Systems Biology for Smart Crops and Agricultural Innovation: Filling the Gaps between Genotype and Phenotype for Complex Traits Linked with Robust Agricultural Productivity and Sustainability.

In recent years, rapid developments in several omics platforms and next generation sequencing technology have generated a huge amount of biological data about plants. Systems biology aims to develop and use well-organized and efficient algorithms, data structure, visualization, and communication tools for the integration of these biological data with the goal of computational modeling and simulation. It studies crop plant systems by systematically perturbing them, checking the gene, protein, and informational pathway responses; integrating these data; and finally, formulating mathematical models that describe the structure of system and its response to individual perturbations. Consequently, systems biology approaches, such as integrative and predictive ones, hold immense potential in understanding of molecular mechanism of agriculturally important complex traits linked to agricultural productivity. This has led to identification of some key genes and proteins involved in networks of pathways involved in input use efficiency, biotic and abiotic stress resistance, photosynthesis efficiency, root, stem and leaf architecture, and nutrient mobilization. The developments in the above fields have made it possible to design smart crops with superior agronomic traits through genetic manipulation of key candidate genes.

[1]  Jacky L. Snoep,et al.  BioModels Database: a free, centralized database of curated, published, quantitative kinetic models of biochemical and cellular systems , 2005, Nucleic Acids Res..

[2]  Gerrit T. S. Beemster,et al.  Leaf development: a cellular perspective , 2014, Front. Plant Sci..

[3]  Markus R Owen,et al.  Growth-induced hormone dilution can explain the dynamics of plant root cell elongation , 2012, Proceedings of the National Academy of Sciences.

[4]  S. Arora,et al.  Modeling of the MAPK machinery activation in response to various abiotic and biotic stresses in plants by a system biology approach , 2013, Bioinformation.

[5]  G. Martin,et al.  Transcriptome and Selected Metabolite Analyses Reveal Multiple Points of Ethylene Control during Tomato Fruit Developmentw⃞ , 2005, The Plant Cell Online.

[6]  Sanjay Mohan Gupta,et al.  Differential expression of genes during banana fruit development, ripening and 1-MCP treatment: Presence of distinct fruit specific, ethylene induced and ethylene repressed expression , 2006 .

[7]  Nicolas Le Novère,et al.  BioModels Database: a repository of mathematical models of biological processes. , 2013, Methods in molecular biology.

[8]  Edison T Liu,et al.  Systems Biology, Integrative Biology, Predictive Biology , 2005, Cell.

[9]  Anil Kumar,et al.  Plant ionomics: a newer approach to study mineral transport and its regulation , 2013, Acta Physiologiae Plantarum.

[10]  Christophe Godin,et al.  Representing and encoding plant architecture: A review , 2000 .

[11]  Jonathan D. G. Jones,et al.  A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence , 2007, Nature.

[12]  Damian Szklarczyk,et al.  STRING v9.1: protein-protein interaction networks, with increased coverage and integration , 2012, Nucleic Acids Res..

[13]  B. Snel,et al.  STRING: a web-server to retrieve and display the repeatedly occurring neighbourhood of a gene. , 2000, Nucleic acids research.

[14]  Jaap Molenaar,et al.  Redefining plant systems biology: from cell to ecosystem. , 2011, Trends in plant science.

[15]  Molly Megraw,et al.  A stele-enriched gene regulatory network in the Arabidopsis root , 2011, Molecular systems biology.

[16]  K. Shinozaki,et al.  Effects of abiotic stress on plants: a systems biology perspective , 2011, BMC Plant Biology.

[17]  Samik Ghosh,et al.  Modeling and simulation using CellDesigner. , 2014, Methods in molecular biology.

[18]  Luonan Chen,et al.  Coexpression network analysis in chronic hepatitis B and C hepatic lesions reveals distinct patterns of disease progression to hepatocellular carcinoma. , 2012, Journal of molecular cell biology.

[19]  Claucia Fernanda Volken de Souza,et al.  Physicochemical and nutritional alterations induced by two-spotted spider mite infestation on strawberry plants , 2014 .

[20]  Yuan Qi,et al.  Modularity and Dynamics of Cellular Networks , 2006, PLoS Comput. Biol..

[21]  Pall I. Olason,et al.  A human phenome-interactome network of protein complexes implicated in genetic disorders , 2007, Nature Biotechnology.

