Analysis of gene co-expression networks of phosphate starvation and aluminium toxicity responses in Populus spp.

English version

Autoři: Thiago Bergamo Cardoso ^aff001; Renan Terassi Pinto ^aff001; Luciano Vilela Paiva ^aff001
Působiště autorů: Central Laboratory of Molecular Biology, Department of Chemistry, Federal University of Lavras, Lavras, Brazil ^aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223217

Souhrn

The adaptation of crops to acid soils is needed for the maintenance of food security in a sustainable way, as decreasing fertilizers use and mechanical interventions in the soil would favor the reduction of agricultural practices’ environmental impact. Phosphate deficiency and the presence of reactive aluminum affect vital processes to the plant in this soil, mostly water and nutrient absorption. From this, the understanding of the molecular response to these stresses can foster strategies for genetic improvement, so the aim was to broadly analyze the transcriptional variations in Poupulus spp. in response to these abiotic stresses, as a plant model for woody crops. A co-expression network was constructed among 3,180 genes differentially expressed in aluminum-stressed plants with 34,988 connections. Of this total, 344 genes presented two-fold transcriptional variation and the group of genes associated with those regulated after 246 hours of stress had higher number of connections per gene, with some already characterized genes related to this stress as main hubs. Another co-expression network was made up of 8,380 connections between 550 genes regulated by aluminum stress and phosphate deficiency, in which 380 genes had similar profile in both stresses and only eight with transcriptional variation higher than 20%. All the transcriptomic data are presented here with functional enrichment and homology comparisons with already characterized genes in another species that are related to the explored stresses, in order to provide a broad analysis of the co-opted responses for both the stresses as well as some specificity. This approach improves our understanding regarding the plants adaptation to acid soils and may contribute to strategies of crop genetic improvement for this condition that is widely present in regions of high agricultural activity.

Klíčová slova:

Gene expression – Gene regulation – Genetic networks – Phosphates – Transcription factors – Arabidopsis thaliana – Transcriptional control – Aluminum

Zdroje

1. Lopes AS, Guimarães Guilherme LR. A career perspective on soil management in the Cerrado region of Brazil. Adv Agron. 2016;137: 1–72. doi: 10.1016/bs.agron.2015.12.004

2. von Uexküll HR, Mutert E. Global Extent, Development and Economic-Impact of Acid Soils. Plant Soil. 1995;171: 1–15. doi: 10.1007/BF00009558

3. Kochian L V, Neros MAP, Liu J, Magalhaes J V. Plant Adaptation to Acid Soils: The Molecular Basis for Crop Aluminum Resistance. Annu Rev Plant Biol. 2015;6623281: 1–23. doi: 10.1146/annurev-arplant-043014-114822 25621514

4. Singh D, Singh NP, Chauhan SK, Singh P. Developing aluminium-tolerant crop plants using biotechnological tools. Curr Sci. 2011;100: 1807–1814.

5. Heuer S, Gaxiola R, Schilling R, Herrera-Estrella L, López-Arredondo D, Wissuwa M, et al. Improving phosphorus use efficiency: a complex trait with emerging opportunities. Plant J. 2017;90: 868–885. doi: 10.1111/tpj.13423 27859875

6. Zhang X, Long Y, Huang J, Xia J. Molecular Mechanisms for Coping with Al Toxicity in Plants. Int J Mol Sci. 2019;20: 1–16. doi: 10.3390/ijms20071551 30925682

7. Crombez H, Motte H, Beeckman T. Review Tackling Plant Phosphate Starvation by the Roots. Dev Cell Rev. Elsevier; 2019;48: 599–615. doi: 10.1016/j.devcel.2019.01.002 30861374

8. Chen ZC, Liao H. Organic acid anions: An effective defensive weapon for plants against aluminum toxicity and phosphorus de ficiency in acidic soils. J Genet Genomics. Elsevier Limited and Science Press; 2016;43: 631–638. doi: 10.1016/j.jgg.2016.11.003 27890545

9. Godon C, Mercier C, Wang X, David P, Richaud P, Nussaume L, et al. Under phosphate starvation conditions, Fe and Al trigger accumulation of the transcription factor STOP1 in the nucleus of Arabidopsis root cells. Plant J. 2019; 1–13. doi: 10.1111/tpj.14374 31034704

10. Sun L, Tian J, Zhang H, Liao H. Phytohormone regulation of root growth triggered by P deficiency or Al toxicity. J Exp Bot. 2016;67: 3655–3664. doi: 10.1093/jxb/erw188 27190050

11. Pooniya V, Palta JA, Chen Y, Delhaize E, Siddique KHM. Impact of the TaMATE1B gene on above and below-ground growth of durum wheat grown on an acid and Al 3 + -toxic soil. Plant Soil. Plant and Soil; 2019; doi: 10.1007/s11104-019-03939-9 31007286

