Nitrate-responsive OBP4-XTH9 regulatory module controls lateral root development in Arabidopsis thaliana
Autoři:
Peipei Xu aff001; Weiming Cai aff001
Působiště autorů:
Laboratory of Photosynthesis and Environment, CAS Center for Excellence in Molecular Plant Sciences, Shanghai Institute of Plant Physiology and Ecology, Chinese Academy of Sciences, Shanghai, China
aff001
Vyšlo v časopise:
Nitrate-responsive OBP4-XTH9 regulatory module controls lateral root development in Arabidopsis thaliana. PLoS Genet 15(10): e32767. doi:10.1371/journal.pgen.1008465
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008465
Souhrn
Plant root system architecture in response to nitrate availability represents a notable example to study developmental plasticity, but the underlying mechanism remains largely unknown. Xyloglucan endotransglucosylases (XTHs) play a critical role in cell wall biosynthesis. Here we assessed the gene expression of XTH1-11 belonging to group I of XTHs in lateral root (LR) primordia and found that XTH9 was highly expressed. Correspondingly, an xth9 mutant displayed less LR, while overexpressing XTH9 presented more LR, suggesting the potential function of XTH9 in controlling LR development. XTH9 gene mutation obviously alters the properties of the cell wall. Furthermore, nitrogen signals stimulated the expression of XTH9 to promote LRs. Genetic analysis revealed that the function of XTH9 was dependent on auxin-mediated ARF7/19 and downstream AFB3 in response to nitrogen signals. In addition, we identified another transcription factor, OBP4, that was also induced by nitrogen treatment, but the induction was much slower than that of XTH9. In contrast to XTH9, overexpressing OBP4 caused fewer LRs while OBP4 knockdown with OBP4-RNAi or an artificial miRNA silenced amiOBP4 line produced more LR. We further found OBP4 bound to the promoter of XTH9 to suppress XTH9 expression. In agreement with this, both OBP4-RNAi and crossed OBP4-RNAi & 35S::XTH9 lines led to more LR, but OBP4-RNAi & xth9 produced less LR, similar to xth9. Based on these findings we propose a novel mechanism by which OBP4 antagonistically controls XTH9 expression and the OBP4-XTH9 module elaborately sustains LR development in response to nitrate treatment.
Klíčová slova:
Arabidopsis thaliana – Gene expression – Genetically modified plants – Nitrates – Plant cell walls – Root growth – Lateral roots – Gravitropism
Zdroje
1. Vidal EA, Tamayo KP Gutierrez RA (2010). Gene networks for nitrogen sensing, signaling, and response in Arabidopsis thaliana. Wiley Interdiscip Rev Syst Biol Med 2, 683–93. doi: 10.1002/wsbm.87 20890965
2. Vidal EA, Moyano TC, Riveras E, Contreras-Lopez O, and Gutierrez RA (2013). Systems approaches map regulatory networks downstream of the auxin receptor AFB3 in the nitrate response of Arabidopsis thaliana roots. P Natl Acad Sci USA 110:12840–12845.
