PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana
Autoři:
Feng Zhang aff001; Wenqing Tao aff001; Ruiqi Sun aff001; Junxia Wang aff001; Cuiling Li aff001; Xiangpei Kong aff001; Huiyu Tian aff001; Zhaojun Ding aff001
Působiště autorů:
The Key Laboratory of the Plant Cell Engineering and Germplasm Innovation, Ministry of Education, School of Life Sciences, Shandong University, Qingdao, Shandong, China
aff001
Vyšlo v časopise:
PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana. PLoS Genet 16(2): e32767. doi:10.1371/journal.pgen.1008044
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008044
Souhrn
The development of lateral roots in Arabidopsis thaliana is strongly dependent on signaling directed by the AUXIN RESPONSE FACTOR7 (ARF7), which in turn activates LATERAL ORGAN BOUNDARIES DOMAIN (LBD) transcription factors (LBD16, LBD18 and LBD29). Here, the product of PRH1, a PR-1 homolog annotated previously as encoding a pathogen-responsive protein, was identified as a target of ARF7-mediated auxin signaling and also as participating in the development of lateral roots. PRH1 was shown to be strongly induced by auxin treatment, and plants lacking a functional copy of PRH1 formed fewer lateral roots. The transcription of PRH1 was controlled by the binding of both ARF7 and LBDs to its promoter region.
Klíčová slova:
Acetic acid – Arabidopsis thaliana – Auxins – Lateral roots – Seedlings – Transcription factors – Transcriptional control – Naphthalenes
Zdroje
1. Malamy JE, Benfey PN. Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development. 1997;124: 33–44. doi:VL—124 9006065
2. Dubrovsky JG, Doerner PW, Colón-Carmona A, Rost TL. Pericycle Cell Proliferation and Lateral Root Initiation in Arabidopsis. Plant Physiology. 2000;124: 1648–1657. doi: 10.1104/pp.124.4.1648 11115882
3. Peret B, Larrieu A, Bennett MJ. Lateral root emergence: a difficult birth. Journal of Experimental Botany. 2009;60: 3637–3643. doi: 10.1093/jxb/erp232 19635746
4. Benková E, Bielach A. Lateral root organogenesis—from cell to organ. Current Opinion in Plant Biology. 2010;13: 677–683. doi: 10.1016/j.pbi.2010.09.006 20934368
5. De Smet I, Tetsumura T, De Rybel B, Frey NF d., Laplaze L, Casimiro I, et al. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development. 2007;134: 681–690. doi: 10.1242/dev.02753 17215297
6. Fukaki H, Tameda S, Masuda H, Tasaka M. Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. The Plant Journal. 2002;29: 153–168. doi: 10.1046/j.0960-7412.2001.01201.x 11862947
7. Notaguchi M, Wolf S, Lucas WJ. Phloem-Mobile Aux / IAA Transcripts Target to the Root Tip and Modify Root Architecture F. Journal of Integrative Plant Biology. 2012;54: 760–772. doi: 10.1111/j.1744-7909.2012.01155.x 22925478
8. Berckmans B, Vassileva V, Schmid SPC, Maes S, Parizot B, Naramoto S, et al. Auxin-Dependent Cell Cycle Reactivation through Transcriptional Regulation of Arabidopsis E2Fa by Lateral Organ Boundary Proteins. The Plant Cell. 2011;23: 3671–3683. doi: 10.1105/tpc.111.088377 22003076
9. Lee HW, Cho C, Kim J. Lateral Organ Boundaries Domain16 and 18 Act Downstream of the AUXIN1 and LIKE-AUXIN3 Auxin Influx Carriers to Control Lateral Root Development in Arabidopsis. Plant Physiology. 2015;168: 1792–1806. doi: 10.1104/pp.15.00578 26059335
10. Kim J, Lee HW. Direct activation of EXPANSIN14 by LBD18 in the gene regulatory network of lateral root formation in Arabidopsis. Plant Signaling & Behavior. 2013;8: e22979. doi: 10.4161/psb.22979 23299420
