Abstract
The pre-germinative metabolism is among the most fascinating aspects of seed biology. The early seed germination phase, or pre-germination, is characterized by rapid water uptake (imbibition), which directs a series of dynamic biochemical events. Among those are enzyme activation, DNA damage and repair, and use of reserve storage compounds, such as lipids, carbohydrates and proteins. Industrial seedling production and intensive agricultural production systems require seed stocks with high rate of synchronized germination and low dormancy. Consequently, seed dormancy, a quantitative trait related to the activation of the pre-germinative metabolism, is probably the most studied seed trait in model species and crops. Single omics, systems biology, QTLs and GWAS mapping approaches have unveiled a list of molecules and regulatory mechanisms acting at transcriptional, post-transcriptional and post-translational levels. Most of the identified candidate genes encode for regulatory proteins targeting ROS, phytohormone and primary metabolisms, corroborating the data obtained from simple molecular biology approaches. Emerging evidences show that epigenetic regulation plays a crucial role in the regulation of these mentioned processes, constituting a still unexploited strategy to modulate seed traits. The present review will provide an up-date of the current knowledge on seed pre-germinative metabolism, gathering the most relevant results from physiological, genetics, and omics studies conducted in model and crop plants. The effects exerted by the biotic and abiotic stresses and priming are also addressed. The possible implications derived from the modulation of pre-germinative metabolism will be discussed from the point of view of seed quality and technology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Akman Z (2009) Comparison of high temperature tolerance in maize, rice and sorghum seeds by plant growth regulators. J Anim Vet Adv 8:358–361
Anup CP, Melvin P, Shilpa N, Gandhi MN, Jadhav M, Ali H, Kini KR (2015) Proteomic analysis of elicitation of downy mildew disease resistance in pearl millet by seed priming with β-aminobutyric acid and Pseudomonas fluorescens. J Proteomics 120:58–74. doi:10.1016/j.jprot.2015.02.013
Araújo SS, Beebe S, Crespi M et al (2015) Abiotic stress responses in legumes: strategies used to cope with environmental challenges. Crit Rev Plant Sci 34:237–280. doi:10.1080/07352689.2014.898450
Araújo SS, Paparella S, Dondi D et al (2016) Physical methods for seed invigoration: advantages and challenges in seed technology. Front Plant Sci 7:646. doi:10.3389/fpls.2016.00646
Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signalling. Nature 448:938–942. doi:10.1038/nature06069
Bailly C, El-Maarouf-Bouteau H, Corbineau F (2008) From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiology. CR Biol 331:806–814. doi:10.1016/j.crvi.2008.07.022
Balestrazzi A, Confalonieri M, Macovei A, Donà M, Carbonera D (2011a) Genotoxic stress and DNA repair in plants: emerging functions and tools for improving crop productivity. Plant Cell Rep 30:287–295. doi:10.1007/s00299-010-0975-9
Balestrazzi A, Confalonieri M, Macovei A, Carbonera D (2011b) Seed imbibition in Medicago truncatula Gaertn.: expression profiles of DNA repair genes in relation to PEG-mediated stress. J Plant Physiol 168:706–713. doi:10.1016/j.jplph.2010.10.008
Balestrazzi A, Donà M, Macovei A, Sabatini ME, Pagano A, Carbonera D (2015) DNA repair and telomere maintenance during seed imbibition: correlation of transcriptional patterns. Telomere Telomerase 2:e496. doi:10.14800/tt.496
Barba-Espin G, Diaz-Vivancos P, Job D, Belghazi M, Job C, Hernandez JA (2011) Understanding the role of H2O2 during pea seed germination: a combined proteomic and hormone profiling approach. Plant Cell Environ 34:1907–1919. doi:10.1111/j.1365-3040.2011.02386.x
Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297. doi:10.1016/S0092-8674(04)00045-5
Basbouss-Serhal I, Soubigou-Taconnat L, Bailly C, Leymarie J (2015) Germination potential of dormant and nondormant arabidopsis seeds is driven by distinct recruitment of messenger RNAs to polysomes. Plant Physiol 168:1049–1065. doi:10.1104/pp.15.00510
Bassel GW, Lan H, Glaab E et al (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108:9709–9714. doi:10.1073/pnas.1100958108
Benatti MR, Yookongkaew N, Meetam M, Guo WJ, Punyasuk N, AbuQamar S, Goldsbrough P (2014) Metallothionein deficiency impacts copper accumulation and redistribution in leaves and seeds of Arabidopsis. New Phytol 202:940–951. doi:10.1111/nph.12718