3. Leran S, Munos S, Brachet C, Tillard P, Gojon A, Lacombe B (2013). Arabidopsis NRT1.1 is a bidirectional transporter involved in root-to-shoot nitrate translocation. Mol Plant 6, 1984–7. doi: 10.1093/mp/sst068 23645597
4. Warzybok A, Migock M (2012). The function of nitrate transporters NRT1 in plants. Postepy Biochem 58, 61–8. 23214130
5. Parker JL, Newstead S (2014). Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507, 68–72. doi: 10.1038/nature13116 24572366
6. Wang C, Zhang W, Li Z, Zhen Li, Bi YJ, Crawford NM, Wang Y (2018). FIP1 Plays an Important Role in Nitrate Signaling and Regulates CIPK8 and CIPK23 Expression in Arabidopsis. Front Plant Sci 9, 593. doi: 10.3389/fpls.2018.00593 29780398
7. Krouk G, Crawford NM, Coruzzi GM, Tsay YF (2010). Nitrate signaling: adaptation to fluctuating environments. Curr Opin Plant Biol 13, 266–73. doi: 10.1016/j.pbi.2009.12.003 20093067
8. Gan Y, Filleur S, Rahman A, Gotensparre S, Forde BG (2005). Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana. Planta 222, 730–42. doi: 10.1007/s00425-005-0020-3 16021502
9. Feng Z, Zhu J, Du X, Cui X (2012). Effects of three auxin-inducible LBD members on lateral root formation in Arabidopsis thaliana. Planta 236, 1227–37. doi: 10.1007/s00425-012-1673-3 22699776
10. Zhao L, Zhang W, Yang Y, Zehui Li, Na Li, Qi SD, Crawford NM, Wang Y (2018). The Arabidopsis NLP7 gene regulates nitrate signaling via NRT1.1-dependent pathway in the presence of ammonium. Sci Rep 8, 1487. doi: 10.1038/s41598-018-20038-4 29367694
11. Alvarez J. M., Riveras E., Vidal E. A., Gras D. E., ntrerasLópez O, & Tamayo K. P., et al. (2015). Systems approach identifies tga1 and tga4 transcription factors as important regulatory components of the nitrate response of arabidopsis thaliana roots. Plant Journal for Cell & Molecular Biology, 80(1), 1–13.
12. Vidal E.A., Araus V., Lu C., Parry G., Green P.J., Coruzzi G.M., and Gutierrez R.A. (2010). Nitrate-responsive miR393/AFB3 regulatory module controls root system architecture in Arabidopsis thaliana. P Natl Acad Sci USA 107:4477–4482.
13. Chatfield SP, Capron R, Severino A, Penttila PA, Alfred S, Nahal H, Trobacher C, Raizada MN, Provart NJ (2014). Incipient stem cell niche conversion in tissue culture: using a systems approach to probe early events in WUSCHEL-dependent conversion of lateral root primordial into shoot meristems. Plant J 77:665–666.
14. Dubrovsky JG, Rost TL, Colon-Carmona A, Doerner P (2001). Early primordium morphogenesis during lateral root initiation in Arabidopsis thaliana. Planta 214:30–36. 11762168
15. Kircher S, Schopfer P (2016). Priming and positioning of lateral roots in Arabidopsis. An approach for an integrating concept. J Exp Bot 67:1411–1420. doi: 10.1093/jxb/erv541 26712828
16. Vilches-Barro A, Maizel A (2015). Talking through walls: mechanisms of lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 23:31–38. doi: 10.1016/j.pbi.2014.10.005 25449724
17. Malamy JE (2005). Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ 28:67–77. 16021787
18. Himanen K, Boucheron E, Vanneste S, Engler JD, Inze D, Beeckman T (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14:2339–2351. doi: 10.1105/tpc.004960 12368490
19. Sanz L, Dewitte W, Forzani C, Patell F, Nieuwland J, Wen B, Quelhas P, De Jager S, Titmus C Campilho A, Ren Hong, Estelle Mark, Wang Hong, Murray James AH (2011). The Arabidopsis D-Type Cyclin CYCD2;1 and the Inhibitor ICK2/KRP2 Modulate Auxin-Induced Lateral Root Formation. Plant Cell 23:641–660. doi: 10.1105/tpc.110.080002 21357490
20. Lewis DR, Olex AL, Lundy SR, Turkett WH, Fetrow JS, Muday GK (2013). A kinetic analysis of the auxin transcriptome reveals cell wall remodeling proteins that modulate lateral root development in Arabidopsis. The Plant cell 25:3329–3346 doi: 10.1105/tpc.113.114868 24045021
21. Lucas M, Kenobi K, von Wangenheim D, Vobeta U, Swarup K, De Smet I, Van Damme D, Lawrence T, Peret B, Moscardi E, Barbeau D, Godin C, Salt D, Guyomarc’h S, Stelzer EHK, Maizel A, Laplaze L, Bennett MJ (2013). Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proceedings of the National Academy of Sciences of the United States of America 110:5229–5234. doi: 10.1073/pnas.1210807110 23479644
22. Swarup K, Benkova E, Swarup R, Casimiro I, Peret B, Yang Y, Parry G, Nielsen E, De Smet I, Vanneste S, Levesque MP, Carrier D, James N, Calvo V, Ljung K, Kramer E, Roberts R, Graham N, Marillonnet S, Patel K, Jones JDG, Taylor CG, Schachtman DP, May S, Sandberg G, Benfey P, Friml J, Kerr I, Beeckman T, Laplaze L, Bennett MJ (2008). The auxin influx carrier LAX3 promotes lateral root emergence. Nat Cell Biol 10:946–954. doi: 10.1038/ncb1754 18622388
23. Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L (2013). Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci 18:455–463.
