[en] 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.
Huynh-Thu, Vân Anh ; Université de Liège - ULiège > GIGA-Management : Coordination ALMA-GRID
Kane, Nolan C.
Arribat, Sandrine
Vares, Didier
Rengel, David
Balzergue, Sandrine
Rieseberg, Loren H.
Vincourt, Patrick
Geurts, Pierre ; Université de Liège - ULiège > Dép. d'électric., électron. et informat. (Inst.Montefiore) > Algorith. des syst. en interaction avec le monde physique
Vignes, Matthieu
Langlade, Nicolas B.
Language :
English
Title :
Bridging physiological and evolutionary time-scales in a gene regulatory network.
Publication date :
2014
Journal title :
New Phytologist
ISSN :
0028-646X
eISSN :
1469-8137
Publisher :
Wiley, Oxford, United Kingdom
Volume :
203
Issue :
2
Pages :
685-696
Peer reviewed :
Peer Reviewed verified by ORBi
Commentary :
(c) 2014 INRA New Phytologist (c) 2014 New Phytologist Trust.
Allouche D, Cierco-Ayrolles C, de Givry S, Guillermin G, Mangin B, Schiex T, Vandel J, Vignes M 2013. A panel of learning methods for the reconstruction of gene regulatory networks in a systems genetics context. In: de la Fuente A, ed. Verification of methods for gene network inference from Systems Genetics data. Heidelberg, Germany: Springer, 9-31.
Assenov Y, Ramirez F, Schelhorn SE, Lengauer T, Albrecht M. 2008. Computing topological parameters of biological networks. Bioinformatics 24: 282-284.
Bazin J, Langlade N, Vincourt P, Arribat S, Balzergue S, El-Maarouf-Bouteau H, Bailly C. 2011. Targeted mRNA oxidation regulates sunflower seed dormancy alleviation during dry after-ripening. Plant Cell 23: 2196-2208.
Boudsocq M, Lauriere C. 2005. Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiology 138: 1185-1194.
Boursiac Y, Léran S, Corratgé-Faillie C, Gojon A, Krouk G, Lacombe B. 2013. ABA transport and transporters. Trends in Plant Science 18: 1878-4372.
Bray E. 2004. Genes commonly regulated by water-deficit stress in Arabidopsis thaliana. Journal of Experimental Botany 55: 2331-2341.
Breiman L. 2001. Random forests. Machine Learning 45: 5-32.
Chinnusamy V, Schumaker K, Zhu JK. 2004. Molecular genetic perspectives on cross-talk and specificity in abiotic stress signalling in plants. Journal of Experimental Botany 55: 225-236.
Crombach A, Wotton KR, Cicin-Sain D, Ashyraliyev M, Jaeger J. 2012. Efficient reverse-engineering of a developmental gene regulatory network. Plos Computational Biology 8: 21.
De Angeli A, Zhang JB, Meyer S, Martinoia E. 2013. AtALMT9 is a malate-activated vacuolar chloride channel required for stomatal opening in Arabidopsis. Nature Communications 4: 1804.
Dikicioglu D, Karabekmez E, Rash B, Pir P, Kirdar B, Oliver SG. 2011. How yeast re-programmes its transcriptional profile in response to different nutrient impulses. BMC Systems Biology 5: 148.
Ernst L, Goodger JQD, Alvarez S, Marsh EL, Berla B, Lockhart E, Jung J, Li PH, Bohnert HJ, Schachtman DP. 2010. Sulphate as a xylem-borne chemical signal precedes the expression of ABA biosynthetic genes in maize roots. Journal of Experimental Botany 61: 3395-3405.
Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K. 2005. AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17: 3470-3488.
Goda H, Sasaki E, Akiyama K, Maruyama-Nakashita A, Nakabayashi K, Li WQ, Ogawa M, Yamauchi Y, Preston J, Aoki K et al. 2008. The AtGenExpress hormone and chemical treatment data set: experimental design, data evaluation, model data analysis and data access. Plant Journal 55: 526-542.