[22]  E. Stone,et al.  The genetics of quantitative traits: challenges and prospects , 2009, Nature Reviews Genetics.

[23]  Chang-xing Zhao,et al.  Some advances in plant stress physiology and their implications in the systems biology era. , 2007, Colloids and surfaces. B, Biointerfaces.

[24]  Nevan J. Krogan,et al.  From systems to structure: bridging networks and mechanism. , 2013, Molecular cell.

[25]  Yukiko Matsuoka,et al.  Using process diagrams for the graphical representation of biological networks , 2005, Nature Biotechnology.

[26]  Nobuhiro Suzuki,et al.  Reactive oxygen species homeostasis and signalling during drought and salinity stresses. , 2010, Plant, cell & environment.

[27]  Tyler Weirick,et al.  Predicting genome-scale Arabidopsis-Pseudomonas syringae interactome using domain and interolog-based approaches , 2014, BMC Bioinformatics.

[28]  T. Ideker,et al.  A new approach to decoding life: systems biology. , 2001, Annual review of genomics and human genetics.

[29]  D. Moller,et al.  New drug targets for type 2 diabetes and the metabolic syndrome , 2001, Nature.

[30]  Se Won Park,et al.  Plant disease resistance genes: Current status and future directions , 2012 .

[31]  Yoko Ikeda,et al.  Plant imprinted genes identified by genome-wide approaches and their regulatory mechanisms. , 2012, Plant & cell physiology.

[32]  Vikram Singh Gaur,et al.  De Novo Assembly and Characterization of Developing Spikes Transcriptome of Finger Millet (Eleusine coracana): a Minor Crop Having Nutraceutical Properties , 2014, Plant Molecular Biology Reporter.

[33]  Sabine Lüthje,et al.  The plasma membrane proteome of maize roots grown under low and high iron conditions. , 2013, Journal of proteomics.

[34]  Yan Li,et al.  Changes in the transcriptomic profiles of maize roots in response to iron-deficiency stress , 2014, Plant Molecular Biology.

[35]  Yves Gibon,et al.  Deciphering genetic diversity and inheritance of tomato fruit weight and composition through a systems biology approach , 2013, Journal of experimental botany.

[36]  Y. Guédon,et al.  Pattern analysis in branching and axillary flowering sequences. , 2001, Journal of theoretical biology.

[37]  Thierry Rouxel,et al.  From model to crop plant-pathogen interactions: cloning of the first resistance gene to Leptosphaeria maculans in Brassica napus. , 2013, The New phytologist.

[38]  François Parcy,et al.  Deciphering gene regulatory networks that control seed development and maturation in Arabidopsis. , 2008, The Plant journal : for cell and molecular biology.

[39]  Nadezhda T. Doncheva,et al.  Topological analysis and interactive visualization of biological networks and protein structures , 2012, Nature Protocols.

[40]  F. Schreiber,et al.  Plant Metabolic Modeling: Achieving New Insight into Metabolism and Metabolic Engineering , 2014, Plant Cell.

[41]  Xiuli Hu,et al.  "Omics" of maize stress response for sustainable food production: opportunities and challenges. , 2014, Omics : a journal of integrative biology.

[42]  P. Urwin,et al.  The interaction of plant biotic and abiotic stresses: from genes to the field. , 2012, Journal of experimental botany.

[43]  J. Stelling Mathematical models in microbial systems biology. , 2004, Current opinion in microbiology.

[44]  M. Bevan,et al.  Genomics reveals new landscapes for crop improvement , 2013, Genome Biology.

[45]  Bhaskar Dutta,et al.  Individual vs. combinatorial effect of elevated CO2 conditions and salinity stress on Arabidopsis thaliana liquid cultures: Comparing the early molecular response using time-series transcriptomic and metabolomic analyses , 2010, BMC Systems Biology.

[46]  Christopher S. Poultney,et al.  Insights into the genomic nitrate response using genetics and the Sungear Software System. , 2007, Journal of experimental botany.

[47]  Gohar Taj,et al.  Identification and characterization of calcium transporter gene family in finger millet in relation to grain calcium content. , 2015, Gene.