11. Lee HW, Kim J. EXPANSINA17 Up-Regulated by LBD18/ASL20 promotes lateral root formation during the auxin response. Plant and Cell Physiology. 2013;54: 1600–1611. doi: 10.1093/pcp/pct105 23872272
12. Lee HW, Kim M-J, Kim NY, Lee SH, Kim J. LBD18 acts as a transcriptional activator that directly binds to the EXPANSIN14 promoter in promoting lateral root emergence of Arabidopsis. The Plant Journal. 2013;73: 212–224. doi: 10.1111/tpj.12013 22974309
13. Lee HW, Park JH, Park MY, Kim J. GIP1 may act as a coactivator that enhances transcriptional activity of LBD18 in Arabidopsis. Journal of Plant Physiology. Elsevier GmbH.; 2014;171: 14–18. doi: 10.1016/j.jplph.2013.11.003 24484953
14. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M. ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis. The Plant Cell. 2007;19: 118–130. doi: 10.1105/tpc.106.047761 17259263
15. Kumpf RP, Shi C-L, Larrieu A, Sto IM, Butenko MA, Peret B, et al. Floral organ abscission peptide IDA and its HAE/HSL2 receptors control cell separation during lateral root emergence. Proceedings of the National Academy of Sciences. 2013;110: 5235–5240. doi: 10.1073/pnas.1210835110 23479623
16. Laird J, Armengaud P, Giuntini P, Laval V, Milner JJ. Inappropriate annotation of a key defence marker in Arabidopsis: Will the real PR-1 please stand up? Planta. 2004;219: 1089–1092. doi: 10.1007/s00425-004-1355-x 15293050
17. Lu S, Friesen TL, Faris JD. Molecular characterization and genomic mapping of the pathogenesis-related protein 1 (PR-1) gene family in hexaploid wheat (Triticum aestivum L.). Molecular Genetics and Genomics. 2011;285: 485–503. doi: 10.1007/s00438-011-0618-z 21516334
18. Chen Y-L, Lee C, Cheng K, Chang W, Huang R, Nam HG, et al. Quantitative Peptidomics Study Reveals That a Wound-Induced Peptide from PR-1 Regulates Immune Signaling in Tomato. The Plant Cell. 2014;26: 4135–4148. doi: 10.1105/tpc.114.131185 25361956
19. Schumann U, Lee J, Kazan K, Ayliffe M, Wang M. DNA-Demethylase Regulated Genes Show Methylation-Independent Spatiotemporal Expression Patterns. Frontiers in Plant Science. 2017;8: 1–15. doi: 10.3389/fpls.2017.00001
20. Yan L, Wei S, Wu Y, Hu R, Li H, Yang W, et al. High-Efficiency Genome Editing in Arabidopsis Using YAO Promoter-Driven CRISPR/Cas9 System. Molecular Plant. 2015;8: 1820–1823. doi: 10.1016/j.molp.2015.10.004 26524930
21. Péret B, Li G, Zhao J, Band LR, Voß U, Postaire O, et al. Auxin regulates aquaporin function to facilitate lateral root emergence. Nature Cell Biology. 2012;14: 991–998. doi: 10.1038/ncb2573 22983115
22. Voß U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, et al. The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nature Communications. 2015;6: 7641. doi: 10.1038/ncomms8641 26144255
23. Lucas M, Godin C, Jay-Allemand C, Laplaze L. Auxin fluxes in the root apex co-regulate gravitropism and lateral root initiation. Journal of Experimental Botany. 2008;59: 55–66. doi: 10.1093/jxb/erm171 17720688
24. Lee HW, Kim NY, Lee DJ, Kim J. LBD18/ASL20 Regulates Lateral Root Formation in Combination with LBD16/ASL18 Downstream of ARF7 and ARF19 in Arabidopsis. Plant Physiology. 2009;151: 1377–1389. doi: 10.1104/pp.109.143685 19717544
25. Lee DJ, Park JW, Lee HW, Kim J. Genome-wide analysis of the auxin-responsive transcriptome downstream of iaa1 and its expression analysis reveal the diversity and complexity of auxin-regulated gene expression. Journal of Experimental Botany. 2009;60: 3935–3957. doi: 10.1093/jxb/erp230 19654206
