Abstract
During seed germination until photoautotrophic establishment, the mobilization of seed-stored reserves represents the main source of carbon structures and energy that all plants need. We report organic and mineral changes coupled with germination and post-germination functional traits of different rubber tree genotypes (wild and PB 260, a clonal variant selected for high latex productivity). By analyzing seeds for their protein, lipid, and carbohydrate contents and the mobilization of these compounds during germination and initial seedling growth, differential mobilization of primary stocks, differences in the enzymatic activities, and changes in mineral nutrient contents were observed between the two genotypes. Furthermore, differential protein profiles were found. Proteins with apparent molecular weights ranging from 7 to 30 kDa and 7 to 40 kDa were observed for wild and clone PB 260 seeds, respectively. Higher mobilization of nitrogen-related compounds indicates that nitrogen metabolism seems to play an essential role in the germination and post-germination processes of H. brasiliensis. The results revealed differences in the primary metabolism between the genotypes studied: our findings provide an integrated understanding of the germination and early post-germination events that could assist rubber tree breeding programs via the creation of histophysiological and biochemical markers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahmad J, Yusup S, Bokhari A, Kamil RNM (2014) Study of fuel properties of rubber seed oil-based biodiesel. Energy Convers Manag 78:266–275. https://doi.org/10.1016/j.enconman.2013.10.056
Aidi-Daslin, (2013) Rubber clone productivity at different environmental conditions on plantations. Agrium 18:1–6
Alencar NLM, Gadelha CG, Gallão MI, Dolder MAH, Prisco JT, Gomes-Filho E (2015) Ultrastructural and biochemical changes induced by salt stress in Jatropha curcas seeds during germination and seedling development. Funct Plant Biol 42(9):865–874. https://doi.org/10.1071/FP15019
Aniche GN (1989) Studies on the effect of germination on the malting quality of a two maizes varieties. Process Biochem 24:183–186
Asuquo JE, Anusiem ACI, Etim EE (2012) Studies on the adsorption of some selected metallic soaps onto hematite. University of Port Harcourt. Niger Int J Mod Chem 3:39–50
Barros TFS, Arriel NHC, Queiroz MF, Fernandes PD, Mendonça S, Ribeiro JAdeA, Medeiros EdeA, (2015) Fatty acid profiles of species of Jatropha curcas L., Jatropha molíssima (Pohl) Baill. and Jatropha gossypiifolia L. Ind Crops Prod 73:106–108. https://doi.org/10.1016/j.indcrop.2015.04.003
Beisson F, Tiss A, Rivière C, Verger R (2000) Methods for lipase detection and assay: a critical review. Eur J Lipid Sci Technol 102:133–153. https://doi.org/10.1002/(SICI)1438-9312(200002)102:2%3c133::AID-EJLT133%3e3.0.CO;2-X
Bellaloui N, Reddy KN, Gillen AM, Abel CA (2010) Nitrogen metabolism and seed composition as influenced by foliar boron application in soybean. Plant Soil 336:43–155. https://doi.org/10.1007/s11104-010-0455-6
Berthelot K, Lecomte S, Estevez Y, Peruch FE (2014) Hevea brasiliensis REF (Hev b 1) and SRPP (Hev b 3): An overview on rubber particle proteins. Biochimie 106:1–9. https://doi.org/10.1016/j.biochi.2014.07.002
Bewley JD, Black M (1994) Seeds: Physiology of development and germination. Plenum Press, New York, pp 1–31