[48]  Charlie Hodgman,et al.  Network Inference Analysis Identifies an APRR2-Like Gene Linked to Pigment Accumulation in Tomato and Pepper Fruits1[W][OA] , 2013, Plant Physiology.

[49]  Dong Xu,et al.  Bioinformatics and its applications in plant biology. , 2006, Annual review of plant biology.

[50]  Meng Zhao,et al.  Cloning and Characterization of Maize miRNAs Involved in Responses to Nitrogen Deficiency , 2012, PloS one.

[51]  E. Baena-González,et al.  Convergent energy and stress signaling. , 2008, Trends in Plant Science.

[52]  Sheng Ying,et al.  Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis , 2011, Planta.

[53]  Xinyou Yin,et al.  Applying modelling experiences from the past to shape crop systems biology: the need to converge crop physiology and functional genomics. , 2008, The New phytologist.

[54]  Jae-Dong Chung,et al.  A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. , 2010, The Plant journal : for cell and molecular biology.

[55]  S. Rothstein,et al.  Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. , 2011, Journal of experimental botany.

[56]  Rodrigo A Gutiérrez,et al.  Systems Biology for the Virtual Plant1 , 2005, Plant Physiology.

[57]  Dennis Shasha,et al.  An integrated genetic, genomic and systems approach defines gene networks regulated by the interaction of light and carbon signaling pathways in Arabidopsis , 2008, BMC Systems Biology.

[58]  John Schiefelbein,et al.  ARABIDOPSIS : A RICH HARVEST 10 YEARS AFTER COMPLETION OF THE GENOME SEQUENCE Getting to the root of plant biology : impact of the Arabidopsis genome sequence on root research , 2010 .

[59]  Jiang Tian,et al.  Proteomics dissection of plant responses to mineral nutrient deficiency , 2013, Proteomics.

[60]  C. Aguirre-Mancilla,et al.  Photosynthesis and chloroplast genes are involved in water-use efficiency in common bean. , 2015, Plant physiology and biochemistry : PPB.

[61]  Philip N Benfey,et al.  Arabidopsis thaliana as a model organism in systems biology , 2009, Wiley interdisciplinary reviews. Systems biology and medicine.

[62]  Wei Jiang,et al.  The analysis of the drug–targets based on the topological properties in the human protein–protein interaction network , 2009, Journal of drug targeting.

[63]  Adriana Alberti,et al.  Whole Genome Profiling provides a robust framework for physical mapping and sequencing in the highly complex and repetitive wheat genome , 2012, BMC Genomics.

[64]  Thomas Becker,et al.  Photosystem II core phosphorylation and photosynthetic acclimation require two different protein kinases , 2005, Nature.

[65]  Katherine J. Denby,et al.  Increased Resistance to Biotrophic Pathogens in the Arabidopsis Constitutive Induced Resistance 1 Mutant Is EDS1 and PAD4-Dependent and Modulated by Environmental Temperature , 2014, PloS one.

[66]  George W Bassel,et al.  Systems Analysis of Plant Functional, Transcriptional, Physical Interaction, and Metabolic Networks , 2012, Plant Cell.

[67]  J. Higgins,et al.  Comparative Genomics of Flowering Time Pathways Using Brachypodium distachyon as a Model for the Temperate Grasses , 2010, PloS one.

[68]  Chris Huntingford,et al.  Aspects of climate change prediction relevant to crop productivity , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[69]  Chih-Hung Jen,et al.  The Arabidopsis co-expression tool (ACT): a WWW-based tool and database for microarray-based gene expression analysis. , 2006, The Plant journal : for cell and molecular biology.

[70]  Francois Tardieu,et al.  Why work and discuss the basic principles of plant modelling 50 years after the first plant models? , 2010, Journal of experimental botany.

[71]  Charles Auffray,et al.  An integrative systems biology approach to understanding pulmonary diseases. , 2010, Chest.

[72]  Xinyou Yin,et al.  Modelling the crop: from system dynamics to systems biology. , 2010, Journal of experimental botany.

[73]  Nathan D. Price,et al.  Reconstruction of genome-scale metabolic models for 126 human tissues using mCADRE , 2012, BMC Systems Biology.

[74]  J. Porter,et al.  Crop responses to climatic variation , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[75]  A. Kumar,et al.  Expression analysis of MAP K 4 and MAP K 6 during pathogenesis of Alternaria blight in susceptible and tolerant genotypes of Brassica juncea , 2015, European Journal of Plant Pathology.