Bennetzen JL, Zhu J-K (2011) Epigenetics of the epigenome. Curr Opin Plant Biol 14:113–115. doi:10.1016/j.pbi.2011.03.015
Bentsink L, Koornneef M (2008) Seed dormancy and germination. Arabidopsis Book 6:e0119. doi:10.1199/tab.0119
Bewley JD (1997) Seed germination and dormancy. Plant Cell 9:1055–1066. doi:10.1105/tpc.9.7.1055
Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: physiology of development, germination and dormancy. Springer, New York. doi:10.1007/978-1-4614-4693-4
Bhattacharjee S (2013) Heat and chilling induced disruption of redox homeostasis and its regulation by hydrogen peroxide in germinating rice seeds (Oryza sativa L., Cultivar Ratna). Physiol Mol Biol Plant 19:199–207. doi:10.1007/s12298-012-0159-x
Bhushan B, Pal A, Kumar S, Rajesh Singh A (2015) Evaluation of post-germinative lipid peroxidation and enzymatic antioxidant potential in lead absorbing oat (Avena sativa) seedlings. J Environ Biol 36:279–288
Bykova NV, Hoehn B, Rampitsch C, Banks T, Stebbing J-A, Fan T, Knox R (2011) Redox-sensitive proteome and antioxidant strategies in wheat seed dormancy control. Proteomics 11:865–882. doi:10.1002/pmic.200900810
Catusse J, Job C, Job D (2008) Transcriptome- and proteome-wide analyses of seed germination. C R Biol 331:815–822. doi:10.1016/j.crvi.2008.07.023
Chavan JK, Kadam SS, Beuchat LR (1989) Nutritional improvement of cereals by sprouting. Crit Rev Food Sci Nutr 28:401–437. doi:10.1080/10408398909527508
Chen H, Chu P, Zhou Y, Li Y, Liu J, Ding Y, Tsang EWT, Jiang L, Wu K, Huang S (2012) Overexpression of AtOGG1, a DNA glycosylase/AP lyase, enhances seed longevity and abiotic stress tolerance in Arabidopsis. J Exp Bot 63:4107–4121. doi:10.1093/jxp/ers093
Cheng J, Wang L, Zeng P, He Y, Zhou R, Zhang H, Wang Z (2016) Identification of genes involved in rice seed priming in the early imbibition stage. Plant Biol (Stuttg.). doi:10.1111/plb.12438
Choudhary M, Jayanand Padaria JC (2015) Transcriptional profiling in pearl millet (Pennisetum glaucum L.R. Br.) for identification of differentially expressed drought responsive genes. Physiol Mol Biol Plant 21:187–196. doi:10.1007/s12298-015-0287-1
Chung PJ, Park BS, Wang H et al (2016) Light-inducible MiR163 targets PXMT1 transcripts to promote seed germination and primary root elongation in Arabidopsis. Plant Physiol 170:1772–1782. doi:10.1104/pp.15.01188
Colville A, Alhattab R, Hu M et al (2011) Role of HD2 genes in seed germination and early seedling growth in Arabidopsis. Plant Cell Rep 30:1969–1979. doi:10.1007/s00299-011-1105-z
Corbineau F, Xia Q, Bailly C, El-Maarouf-Bouteau H (2014) Ethylene, a key factor in the regulation of seed dormancy. Front Plant Sci 5:539. doi:10.3389/fpls.2014.00539
Daszkowska-Golec A (2011) Arabidopsis seed germination under abiotic stress as a concert of action of phytohormones. OMICS 15:763–774. doi:10.1089/omi.2011.0082
Dekkers BJW, Schuurmans JAMJ, Smeekens SCM (2004) Glucose delays seed germination in Arabidopsis thaliana. Planta 218:579–588. doi:10.007/s00425-003-1154-9
Diaz-Vivancos P, Barba-Espin G, Hernandez JA (2013) Elucidating hormonal/ROS networks during seed germination: insights and perspectives. Plant Cell Rep 32:1491–1502. doi:10.1007/s00299-013-1473-7
Donà M, Balestrazzi A, Mondoni A, Rossi G, Ventura L, Buttafava A, Macovei A, Sabatini ME, Valassi A, Carbonera D (2013) DNA profiling, telomere analysis and antioxidant properties as tools for monitoring ex situ seed longevity. Ann Bot 111:987–998. doi:10.1093/aob/mct058
Dutra SM, Von Pinho EV, Santos HO, Lima AC, Von Pinho RG, Carvalho ML (2015) Genes related to high temperature tolerance during maize seed germination. Genet Mol Res 14:18047–18058. doi:10.4238/2015.December.22.31
El-Adawy TA, Rahma EH, El-Bedawey AA, El-Beltagy AE (2003) Nutritional potential and functional properties of germinated mung bean, pea and lentil seeds. Plant Foods Hum Nutr 58:1–13. doi:10.1023/B:QUAL.0000040339.48521.75
El-Maarouf-Bouteau H, Meimoun P, Job C, Job D, Bailly C (2013) Role of protein and mRNA oxidation in seed dormancy and germination. Front Plant Sci 4:77. doi:10.3389/fpls.2013.00077
El-Maarouf-Bouteau H, Sajjad Y, Bazin J, Langlade N, Cristescu SM, Balzergue S, Baudouin E, Bailly C (2015) Reactive oxygen species, abscisic acid and ethylene interact to regulate sunflower seed germination. Plant Cell Environ 38:364–374. doi:10.1111/pce.12371
Essemine J, Ammar S, Bouzid S (2010) Impact of heat stress on germination and growth in higher plants: physiological, biochemical and molecular repercussions and mechanisms of defence. J Biol Sci 10:565–572. doi:10.39923/jbs.2010.565.572
