Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation
Autoři:
Nadia Bouain aff001; Arthur Korte aff002; Santosh B. Satbhai aff003; Hye-In Nam aff005; Seung Y. Rhee aff005; Wolfgang Busch aff003; Hatem Rouached aff001
Působiště autorů:
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
aff001; Evolutionary Genomics, Center for Computational and Theoretical Biology (CCTB), University Würzburg, Würzburg, Germany
aff002; Gregor Mendel Institute (GMI), Austrian Academy of Sciences, Vienna Biocenter (VBC), Vienna, Austria
aff003; Plant Molecular and Cellular Biology Laboratory, and Integrative Biology Laboratory, Salk Institute for Biological Studies, La Jolla, California, United States of America
aff004; Department of Plant Biology, Carnegie Institution for Science, Stanford, California, United States of America
aff005
Vyšlo v časopise:
Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation. PLoS Genet 15(11): e32767. doi:10.1371/journal.pgen.1008392
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008392
Souhrn
The molecular mechanisms by which plants modulate their root growth rate (RGR) in response to nutrient deficiency are largely unknown. Using Arabidopsis thaliana accessions, we analyzed RGR variation under combinatorial mineral nutrient deficiencies involving phosphorus (P), iron (Fe), and zinc (Zn). While -P stimulated early RGR of most accessions, -Fe or -Zn reduced it. The combination of either -P-Fe or -P-Zn led to suppression of the growth inhibition exerted by -Fe or -Zn alone. Surprisingly, root growth responses of the reference accession Columbia (Col-0) were not representative of the species under -P nor -Zn. Using a systems approach that combines GWAS, network-based candidate identification, and reverse genetic screen, we identified new genes that regulate root growth in -P-Fe: VIM1, FH6, and VDAC3. Our findings provide a framework to systematically identifying favorable allelic variations to improve root growth, and to better understand how plants sense and respond to multiple environmental cues.
Klíčová slova:
Arabidopsis thaliana – Gene regulation – Genome-wide association studies – Micronutrient deficiencies – Nutrients – Root growth – Seedlings – Iron deficiency
Zdroje
1. Tomlinson I (2013) Doubling food production to feed the 9 billion: a critical perspective on a key discourse of food security in the UK. Journal of rural studies 29: 81–90.
2. Zhu C, Kobayashi K, Loladze I, Zhu J, Jiang Q, et al. (2018) Carbon dioxide (CO2) levels this century will alter the protein, micronutrients, and vitamin content of rice grains with potential health consequences for the poorest rice-dependent countries. Science advances 4: eaaq1012. doi: 10.1126/sciadv.aaq1012 29806023
3. Hilty FM, Arnold M, Hilbe M, Teleki A, Knijnenburg JTN, et al. (2010) Iron from nanocompounds containing iron and zinc is highly bioavailable in rats without tissue accumulation. Nature nanotechnology 5: 374. doi: 10.1038/nnano.2010.79 20418865
4. Abelson PH (1999) A potential phosphate crisis. Science 283: 2015–2015. doi: 10.1126/science.283.5410.2015 10206902
5. Cordell D, Drangert J-O, White S (2009) The story of phosphorus: global food security and food for thought. Global environmental change 19: 292–305.
6. Bouain N, Krouk G, Lacombe B, Rouached H (2019) Getting to the Root of Plant Mineral Nutrition: Combinatorial Nutrient Stresses Reveal Emergent Properties. Trends Plant Sci 24: 542–552. doi: 10.1016/j.tplants.2019.03.008 31006547
7. Medici A, Szponarski W, Dangeville P, Safi A, Dissanayake IM, et al. (2019) Identification of Molecular Integrators Shows that Nitrogen Actively Controls the Phosphate Starvation Response in Plants. Plant Cell 31: 1171–1184. doi: 10.1105/tpc.18.00656 30872321
8. Secco D, Bouain N, Rouached A, Prom-u-Thai C, Hanin M, et al. (2017) Phosphate, phytate and phytases in plants: from fundamental knowledge gained in Arabidopsis to potential biotechnological applications in wheat. Critical reviews in biotechnology 37: 898–910. doi: 10.1080/07388551.2016.1268089 28076998
9. Hanlon MT, Ray S, Saengwilai P, Luthe D, Lynch JP, et al. (2018) Buffered delivery of phosphate to Arabidopsis alters responses to low phosphate. Journal of experimental botany 69: 1207–1219. doi: 10.1093/jxb/erx454 29304231
10. Heppell J, Talboys P, Payvandi S, Zygalakis KC, Fliege J, et al. (2015) How changing root system architecture can help tackle a reduction in soil phosphate (P) levels for better plant P acquisition. Plant, cell & environment 38: 118–128.
11. Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant physiology 156: 1041–1049. doi: 10.1104/pp.111.175414 21610180
12. Miguel MA, Widrig A, Vieira RF, Brown KM, Lynch JP (2013) Basal root whorl number: a modulator of phosphorus acquisition in common bean (Phaseolus vulgaris). Annals of botany 112: 973–982. doi: 10.1093/aob/mct164 23925972
13. Somssich M (2018) A short history of Arabidopsis thaliana (L.) Heynh. Columbia-0. PeerJ Preprints. 2167–9843 2167–9843.
14. Bouain N, Doumas P, Rouached H (2016) Recent Advances in Understanding the Molecular Mechanisms Regulating the Root System Response to Phosphate Deficiency in Arabidopsis. Curr Genomics 17: 308–304. doi: 10.2174/1389202917666160331201812 27499680
15. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L, et al. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nature Genetics 39: 792–796. doi: 10.1038/ng2041 17496893
16. Ticconi CA, Delatorre CA, Lahner B, Salt DE, Abel S (2004) Arabidopsis pdr2 reveals a phosphate‐sensitive checkpoint in root development. Plant Journal 37: 801–814. doi: 10.1111/j.1365-313x.2004.02005.x 14996215
17. Kang J, Yu H, Tian C, Zhou W, Li C, et al. (2014) Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency. Plant Physiology 165: 1156–1170. doi: 10.1104/pp.114.238725 24868033
18. Mora-Macías J, Ojeda-Rivera JO, Gutiérrez-Alanís D, Yong-Villalobos L, Oropeza-Aburto A, et al. (2017) Malate-dependent Fe accumulation is a critical checkpoint in the root developmental response to low phosphate. Proceedings of the National Academy of Sciences of the United States of America 114: E3563–E3572. doi: 10.1073/pnas.1701952114 28400510
19. Balzergue C, Dartevelle T, Godon C, Laugier E, Meisrimler C, et al. (2017) Low phosphate activates STOP1-ALMT1 to rapidly inhibit root cell elongation. Nature Communications 8: 15300. doi: 10.1038/ncomms15300 28504266
20. Reymond M, Svistoonoff S, Loudet O, Nussaume L, Desnos T (2006) Identification of QTL controlling root growth response to phosphate starvation in Arabidopsis thaliana. Plant Cell Environ 29: 115–125. 17086758
21. Couturier J, Touraine B, Briat J-F, Gaymard F, Rouhier N (2013) The iron-sulfur cluster assembly machineries in plants: current knowledge and open questions. Frontiers in Plant science 4: 259. doi: 10.3389/fpls.2013.00259 23898337
22. White PJ, Broadley MR (2009) Biofortification of crops with seven mineral elements often lacking in human diets—iron, zinc, copper, calcium, magnesium, selenium and iodine. New Phytol 182: 49–84. doi: 10.1111/j.1469-8137.2008.02738.x 19192191
23. Sinclair SA, Krämer U (2012) The zinc homeostasis network of land plants. Biochim Biophys Acta 1823: 1553–1567. doi: 10.1016/j.bbamcr.2012.05.016 22626733
24. Long TA, Tsukagoshi H, Busch W, Lahner B, Salt DE, et al. (2010) The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 22: 2219–2236. doi: 10.1105/tpc.110.074096 20675571
25. Li X, Zhang H, Ai Q, Liang G, Yu D (2016) Two bHLH Transcription Factors, bHLH34 and bHLH104, Regulate Iron Homeostasis in Arabidopsis thaliana. Plant Physiol 170: 2478–2493. doi: 10.1104/pp.15.01827 26921305
26. Satbhai SB, Setzer C, Freynschlag F, Slovak R, Kerdaffrec E, et al. (2017) Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nature communications 8: 15603. doi: 10.1038/ncomms15603 28537266
27. Bouain N, Satbhai SB, Korte A, Saenchai C, Desbrosses G, et al. (2018) Natural allelic variation of the AZI1 gene controls root growth under zinc-limiting condition. PLoS Genet 14: e1007304. doi: 10.1371/journal.pgen.1007304 29608565
28. Rouached H, Rhee SY (2017) System-level understanding of plant mineral nutrition in the big data era. Current Opinion in System Biology 4: 71–77.
