Bridging physiological and evolutionary time-scales in a gene regulatory network.

Gene regulatory networks (GRNs) govern phenotypic adaptations and reflect the trade-offs between physiological responses and evolutionary adaptation that act at different time-scales. To identify patterns of molecular function and genetic diversity in GRNs, we studied the drought response of the common sunflower, Helianthus annuus, and how the underlying GRN is related to its evolution. We examined the responses of 32,423 expressed sequences to drought and to abscisic acid (ABA) and selected 145 co-expressed transcripts. We characterized their regulatory relationships in nine kinetic studies based on different hormones. From this, we inferred a GRN by meta-analyses of a Gaussian graphical model and a random forest algorithm and studied the genetic differentiation among populations (FST ) at nodes. We identified two main hubs in the network that transport nitrate in guard cells. This suggests that nitrate transport is a critical aspect of the sunflower physiological response to drought. We observed that differentiation of the network genes in elite sunflower cultivars is correlated with their position and connectivity. This systems biology approach combined molecular data at different time-scales and identified important physiological processes. At the evolutionary level, we propose that network topology could influence responses to human selection and possibly adaptation to dry environments.

[1]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[2]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[3]  Ulrich Pohl,et al.  Reactive Oxygen Species: Players in the Platelet Game , 2004, Arteriosclerosis, thrombosis, and vascular biology.

[4]  J. Goudet.  HIERFSTAT , a package for R to compute and test hierarchical F -statistics , 2005 .

[5]  Viswanathan Chinnusamy,et al.  Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. , 2003, Journal of experimental botany.

[6]  E. Martinoia,et al.  AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis , 2013, Nature Communications.

[7]  Jérôme Gouzy,et al.  A Gene-Phenotype Network Based on Genetic Variability for Drought Responses Reveals Key Physiological Processes in Controlled and Natural Environments , 2012, PloS one.

[8]  Marie Boudsocq,et al.  Osmotic Signaling in Plants. Multiple Pathways Mediated by Emerging Kinase Families , 2005, Plant Physiology.

[9]  Qingqiu Gong,et al.  An Arabidopsis gene network based on the graphical Gaussian model. , 2007, Genome research.

[10]  N. Langlade,et al.  Targeted mRNA Oxidation Regulates Sunflower Seed Dormancy Alleviation during Dry After-Ripening[C][W] , 2011, Plant Cell.

[11]  P. L. Rodriguez.  Protein phosphatase 2C (PP2C) function in higher plants , 1998, Plant Molecular Biology.

[12]  Kazuo Shinozaki,et al.  The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. , 2008, The Plant journal : for cell and molecular biology.

[13]  S. Thomine,et al.  The proline 160 in the selectivity filter of the Arabidopsis NO(3)(-)/H(+) exchanger AtCLCa is essential for nitrate accumulation in planta. , 2010, The Plant journal : for cell and molecular biology.

[14]  Kazuo Shinozaki,et al.  The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. , 2008 .

[15]  R. Milo,et al.  The relationship between evolutionary and physiological variation in hemoglobin , 2007, Proceedings of the National Academy of Sciences.

[16]  R. Albert,et al.  Predicting Essential Components of Signal Transduction Networks: A Dynamic Model of Guard Cell Abscisic Acid Signaling , 2006, PLoS biology.

[17]  Thomas Schiex,et al.  Gene Regulatory Network Reconstruction Using Bayesian Networks, the Dantzig Selector, the Lasso and Their Meta-Analysis , 2011, PloS one.

[18]  R. E. Miller,et al.  Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. , 1999, Molecular biology and evolution.

[19]  E. Davidson,et al.  Developmental gene regulatory network architecture across 500 million years of echinoderm evolution , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[20]  N. Langlade,et al.  Physiological Aspects of Cluster Root Function and Development in Phosphorus-deficient White Lupin (Lupinus albus L.) , 2000 .

[21]  Russ B. Altman,et al.  Missing value estimation methods for DNA microarrays , 2001, Bioinform..

[22]  E. Bray.  Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. , 2004, Journal of experimental botany.

[23]  Diogo M. Camacho,et al.  Wisdom of crowds for robust gene network inference , 2012, Nature Methods.

[24]  Thomas Girke,et al.  Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. , 2004, The Plant journal : for cell and molecular biology.

[25]  Kemal Kazan,et al.  MYC2: the master in action. , 2013, Molecular plant.

[26]  N. Crawford,et al.  The Nitrate Transporter AtNRT1.1 (CHL1) Functions in Stomatal Opening and Contributes to Drought Susceptibility in Arabidopsis Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.006312. , 2003, The Plant Cell Online.

[27]  Simon de Givry,et al.  A Panel of Learning Methods for the Reconstruction of Gene Regulatory Networks in a Systems Genetics Context , 2013 .

[28]  Kiana Toufighi,et al.  The Botany Array Resource: E-northerns, Expression Angling, and Promoter Analyses , 2022 .