24. De Smet I, Tetsumura T, De Rybel B, Frey NFD, Laplaze L, Casimiro I, Swarup R, Naudts M, Vanneste S, Audenaert D, Inzé D, Bennett MJ, Beeckman T (2007). Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 134:681–690. doi: 10.1242/dev.02753 17215297
25. Farquharson KL (2010). Gibberellin-Auxin Crosstalk Modulates Lateral Root Formation. Plant Cell 22:540–540. doi: 10.1105/tpc.110.220313 20354194
26. Fukaki H, Okushima Y, Tasaka M (2007). Auxin-mediated lateral root formation in higher plants. Int Rev Cytol 256:111–137. doi: 10.1016/S0074-7696(07)56004-3 17241906
27. Peret B, Li GW, Zhao J, Band LR, Voss U, Postaire O, Luu DT, Da Ines O, Casimiro I, Lucas M, Wells DM, Lazzerini L, Nacry P, King JR, Jensen OE, Schäffner AR, Maurel C, Bennett MJ (2012). Auxin regulates aquaporin function to facilitate lateral root emergence. Nature cell biology 14 (10):991. doi: 10.1038/ncb2573 22983115
28. Nibau C, Gibbs DJ, Coates JC (2008). Branching out in new directions: the control of root architecture by lateral root formation. New Phytologist 179:595–614. doi: 10.1111/j.1469-8137.2008.02472.x 18452506
29. Arase F, Nishitani H, Egusa M, Nishimoto N, Sakurai S, Sakamoto N, Kaminaka H (2012). IAA8 Involved in Lateral Root Formation Interacts with the TIR1 Auxin Receptor and ARF Transcription Factors in Arabidopsis. Plos One 7(8):e43414. doi: 10.1371/journal.pone.0043414 22912871
30. Goh T, Kasahara H, Mimura T, Kamiya Y, Fukaki H (2012). Multiple AUX/IAA-ARF modules regulate lateral root formation: the role of Arabidopsis SHY2/IAA3-mediated auxin signalling. Philos T R Soc B 367:1461–1468.
31. Asada K, Okazawa K, Nakagawa T, Sato Y, Kato I, Tomita E, Nishitani K (1993). Molecular-Cloning of Endo-Xyloglucan Transferase (Ext), a New Transferase Involved in Cell-Wall Construction. Faseb J 7:A1299–A1299.