26. Lee HW, Kang NY, Pandey SK, Cho C, Lee SH, Kim J. Dimerization in LBD16 and LBD18 Transcription Factors Is Critical for Lateral Root Formation. Plant Physiology. 2017;174: 301–311. doi: 10.1104/pp.17.00013 28336771
27. Porco S, Larrieu A, Du Y, Gaudinier A, Goh T, Swarup K, et al. Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development. 2016;143: 3340–3349. doi: 10.1242/dev.136283 27578783
28. Swarup K, Benková E, Swarup R, Casimiro I, Péret B, Yang Y, et al. The auxin influx carrier LAX3 promotes lateral root emergence. Nature Cell Biology. 2008;10: 946–954. doi: 10.1038/ncb1754 18622388
29. Yang Y-Z, Ding S, Wang Y, Li C-L, Shen Y, Meeley R, et al. Small kernel2 Encodes a Glutaminase in Vitamin B 6 Biosynthesis Essential for Maize Seed Development. Plant Physiology. 2017;174: 1127–1138. doi: 10.1104/pp.16.01295 28408540
30. Je B Il, Xu F, Wu Q, Liu L, Meeley R, Gallagher JP, et al. The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors. eLife. 2018;7: 1–21. doi: 10.7554/eLife.35673 29543153
31. Kwon YR, Lee HJ, Kim KH, Hong S-W, Lee SJ, Lee H. Ectopic expression of Expansin3 or Expansinβ1 causes enhanced hormone and salt stress sensitivity in Arabidopsis. Biotechnology Letters. 2008;30: 1281–1288. doi: 10.1007/s10529-008-9678-5 18317696
32. Porco S, Larrieu A, Du Y, Gaudinier A, Goh T, Swarup K, et al. Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development. 2016;143: 3340–3349. doi: 10.1242/dev.136283 27578783
33. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, et al. Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19. The Plant Cell. 2005;17: 444–463. doi: 10.1105/tpc.104.028316 15659631
34. Vanneste S, De Rybel B, Beemster GTS, Ljung K, De Smet I, Van Isterdael G, et al. Cell Cycle Progression in the Pericycle Is Not Sufficient for SOLITARY ROOT/IAA14-Mediated Lateral Root Initiation in Arabidopsis thaliana. The Plant Cell. 2005;17: 3035–3050. doi: 10.1105/tpc.105.035493 16243906
35. De Smet I, Lau S, Voss U, Vanneste S, Benjamins R, Rademacher EH, et al. Bimodular auxin response controls organogenesis in Arabidopsis. Proceedings of the National Academy of Sciences. 2010;107: 2705–2710. doi: 10.1073/pnas.0915001107 20133796
36. Piya S, Shrestha SK, Binder B, Stewart CN, Hewezi T. Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science. 2014;5: 1–9. doi: 10.3389/fpls.2014.00744 25566309
37. Laskowski M, Biller S, Stanley K, Kajstura T, Prusty R. Expression Profiling of Auxin-treated Arabidopsis Roots: Toward a Molecular Analysis of Lateral Root Emergence. Plant and Cell Physiology. 2006;47: 788–792. doi: 10.1093/pcp/pcj043 16621846
38. Shuai B, Reynaga-Pen˜a CG, Springer PS. The Lateral Organ Boundaries Gene Defines a Novel, Plant-Specific Gene Family. Plant Physiology. 2002;129: 747–761. doi: 10.1104/pp.010926 12068116
39. Lewis DR, Olex AL, Lundy SR, Turkett WH, Fetrow JS, Muday GK. A Kinetic Analysis of the Auxin Transcriptome Reveals Cell Wall Remodeling Proteins That Modulate Lateral Root Development in Arabidopsis. The Plant Cell. 2013;25: 3329–3346. doi: 10.1105/tpc.113.114868 24045021
40. Himanen K, Boucheron E, Vanneste S, de Almeida Engler J, Inzé D, Beeckman T. Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation. The Plant Cell. 2002;14: 2339–2351. doi: 10.1105/tpc.004960 12368490
