Abstract
The induction, development, and maturation of somatic embryos in cocoa are subjected to numerous failures during the various development stages. Understanding the biochemical/molecular events governing somatic embryogenesis in T. cacao will help to overcome these failures. The present study focused on cocoa somatic embryogenesis proteomic variations with the aim to shed light on the constraints of somatic embryos during their development stages (induction, expression, and maturation). These were investigated using combinations of LC–MS/MS coupled with TripleTOF 5600 + and Orbitrap Fusion methods during cocoa (Theobroma cacao L.) somatic embryogenesis. Non-embryogenic callus (NC), embryogenic callus (EC), somatic embryos (ESN), and zygotic embryos (EZM) were used as samples. Sample analyses followed by bioinformatics research identified a total of 1762 proteins. The differentially expressed proteins (DEPs) were derived from NC (429), EC (301), ESN (911), and EZM (511) and classified according to ontological categories. The analysis of KEGG pathways in NC and EZM showed that they were mainly enriched in metabolic pathways and the biosynthesis of secondary metabolites. While in EC and ESN, they are enriched in endoplasmic reticulum protein processing. Based on protein–protein interaction analysis, proteins in EC and ESN were highly regulated and involved in environmental stress. On the other hand, proteins in NC and EZM, highly regulated were involved in energy metabolism. This proteomic study provides clues to understand the low rate of conversion to plant in somatic embryogenesis and helps to build a model for improved culture medium.
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Abbreviations
- NC:
-
Non-embryogenic callus
- EC:
-
Embryogenic callus
- ED:
-
Embryo development
- ESN:
-
Somatic embryos
- EZM:
-
Zygotic embryos
- KO:
-
KEGG Orthology
- DEPs:
-
Differentially expressed proteins
- KEGG:
-
Kyoto Encyclopedia of Genes and Genomes
- PCG:
-
Primary callus growth
- SCG:
-
Secondary callus growth
- STRING:
-
Search Tool for the Retrieval of Interacting Genes/Proteins
- HAT:
-
Histone acetyltransferase
- TCA:
-
Tricarboxylic acid
References
Abbasi BH, Ali H, Yücesan B, Saeed S, Rehman K, Khan MA (2016) Evaluation of biochemical markers during somatic embryogenesis in Silybum marianum L. 3 Biotech. 6(1):1–8
Alexandra Pila Quinga L, Heringer AS, de Freitas P, Fraga H, do Nascimento VL, Silveira V, Steinmacher DA, Guerra MP (2018) Insights into the conversion potential of Theobroma cacao L. somatic embryos using quantitative proteomic analysis. Sci Hortic 229:65–76
Cao PB (2022) in Silico structural, evolutionary, and expression analysis of small heat shock protein (shsp) encoding genes in cocoa (Theobroma Cacao L.). J Animal Plant Sci 32(5):1394–1402
Chanprame S, Kuo TM, Widholm JM (1998) Soluble carbohydrate content of soybean [Glycine max (L.) Merr] somatic and zygotic embryos during development. In Vitro Cellr Dev Biol-Plant. 34(1):64–68
Danso-Abbeam G, Addai KN, Ehiakpor D (2014) Willingness to Pay for farm insurance by smallholder cocoa farmers in ghana. J Soc Sci Policy Implicat 2(1):163–183
Doering KRS, Taubert S (2019) Epigenetic regulator G9a provides glucose as a sweet key to stress resistance. PLoS Biol 17(4):1–6. https://doi.org/10.1371/journal.pbio.3000236
Driver JA, Kuniyuki AH (1984) In Vitro Propagation of Paradox Walnut Rootstock. HortScience 19(4):507–509. https://doi.org/10.21273/hortsci.19.4.507
Eskes AB, Engels JMM, Lass RA (1998) Working procedures for cacao germplasm evaluation and conservation : Note on the workshop of the CFC/ICCO/IPGRI project on Cocoa germplasm utilization and conservation, a global approach, held at Montpellier from 1–6 February, 1998. Ingenic Newsletter 4:3–4
Fehér A (2015) Somatic embryogenesis-stress-induced remodeling of plant cell fate. Biochimica Et Biophysica Acta-Gene Regul Mechan 1849(4):385–402. https://doi.org/10.1016/j.bbagrm.2014.07.005
