Abstract
Understanding the molecular events that initiate somatic embryogenesis (SE) may help optimize clonal propagation protocols in oil palm. The objective of this work was to identify differentially abundant proteins during the induction of SE in two interspecific F1 hybrids of Elaeis oleifera × Elaeis guineensis with contrasting responses (responsive and non-responsive) to the SE process. Leaf explants were obtained and submitted to SE induction medium for up to 180 days. Explants were collected at 0, 14, 90 and 150 days of induction (doi). Proteins were extracted and analyzed by two-dimensional electrophoresis. Analyses were focused at 14 and 150 doi, representing the initial and late stages of embryogenic competence acquisition, respectively. The results indicate that at 14 doi a high amount of stress is present which results in cellular dedifferentiation. At 90 doi, cells (of the responsive genotype) seem adapted and have kept stress under control, allowing the use of energy for cellular proliferation that occurs at 150 doi. Therefore, the control of stress and oxidation seem to be crucial for callus development. We highlight proteins associated to oxidative stress, protein processing, energy metabolism and development as potentially involved in embryogenic competence acquisition.
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References
Atkinson N, Urwin P (2012) The interaction of plant biotic and abiotic stresses: from genes to the field. J Exp Bot 63:3523–3543
Babu BK, Mathur RK, Kumar PN et al (2017) Development, identification and validation of CAPS marker for SHELL trait which governs dura, pisifera and tenera fruit forms in oil palm (Elaeis guineensis Jacq.). PLoS ONE 12:e0171933
Balzon TA, Luis ZG, Scherwinski-Pereira JE (2013) New approaches to improve the efficiency of somatic embryogenesis in oil palm (Elaeis guineensis Jacq.) from mature zygotic embryos. In Vitro Cell Dev Biol Plant 49:41–50. https://doi.org/10.1007/s11627-012-9479-3
Bauwe H, Hagemann M, Kern R, Timm S (2012) Photorespiration has a dual origin and manifold links to central metabolism. Curr Opin Plant Biol 15:269–275
Beulé T, Camps C, Debiesse S et al (2011) Transcriptome analysis reveals differentially expressed genes associated with the mantled homeotic flowering abnormality in oil palm (Elaeis guineensis). Tree Genet Genomes 7:169–182. https://doi.org/10.1007/s11295-010-0323-9
Carmo LST, Resende RO, Silva LP et al (2013) Identification of host proteins modulated by the virulence factor AC2 of tomato chlorotic mottle virus in Nicotiana benthamiana. Proteomics 13:1947–1960. https://doi.org/10.1002/pmic.201200547
Choi J, Sung Z (1984) Two-dimensional gel analysis of carrot somatic embryonic proteins. Plant Mol Biol Rep 2:19–25. https://doi.org/10.1007/BF02885643
Corley R, Hereward V, Tinker P (2003) The oil palm. Blackwell Science Ltd, Oxford
Dai S, Wang T, Yan X, Chen S (2007) Proteomics of pollen development and germination. J Proteome Res 6:4556–4563
De Gara L, Tommasi F (1999) Ascorbate redox enzymes: a network of reactions involved in plant development. Recent Res Dev Phytochem 3:1–15
de Carvalho Silva R, Carmo LST, Luis ZG et al (2014) Proteomic identification of differentially expressed proteins during the acquisition of somatic embryogenesis in oil palm (Elaeis guineensis Jacq.). J Proteomics 104:1112–1127. https://doi.org/10.1016/j.jprot.2014.03.013
Duval Y, Gasselin TD, Konan K, Pannetier C (1988) Multiplication végétative du palmier à huile (Elaeis guineensis Jacq.) par culture in vitro. Stratégie et résultats. Oléagineux 43:39–47
Fehér A (2015) Somatic embryogenesis—stress-induced remodeling of plant cell fate. Biochim Biophys Acta Gene Regul Mech 1849:385–402
Fehér A, Pasternak TP, Dudits D (2003) Transition of somatic plant cells to an embryogenic state. Plant Cell Tissue Organ Cult 74:201–228. https://doi.org/10.1023/A:1024033216561
Foyer C, Noctor G (2005) Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses. Plant Cell 17:1866–1875. https://doi.org/10.1105/tpc.105.033589
Foyer C, Noctor G (2012) Managing the cellular redox hub in photosynthetic organisms. Plant Cell Environ 35:191–201
Johansen DA (1940) Plant microtechnique. McGraw Hill, New York
Jones LH (1974) Propagation of clonal oil palms by tissue culture. Oil Palm News 17:1–8
Joo JH, Yoo HJ, Hwang I et al (2005) Auxin-induced reactive oxygen species production requires the activation of phosphatidylinositol 3-kinase. FEBS Lett 579:1243–1248