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: Physionoly of development, germination and dormancy. Springer, New York Heidelberg Dordrecht London, Lexington, KY, US, p 392
Bezerra IWL, Teixeira FM, Oliveira AS, Araújo CL, Leite EL, Queiroz KCS, Sales MP (2004) α-amilase inhibitors from Ficus sp. seeds and their activities towards coleopteran sect pests. Protein Pept Lett 11:181–187. https://doi.org/10.2174/0929866043478329
Bonome LTS, Moreira SAF, Oliveira LEM, Sotero AJ (2011) Metabolism of carbohydrates during the development of seeds of the brazilian rubber tree [Hevea brasiliensis (Willd. Ex Adr. de Juss) Muell. Arg.]. Acta Physiol Plant 33:211–219. https://doi.org/10.1007/s11738-010-0540-8
Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein. utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1006/abio.1976.9999
Bremner JM (1996) Nitrogen-total. In Sparks DL (ed) Methods of soil analysis, part 3. Soil Science Society of America, Madison, pp 1085–1121
Chaiya C, Reubroycharoen P (2013) Production of bio oil from para rubber seed using pyrolysis process. Energy Procedia 34:905–911. https://doi.org/10.1016/j.egypro.2013.06.828
Chaudhary S, Devi P, Bhardwaj A, Jha UC, Sharma KD, Prasad PVV, Siddique Kadambot HM, Bindumadhava H, Kumar S, Nayyar H (2020) Identification and characterization of contrasting genotypes/cultivars for developing heat tolerance in agricultural crops: current status and prospects. Front Plant Sci. https://doi.org/10.3389/fpls.2020.587264
de Souza LM, Le Guen V, Cerqueira-Silva CBM, Silva CC, Mantello CC, Conson ARO, Vianna JPG, Zucchi MI, Scaloppi Junior EJ, Fialho JF, Moraes MLT, Gonçalves PS, Souza AP (2015) Genetic diversity strategy for the management and use of rubber genetic resources: more than 561 1,000 wild and cultivated accessions in a 100-genotype core collection. PLoS ONE 10(7):e0134607. https://doi.org/10.1371/journal.pone.0134607
Delgado CML, Coelho CM, Buba GP (2015) Mobilization of reserves and vigor of soybean seeds under desiccation with glufosinate ammonium. J Seed Sci 37:154–161. https://doi.org/10.1590/2317-1545v37n2148445
Deng J, Wang K, Mai K, Chen L, Zhang L, Mi H (2017) Effects of replacing fish meal with rubber seed meal on growth, nutrient utilization, and cholesterol metabolism of tilapia (Oreochromis niloticus × O. aureus). Fish Physiol Biochem 43(4):941–954
Eka HD, Tajul Aris Y, Wan Nadiah WA (2010) Potential use of Malaysian rubber (Hevea brasiliensis) seed as food, feed and biofuel. Int Food Res J 17:527–534
Fan Y, Xin S, Dai X, Yang X, Huang H, Hua Y (2020) Efficient genome editing of rubber tree (Hevea brasiliensis) protoplasts using CRISPR/Cas9 ribonucleoproteins. Ind Crops Prod 146:112–146. https://doi.org/10.1016/j.indcrop.2020.112146
Farzaneh V, Ghodsvali A, Bakhshabadi H, Zared Z, Carvalho IS (2017) The impact of germination time on some selected parameters through malting process. Int J Biol Macromol 94:663–668. https://doi.org/10.1016/j.ijbiomac.2016.10.052
Feng LY, Liu J, Gao CW, Wu HB, Li GH, Gao LZ (2020) Higher genomic variation in wild than cultivated rubber trees, Hevea brasiliensis, revealed by comparative analyses of chloroplast genomes. Front Ecol Evol 8:237. https://doi.org/10.3389/fevo.2020.00237
Fernie AR, Roscher A, Ratcli RG, Kruger NJ (2001) Fructose 2, 6-bisphosphate activates pyrophosphate: fructose-6-phosphate 1-phosphotransferase and increases triose phosphate to hexose phosphate cycling in heterotrophic cells. Planta 212:250–263. https://doi.org/10.1007/s004250000386
