Abstract
Jatropha curcas L. has gained attention as an ideal feedstock for biofuel production. One of the major limitations for profitable cultivation of the crop is the lack of high yielding cultivars with predictable yields. This study describes the exploitation of the mixed mating system including apomixis prevailing in the crop for development of high yielding genotypes. Evaluation of 135 accessions (AC) originating from 15 countries showed apomictic mode of seed development in 33 accessions. Based on the apomictic behavior, crosses were effected between a non-toxic high yielding genotype of Mexican origin (AC-2) and an Indian toxic genotype with synchronous maturity (AC-86). The F1 exhibited high heterosis and continued to produce seeds through both apomixis and sexual reproduction. The F1A1 progeny (n = 94) derived from the F1 hybrid through apomixis were productive with mean seed yield of 335, 586 and 644 g/plant during the 1st, 2nd and 3rd years after planting. The F1A1 progeny continued to reproduce through apomixis which ranged from 9.3 to 88.3%. A dendrogram based on genetic distances obtained from 1172 single nucleotide polymorphisms of 11 apomictic progenies along with the parents and the F1 hybrid unequivocally established the maternal origin of the apomictic plants. Microscopic analysis of developing apomictic ovules showed adventitious embryos. This study demonstrates the possibility of development of high yielding cultivars in a short time frame and in a cost effective manner by combining different mating systems prevalent in the crop viz, hybridization of diverse parents, vegetative propagation of high yielding hybrids through cuttings, and perpetuation of the superior recombinants through apomixis.
Similar content being viewed by others
References
Abdelgadir HA, Johnson SD, Van Staden J (2009) Pollinator effectiveness, breeding system, and tests for inbreeding depression in the biofuel seed crop, Jatropha curcas. J Hort Sci Biotechnol 84:319–324. https://doi.org/10.1080/14620316.2009.11512524
Achten WMJ, Nielsen LR, Aerts R, Lengkeek AG, Kjaer ED, Trabucco A, Hansen JK, Maes WH, Graudal L, Akinnifesi FK, Muys B (2010) Towards domestication of Jatropha curcas. Biofuels 1:91–107. https://doi.org/10.4155/bfs.09.4
Alfredo ZC, Quintero VP (2017) New clonal varieties of Jatropha. In: Tsuchimoto S (ed) The jatropha genome. Compendium of plant genomes. Springer, Cham, pp 275–288. https://doi.org/10.1007/978-3-319-49653-5_16
Alves AA, Bhering LL, Rosado TB, Laviola BG, Formighieri EF, Damiao Cruz C (2013) Joint analysis of phenotypic and molecular diversity provides new insights on the genetic variability of the Brazilian physic nut germplasm bank. Genet Mol Biol 36:371–381. https://doi.org/10.1590/S1415-47572013005000033
Ambrosi DG, Galla G, Purelli M, Barbi T, Fabbri A, Lucretti S, Sharbel TF, Barcaccia G (2010) DNA markers and FCSS analysis shed light on the genetic diversity and reproductive strategy of Jatropha curcas L. Diversity 2(5):810–836. https://doi.org/10.3390/d2050810
Asker S (1979) Progress in apomixis research. Hereditas 91:231–240. https://doi.org/10.1111/j.1601-5223.1979.tb01665.x
Barcaccia G, Albertini E (2013) Apomixis in plant reproduction: a novel perspective on an old dilemma. Plant Reprod 26:159–179. https://doi.org/10.1007/s00497-013-0222-y