29. Briat J-F, Rouached H, Tissot N, Gaymard F, Dubos C (2015) Integration of P, S, Fe, and Zn nutrition signals in Arabidopsis thaliana: potential involvement of PHOSPHATE STARVATION RESPONSE 1 (PHR1). Frontiers in Plant Science 6: 290. doi: 10.3389/fpls.2015.00290 25972885
30. Bouain N, Shahzad Z, Rouached A, Khan GA, Berthomieu P, et al. (2014) Phosphate and zinc transport and signalling in plants: toward a better understanding of their homeostasis interaction. J Exp Bot 65: 5725–5741. doi: 10.1093/jxb/eru314 25080087
31. Kellermeier F, Armengaud P, Seditas TJ, Danku J, Salt DE, et al. (2014) Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26: 1480–1496. doi: 10.1105/tpc.113.122101 24692421
32. Li W, Lan P (2015) Genome-wide analysis of overlapping genes regulated by iron deficiency and phosphate starvation reveals new interactions in Arabidopsis roots. BMC Res Notes 8: 555. doi: 10.1186/s13104-015-1524-y 26459023
33. Misson J, Raghothama KG, Jain A, Jouhet J, Block MA, et al. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc Natl Acad Sci U S A 102: 11934–11939. doi: 10.1073/pnas.0505266102 16085708
34. Franco-Zorrilla JM, Martin AC, Leyva A, Paz-Ares J (2005) Interaction between phosphate-starvation, sugar, and cytokinin signaling in Arabidopsis and the roles of cytokinin receptors CRE1/AHK4 and AHK3. Plant Physiol 138: 847–857. doi: 10.1104/pp.105.060517 15923327
35. Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, et al. (2000) Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. Plant J 24: 559–567. doi: 10.1046/j.1365-313x.2000.00893.x 11123795
36. Seguela M, Briat JF, Vert G, Curie C (2008) Cytokinins negatively regulate the root iron uptake machinery in Arabidopsis through a growth-dependent pathway. Plant J 55: 289–300. doi: 10.1111/j.1365-313X.2008.03502.x 18397377
37. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG (2008) The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiology 147: 1181–1191. doi: 10.1104/pp.108.118562 18467463
38. Gutierrez-Alanis D, Yong-Villalobos L, Jimenez-Sandoval P, Alatorre-Cobos F, Oropeza-Aburto A, et al. (2017) Phosphate Starvation-Dependent Iron Mobilization Induces CLE14 Expression to Trigger Root Meristem Differentiation through CLV2/PEPR2 Signaling. Dev Cell 41: 555–570 e553. doi: 10.1016/j.devcel.2017.05.009 28586647
39. Ristova D, Giovannetti M, Metesch K, Busch W (2018) Natural genetic variation shapes root system responses to phytohormones in Arabidopsis. Plant J 96: 468–481. doi: 10.1111/tpj.14034 30030851
40. Slovak R, Göschl C, Su X, Shimotani K, Shiina T, et al. (2014) A scalable open-source pipeline for large-scale root phenotyping of Arabidopsis. Plant Cell 26: 2390–2403. doi: 10.1105/tpc.114.124032 24920330
41. Chevalier F, Pata M, Nacry P, Doumas P, Rossignol M (2003) Effects of phosphate availability on the root system architecture: large-scale analysis of the natural variation between Arabidopsis accessions. Plant, Cell & Environment 26: 1839–1850.
42. Kawa D, Julkowska M, Sommerfeld HM, ter Horst A, Haring MA, et al. (2016) Phosphate-dependent root system architecture responses to salt stress. Plant physiology: pp. 00712.02016.