12. Zhang L, Li G, Li Y, Min J, Kronzucker HJ, Shi W. Tomato plants ectopically expressing Arabidopsis GRF9 show enhanced resistance to phosphate deficiency and improved fruit production in the field. J Plant Physiol. Elsevier; 2018;226: 31–39. doi: 10.1016/j.jplph.2018.04.005 29698910

13. Li W, Lan P. Genome-wide analysis of overlapping genes regulated by iron deficiency and phosphate starvation reveals new interactions in Arabidopsis roots. BMC Res Notes. BioMed Central; 2015;8: 555. doi: 10.1186/s13104-015-1524-y 26459023

14. Taylor G. Populus: Arabidopsis for Forestry. Do We Need a Model Tree? Ann Bot. 2002;90: 681–689. doi: 10.1093/aob/mcf255 12451023

15. Jansson S, Douglas CJ. Populus: A Model System for Plant Biology. Annu Rev Plant Biol. 2007;58: 58–435. doi: 10.1146/annurev.arplant.58.032806.103956 17280524

16. Tuskan GA, DiFazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science (80-). 2006;313: 1596–1604. doi: 10.1126/science.1128691 16973872

17. Sjödin A, Street NR, Sandberg G, Gustafsson P, Jansson S, Jansson S. The Populus Genome Integrative Explorer (PopGenIE): a new resource for exploring the Populus genome. New Phytol. 2009;182: 1013–1025. doi: 10.1111/j.1469-8137.2009.02807.x 19383103

18. Yadav R, Yadav N, Goutam U, Kumar S, Chaudhury A. Genetic Engineering of Poplar: Current Achievements and Future Goals. Plant Biotechnology: Recent Advancements and Developments. 2017. pp. 361–390. doi: 10.1007/978-981-10-4732-9

19. Fan D, Liu T, Li C, Jiao B, Li S, Hou Y, et al. Efficient CRISPR / Cas9-mediated Targeted Mutagenesis in Populus in the First Generation. Nat Publ Gr. Nature Publishing Group; 2015; 1–7. doi: 10.1038/srep12217 26193631

20. Muhr M, Paulat M, Awwanah M, Brinkkötter M, Teichmann T. Research paper CRISPR / Cas9-mediated knockout of Populus BRANCHED1 and BRANCHED2 orthologs reveals a major function in bud outgrowth control. Tree Physiol. 2018;38: 1588–1597. doi: 10.1093/treephys/tpy088 30265349

21. Bruegmann T, Fladung KD and M. Evaluating the E ffi ciency of gRNAs in CRISPR / Cas9 Mediated Genome Editing in Poplars. Int J Mol Sci. 2019;20: 3623–3642.

22. Lan P, Li W, Schmidt W. “Omics” Approaches Towards Understanding Plant Phosphorus Acquisition and Use. Phosphorus Metabolism in Plants. 2015. doi: 10.3390/plants4040773 27135351

23. Tannert M, May A, Ditfe D, Berger S, Balcke GU, Tissier A, et al. Pi starvation-dependent regulation of ethanolamine metabolism by phosphoethanolamine phosphatase PECP1 in Arabidopsis roots. J Exp Bot. 2018;69: 467–481. doi: 10.1093/jxb/erx408 29294054

24. Ayadi A, David P, Arrighi J-F, Chiarenza S, Thibaud M-C, Nussaume L, et al. Reducing the Genetic Redundancy of Arabidopsis PHOSPHATE TRANSPORTER1 Transporters to Study Phosphate Uptake and Signaling. Plant Physiol. 2015;167: 1511–1526. doi: 10.1104/pp.114.252338 25670816

25. Grisel N, Zoller S, Künzli-Gontarczyk M, Lampart T, Münsterkötter M, Brunner I, et al. Transcriptome responses to aluminum stress in roots of aspen (Populus tremula). BMC Plant Biol. 2010;10: 185. doi: 10.1186/1471-2229-10-185 20727216

26. Xu W, Chen Z, Ahmed N, Han B, Cui Q, Liu A. Genome-wide identification, evolutionary analysis, and stress responses of the GRAS gene family in castor beans. Int J Mol Sci. 2016;17: 1–16. doi: 10.3390/ijms17071004 27347937

27. Liu W, Xiong C, Yan L, Zhang Z, Ma L. Transcriptome Analyses Reveal Candidate Genes Potentially Involved in Al Stress Response in Alfalfa. 2017;8: 1–11. doi: 10.3389/fpls.2017.00026 28217130