Finch-Savage WE, Bassel GW (2016) Seed vigour and crop establishment: extending performance beyond adaptation. J Exp Bot 67:567–591. https://doi.org/10.1093/jxb/erv490
Gimbun J, Ali S, Kanwal CCSC, Shah LA, Hidayah N, Cheng CK, Nurdin S (2012) Biodiesel production from rubber seed oil using activated cement clinker as catalyst. Procedia Eng 53:13–19. https://doi.org/10.1016/j.proeng.2013.02.003
Gomez JB (1982) Anatomy of Hevea and its influence on latex production. Kuala Lumpur (Malaysia) Malaysian Rubber Research and Development Board, Publication No. 15
Graham IA (2008) Seed storage oil mobilization. Annal Revista Plant Biol 59:115–142. https://doi.org/10.1146/annurev.arplant.59.032607.092938
Granjeiro PA, Veríssima CF, Aoyama H (2008) Uso de fosfatase ácida como biomarcador durante a germinação de sementes de mamona (Ricinus communis). Eng Ambient Pesqui Tecnol 5(3):307–322
Hossain ME, Karim MH, Alam S, Nath SK (2015) Valor nutricional de sementes de borracha (Hevea brasiliensis). J Anim Feed Res 5:18–21
Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46. https://doi.org/10.1016/j.jplph.2015.12.011
Jisieike CF, Betiku E (2020) Rubber seed oil extraction: effects of solvent polarity, extraction time and solid-solvent ratio on its yield and quality. Biocatal Agric Biotechnol 24:101522. https://doi.org/10.1016/j.bcab.2020.101522
Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York, p 523
Jurkiewicz P, Batoko H (2018) Protein degradation mechanisms modulate abscisic acid signaling and responses during abiotic stress. Plant Sci 267:48–54. https://doi.org/10.1016/j.plantsci.2017.10.017
Karmakar B, Halder G (2019) Progress and future of biodiesel synthesis: advancements in oil extraction and conversion technologies. Energy Convers Manag 182:307–339. https://doi.org/10.1016/j.enconman.2018.12.066
Kitajima K (2002) Do shade-tolerant tropical tree seedlings depend longer on seed reserves? functional growth analysis of three Bignoniaceae species. Funct Ecol 16:433–444. https://doi.org/10.1046/j.1365-2435.2002.00641.x
Kouassi GF, Koné GA, Good M, Assidjo NE, Kouba M (2020) Effect of Hevea brasiliensis seed meal or Euphorbia heterophylla seed supplemented diets on performance, physicochemical and sensory properties of eggs, and egg yolk fatty acid profile in guinea fowl (Numida meleagris). Poult Sci 99:342–349. https://doi.org/10.3382/ps/pez500
Kummar S, Kikon K, Upadhyay A, Kanwar SS, Gupta R (2005) Production, purification, and characterization of lipase from thermophilic and alkaliphilic Bacillus coagulans BTS-3. Protein Expr Purif 41:38–44. https://doi.org/10.1016/j.pep.2004.12.010
Labouriau LG, Valadares MEB (1976) On the germination of seeds Calotropis procera (Ait) Ait f. Anais Da Acad Bras De Ciênc 48(2):263–284
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Latha M, Dolui AK, Vijayaraj P (2021) Proteoform of Arabidopsis seed storage protein identified by functional proteomics approach exhibits acyl hydrolase activity during germination. Int J Biol Macromol 172:452–463. https://doi.org/10.1016/j.ijbiomac.2021.01.074
Lima RBS, Gonçalves JFC, Pando SC, Fernandes AV, Santos ALW (2008) Primary metabolite mobilization during germination in rosewood (Aniba rosaeodora Ducke) seeds. Revista Árvore 32:19–25. https://doi.org/10.1590/S0100-67622008000100003
Lison L (1960) Histochimie et Cytochimie Animales. Principes et Méthodes. Collection des Actualités Biologiques. Gauthier Villars, ed. Paris, p 397