Fercha A, Capriotti AL, Caruso G, Cavaliere C, Samperi R, Stampachiacchiere S, Laganà A (2014) Comparative analysis of metabolic proteome variation in ascorbate-primed and unprimed wheat seeds during germination under salt stress. J Proteomics 108:238–257. doi:10.1016/j.jprot.2014.04.040
Finch-Savage WE, Bassel GW (2016) Seed vigour and crop establishment: extending performance beyond adaptation. J Exp Bot 67:567–591. doi:10.1093/jxb/erv490
Finch-Savage WE, Cadman CSC, Toorop PE et al (2007) Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J 51:60–78. doi:10.1111/j.1365-313X.2007.03118.x
Finkelstein R, Reeves W, Ariizumi T, Steber C (2008) Molecular aspects of seed dormancy. Annu Rev Plant Biol 59:387–415. doi:10.1146/annurev.arplant.59.032607.092740
Galhaut L, de Lespinay A, Walker DJ, Bernal MP, Correal E, Lutts S (2014) Seed priming of Trifolium repens L improved germination and early seedling growth on heavy metal-contaminated soil. Water Air Soil Pollut 225:1905. doi:10.1007/s11270-014-1905-1
Ghoshal N, Talapatra S, Talukder P, Sengupta M, Ray SK, Chakraborty A, Raychaudhuri SS (2015) Cross-adaptation to cadmium stress in Plantago ovata by pre-exposure to low dose of gamma rays: effects on metallothionein and metal content. Int J Radiat Biol 91:611–623. doi:10.3109/09553002.2015.1047984
Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48:909–930. doi:10.1016/j.plaphy.2010.08.016
Global Seed Market (2016–2020) Mordor Intelligence, India
Global Seed Market Report: 2016 edition. Koncept analytics. http://www.conceptanalytics.com
Golldack D, Li C, Mohan H, Probst N (2013) Gibberellins and abscisic acid signal crosstalk: living and developing under unfavorable conditions. Plant Cell Rep 32:1007–1016. doi:10.1007/s00299-013-1409-2
Gu X-Y, Turnipseed EB, Foley ME (2008) The qSD12 locus controls offspring tissue-imposed seed dormancy in rice. Genetics 179:2263–2273. doi:10.1534/genetics.108.092007
Hasanuzzaman M, Hossain MA, Fujita M (2010) Selenium in higher plants: physiological role, antioxidant metabolism and abiotic stress tolerance. J Plant Sci 5:354–375
Hasanuzzaman M, Nahar K, Alam MM, Roychowdhury R, Fujita M (2013) Physiological, biochemical, and molecular mechanisms of heat stress tolerance in plants. Int J Mol Sci 14:9643–9684. doi:10.3390/ijms14059643
Hatzig SV, Frisch M, Breuer F et al (2015) Genome-wide association mapping unravels the genetic control of seed germination and vigor in Brassica napus. Front Plant Sci 6:221. doi:10.3389/fpls.2015.00221
Hay FR, Probert RJ (2013) Advances in seed conservation of wild plant species: a review of recent research. Conserv Physiol 1:cot030. doi:10.1093/conphys/cot030
Hayashi K (2012) The interaction and integration of auxin signaling components. Plant Cell Physiol 53:965–975. doi:10.1093/pcp/pcs035
He D, Wang Q, Wang K, Yang P (2015) Genome-wide dissection of the MicroRNA expression profile in rice embryo during early stages of seed germination. PLoS One 10:e0145424. doi:10.1371/journal.pone.0145424
He H, Willems LAJ, Batushansky A et al (2016) Effects of parental temperature and nitrate on seed performance are reflected by partly overlapping genetic and metabolic pathways. Plant Cell Physiol 57:473–487. doi:10.1093/pcp/pcv207
Holdsworth MJ, Bentsink L, Soppe WJJ (2008a) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179:33–54. doi:10.1111/j.1469-8137.2008.02437.x
Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008b) Post-genomics dissection of seed dormancy and germination. Trends Plant Sci 13:7–13. doi:10.1016/j.tplants.2007.11.002
Holman TJ, Jones PD, Russell L et al (2009) The N-end rule pathway promotes seed germination and establishment through removal of ABA sensitivity in Arabidopsis. Proc Natl Acad Sci USA 106:4549–4554. doi:10.1073/pnas.0810280106
Hori K, Sato K, Takeda K (2007) Detection of seed dormancy QTL in multiple mapping populations derived from crosses involving novel barley germplasm. Theor Appl Genet 115:869–876. doi:10.1007/s00122-007-0620-3
Howell KA, Narsai R, Carroll A et al (2009) Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol 149:961–980. doi:10.1104/pp.108.129874
Huo H, Henry IM, Coppoolse ER et al (2016a) Rapid identification of lettuce seed germination mutants by bulked segregant analysis and whole genome sequencing. Plant J. doi:10.1111/tpj.13267
Huo H, Wei S, Bradford KJ (2016b) DELAY OF GERMINATION1 (DOG1) regulates both seed dormancy and flowering time through microRNA pathways. Proc Natl Acad Sci USA 113:E2199–E2206. doi:10.1073/pnas.1600558113
Ibrahim EA (2016) Seed priming to alleviate salinity stress in germinating seeds. J Plant Physiol 192:38–46. doi:10.1016/j.jplph.2015.12.011