28. Salgado LR, Lima R, Santos BF dos, Shirakawa KT, Vilela M de A, Almeida NF, et al. De novo RNA sequencing and analysis of the transcriptome of signalgrass (Urochloa decumbens) roots exposed to aluminum. Plant Growth Regul. Springer Netherlands; 2017;83: 157–170. doi: 10.1007/s10725-017-0291-2

29. Gabrielson KM, Cancel JD, Morua LF, Larsen PB. Identification of dominant mutations that confer increased aluminium tolerance through mutagenesis of the Al-sensitive Arabidopsis mutant, als3-1. J Exp Bot. 2006;57: 943–951. doi: 10.1093/jxb/erj080 16488918

30. Kobayashi Y, Kobayashi Y, Watanabe T, Shaff JE, Ohta H, Kochian L V., et al. Molecular and Physiological Analysis of Al3+ and H+ Rhizotoxicities at Moderately Acidic Conditions. Plant Physiol. 2013;163: 180–192. doi: 10.1104/pp.113.222893 23839867

31. Sawaki Y, Kihara-Doi T, Kobayashi Y, Nishikubo N, Kawazu T, Kobayashi Y, et al. Characterization of Al-responsive citrate excretion and citrate-transporting MATEs in Eucalyptus camaldulensis. Planta. 2013;237: 979–989. doi: 10.1007/s00425-012-1810-z 23187679

32. Durrett TP, Gassmann W, Rogers EE. The FRD3-Mediated Efflux of Citrate into the Root Vasculature Is Necessary for Efficient Iron Translocation. Plant Physiol. 2007;144: 197–205. doi: 10.1104/pp.107.097162 17351051

33. Sawaki Y, Iuchi S, Kobayashi Y, Kobayashi Y, Ikka T, Sakurai N, et al. STOP1 Regulates Multiple Genes That Protect Arabidopsis from Proton and Aluminum Toxicities. Plant Physiol. 2009;150: 281–294. doi: 10.1104/pp.108.134700 19321711

34. Kobayashi Y, Ohyama Y, Kobayashi Y, Ito H, Iuchi S, Fujita M, et al. STOP2 activates transcription of several genes for Al- and low pH-tolerance that are regulated by STOP1 in arabidopsis. Mol Plant. © The Authors. All rights reserved.; 2014;7: 311–322. doi: 10.1093/mp/sst116 23935008

35. Mickelbart M V., Hasegawa PM, Bailey-Serres J. Genetic mechanisms of abiotic stress tolerance that translate to crop yield stability. Nat Rev Genet. Nature Publishing Group; 2015;16: 237–251. doi: 10.1038/nrg3901 25752530

36. Jin J, Tian F, Yang DC, Meng YQ, Kong L, Luo J, et al. PlantTFDB 4.0: Toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res. 2017;45: D1040–D1045. doi: 10.1093/nar/gkw982 27924042

37. Skinner MK, Rawls A, Wilson-Rawls J, Roalson EH. Basic helix-loop-helix transcription factor gene family phylogenetics and nomenclature. Differentiation. Elsevier; 2010;80: 1–8. doi: 10.1016/j.diff.2010.02.003 20219281

38. Marzol E, Borassi C, Juárez SPD, Mangano S, Estevez JM. RSL4 Takes Control: Multiple Signals, One Transcription Factor. 2017;22: 553–555. doi: 10.1016/j.tplants.2017.04.007 28487046

39. Zhang C, Simpson RJ, Kim CM, Warthmann N, Delhaize E, Dolan L, et al. Do longer root hairs improve phosphorus uptake? Testing the hypothesis with transgenic Brachypodium distachyon lines overexpressing endogenous RSL genes. New Phytol. 2018;217: 1654–1666. doi: 10.1111/nph.14980 29341123

40. Choe J, Kim B, Yoon EK, Jang S, Kim G, Dhar S, et al. Characterization of the GRAS Transcription Factor SCARECROW- LIKE 28 ‘ s Role in Arabidopsis Root Growth. 2017; 462–471. doi: 10.1007/s12374-017-0112-1

41. Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS, et al. SAUR Inhibition of PP2C-D Phosphatases Activates Plasma Membrane H+-ATPases to Promote Cell Expansion in Arabidopsis. Plant Cell. 2014;26: 2129–2142. doi: 10.1105/tpc.114.126037 24858935

42. Sawaki Y, Kobayashi Y, Kihara-Doi T, Nishikubo N, Kawazu T, Kobayashi M, et al. Identification of a STOP1-like protein in Eucalyptus that regulates transcription of Al tolerance genes. Plant Sci. 2014;223: 8–15. doi: 10.1016/j.plantsci.2014.02.011 24767110