Liu J, Shi C, Shi CC, Li W, Zhang QJ, Zhang Y, Li K, Lu HF, Shi C, Zhu ST, Xiao ZY, Nan H, Yue Y, Zhu XG, Wu Y, Hong XN, Fan GY, Tong Y, Zhang D, Mao CL, Liu YL, Hao SJ, Liu WQ, Lv MQ, Zhang HB, Liu Y, Hu-tang GR, Wang JP, Wang JH, Sun YH, Ni SB, Chen WB, Zhang XC, Jiao YN, Eichler EE, Li GH, Liu X, Gao LZ (2020) The chromosome-based rubber tree genome provides new insights into spurge genome evolution and rubber biosynthesis. Mol Plant 13:336–350. https://doi.org/10.1016/j.molp.2019.10.017
Lopes LS, Gallão MI, Bertini CHCM (2013) Mobilisation of reserves during germination of Jatropha seeds. Rev Ciênc Agron 44:371–378. https://doi.org/10.1590/S1806-66902013000200021
Lourith N, Kanlayavattanakul M (2020) Development of pará rubber seed oil as the efficient makeup remover. Braz J Pharm Sci 56:1–6. https://doi.org/10.1590/s2175-97902019000418029
Lourith N, Kanlayavattanakul M, Sucontphunt A, Ondee T (2014) Rubber seed oil: new promising unconventional oil for cosmetics. J Oleo Sci 63:709–716. https://doi.org/10.5650/jos.ess14015
Mabayo VIF, Aranas JRC, Cagas VJB, Cagas DPA, Ido AL, Arazo RO (2018) Optimization of oil yield from Hevea brasiliensis seeds through ultrasonic-assisted solvent extraction via response surface methodology. Sustain Environ Res 28:39–46. https://doi.org/10.1016/j.serj.2017.08.001
Madsen CK, Brinch-Pedersen H (2020) Globoids and phytase: the mineral storage and release system in seeds. Int J Mol Sci 21:7519. https://doi.org/10.3390/ijms21207519
Magalhães WA, Megaioli TG, Freddi OS, Santos MA (2015) Quantificação de nutrientes em sementes de soja. Rev De Ciênc Agroam 13:95–100
Maguire JD (1962) Speed of germination: aid in selection and evaluation for seedling emergence and vigor. Crop Sci 2:176–177. https://doi.org/10.2135/cropsci1962.0011183X000200020033x
Maia FC, Moraes DM, Moraes RCP (2000) Atividade total da fosfatase ácida e da α-amilase induzidas por ácido jasmônico em sementes de soja. Rev Bras De Sementes 22:259–263
Mesquita AC, Oliveira LEM (2010) Características anatômicas da casca e produção de látex em plantas de seringueira não enxertadas. Acta Amazôn 40:241–246. https://doi.org/10.1590/S0044-59672010000200001
Miray R, Kazaz S, To A, Baud S (2021) Molecular control of oil metabolism in the endosperm of seeds. Int J Mol Sci 22(4):1621
Miyazawa M, Pavan MA, Muraoka T, Carmo CAFS, Mello WJ (1999) Análises químicas de tecido vegetal. In: Silva FC (ed) Manual de análises químicas de solos, plantas e fertilizantes. Brasília: Embrapa Comunicação para Transferência de Tecnologia/Rio de Janeiro: Embrapa Solos/Campinas: Embrapa Informática Agropecuária, pp 171–223
Mohd-Setapar SH, Nian-Yian L, Kamarudin WNW, Idham Z, Norfahana AT (2013) Omega-3 emulsion of Rubber (Hevea brasiliensis) seed oil. Agric Sci 4:84–89. https://doi.org/10.4236/as.2013.45B016
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Nadeem M, Mollier A, Morel C, Vives A, Prud’homme L, Pellerin S (2011) Relative contribution of seed phosphorus reserves and exogenous phosphorus uptake to maize (Zea mays L.) nutrition during early growth stages. Plant Soil 346:231–244. https://doi.org/10.1007/s11104-011-0814-y
Nnadi GL, Simeon-Ahaotub VC, Ríos-Escalante PDL, Ahaotua EO (2022) Replacement level of rubber seed cake for soybean meal on the growth of Japanese quail. Braz J Biol 82:e243242. https://doi.org/10.1590/1519-6984.243242
O’Brien TP, McCully ME (1981) The study of plant structure: principles and selected methods. Termarcaphi Pty Ltd, Melburne 46.