Imtiaz M, Ogbonnaya FC, Oman J, van Ginkel M (2008) Characterization of quantitative trait loci controlling genetic variation for preharvest sprouting in synthetic backcross-derived wheat lines. Genetics 178:1725–1736. doi:10.1534/genetics.107.084939
Ishibashi Y, Tawaratsumida T, Kondo K, Kasa S, Sakamoto M, Aoki N, Zheng SH, Yuasa T, Iwaya-Inoue M (2012) Reactive oxygen species are involved in gibberellin/abscisic acid signaling in barley aleurone cells. Plant Physiol 158:1705–1714. doi:10.1104/pp.111.192740
Ishibashi Y, Koda Y, Zheng SH, Yuasa T, Iwaya-Inoue M (2013) Regulation of soybean seed germination through ethylene production in response to reactive oxygen species. Ann Bot 111:95–102. doi:10.1093/aob/mcs240
Jain M, Prasad PVV, Boote KJ, Hartwell AL, Chourey PS (2007) Effects of season-long high temperature growth conditions on sugar-to-starch metabolis in developing microspores of grain sorghum (Sorghum bicolor L. Moench.). Planta 227:67–79. doi:10.1007/s00425-0595-y
Jones-Rhoades MW, Bartel DP, Bartel B (2006) MicroRNAS and their regulatory roles in plants. Annu Rev Plant Biol 57:19–53. doi:10.1146/annurev.arplant.57.032905.105218
Kalischuk ML, Johnson D, Kawchuk LM (2015) Priming with a double-stranded DNA virus alters Brassica rapa seed architecture and facilitates a defense response. Gene 557:130–137. doi:10.1016/j.gene.2014.12.016
Kapazoglou A, Drosou V, Argiriou A et al (2013) The study of a barley epigenetic regulator, HvDME, in seed development and under drought. BMC Plant Biol 13:172. doi:10.1186/1471-2229-13-172
Kaushal N, Bhandari K, Siddique KHM, Nayyar H (2016) Food crops face rising temperatures: an overview of responses, adaptative mechanisms, and approaches to improve heat tolerance. Conget Food Agric 2:1134380. doi:10.1080/23311932.2015.1134380
Kim JH, Hyun WY, Nguyen HN, Jeong CY, Xiong L, Hong SW, Lee H (2015) AtMyb7, a subgroup 4 R2R3 Myb, negatively regulates ABA-induced inhibition of seed germination by blocking the expression of the bZIP transcription factor ABI5. Plant Cell Environ 38:559–571. doi:10.1111/pce.12415
Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9:29. doi:10.1186/1746-4811-9-29
Kranner I, Colville L (2011) Metals and seeds: biochemical and molecular implications and their significance for seed germination. Environ Exp Bot 72:93–105
Kranner I, Kastberger G, Hartbauer M, Pritchard HW (2010a) Noninvasive diagnosis of seed viability using infrared thermography. Proc Natl Acad Sci USA 107:3912–3917. doi:10.1073/pnas.0914197107
Kranner I, Minibayeva FV, Beckett RP, Seal CE (2010b) What is stress? Concepts, definitions and applications in seed science. New Phytol 188:655–673. doi:10.1111/j.1469-8137.2010.03461.x
Kretzschmar T, Pelayo MAF, Trijatmiko KR, Gabunada LFM, Alam R, Jimenez R, Mendioro MS, Slamet-Loedin IH, Sreenivasulu N, Bailey-Serres J, Ismail AM, Mackill DJ, Septiningsih EM (2015) A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice. Nat Plants. doi:10.1038/nplants.2015.124
Kubala S, Garnczarska M, Wojtyla L, Clippe A, Kosmala A, Zmienko A, Lutts S, Quinet M (2015) Deciphering priming-induced improvement of rapeseed (Brassica napus L.) germination through an integrated transcriptomic and proteomic approach. Plant Sci 231:94–113. doi:10.1016/j.plantsci.2014.11.008
Kumar S, Gupta D, Nayyar H (2012) Comparative response of maize and rice genotypes to heat stress: status of oxidative stress and antioxidants. Acta Physiol Plant 34:75–86. doi:10.1007/s11738-011-0806-9
Kumar JSP, Prasad RS, Banerjee R, Thammineni C (2015) Seed birth to death: dual actions of reactive oxygen species in seed physiology. Ann Bot 116:663–668. doi:10.1093/aob/mcv098
Lafta A, Mou B (2013) Evaluation of lettuce genotypes for seed thermotolerance. HortScience 48:708–714
Lariguet P, Ranocha P, De Meyer M, Barbier O, Penel C, Dunand C (2013) Identification of a hydrogen peroxide signalling pathway in the control of light-dependent germination in Arabidopsis. Planta 238:381–395. doi:10.1007/s00425-013-1901-5
Lee SC, Luan S (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant Cell Environ 35:53–60. doi:10.1111/j.1365-3040.2011.02426.x
Lefevre I, Marchal G, Correal E, Zanuzzi A, Lutts S (2009) Variation in response to heavy metals during vegetative growth in Dorycnium pentaphyllum Scop. Plant Growth Regul 59:1–11. doi:10.1007/s10725-009-9382-z
Li WQ, Khan MA, Yamaguchi S, Kamiya Y (2005) Effects of heavy metals on seed germination and early seedling growth of Arabidopsis thaliana. Plant Growth Regul 46:45–50. doi:10.1007/s10725-005-6324-2
