marker. Plant Cell, Tissue and Organ Culture 77, 287–289.
| Origin of embryo-like structures in soybean anther culture investigated using SSR marker.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhslGjur0%3D&md5=2ff2467a0268a7bf574524beb51f8b9bCAS |
Rout GR, Das P (2001) Studies on in vitro somatic embryogenesis of Psoralea corylifolia Linn.—An endangered medicinal plant. Gartenbauwissenschaft 66, 202–206.
Sahrawat AK, Chand S (2001) High-frequency plant regeneration from coleoptile tissue of indica rice (Oryza sativa L.). In Vitro Cellular and Developmental Biology Plant 37, 55–61.
| High-frequency plant regeneration from coleoptile tissue of indica rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlt1Srtr4%3D&md5=61e0bc2e406f1557100269d6ad6894a9CAS |
Shikishima Y, Takaishi Y, Honda G, Ito M, Takeda Y, Kodzhimatov OK, Ashurmetov O, Lee KH (2001) Chemical constituents of Prangos tschimganica; structure elucidation and absolute configuration of coumarin and furanocoumarins derivatives with anti-HIV activity. Chemical & Pharmaceutical Bulletin 49, 877–880.
| Chemical constituents of Prangos tschimganica; structure elucidation and absolute configuration of coumarin and furanocoumarins derivatives with anti-HIV activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkvVartb8%3D&md5=22d559e77ffc39944402e35157f10322CAS |
Shivanna M, Vasanthakumari M, Mangala M (2009) Regeneration of Biophytum sensitivum (Linn.) DC. through organogenesis and somatic embryogenesis. Indian Journal of Biotechnology 8, 127–131.
Sofiari E, Raemakers C, Bergervoet J, Jacobsen E, Visser R (1998) Plant regeneration from protoplasts isolated from friable embryogenic callus of cassava. Plant Cell Reports 18, 159–165.
| Plant regeneration from protoplasts isolated from friable embryogenic callus of cassava.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvF2hu7k%3D&md5=be392a71192894eff7e035558bab5c30CAS |
Stirton CH (1981) Tribe 11. Psoraleae (Benth.) Rydb. (1919). In ‘Advances in legume systematics Part 1’. (Eds RM Polhill, R Raven) pp. 337–343. (Royal Botanic Gardens: Kew, UK)
Vergne P, Delvallee I, Dumas C (1987) Rapid assessment of microspore and pollen development stage in wheat and maize using DAPI and membrane permeablilization. Stain Technology 2, 299–304.
Vicient CM, Martínez FX (1998) The potential uses of somatic embryogenesis in agroforestry are not limited to synthetic seed technology. Revista Brasileira de Fisiologia Vegetal 10, 1–12.
Walker DJ, Moñino I, Correal E (2006) Genome size in Bituminaria bituminosa (L.) C.H. Stirton (Fabaceae) populations: separation of ‘true’ differences from environmental effects on DNA determination. Environmental and Experimental Botany 55, 258–265.
| Genome size in Bituminaria bituminosa (L.) C.H. Stirton (Fabaceae) populations: separation of ‘true’ differences from environmental effects on DNA determination.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlWhsLnK&md5=79a79c3db9bcb570c735d43a8ba9964aCAS |
Williams DJ, McHughen A (1986) Plant regeneration of the legume Lens culinaris Medik (lentil) in vitro. Plant Cell, Tissue and Organ Culture 7, 149–153.
| Plant regeneration of the legume Lens culinaris Medik (lentil) in vitro.Crossref | GoogleScholarGoogle Scholar |
Yuan HY, Lulsdorf M, Tullu A, Gurusamy V, Vandenberg A (2011) In vivo grafting of wild Lens species to Vicia faba rootstocks. Plant Genetic Resources; Characterization and Utilization 9, 543–548.
| In vivo grafting of wild Lens species to Vicia faba rootstocks.Crossref | GoogleScholarGoogle Scholar |
Zeynali M, Zanjani M, Amiri M, Noruzian M, Aghajari S (2010) Influence of genotype and plant growth regulator on somatic embryogenesis in rapeseed (Brassica napus L.). African Journal of Biotechnology 9, 4050–4055.
Zhou P, Takaishi Y, Duan H, Chen B, Honda G, Ito M, Takeda Y, Olimjon KK, Lee KH (2000) Coumarins and bicoumarin from Ferula sumbul: anti-HIV activity and inhibition of cytokine release. Phytochemistry 53, 689–697.
| Coumarins and bicoumarin from Ferula sumbul: anti-HIV activity and inhibition of cytokine release.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXitVeiurg%3D&md5=d1ba53b8b441851afcfb160cae2d6942CAS | 10746882PubMed |