Basha SD, Sujatha M (2007) Inter and intra-population variability of Jatropha curcas (L.) characterized by RAPD and ISSR markers and development of population specific SCAR markers. Euphytica 156:375–386. https://doi.org/10.1007/s10681-007-9387-5
Basha SD, Francis G, Makkar HPS, Becker K, Sujatha M (2009) A comparative study of biochemical traits and molecular markers for assessment of genetic relationships between Jatropha curcas L. germplasm from different countries. Plant Sci 176:812–823. https://doi.org/10.1016/j.plantsci.2009.03.008
Bhattacharya A, Datta K, Datta SK (2005) Floral biology floral resource constraints and pollination limitations in Jatropha curcas L. Pak J Biol Sci 8:456–460. https://doi.org/10.3923/pjbs.2005.456.460
Bhojwani SS, Bhatnagar SP (1992) The embryology of angiosperms. Vikas Publications, New Delhi
Biabani A, Rafii MY, Saleh GB, Shabanimofrad M, Latif A (2012) Phenotypic and genetic variation of Jatropha curcas L. populations from different countries. Maydica 57:164–174
Bressan EA, Sebbenn AM, Ferreira RR, Lee TSG, Figueira A (2013) Jatropha curcas L. (Euphorbiaceae) exhibits a mixed mating system, high correlated mating and apomixis. Tree Genet Genomes 9:1089–1097. https://doi.org/10.1007/s11295-013-0623-y
Carels N (2009) Jatropha curcas: a review. Adv Bot Res 50:48–86. https://doi.org/10.1016/S0065-2296(08)00802-1
Chang-Wei L, Kun L, You C, Yong-Yu S (2007) Floral display and breeding system of Jatropha curcas L. For Stud China 9:114–119. https://doi.org/10.1007/s11632-007-0017-z
Francis G, Edinger R, Becker K (2005) A concept for simultaneous wasteland reclamation, fuel production, and socioeconomic development in degraded areas in India: need, potential and perspectives of Jatropha plantations. Nat Res Forum 29:12–24. https://doi.org/10.1111/j.1477-8947.2005.00109.x
Francis G, Oliver J, Sujatha M (2013) Non-toxic jatropha plants as a perennial multipurpose multi-use oilseed crop. Ind Crops Prod 42:397–401. https://doi.org/10.1016/j.indcrop.2012.06.015
Francis G, Oliver J, Sujatha M (2018) High yielding and trait specific genotypes and genetic associations among yield and yield contributing traits in Jatropha curcas L. Agrofor Syst 92:1417–1436. https://doi.org/10.1007/s10457-017-0089-2
Freitas DVH, Nassar NMA (2013) Apomixis in cassava: advances and challenges. Genet Mol Res 12:988–994. https://doi.org/10.4238/2013.April.2.14
Hanna WW, Bashaw EC (1987) Apomixis: its identification and use in plant breeding. Crop Sci 27:1136–1139. https://doi.org/10.2135/cropsci1987.0011183X002700060010x
Hojsgaard D, Hörandl E (2019) The rise of apomixis in natural plant populations. Front Plant Sci. https://doi.org/10.3389/fpls.2019.00358
Juhasz ACP, Pimenta S, Soares BO, Morais DLB, Rabello HO (2009) Biologia floral e polinizacao artificial de pinhao manso no norte de Minas Gerais. Pesqui Agropecu Bras 44:1073–1077. https://doi.org/10.1590/S0100-204X2009000900001
Kaur K, Dhillon GPS, Gill RTS (2011) Floral biology and breeding system of Jatropha curcas in North-Western India. J Trop For Sci 23(1):4–9
Koltunow AM, Grossniklaus U (2003) Apomixis: a developmental perspective. Ann Rev Plant Biol 54:547–574. https://doi.org/10.1146/annurev.arplant.54.110901.160842
Laviola BG, Oliveira AMCE, Bhering LL, Alves AA, Rocha RB, Lopes-Gomes BE, Damiao Cruz C (2013) Estimates of repeatability coefficients and selection gains in Jatropha indicate that higher cumulative genetic gains can be obtained by relaxing the degree of certainty in predicting the best families. Ind Crops Prod 51:70–76. https://doi.org/10.1016/j.indcrop.2013.08.016