Goudet J. 2005. HIERFSTAT, a package for R to compute and test hierarchical F-statistics. Molecular Ecology Notes 5: 184-186.
Guo FO, Young J, Crawford NM. 2003. The nitrate transporter AtNRT1.1 (CHL1) functions in stomatal opening and contributes to drought susceptibility in arabidopsis. Plant Cell 15: 107-117.
Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK. 2006. Natural genetic variation of freezing tolerance in arabidopsis. Plant Physiology 142: 98-112.
Hinman VF, Nguyen AT, Cameron RA, Davidson EH. 2003. Developmental gene regulatory network architecture across 500 million years of echinoderm evolution. Proceedings of the National Academy of Sciences, USA 100: 13356-13361.
Hirayama T, Shinozaki K. 2010. Research on plant abiotic stress responses in the post-genome era: past, present and future. Plant Journal 61: 1041-1052.
Huynh-Thu VA, Irrthum A, Wehenkel L, Geurts P. 2010. Inferring regulatory networks from expression data using tree-based methods. PLoS ONE 5: e12776.
Jossier M, Kroniewicz L, Dalmas F, Le Thiec D, Ephritikhine G, Thomine S, Barbier-Brygoo H, Vavasseur A, Filleur S, Leonhardt N. 2010. The Arabidopsis vacuolar anion transporter, AtCLCc, is involved in the regulation of stomatal movements and contributes to salt tolerance. Plant Journal 64: 563-576.
Kawaguchi R, Girke T, Bray E, Bailey-Serres J. 2004. Differential mRNA translation contributes to gene regulation under non-stress and dehydration stress conditions in Arabidopsis thaliana. Plant Journal 38: 823-839.
Kazan K, Manners JM. 2013. MYC2: the master in action. Molecular Plant 6: 686-703.
Kim S, Choi HI, Ryu HJ, Park JH, Kim MD, Kim SY. 2004. ARIA, an Arabidopsis arm repeat protein interacting with a transcriptional regulator of abscisic acid-responsive gene expression, is a novel abscisic acid signaling component. Plant Physiology 136: 3639-3648.
Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data P. 2009. The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078-2079.
Li S, Assmann S, Albert R. 2006. Predicting essential components of signal transduction networks: a dynamic model of guard cell abscisic acid signaling. PLoS Biology 4: 1732-1748.
Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
Ma SS, Gong QQ, Bohnert HJ. 2007. An Arabidopsis gene network based on the graphical Gaussian model. Genome Research 17: 1614-1625.
Marbach D, Costello J, Kuffner R, Vega N, Prill R, Camacho D, Allison K, Kellis M, Collins J, Stolovitzky G, Consortium D. 2012. Wisdom of crowds for robust gene network inference. Nature Methods 9: 796-804.
Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R. 2009. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, Cell & Environment 33: 453-467.
Milo R, Hou JH, Springer M, Brenner MP, Kirschner MW. 2007. The relationship between evolutionary and physiological variation in hemoglobin. Proceedings of the National Academy of Sciences, USA 104: 16998-17003.
Neumann G, Massonneau A, Langlade N, Dinkelaker B, Hengeler C, Romheld V, Martinoia E. 2000. Physiological aspects of cluster root function and development in phosphorus-deficient white lupin (Lupinus albus L.). Annals of Botany 85: 909-919.
Osborn HF. 1896. A mode of evolution requiring neither natural selection nor the inheritance of acquired characters. Transactions of the New York Academy of Sciences 15: 141-142.
Pastori G, Foyer C. 2002. Common components, networks, and pathways of cross-tolerance to stress. The central role of "redox" and abscisic acid-mediated controls. Plant Physiology 129: 460-468.
Queitsch C, Sangster TA, Lindquist S. 2002. Hsp90 as a capacitor of phenotypic variation. Nature 417: 618-624.
Ramsay H, Rieseberg LH, Ritland K. 2009. The correlation of evolutionary rate with pathway position in plant terpenoid biosynthesis. Molecular Biology and Evolution 26: 1045-1053.
Rausher M, Miller R, Tiffin P. 1999. Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. Molecular Biology and Evolution 16: 266-274.