43. Horton MW, Hancock AM, Huang YS, Toomajian C, Atwell S, et al. (2012) Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nature genetics 44: 212–216. doi: 10.1038/ng.1042 22231484
44. Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163: 161–179. doi: 10.1104/pp.113.218453 23852440
45. Lynch M, Walsh B (1998) Genetics and analysis of quantitative traits: Sinauer Sunderland, MA.
46. Kang HM, Zaitlen NA, Wade CM, Kirby A, Heckerman D, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics 178: 1709–1723. doi: 10.1534/genetics.107.080101 18385116
47. Gan X, Stegle O, Behr J, Steffen JG, Drewe P, et al. (2011) Multiple reference genomes and transcriptomes for Arabidopsis thaliana. Nature 477: 419–423. doi: 10.1038/nature10414 21874022
48. Garcia ME, Lynch T, Peeters J, Snowden C, Finkelstein R (2008) A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol Biol 67: 643–658. doi: 10.1007/s11103-008-9344-2 18484180
49. Bernal M, Casero D, Singh V, Wilson GT, Grande A, et al. (2012) Transcriptome sequencing identifies SPL7-regulated copper acquisition genes FRO4/FRO5 and the copper dependence of iron homeostasis in Arabidopsis. Plant Cell 24: 738–761. doi: 10.1105/tpc.111.090431 22374396
50. Davila Olivas NH, Kruijer W, Gort G, Wijnen CL, van Loon JJ, et al. (2017) Genome-wide association analysis reveals distinct genetic architectures for single and combined stress responses in Arabidopsis thaliana. New Phytol 213: 838–851. doi: 10.1111/nph.14165 27604707
51. Thoen MP, Davila Olivas NH, Kloth KJ, Coolen S, Huang PP, et al. (2017) Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping. New Phytol 213: 1346–1362. doi: 10.1111/nph.14220 27699793
52. Torabinejad J, Donahue JL, Gunesekera BN, Allen-Daniels MJ, Gillaspy GE (2009) VTC4 Is a Bifunctional Enzyme That Affects Myoinositol and Ascorbate Biosynthesis in Plants. Plant Physiology 150: 951–961. doi: 10.1104/pp.108.135129 19339506
53. Bustos R, Castrillo G, Linhares F, Puga MI, Rubio V, et al. (2010) A central regulatory system largely controls transcriptional activation and repression responses to phosphate starvation in Arabidopsis. PLoS Genet 6: e1001102. doi: 10.1371/journal.pgen.1001102 20838596
54. Lee T, Yang S, Kim E, Ko Y, Hwang S, et al. (2014) AraNet v2: an improved database of co-functional gene networks for the study of Arabidopsis thaliana and 27 other nonmodel plant species. Nucleic acids research 43: D996–D1002. doi: 10.1093/nar/gku1053 25355510
55. Schachtman DP, Shin R (2007) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58: 47–69. doi: 10.1146/annurev.arplant.58.032806.103750 17067284
56. López-Bucio J, Cruz-Ramırez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6: 280–287. 12753979
57. Shahzad Z, Kellermeier F, Armstrong EM, Rogers S, Lobet G, et al. (2018) EZ-Root-VIS: A Software Pipeline for the Rapid Analysis and Visual Reconstruction of Root System Architecture. Plant Physiol.
58. Rai V, Sanagala R, Sinilal B, Yadav S, Sarkar AK, et al. (2015) Iron Availability Affects Phosphate Deficiency-Mediated Responses, and Evidence of Cross-Talk with Auxin and Zinc in Arabidopsis. Plant Cell Physiol 56: 1107–1123. doi: 10.1093/pcp/pcv035 25759329
59. Khan GA, Bouraine S, Wege S, Li Y, De Carbonnel M, et al. (2014) Coordination between zinc and phosphate homeostasis involves the transcription factor PHR1, the phosphate exporter PHO1, and its homologue PHO1; H3 in Arabidopsis. Journal of experimental botany 65: 871–884. doi: 10.1093/jxb/ert444 24420568
60. Kisko M, Bouain N, Safi A, Medici A, Akkers RC, et al. (2018) LPCAT1 controls phosphate homeostasis in a zinc-dependent manner. Elife 7.