Garcia C, Corrêa F, Findley S, Almeida AA, Costa M, Motamayor JC, Schnell R, Marelli JP (2016) Optimization of somatic embryogenesis procedure for commercial clones of Theobroma cacao L. Afr J Biotech 15(36):1936–1951. https://doi.org/10.5897/AJB2016.15513
Gorka M, Swart C, Siemiatkowska B, Martínez-Jaime S, Skirycz A, Streb S, Graf A (2019) Protein complex identification and quantitative complexome by CN-PAGE. Sci Rep 9(1):11523. https://doi.org/10.1038/s41598-019-47829-7
Gulzar B, Mujib A, Rajam MV, Frukh A, Zafar N (2019) Identification of somatic embryogenesis (SE) related proteins through label-free shotgun proteomic method and cellular role in Catharanthus roseus (L.) G Don. Plant Cell, Tissue Organ Cult 137(2):225–237
Guo W, Gao J, Wang HJ, Su RY, Sun CY, Gao SH, Liu JZ, Chen GY (2020) Phosphoglycerate kinase Is involved in carbohydrate utilization, extracellular polysaccharide biosynthesis, and cell motility of Xanthomonas axonopodis pv. glycines independent of Clp. Front Microbiol. https://doi.org/10.3389/fmicb.2020.00091
Henao Ramírez AM, de la Hoz VT, Ospina Osorio TM, Garcés LA (2017) Urrea Trujillo AI (2018) Evaluation of the potential of regeneration of different Colombian and commercial genotypes of cocoa (Theobroma cacao L.) via somatic embryogenesis. Sci Hortic 229:148–156. https://doi.org/10.1016/j.scienta.2017.10.040
Heringer AS, Barroso T, Macedo AF, Santa-Catarina C, Souza GHMF, Floh EIS, De Souza-Filho GA, Silveira V (2015) Label-free quantitative proteomics of embryogenic and non-embryogenic callus during sugarcane somatic embryogenesis. PLoS ONE 10(6):1–23. https://doi.org/10.1371/journal.pone.0127803
Iraqi D, Tremblay FM (2001) Analysis of carbohydrate metabolism enzymes and cellular contents of sugars and proteins during spruce somatic embryogenesis suggests a regulatory role of exogenous sucrose in embryo development. J Exp Bot 52(365):2301–2311. https://doi.org/10.1093/jexbot/52.365.2301
Isah T (2019) Proteome study of somatic embryogenesis in Nothapodytes nimmoniana (J. Graham) Mabberly. 3 Biotech 9(4):1–23. https://doi.org/10.1007/s13205-019-1637-4
Ji J, Yang L, Fang Z, Zhuang M, Zhang Y, Lv H, Liu Y, Li Z (2018) Complementary transcriptome and proteome profiling in cabbage buds of a recessive male sterile mutant provides new insights into male reproductive development. J Proteomics 179(March):80–91. https://doi.org/10.1016/j.jprot.2018.03.003
Laxalt AM, Cassial RO, Sanllorenti PM, Madrid EA, Andreu AB, Raû G, Conde RD, Lamattina L (1996) Accumulation of cytosolic gIyceraIdehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol Biol 30(5):961–972. https://doi.org/10.1007/BF00020807
Li Z, Traore A, Maximova SN, Guiltinan MJ (1998) Somatic embryogenesis and plant regeneration from floral explants of cacao (Theobroma cacao L.) using thidiazuron. In Vitro Cell Dev Bio-Plant 34(4):293–299. https://doi.org/10.1007/BF02822737
Liu Y, Lu S, Liu K, Wang S, Huang L, Guo L (2019) Proteomics: A powerful tool to study plant responses to biotic stress. Plant Methods 15(1):1–20. https://doi.org/10.1186/s13007-019-0515-8
Maximova SN, Alemanno L, Young A, Ferriere N, Traore A, Guiltinan MJ (2002) Efficiency, genotypic variability, and cellular origin of primary and secondary somatic embryogenesis of Theobroma Cacao L. In Vitro Cell Dev Biol Plant 38(3):252–259. https://doi.org/10.1079/IVP2001257
Maximova SN, Florez S, Shen X, Niemenak N, Zhang Y, Curtis W, Guiltinan MJ (2014) Genome-wide analysis reveals divergent patterns of gene expression during zygotic and somatic embryo maturation of Theobroma cacao L., the chocolate tree. BMC Plant Biol 14(1):185. https://doi.org/10.1186/1471-2229-14-185
Myeki LW, Bahta YT, Matthews N (2022) Exploring the growth of agricultural productivity in AFRICA: a färe-primont index approach. Agriculture 12(8):1236. https://doi.org/10.3390/agriculture12081236
Niemenak N, Kaiser E, Maximova SN, Laremore T, Guiltinan MJ (2015) Proteome analysis during pod, zygotic and somatic embryo maturation of Theobroma cacao. J Plant Physiol 180:49–60. https://doi.org/10.1016/j.jplph.2015.02.011