[76]  Hong Gil Nam,et al.  Plant leaf senescence and death – regulation by multiple layers of control and implications for aging in general , 2013, Journal of Cell Science.

[77]  A. Barabasi,et al.  The human disease network , 2007, Proceedings of the National Academy of Sciences.

[78]  B. Palsson,et al.  The evolution of molecular biology into systems biology , 2004, Nature Biotechnology.

[79]  A. Lindenmayer Mathematical models for cellular interactions in development. I. Filaments with one-sided inputs. , 1968, Journal of theoretical biology.

[80]  Sandeep Arora,et al.  In silico analysis of expression data for identification of genes involved in spatial accumulation of calcium in developing seeds of rice. , 2012, Omics : a journal of integrative biology.

[81]  S. Rothstein,et al.  Genome-Wide Identification of MicroRNAs in Response to Low Nitrate Availability in Maize Leaves and Roots , 2011, PloS one.

[82]  R. Redden,et al.  New Approaches for Crop Genetic Adaptation to the Abiotic Stresses Predicted with Climate Change , 2013 .

[83]  Kazuki Saito,et al.  Integrated omics approaches in plant systems biology. , 2009, Current opinion in chemical biology.

[84]  Sandeep Arora,et al.  Identification of genes involved in carbon metabolism from Eleusine coracana (L.) for understanding their light-mediated entrainment and regulation , 2014, Plant Cell Reports.

[85]  Michelle L. Wynn,et al.  Logic-based models in systems biology: a predictive and parameter-free network analysis method. , 2012, Integrative biology : quantitative biosciences from nano to macro.

[86]  Yong-Mei Bi,et al.  High throughput RNA sequencing of a hybrid maize and its parents shows different mechanisms responsive to nitrogen limitation , 2014, BMC Genomics.

[87]  Pankaj Pandey,et al.  DRE-binding transcription factor gene (LlaDREB1b) is regulated by various abiotic stresses in Lepidium latifolium L. , 2012, Molecular Biology Reports.

[88]  H. Kitano Systems Biology: A Brief Overview , 2002, Science.

[89]  Liliana López Kleine,et al.  Identification of Immunity-related Genes in Arabidopsis and Cassava Using Genomic Data , 2013, Genom. Proteom. Bioinform..

[90]  R. M. Rivero,et al.  Abiotic and biotic stress combinations. , 2014, The New phytologist.

[91]  Alisdair R. Fernie,et al.  Systems Biology of Gibberellin Induced Plant Cell Growth , 2012, Front. Plant Sci..

[92]  Casey S Greene,et al.  Integrative systems biology for data-driven knowledge discovery. , 2010, Seminars in nephrology.

[93]  Karine Chenu,et al.  Individual leaf development in Arabidopsis thaliana: a stable thermal-time-based programme. , 2002, Annals of botany.

[94]  Colin P. Osborne,et al.  Towards an integrative model of C4 photosynthetic subtypes: insights from comparative transcriptome analysis of NAD-ME, NADP-ME, and PEP-CK C4 species , 2014, Journal of experimental botany.

[95]  G. Coruzzi,et al.  Cell-specific nitrogen responses mediate developmental plasticity , 2008, Proceedings of the National Academy of Sciences.

[96]  A. Fernie,et al.  Molecular regulation of fruit ripening , 2013, Front. Plant Sci..

[97]  Xin-Guang Zhu,et al.  Improving photosynthetic efficiency for greater yield. , 2010, Annual review of plant biology.

[98]  M. Lucas,et al.  Plant systems biology: network matters. , 2011, Plant, cell & environment.

[99]  Rajeev K Varshney,et al.  Agricultural biotechnology for crop improvement in a variable climate: hope or hype? , 2011, Trends in plant science.

[100]  Luis Herrera-Estrella,et al.  APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. , 2013, Plant science : an international journal of experimental plant biology.

[101]  Anushya Muruganujan,et al.  Large-scale gene function analysis with the PANTHER classification system , 2013, Nature Protocols.

[102]  H. Kitano,et al.  Software for systems biology: from tools to integrated platforms , 2011, Nature Reviews Genetics.