Li J, Naeem MS, Wang X et al (2015) Nano-TiO2 is not phytotoxic as revealed by the oilseed rape growth and photosynthetic apparatus ultra-structural response. PLoS One 10:e0143885. doi:10.1371/journal.pone.0143885
Llanes A, Andrade A, Masciarelli O, Alemano S, Luna V (2015) Drought and salinity alter endogenous hormonal profiles at the seed germination phase. Seed Sci Res. doi:10.1017/S0960258515000331
Long TA, Brady SM, Benfey PN (2008) Systems approaches to identifying gene regulatory networks in plants. Annu Rev Cell Dev Biol 24:81–103. doi:10.1146/annurev.cellbio.24.110707.175408
Lu X-J, Zhang X-L, Mei M et al (2016) Proteomic analysis of Magnolia sieboldii K. Koch seed germination. J Proteomics 133:76–85. doi:10.1016/j.jprot.2015.12.005
Ma F, Ni L, Liu L, Li X, Zhang H, Zhang A, Tan M, Jiang M (2016) ZmABA2, an interacting protein of ZmMPK5, is involved in abscisic acid biosynthesis and functions. Plant Biotechnol J 14:771–782. doi:10.1111/pbi.12427
Macovei A, Balestrazzi A, Confalonieri M, Faé M, Carbonera D (2011a) New insights on the barrel medic MtOGG1 and MtFPG functions in relation to oxidative stress response in planta and during seed imbibition. Plant Physiol Biochem 49:1040–1050. doi:10.1016/j.plaphy.2011.05.007
Macovei A, Balestrazzi A, Confalonieri M, Buttafava A, Carbonera D (2011b) The TFIIS and TFIIS-like genes from Medicago truncatula are involved in the oxidative stress response. Gene 470:20–30. doi:10.1016/j.gene.2010.09.004
Macovei A, Garg B, Raikwar S, Balestrazzi A, Carbonera D, Buttafava A, Bremont JF, Gill SS, Tuteja N (2014) Synergistic exposure of rice seeds to different doses of γ-ray and salinity stress resulted in increased antioxidant enzyme activities and gene-specific modulation of TC-NER pathway. Biomed Res Int 2014:676934. doi:10.1155/2014/676934
Magwa RA, Zhao H, Xing Y (2016) Genome-wide association mapping revealed a diverse genetic basis of seed dormancy across subpopulations in rice (Oryza sativa L.). BMC Genet 17:28. doi:10.1186/s12863-016-0340-2
Malan HL, Farrat JM (1998) Effects of the metal pollutants cadmium and nickel on soybean seed development. Seed Sci Res 8:445–453
Mene-Saffrane L, Jones AD, DellaPenna D (2010) Plastochromanol-8 and tocopherols are essential lipid-soluble antioxidants during seed desiccation and quiescence in Arabidopsis. Proc Nat Acad Sci USA 107:17815–17820. doi:10.1073/pnas.1006971107
Miransari M, Smith DL (2009) Rhizobial lipo-chitooligosaccharides and gibberellins enhance barley (Hordeum vulgare L.) seed germination. Biotechnology 8:270–275. doi:10.3923/biotech.2009.270.275
Miransari M, Smith DL (2014) Plant hormones and seed germination. Environ Exp Bot 99:110–121. doi:10.1016/j.envexpbot.2013.11.005
Mochida K, Shinozaki K (2011) Advances in omics and bioinformatics tools for systems analyses of plant functions. Plant Cell Physiol 52:2017–2038. doi:10.1093/pcp/pcr153
Mock H-P, Dietz K-J (2016) Redox proteomics for the assessment of redox-related posttranslational regulation in plants. Biochem Biophys Acta. doi:10.1016/j.bbapap.2016.01.005
Molitor AM, Bu Z, Yu Y, Shen W-H (2014) Arabidopsis AL PHD-PRC1 complexes promote seed germination through H3K4me3-to-H3K27me3 chromatin state switch in repression of seed developmental genes. PLoS Genet 10:e1004091. doi:10.1371/journal.pgen.1004091
Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72:452–474. doi:10.1016/j.jprot.2008.12.002
Moreno-Risueno MA, Busch W, Benfey PN (2010) Omics meet networks—using systems approaches to infer regulatory networks in plants. Curr Opin Plant Biol 13:126–131. doi:10.1016/j.pbi.2009.11.005
Mostek A, Borner A, Weidner S (2016) Comparative proteomic analysis of β-aminobutyric acid-mediated alleviation of salt stress in barley. Plant Physiol Biochem 99:150–161. doi:10.1016/j.plaphy.2015.12.007
Muscolo A, Junker A, Klukas C, Weigelt-Fischer K, Riewe D, Altmann T (2015) Phenotypic and metabolic responses to drought and salinity of four contrasting lentil accessions. J Exp Bot 66:5467–5480. doi:10.1093/jxb/erv208
Nakabayashi K, Okamoto M, Koshiba T, Kamiya Y, Nambara E (2005) Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41:697–709. doi:10.1111/j.1365-313X.2005.02337.x
Nambara E, Nonogaki H (2012) Seed biology in the 21st Century: perspectives and new directions. Plant Cell Physiol 53:1–4. doi:10.1093/pcp/pcr184
Nawaz F, Ashraf MY, Ahmad R, Waraich EA (2013) Selenium (Se) seed priming induced growth and biochemical changes in wheat under water deficit conditions. Biol Trace Elem Res 151:284–293. doi:10.1007/s12011-012-9556-9