61. Huang C, Barker SJ, Langridge P, Smith FW, Graham RD (2000) Zinc deficiency up-regulates expression of high-affinity phosphate transporter genes in both phosphate-sufficient and-deficient barley roots. Plant Physiology 124: 415–422. doi: 10.1104/pp.124.1.415 10982454
62. Alonso-Blanco C, Andrade J, Becker C, Bemm F, Bergelson J, et al. (2016) 1,135 genomes reveal the global pattern of polymorphism in Arabidopsis thaliana. Cell 166: 481–491. doi: 10.1016/j.cell.2016.05.063 27293186
63. Belhaj K, Chaparro-Garcia A, Kamoun S, Patron NJ, Nekrasov V (2015) Editing plant genomes with CRISPR/Cas9. Curr Opin Biotechnol 32: 76–84. doi: 10.1016/j.copbio.2014.11.007 25437637
64. Liu S, Yu Y, Ruan Y, Meyer D, Wolff M, et al. (2007) Plant SET- and RING-associated domain proteins in heterochromatinization. Plant J 52: 914–926. doi: 10.1111/j.1365-313X.2007.03286.x 17892444
65. Young KG, Copeland JW (2010) Formins in cell signaling. Biochim Biophys Acta 1803: 183–190. doi: 10.1016/j.bbamcr.2008.09.017 18977250
66. Yong-Villalobos L, Gonzalez-Morales SI, Wrobel K, Gutierrez-Alanis D, Cervantes-Perez SA, et al. (2015) Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation. Proc Natl Acad Sci U S A 112: E7293–7302. doi: 10.1073/pnas.1522301112 26668375
67. Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E, et al. (2013) Arabidopsis ferritin 1 (AtFer1) gene regulation by the phosphate starvation response 1 (AtPHR1) transcription factor reveals a direct molecular link between iron and phosphate homeostasis. Journal of Biological Chemistry 288: 22670–22680. doi: 10.1074/jbc.M113.482281 23788639
68. Baluska F, Salaj J, Mathur J, Braun M, Jasper F, et al. (2000) Root hair formation: F-actin-dependent tip growth is initiated by local assembly of profilin-supported F-actin meshworks accumulated within expansin-enriched bulges. Dev Biol 227: 618–632. doi: 10.1006/dbio.2000.9908 11071779
69. Bibikova TN, Blancaflor EB, Gilroy S (1999) Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant J 17: 657–665. doi: 10.1046/j.1365-313x.1999.00415.x 10230063
70. Favery B, Chelysheva LA, Lebris M, Jammes F, Marmagne A, et al. (2004) Arabidopsis formin AtFH6 is a plasma membrane-associated protein upregulated in giant cells induced by parasitic nematodes. Plant Cell 16: 2529–2540. doi: 10.1105/tpc.104.024372 15319477
71. Robert N, d'Erfurth I, Marmagne A, Erhardt M, Allot M, et al. (2012) Voltage-dependent-anion-channels (VDACs) in Arabidopsis have a dual localization in the cell but show a distinct role in mitochondria. Plant Mol Biol 78: 431–446. doi: 10.1007/s11103-012-9874-5 22294207
72. Zhang M, Takano T, Liu S, Zhang X (2015) Arabidopsis mitochondrial voltage-dependent anion channel 3 (AtVDAC3) protein interacts with thioredoxin m2. FEBS Lett 589: 1207–1213. doi: 10.1016/j.febslet.2015.03.034 25862497
73. Müller J, Toev T, Heisters M, Teller J, Moore KL, et al. (2015) Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Developmental Cell 33: 216–230. doi: 10.1016/j.devcel.2015.02.007 25898169
74. Huang TK, Puchta H (2019) CRISPR/Cas-mediated gene targeting in plants: finally a turn for the better for homologous recombination. Plant Cell Rep 38: 443–453. doi: 10.1007/s00299-019-02379-0 30673818
75. Xu Y-C, Niu X-M, Li X-X, He W, Chen J-F, et al. (2019) Adaptation and Phenotypic Diversification in Arabidopsis through Loss-of-Function Mutations in Protein-Coding Genes. The Plant Cell 31: 1012–1025. doi: 10.1105/tpc.18.00791 30886128
76. Seren Ü, Vilhjálmsson BJ, Horton MW, Meng D, Forai P, et al. (2012) GWAPP: a web application for genome-wide association mapping in Arabidopsis. The Plant Cell 24: 4793–4805. doi: 10.1105/tpc.112.108068 23277364
77. Kang HM, Sul JH, Service SK, Zaitlen NA, Kong SY, et al. (2010) Variance component model to account for sample structure in genome-wide association studies. Nat Genet 42: 348–354. doi: 10.1038/ng.548 20208533
78. Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, et al. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13: 2498–2504. doi: 10.1101/gr.1239303 14597658
79. Heberle H, Meirelles GV, da Silva FR, Telles GP, Minghim R (2015) InteractiVenn: a web-based tool for the analysis of sets through Venn diagrams. BMC Bioinformatics 16: 169. doi: 10.1186/s12859-015-0611-3 25994840
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