Systems biology of seeds: deciphering the molecular mechanisms of seed storage, dormancy and onset of germination
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Seeds are heterogeneous storage reserves with wide array of storage compounds that include various soluble carbohydrates, starch polymer, storage proteins and lipids. These stored reserves comprise 70% of the world’s caloric intake in the form of food and animal feed produced through sustainable agriculture, which contributes to food and nutritional security. Seed systems biology remains an enigmatic subject in understanding seed storage processes, maturation and pre-germinative metabolism. The reviews and research articles covered in this special issue of Plant Cell Reports highlight recent advances made in the area of seed biology that cover various systems biology applications such as gene regulatory networks, metabolomics, epigenetics and the role of micro-RNA in seed development.
A developing seed consists of triploid endosperm and diploid embryo, which are enclosed by the maternal seed coat. In dicots, the embryo encompasses most of the space in the seed along with major lipid and protein reserves (Borisjuk et al. 2013). In cereals, the endosperm is the major storage sink where starch and storage proteins are accumulated (Olsen 2001). Vast seed genomics resources have been created from various model organisms (North et al. 2010; Olsen 2001; Sreenivasulu and Wobus 2013). The systems biology strategies provide an opportunity to discover complex developmental processes of seeds and decipher holistic molecular mechanisms using large-scale genomics data, transcriptome, metabolome, proteome, non-coding RNAs and epigenetics (Chen et al. 2014; Francki et al. 2016; Le et al. 2010; Li et al. 2016; Wan et al. 2016; Yang et al. 2016). Such top-down systems biology is concerned with the identification of the structure of the molecular network that underlies system behavior. Integration of multiple ‘-omics’ data is required to reconstruct complex networks that characterize the phenotypes in the cell. This leads to the identification of central hub regulatory genes that influence seed storage, maturation, dormancy and transition to seed germination. Exploring central hubs of regulatory networks involved in key transcriptional reprogramming events that assure phase transitions during seed storage is a central component to identify key hub genes that could potentially be used to manipulate seed metabolism (Belmonte et al. 2013; Sreenivasulu et al. 2006). Systems biology approaches combined with flux and spatial data using nuclear magnetic resonance can be used to systematically reveal the molecular mechanisms of seed biology and to decipher the metabolic rate limiting steps influencing seed storage metabolism (Borisjuk et al. 2013; Gupta et al. 2017; Sreenivasulu et al. 2010). Latest advances in seed oil and protein synthesis in dicots pointed out that the efficient conversion of sucrose to glycolysis intermediates in conjunction with higher copies of fatty acid synthesis genes in canola compared to that in soybean might be the causal factor of higher accumulation of oil in canola over soybean (Gupta et al. 2017).
Methionine a sulfur-containing essential amino acid is elevated in Arabidopsis seeds by suppressing Cystathione γ-synthase (CGS) gene, where the RNAi::AtCGS transgenic seeds showed reduced expression (Cohen and Amir 2017). The elevated methionine level in RNAi::AtCGS seeds supports the hypothesis that methionine is synthesized de novo in seeds by decreasing carbon/amino availability in the aspartate pathway using CGS regulatory enzyme. Alternative route to increase methionine in seeds is that a precursor of S-methylmethionine (SMM) that is synthesized in vegetative tissues and transported into the seeds via the phloem, is converted to methionine through homocysteine S-methyltransferase AtHMT3 (Cohen et al. 2017). The data obtained by these two studies shed interesting insights into the functional role of the SMM cycle in seeds and also provided an idea on how to exploit an intrinsic property in the aspartate pathway to manipulate the methionine level in developing seeds.
Small non-coding RNAs are important regulators that control distinct phase transitions such as cellularization (miR165, miR394), seed storage (miR156, miR160) and dormancy (miR159, miR172) during seed development (Rodrigues and Miguel 2017). Liu and El-Kassaby (2017) used small RNA sequencing to identify 14 candidate microRNAs that included a novel miR8172 family that was characterized to be involved in seed storage and dormancy. They highlighted the roles of miR159 and miR319 in regulating the GAMYB transcription factor under the cascade of gibberellic acid responses during the breaking of seed dormancy. The importance of abscisic acid/gibberellic acid signaling network in controlling seed maturation and seed germination processes, respectively, has been reviewed through systems biology implications (Yan and Chen 2017). The current state of the field of pre-germinative seed biology through genomics and reverse genetic approaches has been captured (Macovei et al. 2017). The review highlighted the implications of reactive oxygen species and interconnections to hormones in transitioning from mature to pre-germination events. In addition, basic scientific findings were put into the context of agricultural application by creating links to current trends in seed technology such as seed priming. Results of comparative proteomics studies for instance showed that the accumulation of vicilin during the pre-treatment of two defense elicitors β-amino butyric acid and γ-amino butyric acid in citrus seed germination under salt stress conditions reversed salt stress impediment and improved germination vigor (Ziogas et al. 2017). Two additional studies unraveled the salt tolerance mechanisms through epigenetics (Pandey et al. 2016) and proteomics (Parveda et al. 2017).