Renaut S, Grassa CJ, Yeaman S, Moyers BT, Lai Z, Kane NC, Bowers JE, Burke JM, Rieseberg LH. 2013. Genomic islands of divergence are not affected by geography of speciation in sunflowers. Nature Communications 4: 1827.
Rengel D, Arribat S, Maury P, Martin-Magniette ML, Hourlier T, Laporte M, Vares D, Carrere S, Grieu P, Balzergue S et al. 2012. A gene-phenotype network based on genetic variability for drought responses reveals key physiological processes in controlled and natural environments. PLoS ONE 7: e45249.
Rock CD, Zeevaart JAD. 1991. The aba mutant of Arabidopsis thaliana is impaired in epoxy-carotenoid biosynthesis. Proceedings of the National Academy of Sciences, USA 88: 7496-7499.
Rodriguez PL. 1998. Protein phosphatase 2C (PP2C) function in higher plants. Plant Molecular Biology 38: 919-927.
Rook F, Hadingham S, Li Y, Bevan M. 2006. Sugar and ABA response pathways and the control of gene expression. Plant, Cell & Environment 29: 426-434.
Seiler GJ, Rieseberg LH 1997. Systematics, origin, and germplasm resources of the wild and domesticated sunflower. In: Schneiter AA, ed. Sunflower science and technology. Madison, WI, USA: ASA, CSSA, and ASSA, 21-66.
Seki M, Umezawa T, Urano K, Shinozaki K. 2007. Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology 10: 296-302.
Shinozaki K, Yamaguchi-Shinozaki K. 1997. Gene expression and signal transduction in water-stress response. Plant Physiology 115: 327-334.
Shinozaki K, Yamaguchi-Shinozaki K. 2007. Gene networks involved in drought stress response and tolerance. Journal of Experimental Botany 58: 221-227.
Sirichandra C, Wasilewska A, Vlad F, Valon C, Leung J. 2009. The guard cell as a single-cell model towards understanding drought tolerance and abscisic acid action. Journal of Experimental Botany 60: 1439-1463.
Spurgeon SL, Jones RC, Ramakrishnan R. 2008. High throughput gene expression measurement with real time PCR in a microfluidic dynamic array. PLoS ONE 3: e1662.
Troyanskaya O, Cantor M, Sherlock G, Brown P, Hastie T, Tibshirani R, Botstein D, Altman RB. 2001. Missing value estimation methods for DNA microarrays. Bioinformatics 17: 520-525.
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K. 2010. Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant and Cell Physiology 51: 1821-1839.
Valliyodan B, Nguyen H. 2006. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Current Opinion in Plant Biology 9: 189-195.
Vignes M, Vandel J, Allouche D, Ramadan-Alban N, Cierco-Ayrolles C, Schiex T, Mangin B, de Givry S. 2011. Gene regulatory network reconstruction using Bayesian networks, the Dantzig Selector, the Lasso and their meta-analysis. PLoS ONE 6: e29165.
Waddington CH. 1942. Canalization of development and the inheritance of acquired characters. Nature 150: 563-565.
Wang W, Vinocur B, Altman A. 2003. Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218: 1-14.
Wasilewska A, Vlad F, Sirichandra C, Redko Y, Jammes F, Valon C, Frey N, Leung J. 2008. An update on abscisic acid signaling in plants and more. Molecular Plant 1: 198-217.
Wege S, Jossier M, Filleur S, Thomine S, Barbier-Brygoo H, Gambale F, De Angeli A. 2010. The proline 160 in the selectivity filter of the Arabidopsis NO3-/H+ exchanger AtCLCa is essential for nitrate accumulation in planta. Plant Journal 63: 861-869.
Wilkins AS. 2005. Recasting developmental evolution in terms of genetic pathway and network evolution ... and the implications for comparative biology. Brain Research Bulletin 66: 495-509.
Wilkinson S, Kudoyarova GR, Veselov DS, Arkhipova TN, Davies WJ. 2012. Plant hormone interactions: innovative targets for crop breeding and management. Journal of Experimental Botany 63: 3499-3509.