Noah AM, Niemenak N, Sunderhaus S, Haase C, Omokolo DN, Winkelmann T (2014) Braun HP (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
Pan L, Wan L, He L, Song L, Long H, Ji X, Jiang N, Huo J, Wei S, Fu J (2021) Comparative proteomic analysis of parasitic loranthus seeds exposed to dehydration stress. Plant Biotechnol Rep 15(1):95–108. https://doi.org/10.1007/s11816-020-00651-4
Pfab A, Breindl M, Grasser KD (2018) The Arabidopsis histone chaperone FACT is required for stress-induced expression of anthocyanin biosynthetic genes. Plant Mol Biol 96(4–5):367–374. https://doi.org/10.1007/s11103-018-0701-5
Rode C, Gallien S, Heintz D, Van Dorsselaer A, Braun HP, Winkelmann T (2011) Enolases: storage compounds in seeds? Evidence from a proteomic comparison of zygotic and somatic embryos of Cyclamen persicum Mill. Plant Mol Biol 75(3):305–319. https://doi.org/10.1007/s11103-010-9729-x
Rosado-Souza L, Proost S, Moulin M, Bergmann S, Bocobza SE, Aharoni A, Fitzpatrick TB, Mutwil M, Fernie AR, Obata T (2019) Appropriate thiamin pyrophosphate levels are required for acclimation to changes in photoperiod. Plant Physiol 180(1):185–197. https://doi.org/10.1104/pp.18.01346
Squicciarini MP, Swinnen J (2016) The economics of chocolate. The Econ Choco. https://doi.org/10.1093/acprof:oso/9780198726449.003.0001
Su H, Chen G, Yang L, Zhang Y, Wang Y, Fang Z, Lv H (2020) Proteomic variations after short-term heat shock treatment reveal differentially expressed proteins involved in early microspore embryogenesis in cabbage (Brassica oleracea). PeerJ. https://doi.org/10.7717/peerj.8897
Tolley E, Craig I (1975) Presence of two forms of fumarase (fumarate hydratase E.C. 4.2 1.2) in mammalian cells: Immunological characterization and genetic analysis in somatic cell hybrids Confirmation of the assignment of a gene necessary for the enzyme expression to human chro. Biochem Genet 13(11–12):867–883. https://doi.org/10.1007/BF00484417
Tripathi AK, Pareek A, Singla-Pareek SL (2016) A NAP-family histone chaperone functions in abiotic stress response and adaptation. Plant Physiol 171(4):2854–2868. https://doi.org/10.1104/pp.16.00408
Wang C, Zhang LJ, Huang RD (2011a) Cytoskeleton and plant salt stress tolerance. Plant Signal Behav 6(1):29–31. https://doi.org/10.4161/psb.6.1.14202
Wang Q, Zhang X, Li F, Hou Y, Liu X, Zhang X (2011b) Identification of a UDP-glucose pyrophosphorylase from cotton (Gossypium hirsutum L.) involved in cellulose biosynthesis in Arabidopsis thaliana. Plant Cell Rep 30(7):1303–1312. https://doi.org/10.1007/s00299-011-1042-x
Wessel M, Quist-Wessel PMF (2015) Cocoa production in West Africa, a review and analysis of recent developments. NJAS - Wageningen Journal of Life Sciences 74–75:1–7. https://doi.org/10.1016/j.njas.2015.09.001
Zhao H, Chen G, Sang L, Deng Y, Gao L, Yu Y, Liu J (2021) Mitochondrial citrate synthase plays important roles in anthocyanin synthesis in petunia. Plant Sci 305(February):110835. https://doi.org/10.1016/j.plantsci.2021.110835
Zimmerman JL (1993) Somatic embryogenesis: a model for early development in higher plants. Plant Cell 5(10):1411–1423. https://doi.org/10.2307/3869792
Acknowledgements
The authors are grateful to the ICRAF Côte d’Ivoire’s Somatic Embryogenesis Laboratory staff for their technical support. The financial support offered by Mars Incorporated is highly appreciated.
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NPG, ME, KKM, KC and DNT designed the experiments, analyzed and interpreted the data and was a major contributor in writing the manuscript. NC and ND conducted experiments and analyzed the data. All authors read and approved the final manuscript.
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N’goran, G.P.K., Minyaka, E., N’zi, JC. et al. Comparative proteomic analysis of non-embryogenic and embryogenic callus, somatic and zygotic embryos of Theobroma cacao L.. Plant Biotechnol Rep 17, 687–699 (2023). https://doi.org/10.1007/s11816-022-00812-7
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DOI: https://doi.org/10.1007/s11816-022-00812-7