Konan KE, Durand-Gasselin T, Kouadio YJ et al (2010) In vitro conservation of oil palm somatic embryos for 20 years on a hormone-free culture medium: characteristics of the embryogenic cultures, derived plantlets and adult palms. Plant Cell Rep 29:1–13. https://doi.org/10.1007/s00299-009-0787-y
Laohavisit A, Davies J (2011) Annexins. New Phytol 189:40–53
Lin HC, Morcillo F, Dussert S et al (2009) Transcriptome analysis during somatic embryogenesis of the tropical monocot Elaeis guineensis: evidence for conserved gene functions in early development. Plant Mol Biol 70:173–192. https://doi.org/10.1007/s11103-009-9464-3
Liu Y, Chaturvedi P, Fu J et al (2016) Induction and quantitative proteomic analysis of cell dedifferentiation during callus formation of lotus (Nelumbo nucifera Gaertn.spp. baijianlian). J Proteomics 131:61–70. https://doi.org/10.1016/j.jprot.2015.10.010
Lopes R, Cunha RNV da, Resende MDV de (2012) Produção de cachos e parâmetros genéticos de híbridos de caiaué com dendezeiro. Pesqui Agropecu Bras 47:1496–1503. https://doi.org/10.1590/S0100-204X2012001000012
Low E-T, Alias H, Boon S-H et al (2008) Oil palm (Elaeis guineensis Jacq.) tissue culture ESTs: identifying genes associated with callogenesis and embryogenesis. BMC Plant Biol 8:62. https://doi.org/10.1186/1471-2229-8-62
Mahdavi-Darvari F, Noor NM, Ismanizan I (2015) Epigenetic regulation and gene markers as signals of early somatic embryogenesis. Plant Cell Tissue Organ Cult 120:407–422. https://doi.org/10.1007/s11240-014-0615-0
McCarthy FM, Wang N, Magee GB et al (2006) AgBase: a functional genomics resource for agriculture. BMC Genomics 7:229
Morel A, Trontin JF, Corbineau F et al (2014) Cotyledonary somatic embryos of Pinus pinaster Ait. most closely resemble fresh, maturing cotyledonary zygotic embryos: biological, carbohydrate and proteomic analyses. Planta 240:1075–1095. https://doi.org/10.1007/s00425-014-2125-z
Moss S, Morgan R (2004) The annexins. Genome Biol 5:219.1-219.8
Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15:473–497. https://doi.org/10.1111/j.1399-3054.1962.tb08052.x
Noah AM, Niemenak N, Sunderhaus S et al (2013) Comparative proteomic analysis of early somatic and zygotic embryogenesis in Theobroma cacao L. J Proteomics 78:123–133. https://doi.org/10.1016/j.jprot.2012.11.007
Nunes-Nesi A, Florian A, Howden A et al (2014) Is there a metabolic requirement for photorespiratory enzyme activities in heterotrophic tissues? Mol Plant 7:248–251. https://doi.org/10.1093/mp/sst111
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373. https://doi.org/10.1007/BF01248568
Ribeiro DG, Almeida RF, Fontes W, Castro MS, Souza MV, Ricart CAO, Cunha RNV, Lopes R, Scherwinski-Pereira JV (2018) Stress and cell cycle regulation during somatic embryogenesis plays a key role in oil palm callus development. J Proteomics 192:137–146
Rocha DI, Vieira LM, Tanaka FAO et al (2012) Somatic embryogenesis of a wild passion fruit species Passiflora cincinnata Masters: histocytological and histochemical evidences. Protoplasma 249:747–758. https://doi.org/10.1007/s00709-011-0318-x
Rode C, Gallien S, Heintz D et al (2011) Enolases: storage compounds in seeds? Evidence from a proteomic comparison of zygotic and somatic embryos of Cyclamen persicum Mill. Plant Mol Biol 75:305–319. https://doi.org/10.1007/s11103-010-9729-x
Rogowska-Wrzesinska A, Le Bihan MC, Thaysen-Andersen M, Roepstorff P (2013) 2D gels still have a niche in proteomics. J Proteomics 88:4–13. https://doi.org/10.1016/j.jprot.2013.01.010
Roowi SH, Ho CL, Alwee SSRS et al (2010) Isolation and characterization of differentially expressed transcripts from the suspension cells of oil palm (Elaeis guineensis Jacq.) in response to different concentration of auxins. Mol Biotechnol 46:1–19. https://doi.org/10.1007/s12033-010-9262-9
Santos IR, Maximiano MR, Almeida RF, Cunha RNV, Lopes R, Scherwinski-Pereira JE, Mehta A (in press) Genotype-dependent changes of gene expression during somatic embryogenesis in oil palm hybrids (Elaeis oleifera × E. guineensis). PLoS ONE
Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68:850–858
Silveira V, Santa-catarina C, Iochevet E, Floh S (2004) Effect of plant growth regulators on the cellular growth and levels of intracellular protein, starch and polyamines in suspension cultures of Pinus taeda. Plant Cell Tissue Organ Cult 76:53–60