Onoji SE, Iyuke SE, Igbafe AI (2016) Hevea brasiliensis (rubber seed) oil: extraction, characterization, and kinetics of thermo-oxidative degradation using classical chemical methods. Energy Fuels 30:10555–10567. https://doi.org/10.1021/acs.energyfuels.6b02267
Oyekunle JAO, Omode AA (2008) Chemical composition and fatty acid profile of the lipid fractions of selected Nigerian indigenous oilseeds. Int J Food Prop 11:273–281. https://doi.org/10.1080/10942910701302598
Padilha MS, Coelho CMM, Andrade GC (2020) Seed reserve mobilization evaluation for selection of highvigor common bean cultivars. Revis Caatinga 33:927–935. https://doi.org/10.1590/1983-21252020v33n407rc
Patiño JC (1986) Microtecnia vegetal, México: Trillas
Perron T, Mareschal L, Laclau JP, Deffontaines L, Deleporte P, Masson A, Cauchy T, Gay F (2021) Dynamics of biomass and nutrient accumulation in rubber (Hevea brasiliensis) plantations established on two soil types: implications for nutrient management over the immature phase. Ind Crops Prod 159:113084. https://doi.org/10.1016/j.indcrop.2020.113084
Pizzi A, Duca D, Rossini G, Fabrizi S, Toscano G (2020) Biofuel, bioenergy and feed valorization of by-products and residues from hevea brasiliensis cultivation to enhance sustainability. Resources 9(9):114. https://doi.org/10.3390/resources9090114
Raknam P, Pinsuwan S, Amnuaikit T (2018) The effect of extraction methods on the physicochemical properties of para-rubber seed oil and manufacturing worthiness for used as a cosmetic ingrediente. Chiang Mai J Sci 45:440–453
Reshad AS, Tiwari P, Goud VV (2015) Extraction of oil from rubber seeds for biodiesel application: Optimization of parameters. Fuel 150:636–644. https://doi.org/10.1016/j.fuel.2015.02.058
Roschat W, Siritanon T, Yoosuk B (2017) Rubber seed oil as potential non-edible feedstock for biodiesel production using heterogeneous catalyst in Thailand. Renew Energy 101:937–944. https://doi.org/10.1016/j.renene.2016.09.057
Sant’Anna IC, Gouvêa LRL, Spitti AMDS, Martins ALM, Gonçalves PS, (2020) Relationships between yield and some anatomical and morphological traits in rubber tree progenies. Ind Crops Prod 147:112221. https://doi.org/10.1016/j.indcrop.2020.112221
Sant’Anna IC, Gouvêa LRL, Martins MA, Scaloppi Junior EJ, Freitas RS, Gonçalves PS, (2021) Genetic diversity associated with natural rubber quality in elite genotypes of the rubber tree. Sci Rep 11:1081. https://doi.org/10.1038/s41598-020-80110-w
Shao Q, Liu X, Su T, Ma C, Wang P (2019) New Insights Into the Role of Seed Oil Body Proteins in Metabolism and Plant Development. Front Plant Sci 10:1568. https://doi.org/10.3389/fpls.2019.01568
Silva DJ (2010) Análise de alimentos (métodos químicos e biológicos). Universidade Federal de Viçosa, Viçosa, MG, p 165
Silva GP, Sales JF, Nascimento KJT, Rodrigues AA, Camelo GN, Borges EEDL (2020a) Biochemical and physiological changes in Dipteryx alata Vog. seeds during germination and accelerated aging. S Afr J Bot 131:84–92. https://doi.org/10.1016/j.sajb.2020.02.007
Silva AG, Costa E, Pereira TCC, Binotti FFS, Scaloppi Junior EJ, Zoz T (2020b) Quality of rubber tree rootstock seedlings grown in protected environments and alternative substrates. Acta Sci Agron. https://doi.org/10.4025/actasciagron.v42i1.43469