The key target genes identified through systems biology approaches need to be subjected to functional validation. CRISPR/Cas9 and CRISPR-Cpf genome editing tools may be used to create mutants where target genes are silenced. Yin et al. (2017) used this technology to knockout EPFL9, a positive regulator of stomatal development. The future scope of seed biology will be to validate the rate limiting enzymes and key regulatory targets influencing seed storage components by characterizing the functional mutants through systems approaches and revalidate the models to engineer seed sink for translational health benefits of consumers. It would not have been possible to bring this special issue without the due help of Editor-in Chief (Dr. G. Hahne and Dr. J. R. Liu) and managing editor Dr. B. Hahne and support team. Their support is greatly appreciated.
- Belmonte MF, Kirkbride RC, Stone SL, Pelletier JM, Bui AQ, Yeung EC, Hashimoto M, Fei J, Harada CM, Munoz MD, Le BH, Drews GN, Brady SM, Goldberg RB, Harada JJ (2013) Comprehensive developmental profiles of gene activity in regions and subregions of the Arabidopsis seed. Proc Natl Acad Sci USA 110:E435–E444CrossRefPubMedPubMedCentralGoogle Scholar
- Cohen H, Amir R (2017) Dose-dependent effects of higher methionine levels on the transcriptome and metabolome of transgenic Arabidopsis seeds. Plant Cell Rep 36:719–730Google Scholar
- Cohen H, Salmon A, Tietel Z, Hacham Y, Amir R (2017) The relative contribution of genes operating in the S-methylmethionine cycle to methionine metabolism in Arabidopsis seeds. Plant Cell Rep. doi: 10.1007/s00299-017-2124-1
- Gupta M, Bhaskar PB, Sriram S, Wang PH (2017) Integration of omics approaches to understand oil/protein content during seed development in oilseed crops. Plant Cell Rep 36:637–652Google Scholar
- Le BH, Cheng C, Bui AQ, Wagmaister JA, Henry KF, Pelletier J, Kwong L, Belmonte M, Kirkbride R, Horvath S, Drews GN, Fischer RL, Okamuro JK, Harada JJ, Goldberg RB (2010) Global analysis of gene activity during Arabidopsis seed development and identification of seed-specific transcription factors. Proc Natl Acad Sci USA 107:8063–8070CrossRefPubMedPubMedCentralGoogle Scholar
- Liu Y, El-Kassaby YA (2017) Regulatory cross-talk between microRNAs and hormone signalling cascades controls the variation on seed dormancy phenotype at Arabidopsis thaliana seed set. Plant Cell Rep. doi: 10.1007/s00299-017-2111-6
- Macovei A, Pagano A, Leonetti P, Carbonera D, Balestrazzi A, Araujo SS (2017) 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 36:669–688Google Scholar
- Pandey G, Yadav CB, Sahu PP, Muthamilarasan M, Prasad M (2016) Salinity induced differential methylation patterns in contrasting cultivars of foxtail millet (Setaria italica L.). Plant Cell Rep. doi: 10.1007/s00299-016-2093-9
- Parveda M, Kiran B, Punita DL, Kavi Kishor PB (2017) Overexpression of SbAP37 in rice alleviates concurrent imposition of combination stresses and modulates different sets of leaf protein profiles. Plant Cell Rep. doi: 10.1007/s00299-017-2134-z
- Rodrigues AS, Miguel CM (2017) The pivotal role of small non-coding RNAs in the regulation of seed development. Plant Cell Rep. doi: 10.1007/s00299-017-2120-5
- Yan A, Chen Z (2017) The pivotal role of abscisic acid signaling during transition from seed maturation to germination. Plant Cell Rep 36:689–703Google Scholar
- Yin X, Biswal AK, Perdigon KM, Balahadia CP, Mazumdar S, Chater C, Dionara J, Lin H, Coe1 R, Kretzschmar C, Gray JE, Quick PW, Bandyopadhyay A (2017) CRISPR-Cas9 and CRISPR-Cpf1 mediated targeting of a stomotal developmental gene EPFL9 in rice. Plant Cell Rep. doi: 10.1007/s00299-017-2118-z
- Ziogas V, Tanou G, Belghazi M, Diamantidis G, Molassiotis A (2017) Characterization of beta-amino- and gamma-amino butyric acid-induced citrus seeds germination under salinity using nanoLC-MS/MS analysis. Plant Cell Rep 36:787–790Google Scholar