Li H, Tsuchimoto S, Harada K, Yamasaki M, Sakai H, Wada N, Alipour A, Sasai T, Tsunekawa A, Tsujimoto H, Ando T, Tomemori H, Sato S, Hirakawa H, Quintero VP, Zamarripa A, Santos P, Hegazy A, Ali AM, Fukui K (2017) Genetic tracing of Jatropha curcas L. from its mesoamerican origin to the world. Front Plant Sci 8:1539. https://doi.org/10.3389/fpls.2017.01539
Martin M, Montes JM (2015) Quantitative genetic parameters of agronomic and quality traits in a global germplasm collection reveal excellent breeding perspectives for Jatropha curcas L. GCB Bioenergy 7:1335–1343. https://doi.org/10.1111/gcbb.12227
Martinez-Herrera J, Siddhuraju P, Francis G, Davila-Ortiz G, Becker K (2006) Chemical composition, toxic/antimetabolic constituents, and effects of different treatments on their levels, in four provenances of Jatropha curcas L. from Mexico. Food Chem 96:80–89. https://doi.org/10.1016/j.foodchem.2005.01.059
Mieulet D, Jolivet S, Rivard M, Cromer L, Vernet A, Mayonove P et al (2016) Turning rice meiosis into mitosis. Cell Res 26:1242–1254. https://doi.org/10.1038/cr.2016.117
Montes Osorio LR, Torres Salvador AF, Jongschaap REE, Perez CAA, Sandoval JEB, Trindade LM, Visser RGF, van Loo EN (2014) High level of molecular and phenotypic biodiversity in Jatropha curcas from Central America compared to Africa, Asia and South America. BMC Plant Biol 14(1):77. https://doi.org/10.1186/1471-2229-14-77
Nassar NMA, Vieira MA, Vieira C, Grattapaglia D (1998) A molecular and embryonic study of apomixis in cassava (Manihot esculenta Crantz). Euphytica 102:9–13. https://doi.org/10.1023/A:1018303109798
Nassar NMA, Hashimoto D, Castilho AP (2008) Apomixis induces new species of Manihot. Gene Conserv 7:636–642
Negussie A, Achten WMJ, Verboven HAF, Hermy M, Muys B (2014) Floral display and effects of natural and artificial pollination on fruiting and seed yield of the tropical biofuel crop, Jatropha curcas L. GCB Bioenergy 6:210–218. https://doi.org/10.1111/gcbb.12072
Nietsche S, Vendrame WA, Crane JH, Pereira MCT (2014) Assessment of reproductive characteristics of Jatropha curcas L. in South Florida. GCB Bioenergy 6:351–359. https://doi.org/10.1111/gcbb.12051
Ozias-Akins P, Akiyama Y, Hanna WW (2003) Molecular characterization of the genomic region linked with apomixis in Pennisetum/Cenchrus. Funct Integr Genom 3(3):94–104. https://doi.org/10.1007/s10142-003-0084-8
Pecina-Quintero V, Anaya JL, Zamarripa CA, Montes GN, Núñez C, Solís J (2011) Molecular characterization of Jatropha curcas L. genetic resources from Chiapas, México through AFLP markers. Biomass Bioenergy 35(5):1897–1905. https://doi.org/10.1016/j.biombioe.2011.01.027
Pranesh KJ, Gururaja Rao MR, Sowmya HC, Gowda B, Savithramma DL, Naveen NL (2010) Studies on floral display and mode of reproduction in jatropha (Jatropha curcas L.). Electron J Plant Breed 1(4):832–838
Priyadarshan PM, Clément-Demange A (2004) Breeding Hevea rubber: formal and molecular genetics. Adv Genet 52:51–115. https://doi.org/10.1016/S0065-2660(04)52003-5
Rao GR, Korwar GR, Shanker AK, Ramakrishna YS (2008) Genetic associations, variability and diversity in seed characters, growth, reproductive phenology and yield in Jatropha curcas (L.) accessions. Trees 22:697–709. https://doi.org/10.1007/s00468-008-0229-4