41. Pandey SK, Kim J. Coiled-coil motif in LBD16 and LBD18 transcription factors are critical for dimerization and biological function in arabidopsis. Plant Signaling & Behavior. Taylor & Francis; 2018;13: e1411450. doi: 10.1080/15592324.2017.1411450 29227192
42. Xu C, Cao H, Zhang Q, Wang H, Xin W, Xu E, et al. Control of auxin-induced callus formation by bZIP59–LBD complex in Arabidopsis regeneration. Nature Plants. Springer US; 2018;4: 108–115. doi: 10.1038/s41477-017-0095-4 29358751
43. Fan M, Xu C, Xu K, Hu Y. LATERAL ORGAN BOUNDARIES DOMAIN transcription factors direct callus formation in Arabidopsis regeneration. Cell Research. 2012;22: 1169–1180. doi: 10.1038/cr.2012.63 22508267
44. Xu C, Cao H, Xu E, Zhang S, Hu Y. Genome-Wide Identification of Arabidopsis LBD29 Target Genes Reveals the Molecular Events behind Auxin-Induced Cell Reprogramming during Callus Formation. Plant and Cell Physiology. 2018;59: 749–760. doi: 10.1093/pcp/pcx168 29121271
45. Karimi M, Inzé D, Depicker A. GATEWAYTM vectors for Agrobacterium- mediated plant transformation. Trends in Plant Science. 2002;7: 193–195. doi: 10.1016/s1360-1385(02)02251-3 11992820
46. Clough SJ, Bent AF. Floral dip: a simplified method for Agrobacterium -mediated transformation ofArabidopsis thaliana. The Plant Journal. 1998;16: 735–743. doi: 10.1046/j.1365-313x.1998.00343.x 10069079
47. Liu G, Gao S, Tian H, Wu W, Robert HS, Ding Z. Local Transcriptional Control of YUCCA Regulates Auxin Promoted Root-Growth Inhibition in Response to Aluminium Stress in Arabidopsis. Yu H, editor. PLOS Genetics. 2016;12: e1006360. doi: 10.1371/journal.pgen.1006360 27716807
48. Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, et al. Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. Muday GK, editor. PLOS Genetics. 2018;14: e1007144. doi: 10.1371/journal.pgen.1007144 29324765
49. Chinnusamy V, Ohta M, Kanrar S, Lee B-H, Hong X, Agarwal M, et al. ICE1: a regulator of cold-induced transcriptome and freezing tolerance in Arabidopsis. Genes & development. 2003;17: 1043–54. doi: 10.1101/gad.1077503 12672693
50. Gendrel A-V, Lippman Z, Martienssen R, Colot V. Profiling histone modification patterns in plants using genomic tiling microarrays. Nature Methods. 2005;2: 213–218. doi: 10.1038/nmeth0305-213 16163802
51. Yoo S-D, Cho Y-H, Sheen J. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nature Protocols. 2007;2: 1565–1572. doi: 10.1038/nprot.2007.199 17585298
52. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, et al. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods. 2005;1: 1–14. doi: 10.1186/1746-4811-1-1
Článek vyšel v časopise
PLOS Genetics
2020 Číslo 2
- Antibiotika na nachlazení nezabírají! Jak můžeme zpomalit šíření rezistence?
- FDA varuje před selfmonitoringem cukru pomocí chytrých hodinek. Jak je to v Česku?
- Prof. Jan Škrha: Metformin je bezpečný, ale je třeba jej bezpečně užívat a léčbu kontrolovat
- Ibuprofen jako alternativa antibiotik při léčbě infekcí močových cest
- Jak a kdy u celiakie začíná reakce na lepek? Možnou odpověď poodkryla čerstvá kanadská studie
Nejčtenější v tomto čísle
- Planarian EGF repeat-containing genes megf6 and hemicentin are required to restrict the stem cell compartment
- Evolutionary dynamics of microRNA target sites across vertebrate evolution
- Rab11 activation by Ik2 kinase is required for dendrite pruning in Drosophila sensory neurons
- Identification of a novel base J binding protein complex involved in RNA polymerase II transcription termination in trypanosomes