Nguyen HT, Silva JE, Podicheti R, Macrander J, Yang W, Nazarenus TJ, Nam J-W, Jaworski JG, Lu C, Scheffer BE, Mockaitis K, Cahoon EB (2013) Camelina seed transcriptome: a tool for meal and oil improvement and translational research. Plant Biotechnol J 11:759–769
Nonogaki H (2014) Seed dormancy and germination-emerging mechanisms and new hypotheses. Front Plant Sci 5:233. doi:10.3389/fpls.2014.00233
Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Saquar R, Fevereiro PS, Davis BG, Paul MJ (2013) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose 1-phosphate in combination with trehalose 6-phosphate. Plant Physiol Biochem 63:89–98. doi:10.1016/j.plaphy.2012.11.011
Ogawa M, Hanada A, Yamauchi Y, Kuwahara A, Kamiyara Y, Yamaguchi S (2003) Gibberellin biosynthesis and response during Arabidopsis seed germination. Plant Cell 15:1591–1604
Ogbonnaya FC, Imtiaz M, Ye G et al (2008) Genetic and QTL analyses of seed dormancy and preharvest sprouting resistance in the wheat germplasm CN10955. Theor Appl Genet 116:891–902. doi:10.1007/s00122-008-0712-8
Oracz K, El-Maarouf-Bouteau H, Kranner I, Bogatek R, Corbineau F, Bailly C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiol 150:494–505. doi:10.1104/pp.109.138107
Pandey GK, Cheong YH, Kim K-N et al (2004) The calcium sensor calcineurin B-like 9 modulates abscisic acid sensitivity and biosynthesis in Arabidopsis. Plant Cell 16:1912–1924. doi:10.1105/tpc.021311
Paparella S, Araújo SS, Rossi G, Wijayasinghe M, Carbonera D, Balestrazzi A (2015) Seed priming: state of the art and new perspectives. Plant Cell Rep 34:1281–1293. doi:10.1007/s00299-015-1784-y
Parreira JR, Bouraada J, Fitzpatrick MA, Silvestre S, Bernardes da Silva A, Marques da Silva J, Almeida AM, Fevereiro P, Altelaar AF, Araujo SS (2016) Differential proteomics reveals the hallmarks of seed development in common bean (Phaseolus vulgaris L.). J Proteomics. doi:10.1016/j.jprot.2016.03.002
Pawłowski TA, Staszak AM (2016) Analysis of the embryo proteome of sycamore (Acer pseudoplatanus L.) seeds reveals a distinct class of proteins regulating dormancy release. J Plant Physiol 195:9–22. doi:10.1016/j.jplph.2016.02.017
Penfield S, Li Y, Gilday AD, Graham S, Graham IA (2006) Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. Plant Cell 18:1887–1899. doi:10.1105/tpc.106.041277
Piramila BHM, Prabha AL, Nandagopalan V, Stanley AL (2012) Effect of heat treatment on germination, seedling growth and some biochemical parameters of dry seeds of black gram. eIJPPR 1:194–202
Qi W, Zhang L, Wang L, Xu H, Jin Q, Jiao Z (2015) Pretreatment with low-dose gamma irradiation enhances tolerance to the stress of cadmium and lead in Arabidopsis thaliana seedlings. Ecotoxicol Environ Saf 115:243–249. doi:10.1016/j.ecoenv.2015.02.026
Ragonnaud M (2013) The EU seed and plant reproductive material market in perspective: a focus on companies and market shares. Policy Department B: Structural and Cohesion Policies. European Parliament Committee on Agriculture and Rural Development. Brussels: European Commission. doi:10.2861/46869
Rajjou L, Belghazi M, Huguet R, Robin C, Moreau A, Job C, Job D (2006) Proteomic investigation of the effect of salicylic acid on Arabidopsis seed germination and establishment of early defense mechanisms. Plant Physiol 141:910–923. doi:10.1104/pp.106.082057
Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533. doi:10.1146/annurev-arplant-042811-105550
Rasheed R, Wahid A, Farooq M, Hussain I, Basra SMA (2011) Role of proline and glycinebetaine pretreatments in improving tolerance of sprouting sugarcane (Saccharum sp.). Plant Growth Regul 65:35. doi:10.1007/s10725-011-9572-3
Rohn H, Junker A, Hartmann A et al (2012) VANTED v2: a framework for systems biology applications. BMC Syst Biol 6:139. doi:10.1186/1752-0509-6-139
Ruffini Castiglione M, Giorgetti L, Cremonini R, Bottega S, Spanò C (2014) Impact of TiO2 nanoparticles on Vicia narbonensis L.: potential toxicity effects. Protoplasma 251:1471–1479. doi:10.1007/s00709-014-0649-5
Ruppel NJ, Hangarter RP (2007) Mutations in a plastid-localized elongation factor G alter early stages of plastid development in Arabidopsis thaliana. BMC Plant Biol 7:37. doi:10.1186/1471-2229-7-37
Sato K, Yamane M, Yamaji N et al (2016) Alanine aminotransferase controls seed dormancy in barley. Nat Commun 7:11625. doi:10.1038/ncomms11625
Sharma KK, Singh US, Sharma P, Kumar A, Sharma L (2015) Seed treatment for sustainable agriculture—a review. J Appl Nat Sci 7:521–539
Shu K, Zhang H, Wang S et al (2013) ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in arabidopsis. PLoS Genet 9:e1003577. doi:10.1371/journal.pgen.1003577
Shu K, Meng YJ, Shuai HW et al (2015) Dormancy and germination: how does the crop seed decide? Plant Biol (Stuttg) 17:1104–1112. doi:10.1111/plb.12356
Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45. doi:10.1016/j.molp.2015.08.010
Sreenivasulu N, Wobus U (2013) Seed-development programs: a systems biology-based comparison between dicots and monocots. Annu Rev Plant Biol 64:189–217. doi:10.1146/annurev-arplant-050312-120215
Sreenivasulu N, Usadel B, Winter A et al (2008) Barley grain maturation and germination: metabolic pathway and regulatory network commonalities and differences highlighted by new MapMan/PageMan profiling tools. Plant Physiol 146:1738–1758. doi:10.1104/pp.107.111781
Sugimoto K, Takeuchi Y, Ebana K et al (2010) Molecular cloning of Sdr4, a regulator involved in seed dormancy and domestication of rice. Proc Natl Acad Sci U S A 107:5792–5797. doi:10.1073/pnas.0911965107
Tan L, Chen S, Wang T, Dai S (2013) Proteomic insights into seed germination in response to environmental factors. Proteomics 13:1850–1870
Tang D, Dong Y, Guo N et al (2014) Metabolomic analysis of the polyphenols in germinating mung beans (Vigna radiata) seeds and sprouts. J Sci Food Agric 94:1639–1647. doi:10.1002/jsfa.6471
Tanou G, Fotopoulos V, Molassiotis A (2012) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front Plant Sci 3:216. doi:10.3389/fpls.2012.00216
Thiam M, Champion A, Diouf D, Ourèye Sy M (2013) NaCl Effects on in vitro germination and growth of some senegalese cowpea (Vigna unguiculata (L.) Walp.) cultivars. ISRN Biotechnol 2013:382–417. doi:10.5402/2013/382417
Thorstensen T, Fischer A, Sandvik SV et al (2006) The Arabidopsis SUVR4 protein is a nucleolar histone methyltransferase with preference for monomethylated H3K9. Nucleic Acids Res 34:5461–5470. doi:10.1093/nar/gkl687
Vaistij FE, Gan Y, Penfield S et al (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proc Natl Acad Sci 110:10866–10871. doi:10.1073/pnas.1301647110
Ventura L, Donà M, Macovei A, Carbonera D, Buttafava A, Mondoni A, Rossi G, Balestrazzi A (2012) Understanding the molecular pathways associated with seed vigor. Plant Physiol Biochem 60:196–206. doi:10.1016/j.plaphy.2012.07.031
Verdier J, Kakar K, Gallardo K, Le Signor C, Aubert G, Schlereth A, Town CD, Udvardi MK, Thompson RD (2008) Gene expression profiling of M. truncatula transcription factors identifies putative regulators of grain legume seed filling. Plant Mol Biol 67:567–580. doi:10.1007/s11103-008-9320-x
Wan JM, Cao YJ, Wang CM, Ikehashi H (2005) Quantitative trait loci associated with seed dormancy in rice. Crop Sci 45:712. doi:10.2135/cropsci2005.0712
Wang LJ, Fan L, Loescher W, Duan W, Liu GJ, Cheng JS, Luo HB, Li SH (2010) Salicylic acid alleviates decreases in photosynthesis under heat stress and accelerates recovery in grapevine leaves. BMC Plant Biol 10:34. doi:10.1186/1471-2229-10-34
Wang Y, Li L, Ye T et al (2011) Cytokinin antagonizes ABA suppression to seed germination of Arabidopsis by downregulating ABI5 expression. Plant J 68:249–261. doi:10.1111/j.1365-313X.2011.04683.x
Wani PA, Khan MS, Zaidi A (2007a) Impact of heavy metal toxicity on plant growth, symbiosis, seed yield and nitrogen uptake in chickpea. Aust J Exp Agric 47:712–720
Wani PA, Khan MS, Zaidi A (2007b) Cadmium, chromium and copper in greengram plants. Agron Sustain Dev 27:145–153
Wani PA, Khan MS, Zaidi A (2008) Effects of heavy metal toxicity on growth, symbiosis, seed yield and metal uptake in pea grown on metal amended soil. B Environ Contam Toxicol 81:152–158. doi:10.1007/s00128-008-9383-z
Waterworth WM, Masnavi G, Bhardwaj RM, Jiang Q, Bray CM, West CE (2010) A plant DNA ligase is an important determinant of seed longevity. Plant J 63:848–860. doi:10.111/j.1365-313X.2010.04285.x
Waterworth WM, Bray CM, West CE (2015) The importance of safeguarding genome integrity in germination and seed longevity. J Exp Bot 66:3549–3558. doi:10.1093/jxb/erv080
Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707. doi:10.1093/jxb/eru392
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309. doi:10.1093/jxb/err030
Wilson HT, Xu K, Taylor AG (2015) Transcriptome analysis of gelatin seed treatment as a biostimulant of cucumber plant growth. Sci World J 2015:1–14. doi:10.1155/2015/391234
Wojtyla L, Lechowska K, Kubala S, Garnczarska M (2016) Different modes of hydrogen peroxide action during seed germination. Front Plant Sci. doi:10.3389/fpls.2016.00066
Xi W, Liu C, Hou X, Yu H (2010) MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 22:1733–1748. doi:10.1105/tpc.109.073072
Xin X, Wan Y, Wang W, Yin G, McLamore ES, Lu X (2013) A real-time, non-invasive, micro-optrode technique for detecting seed viability by using oxigen influx. Sci Rep 3:3057. doi:10.1038/srep03057