43. Fan W, Lou HQ, Yang JL, Zheng SJ. The roles of STOP1-like transcription factors in aluminum and proton tolerance. Plant Signal Behav. Taylor & Francis; 2016;11: e1131371. doi: 10.1080/15592324.2015.1131371 26689896

44. Dmitriev AA, Krasnov GS, Rozhmina TA, Kishlyan N V., Zyablitsin A V., Sadritdinova AF, et al. Glutathione S-transferases and UDP-glycosyltransferases Are Involved in Response to Aluminum Stress in Flax. Front Plant Sci. 2017;7. doi: 10.3389/fpls.2016.01920 28066475

45. Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature. 2012;488: 535-+. doi: 10.1038/nature11346 22914168

46. Chen ZC, Liao H. Organic acid anions: An effective defensive weapon for plants against aluminum toxicity and phosphorus deficiency in acidic soils. J Genet Genomics. Elsevier Limited and Science Press; 2016;43: 631–638. doi: 10.1016/j.jgg.2016.11.003 27890545

47. Grisel N, Zoller S, Künzli-Gontarczyk M, Lampart T, Münsterkötter M, Brunner I, et al. Transcriptome responses to aluminum stress in roots of aspen (Populus tremula). BMC Plant Biol. 2010;10. doi: 10.1186/1471-2229-10-185 20727216

48. Zhang C, Meng S, Li M, Zhao Z. Genomic Identification and Expression Analysis of the Phosphate Transporter Gene Family in Poplar. Front Plant Sci. 2016;7. doi: 10.3389/fpls.2016.01398 27695473

49. Parra-almuna L, Diaz-cortez A, Ferrol N, De M, Mora L. Plant Physiology and Biochemistry Aluminium toxicity and phosphate de fi ciency activates antioxidant systems and up-regulates expression of phosphate transporters gene in ryegrass (Lolium perenne L.) plants. Plant Physiol Biochem. Elsevier; 2018;130: 445–454. doi: 10.1016/j.plaphy.2018.07.031 30077920

50. CHAVEZ VA. ANALYSIS OF THE ARABIDOPSIS NAC GENE SUPERFAMILY IN PLANT DEVELOPMENT. 2007.

51. Jensen MK, Skriver K. NAC transcription factor gene regulatory and protein-protein interaction networks in plant stress responses and senescence. IUBMB Life. 2014;66: 156–166. doi: 10.1002/iub.1256 24659537

52. Wang Y-L, Almvik M, Clarke N, Eich-Greatorex S, Øgaard AF, Krogstad T, et al. Contrasting responses of root morphology and root-exuded organic acids to low phosphorus availability in three important food crops with divergent root traits. AoB Plants. 2015;7: plv097. doi: 10.1093/aobpla/plv097 26286222

53. Sasaki M, Yamamoto Y, Matsumoto H. Lignin deposition induced by aluminum in wheat (Triticum aestivum) roots. Physiol Plant. 1996;96: 193–198. doi: 10.1111/j.1399-3054.1996.tb00201.x

54. Janz D, Behnke K, Schnitzler J-P, Kanawati B, Schmitt-Kopplin P, Polle A. Pathway analysis of the transcriptome and metabolome of salt sensitive and tolerant poplar species reveals evolutionary adaption of stress tolerance mechanisms. BMC Plant Biol. 2010;10: 150. doi: 10.1186/1471-2229-10-150 20637123

55. Gautier L, Cope L, Bolstad BM, Irizarry RA. Affy—Analysis of Affymetrix GeneChip data at the probe level. Bioinformatics. 2004;20: 307–315. doi: 10.1093/bioinformatics/btg405 14960456

56. Kauffmann A, Rayner TF, Parkinson H, Kapushesky M, Lukk M, Brazma A, et al. Importing ArrayExpress datasets into R/Bioconductor. Bioinformatics. 2009;25: 2092–2094. doi: 10.1093/bioinformatics/btp354 19505942

57. Usadel B, Obayashi T, Mutwil M, Giorgi FM, Bassel GW, Tanimoto M, et al. Co-expression tools for plant biology: opportunities for hypothesis generation and caveats. Plant Cell Environ. 2009;32: 1633–1651. doi: 10.1111/j.1365-3040.2009.02040.x 19712066

58. Kavka M, Polle A. Phosphate uptake kinetics and tissue-specific transporter expression profiles in poplar (Populus × canescens) at different phosphorus availabilities. BMC Plant Biol. BMC Plant Biology; 2016;16: 206. doi: 10.1186/s12870-016-0892-3 27663513

59. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21: 3674–3676. doi: 10.1093/bioinformatics/bti610 16081474

Analysis of gene co-expression networks of phosphate starvation and aluminium toxicity responses in Populus spp.

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