32. Nishitani K, Tominaga R (1992). Endoxyloglucan Transferase, a Novel Class of Glycosyltransferase That Catalyzes Transfer of a Segment of Xyloglucan Molecule to Another Xyloglucan Molecule. J Biol Chem 267:21058–21064. 1400418
33. Rose JKC, Braam J, Fry SC, Nishitani K (2002). The XTH family of enzymes involved in xyloglucan endotransglucosylation and endohydrolysis: Current perspectives and a new unifying nomenclature. Plant and Cell Physiology 43:1421–1435. doi: 10.1093/pcp/pcf171 12514239
34. Yokoyama R, Nishitani K (2001). A comprehensive expression analysis of all members of a gene family encoding cell-wall enzymes allowed us to predict cis-regulatory regions involved in cell-wall construction in specific organs of Arabidopsis. Plant and Cell Physiology 42:1025–1033. doi: 10.1093/pcp/pce154 11673616
35. Osato Y, Yokoyama R, Nishitani K (2006). A principal role for AtXTH18 in Arabidopsis thaliana root growth: a functional analysis using RNAi plants. Journal of plant research 119:153–162. doi: 10.1007/s10265-006-0262-6 16477366
36. Matsui A, Yokoyama R, Seki M, Ito T, Shinozaki K, Takahashi T, Komeda Y, Nishitani K (2005). AtXTH27 plays an essential role in cell wall modification during the development of tracheary elements. Plant J 42:525–534. doi: 10.1111/j.1365-313X.2005.02395.x 15860011
37. Zhu XF, Shi YZ, Lei GJ, Fry SC, Zhang BC, Zhou YH, Braam J, Jiang T, Xu XY, Mao CZ, Pan YJ, Yang JL, Wu P, Zheng SJ (2012). XTH31, Encoding an in Vitro XEH/XET-Active Enzyme, Regulates Aluminum Sensitivity by Modulating in Vivo XET Action, Cell Wall Xyloglucan Content, and Aluminum Binding Capacity in Arabidopsis. Plant Cell 24:4731–4747. doi: 10.1105/tpc.112.106039 23204407
38. Becnel J, Natarajan M, Kipp A, Braam J. (2006). Developmental expression patterns of Arabidopsis XTH genes reported by transgenes and Genevestigator. Plant Mol Biol 61:451–467. doi: 10.1007/s11103-006-0021-z 16830179
39. Kaewthai N, Gendre D, Eklof JM, Ibatullin FM, Ezcurra I, Bhalerao RP, Brumer H (2013). Group III-A XTH Genes of Arabidopsis Encode Predominant Xyloglucan Endohydrolases That Are Dispensable for Normal Growth. Plant Physiol 161:440–454. doi: 10.1104/pp.112.207308 23104861
40. Okamoto S, Tomita E, Nishitani K (1997). Expression pattern of endoxyloglucan transferase (EXGT-A1) in Arabidopsis thaliana, and its implications for cell wall construction. Plant Physiol 114:23–23.
41. Parizot B, De Rybel B, Beeckman T (2010). VisuaLRTC: a new view on lateral root initiation by combining specific transcriptome data sets. Plant physiology 153:34–40. doi: 10.1104/pp.109.148676 20219832
42. Ditengou FA, Tealea WD, Kochersperger P, Flittner KA, Kneuper I, van der Graaff E, Nziengui H, Pinosa F, Li XG., Nitschke R, Laux T, Palme K (2008). Mechanical induction of lateral root initiation in Arabidopsis thaliana. P Natl Acad Sci USA 105:18818–18823.
43. Malamy JE, Ryan KS (2001). Environmental regulation of lateral root initiation in Arabidopsis. Plant Physiol 127:899–909. 11706172
44. Wightman F, Thimann KV (1976). Hormonal-Regulation of Lateral Root Initiation in Pisum-Sativum. Plant Physiol 57:52–52.
45. Voss U, Wilson MH, Kenobi K, Gould PD, Robertson FC, Peer WA, Lucas M, Swarup K, Casimiro I, Holman TJ, Wells DM, Péret BJ, Goh T, Fukaki H, Charlie Hodgman T., Laplaze L, Halliday KJ, Ljung K, Murphy AS, Hall AJ, Webb AR, Bennett MJ (2015). The circadian clock rephases during lateral root organ initiation in Arabidopsis thaliana. Nat Commun 6.
46. Perrine-Walker FM, Jublanc E (2014). The localization of auxin transporters PIN3 and LAX3 during lateral root development in Arabidopsis thaliana. Biol Plantarum 58:778–782.