[29]  S. Thomine,et al.  The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. , 2010, The Plant journal : for cell and molecular biology.

[30]  P. Geurts,et al.  Inferring Regulatory Networks from Expression Data Using Tree-Based Methods , 2010, PloS one.

[31]  A. Altman,et al.  Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance , 2003, Planta.

[32]  M. Bevan,et al.  Sugar and ABA response pathways and the control of gene expression. , 2006, Plant, cell & environment.

[33]  Leo Breiman,et al.  Random Forests , 2001, Machine Learning.

[34]  C. Waddington.  Canalization of Development and the Inheritance of Acquired Characters , 1942, Nature.

[35]  Kazuo Shinozaki,et al.  Research on plant abiotic stress responses in the post-genome era: past, present and future. , 2010, The Plant journal : for cell and molecular biology.

[36]  G. Pastori,et al.  Common Components, Networks, and Pathways of Cross-Tolerance to Stress. The Central Role of “Redox” and Abscisic Acid-Mediated Controls1 , 2002, Plant Physiology.

[37]  Ramesh Ramakrishnan,et al.  High Throughput Gene Expression Measurement with Real Time PCR in a Microfluidic Dynamic Array , 2008, PloS one.

[38]  C. Rock,et al.  The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[39]  Kazuo Shinozaki,et al.  AREB1 Is a Transcription Activator of Novel ABRE-Dependent ABA Signaling That Enhances Drought Stress Tolerance in Arabidopsis[W][OA] , 2005, The Plant Cell Online.

[40]  K Botzenhart,et al.  Reactive Oxygen Species , 2014 .

[41]  C. Valon,et al.  The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. , 2009, Journal of experimental botany.

[42]  Oliver Fiehn,et al.  Natural Genetic Variation of Freezing Tolerance in Arabidopsis[W][OA] , 2006, Plant Physiology.

[43]  Fidel Ramírez,et al.  Computing topological parameters of biological networks , 2008, Bioinform..

[44]  E. Kandel,et al.  Proceedings of the National Academy of Sciences of the United States of America. Annual subject and author indexes. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[45]  C. Valon,et al.  An Update on Abscisic Acid Signaling in Plants and More , 2022 .

[46]  L. Rieseberg,et al.  Systematics, Origin, and Germplasm Resources of the Wild and Domesticated Sunflower , 2015 .

[47]  K. Shinozaki,et al.  Gene networks involved in drought stress response and tolerance. , 2006, Journal of experimental botany.

[48]  G. Krouk,et al.  ABA transport and transporters. , 2013, Trends in plant science.

[49]  Ji Hye Park,et al.  ARIA, an Arabidopsis Arm Repeat Protein Interacting with a Transcriptional Regulator of Abscisic Acid-Responsive Gene Expression, Is a Novel Abscisic Acid Signaling Component1 , 2004, Plant Physiology.

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

[51]  A. Wilkins.  Recasting developmental evolution in terms of genetic pathway and network evolution … and the implications for comparative biology , 2005, Brain Research Bulletin.

[52]  K. Shinozaki,et al.  Gene Expression and Signal Transduction in Water-Stress Response , 1997, Plant physiology.

[53]  H. Reichenbach.  A new approach to a synthesis of neurology and psychology. , 1953, Transactions of the New York Academy of Sciences.

[54]  L. Rieseberg,et al.  The correlation of evolutionary rate with pathway position in plant terpenoid biosynthesis. , 2009, Molecular biology and evolution.

[55]  Kazuo Shinozaki,et al.  Regulatory metabolic networks in drought stress responses. , 2007, Current opinion in plant biology.

[56]  Anton Crombach,et al.  Efficient Reverse-Engineering of a Developmental Gene Regulatory Network , 2012, PLoS Comput. Biol..

[57]  Brook T. Moyers,et al.  Genomic islands of divergence are not affected by geography of speciation in sunflowers , 2013, Nature Communications.

[58]  T. Kuromori,et al.  Molecular Basis of the Core Regulatory Network in ABA Responses: Sensing, Signaling and Transport , 2010, Plant & cell physiology.

[59]  H. Nguyen,et al.  Understanding regulatory networks and engineering for enhanced drought tolerance in plants. , 2006, Current opinion in plant biology.

[60]  S. Lindquist,et al.  Hsp90 as a capacitor of phenotypic , 2002 .

[61]  A. Barabasi,et al.  Network biology: understanding the cell's functional organization , 2004, Nature Reviews Genetics.

[62]  S. Lindquist,et al.  Hsp90 as a capacitor of phenotypic variation , 2002, Nature.

[63]  Duygu Dikicioglu,et al.  How yeast re-programmes its transcriptional profile in response to different nutrient impulses , 2011, BMC Systems Biology.

[64]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[65]  S. Wilkinson,et al.  Plant hormone interactions: innovative targets for crop breeding and management. , 2012, Journal of experimental botany.

[66]  Bertram M. Berla,et al.  Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. , 2010, Journal of experimental botany.