[103]  Mawsheng Chern,et al.  Comparative analysis of protein-protein interactions in the defense response of rice and wheat , 2013, BMC Genomics.

[104]  Shunsuke Miyashima,et al.  Stem cell function during plant vascular development , 2009, The EMBO journal.

[105]  Christophe Godin,et al.  An Auxin Transport-Based Model of Root Branching in Arabidopsis thaliana , 2008, PloS one.

[106]  S. S. Sun,et al.  Transgenic approaches to improve the nutritional quality of plant proteins , 2004, In Vitro Cellular & Developmental Biology - Plant.

[107]  Anil Kumar,et al.  Development and molecular characterization of genic molecular markers for grain protein and calcium content in finger millet (Eleusine coracana (L.) Gaertn.) , 2013, Molecular Biology Reports.

[108]  Michael E Phelps,et al.  Systems Biology and New Technologies Enable Predictive and Preventative Medicine , 2004, Science.

[109]  Yi Zhang,et al.  OsWRKY30 is activated by MAP kinases to confer drought tolerance in rice , 2012, Plant Molecular Biology.

[110]  Haibao Tang,et al.  Insights from the comparison of plant genome sequences. , 2010, Annual review of plant biology.

[111]  Shigehiko Kanaya,et al.  Systems Biology in the Context of Big Data and Networks , 2014, BioMed research international.

[112]  P. Prusinkiewicz Modeling plant growth and development. , 2004, Current opinion in plant biology.

[113]  Uwe Scholz,et al.  Unlocking the Barley Genome by Chromosomal and Comparative Genomics[W][OA] , 2011, Plant Cell.

[114]  Hiroaki Kitano,et al.  Structure of Protein Interaction Networks and Their Implications on Drug Design , 2009, PLoS Comput. Biol..

[115]  Insuk Lee,et al.  Towards Establishment of a Rice Stress Response Interactome , 2011, PLoS genetics.

[116]  H. Kitano,et al.  Computational systems biology , 2002, Nature.

[117]  Muktesh Chandra,et al.  Transcriptome Wide Identification and Validation of Calcium Sensor Gene Family in the Developing Spikes of Finger Millet Genotypes for Elucidating Its Role in Grain Calcium Accumulation , 2014, PloS one.

[118]  Monica Höfte,et al.  Making sense of hormone-mediated defense networking: from rice to Arabidopsis , 2014, Front. Plant Sci..

[119]  M. Stitt,et al.  Modelling temperature-compensated physiological rates, based on the co-ordination of responses to temperature of developmental processes. , 2010, Journal of experimental botany.

[120]  P. Hasegawa,et al.  Regulation of Transpiration to Improve Crop Water Use , 2009 .

[121]  P. Benfey,et al.  From Genotype to Phenotype: Systems Biology Meets Natural Variation , 2008, Science.

[122]  J. Dumont,et al.  Boolean analysis of cell regulation networks. , 1983, Journal of theoretical biology.

[123]  Aidong Zhang,et al.  MADS-box Transcription Factor OsMADS25 Regulates Root Development through Affection of Nitrate Accumulation in Rice , 2015, PloS one.

[124]  Nese Sreenivasulu,et al.  Seed-development programs: a systems biology-based comparison between dicots and monocots. , 2013, Annual review of plant biology.

[125]  Xavier Draye,et al.  Root Systems Biology: Integrative Modeling across Scales, from Gene Regulatory Networks to the Rhizosphere1 , 2013, Plant Physiology.

[126]  Je-Gun Joung,et al.  Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation. , 2012, The Plant journal : for cell and molecular biology.

[127]  Zoran Nikoloski,et al.  Integrative Comparative Analyses of Transcript and Metabolite Profiles from Pepper and Tomato Ripening and Development Stages Uncovers Species-Specific Patterns of Network Regulatory Behavior[W][OA] , 2012, Plant Physiology.

[128]  S. C. Falco,et al.  Expression of de novo high-lysine α-helical coiled-coil proteins may significantly increase the accumulated levels of lysine in mature seeds of transgenic tobacco plants , 1997, Plant Molecular Biology.

[129]  Leon G. Higley,et al.  Biotic stress and yield loss. , 2000 .

[130]  A. Lindenmayer,et al.  Developmental algorithms for multicellular organisms: a survey of L-systems. , 1975, Journal of theoretical biology.