Rincón-Rabanales M, Vargas-Lopez LI, Adriano-Anaya L, Vasquez-Ovando A, Salvador-Figueroa M, Ovando-Medina I (2016) Reproductive biology of the biofuel plant Jatropha curcas in its center of origin. Peer J 4:e1819. https://doi.org/10.7717/peerj.1819
Santos DN, Ferreira JL, Pasqual M, Generosos AL, Setotaw TA, Cancado GMA, Vendrame WA (2016) Population structure of jatropha and its implication for the breeding program. Genet Mol Res. https://doi.org/10.4238/gmr.15017770
Savidan Y (2001) Transfer of apomixis through wide crosses. In: Savidan Y, Carman JG, Dresselhaus T (eds) The flowering of apomixis: from mechanisms to genetic engineering. CIMMYT, Mexico, pp 153–167
Shabanimofrad M, Rafii MY, Megat Wahab PE, Biabani AR, Latif MA (2013) Phenotypic, genotypic and genetic divergence found in 48 newly collected Malaysian accessions of Jatropha curcas L. Ind Crops Prod 42:543–551. https://doi.org/10.1016/j.indcrop.2012.06.023
Sowmyalatha MKS, Priyadarshan PM, Dey SK, Varghese YA (1997) Low fruit set in Hevea brasiliensis in Tripura: implications of floral attributes. Indian J Nat Rubber Res 10:15–26
Sun QB, Li LF, Li Y, Wu GJ, Ge XJ (2008) SSR and AFLP markers reveal low genetic diversity in the biofuel plant Jatropha curcas in China. Crop Sci 48:1865–1871. https://doi.org/10.2135/cropsci2008.02.0074
Trebbi D, Ravi S, Broccanello C, Chiodi C, Francis G, Oliver J, Mulpuri S, Srinivasan S, Stevanato P (2019) Identification and validation of SNP markers linked to seed toxicity in Jatropha curcas L. Sci Rep 9:10220. https://doi.org/10.1038/s41598-019-46698-4
Yi C, Zhang S, Liu X, Bui HTN, Hong Y (2010) Does epigenetic polymorphism contribute to phenotypic variances in Jatropha curcas L. BMC Plant Biol 10:259. https://doi.org/10.1186/1471-2229-10-259
Yi C, Reddy C, Varghese K, Bui TNH, Zhang S, Kallath M, Hong Y (2014) A new Jatropha curcas variety (JO S2) with improved seed productivity. Sustainability 6:4355–4368. https://doi.org/10.3390/su6074355
Acknowledgements
The authors thank Dr. Pankaj Kaushal, IGFRI, Jhansi, India for useful suggestions and providing the methodology of ovule clearing technique.
Funding
The financial support of Jatropower AG, Switzerland for this study is acknowledged.
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
10722_2019_851_MOESM1_ESM.jpg
Figure S1 Seed yield (g/plant) in F2 population (n = 148) during the 2nd, 3rd, 4th years of planting and cumulative yield and comparable yields of F1A1 progeny (n = 94) during the 1st, 2nd and 3rd years of planting along with the cumulative yield of the corresponding 3 years for the respective populations. I, II, III and IV represent the years after planting and Cum represents cumulative seed yield. For F2 population, correlations for seed yield for 1st and 2nd years, 1st and 3rd years and 2nd and 3rd years were 0.466, 0.306 and 0.509, respectively. For F1A1 progeny, correlations for seed yield for 1st and 2nd years, 1st and 3rd years and 2nd and 3rd years were 0.597, 0.319 and 0.654, respectively. (JPG 2680 kb)
Rights and permissions
About this article
Cite this article
Francis, G., John, O., Piergiorgio, S. et al. Apomixis as a tool for development of high yielding clones and selections in Jatropha curcas L.. Genet Resour Crop Evol 67, 727–743 (2020). https://doi.org/10.1007/s10722-019-00851-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10722-019-00851-0