Sin T, Liddell S, Abdullah M et al (2016) Differential proteomic analysis of embryogenic lines in oil palm (Elaeis guineensis Jacq). J Proteomics 143:334–345. https://doi.org/10.1016/j.jprot.2016.04.039
Smertenko A, Franklin-Tong V (2011) Organisation and regulation of the cytoskeleton in plant programmed cell death. Cell Death Differ 18:1263–1270
Supek F, Bošnjak M, Škunca N, Šmuc T (2011) Revigo summarizes and visualizes long lists of gene ontology terms. PLoS ONE. https://doi.org/10.1371/journal.pone.0021800
Tonietto Â, Sato JH, Teixeira JB et al (2012) Proteomic analysis of developing somatic embryos of Coffea arabica. Plant Mol Biol Rep 30:1393–1399. https://doi.org/10.1007/s11105-012-0425-7
Vidal BC (1969) Dichroism in collagen bundles stained with Xylidine-Ponceau 2R. Ann d’histochim 15:289–296
Wang W, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Youssefian S, Nakamura M, Orudgev E, Kondo N (2001) Increased cysteine biosynthesis capacity of transgenic tobacco overexpressing an O-acetylserine (thiol) lyase modifies plant responses to oxidative stress. Plant Physiol 126:1001–1011
Zhang D, Ren L, Chen G, qun et al (2015) ROS-induced oxidative stress and apoptosis-like event directly affect the cell viability of cryopreserved embryogenic callus in Agapanthus praecox. Plant Cell Rep 34:1499–1513. https://doi.org/10.1007/s00299-015-1802-0
Zhou T, Yan X, Guo K et al (2016) ROS homeostasis regulates somatic embryogenesis via the regulation of auxin signaling in cotton. Mol Cell Proteomics 15:2108–2124. https://doi.org/10.1074/mcp.M115.049338
Zi J, Zhang J, Wang Q et al (2013) Stress responsive proteins are actively regulated during rice (Oryza sativa) embryogenesis as indicated by quantitative proteomics analysis. PLoS ONE. https://doi.org/10.1371/journal.pone.0074229
Acknowledgements
This work was sponsored by Embrapa, Coordenaçao de Aperfeiçoamento de Pessoal de Nivel Superior- CAPES, Ministério da Ciência e Tecnologia—MCT, Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq.
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RFA performed and designed experiments, analyzed and interpreted data and wrote the manuscript. IRS assisted in proteomic data analysis. FSM assisted in morfo-anatomical and histochemical analysis. PG assisted in bioinformatic data analysis and interpretation. RL and RNVdC assisted in selection and collection of oil palm material in the field. OLF assisted with mass spectrometry analysis. JES-P and AM designed experiments, analyzed data and wrote the manuscript.
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Communicated by Ming-Tsair Chan.
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Key Message
The non-responsive genotype is not able to control stress, while the responsive genotype keeps stress under control, allowing the use of energy for cellular proliferation, which leads to callus formation.
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Supplementary Fig. 1
. Enlarged image of the protein profiles of the oil palm genotypes responsive and non-responsive to the acquisition of embryogenic competence at 0, 14, 90 and 150 days of induction (doi). Circled numbers indicate unique spots. (PPTX 3240 KB)
Supplementary Fig. 2
. Time course of the proteins identified as possibly involved in the acquisition of embryogenic competence in the interspecific F1 hybrids of Elaeis oleifera x E. guineensis. Red = responsive genotype; Blue = non-responsive genotype. ACT1 = Actin-3-like; ANN1 = Annexin D1; CAT2 = Catalase isozyme 2; ENO1 = Enolase-like; GND1 = 6-phosphogluconate dehydrogenase, decarboxylating 1-like; HSP81-1= Heat shock protein 81-1; MDAR5 = Monodehydroascorbate reductase 5, mitochondrial; OASA = Cysteine synthase; PFP-BETA = pyrophosphate fructose 6-phosphate 1phosphotransferase subunit beta-like; PGM = 2,3-bisphosphoglycerate-independent phosphoglycerate mutase; RBCL = RuBisCO large subunit; RUBA = RuBisCO large subunit-binding protein subunit alpha, isoform X2. (TIF 10259 KB)
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Almeida, R.F., Santos, I.R., Meira, F.S. et al. Differential protein profiles in interspecific hybrids between Elaeis oleifera and E. guineensis with contrasting responses to somatic embryogenesis competence acquisition. Plant Cell Tiss Organ Cult 137, 11–21 (2019). https://doi.org/10.1007/s11240-018-01545-8
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DOI: https://doi.org/10.1007/s11240-018-01545-8