[131]  Youzhi Ma,et al.  Overexpression of the soybean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerances to salt, drought, and diseases in transgenic tobacco , 2009, Journal of experimental botany.

[132]  Tomoyuki Higuchi,et al.  Bayesian experts in exploring reaction kinetics of transcription circuits , 2010, Bioinform..

[133]  Luca Espen,et al.  Open Access Bmc Plant Biology Evaluation of Protein Pattern Changes in Roots and Leaves of Zea Mays Plants in Response to Nitrate Availability by Two-dimensional Gel Electrophoresis Analysis , 2022 .

[134]  Atul Grover,et al.  Identification of Abiotic Stress Responsive Genes from Indian High Altitude Lepidium latifolium L. (Short Communication) , 2012 .

[135]  Arpita Mishra,et al.  Involvement of hsr203J like gene homologue, protease and protease inhibitors in triggering differential defense response against Alternaria blight in Brassica , 2011, Australasian Plant Pathology.

[136]  Pankaj Pandey,et al.  Cloning and characterization of GPAT gene from Lepidium latifolium L.: a step towards translational research in agri-genomics for food and fuel , 2013, Molecular Biology Reports.

[137]  Gabriel Krouk,et al.  A Systems View of Responses to Nutritional Cues in Arabidopsis: Toward a Paradigm Shift for Predictive Network Modeling1 , 2009, Plant Physiology.

[138]  J. Vik,et al.  Bridging the genotype–phenotype gap: what does it take? , 2013, The Journal of physiology.

[139]  Brajesh Kumar,et al.  Progression of Alternaria blight of mustard in relation to components of resistance , 2001 .

[140]  Godin,et al.  A multiscale model of plant topological structures , 1998, Journal of theoretical biology.

[141]  Julian Ramirez-Villegas,et al.  Identifying traits for genotypic adaptation using crop models. , 2015, Journal of experimental botany.

[142]  K. V. Venkatesh,et al.  A conceptual review on systems biology in health and diseases: from biological networks to modern therapeutics , 2014, Systems and Synthetic Biology.

[143]  M. Campbell,et al.  PANTHER: a library of protein families and subfamilies indexed by function. , 2003, Genome research.

[144]  German Spangenberg,et al.  Improving yield potential in crops under elevated CO2: Integrating the photosynthetic and nitrogen utilization efficiencies , 2012, Front. Plant Sci..

[145]  Dennis Shasha,et al.  Nitrogen economics of root foraging: Transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs. demand , 2011, Proceedings of the National Academy of Sciences.

[146]  Prateek Tripathi,et al.  The potential of transcription factor-based genetic engineering in improving crop tolerance to drought. , 2014, Omics : a journal of integrative biology.

[147]  B. Forde,et al.  An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. , 1998, Science.

[148]  Feng Gao,et al.  OsNAC52, a rice NAC transcription factor, potentially responds to ABA and confers drought tolerance in transgenic plants , 2010, Plant Cell, Tissue and Organ Culture (PCTOC).

[149]  Bo Yang,et al.  Characterization of Defense Signaling Pathways of Brassica napus and Brassica carinata in Response to Sclerotinia sclerotiorum Challenge , 2010, Plant Molecular Biology Reporter.

[150]  Malcolm J. McConville,et al.  Systems Biology: The Next Frontier for Bioinformatics , 2011, Adv. Bioinformatics.

[151]  Kazuki Saito,et al.  Metabolomics for functional genomics, systems biology, and biotechnology. , 2010, Annual review of plant biology.

[152]  Chris Dardick,et al.  Molecular basis of angiosperm tree architecture. , 2015, The New phytologist.

[153]  Kathleen L. Hefferon,et al.  Nutritionally Enhanced Food Crops; Progress and Perspectives , 2015, International journal of molecular sciences.

[154]  Guohua Xu,et al.  Plant nitrogen assimilation and use efficiency. , 2012, Annual review of plant biology.

[155]  Yang Liu,et al.  System-Level Insights into the Cellular Interactome of a Non-Model Organism: Inferring, Modelling and Analysing Functional Gene Network of Soybean (Glycine max) , 2014, PloS one.

[156]  Ben Scheres,et al.  Stem-cell niches: nursery rhymes across kingdoms , 2007, Nature Reviews Molecular Cell Biology.