Abstract
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This work provides a detailed histological analysis of the development of Jatropha curcas seeds, together with an assessment of the role of programmed cell death in this process.
Abstract
Seeds of Jatropha curcas are a potential source of raw material for the production of biodiesel, but very little is known about how the architecture of the seeds is shaped by the coordinated development of the embryo, endosperm and maternal tissues, namely integuments and nucellus. This study used standard anatomical and ultrastructural techniques to evaluate seed development and programmed cell death (PCD) in the inner integument was monitored by qPCR. In these studies, we found that the embryo sac formation is of the Polygonum type. We also found that embryogenesis is a slow process and the embryo is nourished by the suspensor at earlier stages and by nutrients remobilized from the lysis of the inner integument at later stages. Two types of programmed cell death contribute to the differentiation of the inner integument that begins at early stages of seed development. In addition, the mature embryo presents features of adaptation to dry environments such as the presence of four seminal roots, water absorbing stomata in the root zone and already differentiated protoxylem elements. The findings in this study fill in gaps related to the ontogeny of J. curcas seed development and provide novel insights regarding the types of PCD occurring in the inner integument.
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References
Battelli R, Lombardi L, Picciarelli P et al (2014) Expression and localisation of a senescence-associated KDEL-cysteine protease from Lilium longiflorum tepals. Plant Sci 214:38–46. doi:10.1016/j.plantsci.2013.09.011
Carmichael JS, Selbo SM (1999) Ovule, embryo sac, embryo, and endosperm development in leafy spurge (Euphorbia esula). Can J Bot 77:599–610
Christodoulakis NS, Menti J, Galatis B (2002) Structure and development of stomata on the primary root of Ceratonia siliqua L. Ann Bot 89:23–29. doi:10.1093/aob/mcf002
Costa GGL, Cardoso KC, Del Bem LEV et al (2010) Transcriptome analysis of the oil-rich seed of the bioenergy crop Jatropha curcas L. BMC Genom 11:462. doi:10.1186/1471-2164-11-462
Flores J, Briones O (2001) Plant life-form and germination in a Mexican inter-tropical desert: effects of soil water potential and temperature. J Arid Environ 47:485–497. doi:10.1006/jare.2000.0728
Greenwood JS, Bewley JD (1981) Seed development in Ricinus communis (castor bean). I. Descriptive morphology. Can J Bot 60:1751–1760
Greenwood JS, Helm M, Gietl C (2005) Ricinosomes and endosperm transfer cell structure in programmed cell death of the nucellus during Ricinus seed development. Proc Natl Acad Sci USA 102:2238–2243. doi:10.1073/pnas.0409429102
Helm M, Schmid M, Hierl G et al (2008) KDEL-tailed cysteine endopeptidases involved in programmed cell death, intercalation of new cells, and dismantling of extensin scaffolds. Am J Bot 95:1049–1062. doi:10.3732/ajb.2007404
Hirakawa H, Tsuchimoto S, Sakai H et al (2012) Upgraded genomic information of Jatropha curcas L. Plant Biotechnol 29:123–130. doi:10.5511/plantbiotechnology.12.0515a
Junqueira CU (1990) O uso de cortes finos de tecidos na Medicina e Biologia. Meios e Métodos 66:167–171
Karnovsky MJJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138
King AJ, Li Y, Graham IA (2011) Profiling the developing Jatropha curcas L. seed transcriptome by pyrosequencing. Bioenergy Res 4:211–221
Kull T, Arditti J (eds) (2002) Orchid biology: reviews and perspectives, vol 8. Springer
Laosatit K, Tanya P, Somta P et al (2016) De novo transcriptome analysis of apical meristem of Jatropha spp. Using 454 pyrosequencing platform, and identification of SNP and EST-SSR markers. Plant Mol Biol Rep 34:786–793. doi:10.1007/s11105-015-0961-z
Lima NB, Trindade FG, da Cunha M et al (2015) Programmed cell death during development of cowpea (Vigna unguiculata (L.) Walp.) seed coat. Plant Cell Environ 38:718–728. doi:10.1111/pce.12432
Liu H, Wang C, Komatsu S et al (2013) Proteomic analysis of the seed development in Jatropha curcas: from carbon flux to the lipid accumulation. J Proteom 91:23–40. doi:10.1016/j.jprot.2013.06.030
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta DeltaC(T)) method. Methods 25:402–408. doi:10.1006/meth.2001.1262