Xing M-Q, Zhang Y-J, Zhou S-R et al (2015) Global analysis reveals the crucial roles of DNA methylation during rice seed development. Plant Physiol 168:1417–1432. doi:10.1104/pp.15.00414
Yacoubi R, Job C, Belghazi M, Chaibi W, Job D (2011) Toward characterizing seed vigor in alfalfa through proteomic analysis of germination and priming. J Proteome Res 10:3891–3903. doi:10.1021/pr101274f
Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn JE (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65:1051–1068. doi:10.1093/jxb/ert457
Yan D, Duermeyer L, Leoveanu C, Nambara E (2014) The functions of the endosperm during seed germination. Plant Cell Physiol 55:1521–1533. doi:10.1093/pcp/pcu089
Yano R, Takebayashi Y, Nambara E et al (2013) Combining association mapping and transcriptomics identify HD2B histone deacetylase as a genetic factor associated with seed dormancy in Arabidopsis thaliana. Plant J 74:815–828. doi:10.1111/tpj.12167
Ye N, Zhu G, Liu Y, Zhang A, Li Y, Liu R, Shi L, Jia L, Zhang J (2012) Ascorbic acid and reactive oxygen species are involved in the inhibition of seed germination by abscisic acid in rice seeds. J Exp Bot 63:1809–1822. doi:10.1093/jxb/err336
Yin X, He D, Gupta R, Yang P (2015) Physiological and proteomic analyses on artificially aged Brassica napus seed. Front Plant Sci 6:112. doi:10.3389/fpls.2015.00112
Yu L-X, Liu X, Boge W, Liu X-P (2016a) Genome-wide association study identifies loci for salt tolerance during germination in autotetraploid alfalfa (Medicago sativa L.) using genotyping-by-sequencing. Front Plant Sci 7:956. doi:10.3389/fpls.2016.00956
Yu Y, Zhen S, Wang S et al (2016b) Comparative transcriptome analysis of wheat embryo and endosperm responses to ABA and H2O2 stresses during seed germination. BMC Genom 17:97. doi:10.1186/s12864-016-2416-9
Zhang Y, Chen B, Xu Z, Shi Z, Chen S, Huang X, Chen J, Wang X (2014a) Involvement of reactive oxygen species in endosperm cap weakening and embryo elongation growth during lettuce seed germination. J Exp Bot 65:3189–3200. doi:10.1093/jxb/eru167
Zhang D, Chen L, Li D, Lv B, Chen Y, Chen J, Yan X, Liang J (2014b) OsRACK1 is involved in abscisic acid- and H2O2-mediated signaling to regulate seed germination in rice (Oryza sativa L.). PLoS One 9:e97120. doi:10.1371/journal.pone.0097120
Zhang T, Yu L-X, Zheng P et al (2015) Identification of loci associated with drought resistance traits in heterozygous autotetraploid alfalfa (Medicago sativa L.) using genome-wide association studies with genotyping by sequencing. PLoS One 10:e0138931. doi:10.1371/journal.pone.0138931
Zheng J, Chen F, Wang Z et al (2012) A novel role for histone methyltransferase KYP/SUVH4 in the control of Arabidopsis primary seed dormancy. New Phytol 193:605–616. doi:10.1111/j.1469-8137.2011.03969.x
Zhou C, Labbe H, Sridha S et al (2004) Expression and function of HD2-type histone deacetylases in Arabidopsis development. Plant J 38:715–724. doi:10.1111/j.1365-313X.2004.02083.x
Zhu G, Ye N, Zhang J (2009) Gluctherose-induced delay of seed germination in rice is mediated by the suppression of ABA catabolism rather than an enhancement of ABA biosynthesis. Plant Cell Physiol 50:644–651. doi:10.1093/pcp/pcp022
Acknowledgments
The financial support from University of Pavia (Italy) and Fundação para a Ciência e a Tecnologia (Lisbon, Portugal) is acknowledged through the research unit “GREEN-it: Bioresources for Sustainability” (UID/Multi/04551/2013), as well as S.S.A. post-doctoral grant (SFRH/BPD/108032/2015). A.P. has been awarded with a PhD fellowship granted by the IUSS-Institute for Advanced Study of Pavia. This work has been partially supported by Reg.CE n. 1698/2005 Programma di Sviluppo rurale per la Puglia 2007/2013 (Misura 214—Azione 4 Sub azione a) “SaVeGraINPuglia—Progetti integrati per la Biodiversità-Recupero, caratterizzazione, salvaguardia e valorizzazione di leguminose, cereali da granella e foraggio in Puglia”.Network sponsorship from COST Action FA1306 Plant Phenotyping “The quest for tolerant varieties—phenotyping at the plant and cellular level” is acknowledged.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by N. Sreenivasulu.
Rights and permissions
About this article
Cite this article
Macovei, A., Pagano, A., Leonetti, P. et al. Systems biology and genome-wide approaches to unveil the molecular players involved in the pre-germinative metabolism: implications on seed technology traits. Plant Cell Rep 36, 669–688 (2017). https://doi.org/10.1007/s00299-016-2060-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-016-2060-5