Smith H, Lu J, To PX, Mienmany S, Soukphaxay K (2020) Rubber Plantation Value Chains in Laos: Opportunities and Constraints in Policy, Legality and Wood Processing, report produced for ACIAR project FST/2016/151 - Advancing enhanced wood manufacturing industries in Laos and Australia and Forest Trends. https://www.forest-trends.org/wp-content/uploads/2020/07/Rubber-Plantation-Value-Chains-in-Laos.pdf
Sniezko RA, Koch J (2017) Breeding trees resistant to insects and diseases: putting theory into application. Biol Invasions 19:3377–3400. https://doi.org/10.1007/s10530-017-1482-5
Soltani A, Gholipor M, Zeinali E (2006) Seed reserve utilization and seedling growth of wheat as affected by drought and salinity. Environ Exp Bot 55:195–200. https://doi.org/10.1016/j.envexpbot.2004.10.012
Soriano D, Alvarado-López S, Zúñiga-Sánchez E, Orozco-Segovia A, Gamboa-Debuen A (2015) Analysis of nitrogen seed reserves of ten tree species of the tropical dry forest. S Afr J Bot 97:149–153. https://doi.org/10.1016/j.sajb.2015.01.003
Souza GAD, Dias DCFS, Pimenta TM, Cardoso AA, Pires RMO, Alvarenga AP, Pícoli EAT (2018a) Morpho-anatomical, physiological and biochemical changes in rubber tree seeds. An Acad Bras Ciênc 90:1625–1641. https://doi.org/10.1590/0001-3765201820170340
Souza GAD, Dias DCFS, Pimenta TM, Almeida AL, Toledo Picoli EA, Alvarenga A, Silva JCF (2018b) Sugar metabolism and developmental stages of rubber tree (Hevea brasiliensis L.) seeds. Physiol Plant 162:495–505. https://doi.org/10.1111/ppl.12650
Suda CNK, Giorgini JF (2000) Seed reserve composition and mobilization during germination and initial seedling development of Euphorbia heterophylla. Rev Bras Fisiol Veg 12:226–245. https://doi.org/10.1590/S0103-31312000000300006
Teixeira SP, Machado SR (2008) Storage sites in seeds of Caesalpinia echinata and Caesalpini ferrea (leguminosae) with considerations on nutrients flow. Braz Arch Biol Technol 51:127–136. https://doi.org/10.1590/S1516-89132008000100016
Theodoro GF, Batista TS (2014) Detection of fungi in rubber tree (Hevea brasiliensis) seeds harvested in northeast of Mato Grosso do Sul, Brazil. Revis Agrar 24:365–368
Verma G, Mishra S, Sangwan N, Sharma S (2015) Reactive oxygen species mediate axis-cotyledon signaling to induce reserve mobilization during germination and seedling establishment in Vigna radiata. J Planty Physiol 20:79–88. https://doi.org/10.1016/j.jplph.2015.07.001
Wen Z, Wu Y, Qi Z, Li X, Li F, Wu X, Yanga P (2019) Rubber seed oil supplementation enriches n-3 polyunsaturated fatty acids and reduces cholesterol contents of egg yolks in laying hens. Food Chem 301:125198. https://doi.org/10.1016/j.foodchem.2019.125198
Widyarania E, Ratnaningsihc JPM, Sanders ME (2014) Biorefinery methods for separation of protein and oil fractions from rubber seed kernel. Ind Crops Prod 62:323–332. https://doi.org/10.1016/j.indcrop.2014.09.005
Wu S, Guyot R, Bocs S, Droc G, Oktavia F, Hu S, Tang C, Montoro C, Leclercq J (2020) Structural and Functional Annotation of Transposable Elements Revealed a Potential Regulation of Genes Involved in Rubber Biosynthesis by TE-Derived siRNA Interference in Hevea brasiliensis. Int J Mol Sci 21(12):4220. https://doi.org/10.3390/ijms21124220