Mardhiah HH, Ong HC, Masjuki HH et al (2017) A review on latest developments and future prospects of heterogeneous catalyst in biodiesel production from non-edible oils. Renew Sustain Energy Rev 67:1225–1236
Natarajan P, Parani M (2011) De novo assembly and transcriptome analysis of five major tissues of Jatropha curcas L. using GS FLX titanium platform of 454 pyrosequencing. BMC Genomics 12:191. doi:10.1186/1471-2164-12-191
Natarajan P, Kanagasabapathy D, Gunadayalan G et al (2010) Gene discovery from Jatropha curcas by sequencing of ESTs from normalized and full-length enriched cDNA library from developing seeds. BMC Genom 11:606. doi:10.1186/1471-2164-11-606
Nogueira FCS, Palmisano G, Soares EL et al (2012) Proteomic profile of the nucellus of castor bean (Ricinus communis L.) seeds during development. J Proteom 75:1933–1939. doi:10.1016/j.jprot.2012.01.002
Noy-Meir I (1973) Desert ecosystems: environment and producers. Annu Rev Ecol Syst 4:25–51. doi:10.1146/annurev.es.04.110173.000325
Oparka KJ, Prior DAM (1988) Movement of Lucifer Yellow CH in potato tuber storage tissues: a comparison of symplastic and apoplastic transport. Planta 176:533–540. doi:10.1007/BF00397661
Rocha AJ, Soares EL, Costa JH et al (2013) Differential expression of cysteine peptidase genes in the inner integument and endosperm of developing seeds of Jatropha curcas L. (Euphorbiaceae). Plant Sci. doi:10.1016/j.plantsci.2013.08.009
Rudall PJ (1987) Laticifers in Euphorbiaceae a conspectus. Bot J Linn Soc 94:143–163. doi:10.1111/j.1095-8339.1987.tb01043.x
Sato S, Hirakawa H, Isobe S et al (2011) Sequence analysis of the genome of an oil-bearing tree, Jatropha curcas L. DNA Res 18:65–76. doi:10.1093/dnares/dsq030
Schmid M, Simpson D, Gietl C (1999) Programmed cell death in castor bean endosperm is associated with the accumulation and release of a cysteine endopeptidase from ricinosomes. PNAS 96:14159–14164
Shah M, Soares EL, Carvalho PC et al (2015) Proteomic analysis of the endosperm ontogeny of Jatropha curcas L seeds. J Proteome Res. doi:10.1021/acs.jproteome.5b00106
Shah M, Soares EL, Lima MLB et al (2016) Deep proteome analysis of gerontoplasts from the inner integument of developing seeds of Jatropha curcas. J Proteom 143:346–352. doi:10.1016/j.jprot.2016.02.025
Singh RP (1954) Structure and development of seeds in Euphorbiaceae—Ricinus communis L. Phytomorphology 4:118–123
Singh RP (1970) Structure and development of seeds in Euphorbiaceae: Jatropha species. Beitr Biol Pflanz 47:79–90
Soares EL, Shah M, Soares AA et al (2014) Proteome analysis of the inner integument from developing Jatropha curcas L. seeds. J Proteome Res 13:3562–3570. doi:10.1021/pr5004505
Trobacher CP, Senatore A, Holley C, Greenwood JS (2013) Induction of a ricinosomal-protease and programmed cell death in tomato endosperm by gibberellic acid. Planta 237:665–679. doi:10.1007/s00425-012-1780-1
Van Doorn WG (2011) Classes of programmed cell death in plants, compared to those in animals. J Exp Bot 62:4749–4761. doi:10.1093/jxb/err196
Xu R, Wang R, Liu A (2011) Expression profiles of genes involved in fatty acid and triacylglycerol synthesis in developing seeds of Jatropha (Jatropha curcas L.). Biomass Bioenerg 35:1683–1692. doi:10.1016/j.biombioe.2011.01.001
Zhou LZ, Howing T, Muller B et al (2016) Expression analysis of KDEL-CysEPs programmed cell death markers during reproduction in Arabidopsis. Plant Reprod 29:265–272
Acknowledgements
We thank Laboratório Temático de Microscopia Óptica e Eletrônica (LTMOE) at Instituto Nacional de Pesquisas da Amazônia (Manaus, Brazil) for the assistance with electron microscopy analysis, Central Analítica/UFC for the support with confocal microscopy, EMBRAPA Agroindústria Tropical/Fortaleza for the support with scanning electron microscopy. This work was supported by Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico (Grant no. BFP-1810026-00898.0l.00/05) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior and Conselho Nacional de Desenvolvimento Científico e Tecnológico (Grant no. 405936/2013-3).
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Communicated by Qiaochun Wang.
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Soares, E.L., Lima, M.L.B., Nascimento, J.R.S. et al. Seed development of Jatropha curcas L. (Euphorbiaceae): integrating anatomical, ultrastructural and molecular studies. Plant Cell Rep 36, 1707–1716 (2017). https://doi.org/10.1007/s00299-017-2184-2
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DOI: https://doi.org/10.1007/s00299-017-2184-2