Xavier-Filho J, Campos F, Maria AP, Ary B, Silva CP, Carvalho MMM (1989) Poor correlation between the levels of proteinase inhibitors found in seeds of different cultivars of cowpea (Vigna unguiculata) and the resistance/susceptibility to predation by Callosobruchus maculatus. J Agric Food Chem 37:1139–1143. https://doi.org/10.1021/jf00088a071
Yamashita S, Takahashi S (2020) Molecular Mechanisms of Natural Rubber Biosynthesis. Annu Rev Biochem 89(1):821–851. https://doi.org/10.1146/annurev-biochem-013118-111107
Yang MF, Liu YJ, Liu Y, Chen H, Chen F, Shen SH (2009) Proteomic analysis of oil mobilization in seed germination and post germination development of Jathropa curcas. J Proteome Res 8:1441–1451. https://doi.org/10.1021/pr800799s
Yang M, Zhu W, Cao H (2021) Biorefinery methods for extraction of oil and protein from rubber seed. Bioresour Bioprocess 8:45. https://doi.org/10.1186/s40643-021-00386-2
Yu Y, Guo G, Lv D, Hu Y, Li J, Li X, Yan Y (2014) Transcriptome analysis during seed germination of elite Chinese bread wheat cultivar Jimai 20. BMC Plant Biol 14:20. https://doi.org/10.1186/1471-2229-14-20
Zaynab M, Pan D, Fatima M, Sharif Y, Chen S, Chen W (2021) Proteomics analysis of Cyclobalanopsis gilva provides new insights of low seed germination. Biochimie 180:68–78. https://doi.org/10.1016/j.biochi.2020.10.008
Zhao M, Zhang H, Yan H, Qiu L, Baskin CC (2018) Mobilization and Role of Starch, Protein, and Fat Reserves during Seed Germination of Six Wild Grassland Species. Front Plant Sci. https://doi.org/10.3389/fpls.2018.00234
Acknowledgements
The authors thank the Ministry of Science, Technology and Innovations/National Institute for Amazonian Research (MCTI/INPA), as well as the members of the Laboratory of Physiology and Plant Biochemistry of INPA (LFBV) for the availability of equipment and infrastructure for analysis, in especially MSc. Rafaela Oliveira da Silva and Dra. Joelma Keith Rodrigues for helping with enzymatic and histochemical analysis, respectively. We too want to thank the Coordination for the Improvement of Higher-Level Personnel (CAPES—Pro-Amazonia: Biodiversity and Sustainability—Nº52/2012)—Brazil, National Council for Scientific and Technological Development (CNPq, Brazil) and Amazonas State Research Support Foundation (FAPEAM) for finantial supporting this study. José F. de C. Gonçalves, Eduardo E. de L. e Borges, Marcio V. Ramos, Adriano N. Nesi and Wagner L. Araújo acknowledge research productivity grant – PQ provided by CNPq.
Funding
Coordenação de Aperfeiçoamento de Pessoal de Nível Superior,Finance Code 001 José Francisco de Carvalho Gonçalves,Conselho Nacional de Desenvolvimento Científico e Tecnológico 308373/2019-7,José Francisco de Carvalho Gonçalves.
Author information
Authors and Affiliations
Contributions
JCC and JFC—planned and designed the research. JCC—performed the experiments. JCC—analyzed the data. JCC, AVF, DPS, WLA, MVR, ANN, BR and JFC wrote the text. All authors read, commented on and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by A. Gniazdowska-Piekarska.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
de Carvalho, J.C., de Carvalho Gonçalves, J.F., Fernandes, A.V. et al. Reserve mobilization and the role of primary metabolites during the germination and initial seedling growth of rubber tree genotypes. Acta Physiol Plant 44, 80 (2022). https://doi.org/10.1007/s11738-022-03415-5
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11738-022-03415-5