47. Porco S, Larrieu A, Du YJ, Gaudinier A, Goh T, Swarup K, Swarup R, Kuempers B, Bishopp A, Lavenus J, Casimiro I, Hill K, Benkova E, Fukaki H, Brady SM, Scheres B, Péret B, Bennett MJ (2016). Lateral root emergence in Arabidopsis is dependent on transcription factor LBD29 regulation of auxin influx carrier LAX3. Development 143:3340–3349. doi: 10.1242/dev.136283 27578783
48. Lavenus J, Goh T, Guyomarc’h S, Hill K, Lucas M, Voss U, Kenobi K, Wilson MH, Farcot E, Hagen G, Guilfoyle TJ, Fukaki H, Laplaze L, Bennett MJ (2015). Inference of the Arabidopsis Lateral Root Gene Regulatory Network Suggests a Bifurcation Mechanism That Defines Primordia Flanking and Central Zones. Plant Cell 27:1368–1388. doi: 10.1105/tpc.114.132993 25944102
49. Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010). Distinct signaling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant Cell Environ 33:1486–1501. doi: 10.1111/j.1365-3040.2010.02158.x 20444219
50. Okushima Y, Fukaki H, Theologis A, Tasaka M (2005a). Analysis of ARF7- and ARF19-regulated genes in Arabidopsis lateral root formation. Plant and Cell Physiology 46:S197–S197.
51. Ito J, Fukaki H, Onoda M, Li L, Li CY, Tasaka M, Furutani M (2016). Auxin-dependent compositional change in Mediator in ARF7-and ARF19-mediated transcription. P Natl Acad Sci USA 113:6562–6567.
52. Okushima Y, Fukaki H, Onoda M, Theologis A, Tasaka M (2007). ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell 19:118–130. doi: 10.1105/tpc.106.047761 17259263
53. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Alison Smith, Yu G, Theologis A (2005b). Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: Unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463.
54. Xu PP, Chen HY, Ying L, Cai WM (2016). AtDOF5.4/OBP4, a DOF Transcription Factor Gene that Negatively Regulates Cell Cycle Progression and Cell Expansion in Arabidopsis thaliana. Sci Rep-Uk 6.
55. Ramirez-Parra E, Perianez-Rodriguez J, Navarro-Neila S, Gude I, Moreno-Risueno MA, Del Pozo JC (2017). The transcription factor OBP4 controls root growth and promotes callus formation. The New phytologist 213:1787–1801. doi: 10.1111/nph.14315 27859363
56. Clough SJ, and Bent AF (1998). Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x 10069079
57. Xu PP, Cai WM (2017). Functional characterization of the BnNCED3 gene in Brassica napus. Plant Sci 256:16–24. doi: 10.1016/j.plantsci.2016.11.012 28167029
58. Zeng Y, Raimondi N, Kermode AR (2003). Role of an ABI3 homologue in dormancy maintenance of yellow-cedar seeds and in the activation of storage protein and Em gene promoters. Plant molecular biology 51:39–49. doi: 10.1023/a:1020762304937 12602889
59. Murashige T, Skoog F (1962). A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol Plantarum 15:473–497.
60. Vissenberg K., & Fry S. C. (2000). In vivo colocalization of xyloglucan endotransglycosylase activity and its donor substrate in the elongation zone of arabidopsis roots. Plant Cell, 12(7), 1229–1237. doi: 10.1105/tpc.12.7.1229 10899986
61. Fry SC, Smith RC, Renwick KF, Martin DJ, Hodge SK, Matthews KJ (1992) Xyloglucan endotransglycosylase, a new wall-loosening enzyme activity from plants. Biochem J 282 (3):821–828.
62. Cavalier D. M., Olivier L., Lutz N., Kazuchika Y., Antje R., & Glenn F., et al. (2008). Disrupting two Arabidopsis thaliana xylosyltransferase genes results in plants deficient in xyloglucan, a major primary cell wall component. Plant Cell, 20(6), 1519–1537. doi: 10.1105/tpc.108.059873 18544630
63. Rocha J., Félix Cicéron, Sanctis D. D., Lelimousin M., & Breton C. (2016). Structure of Arabidopsis thaliana fut1 reveals a variant of the gt-b class fold and provides insight into xyloglucan fucosylation. The Plant Cell, 28 (10), 2352. doi: 10.1105/tpc.16.00519 27637560
64. Malamy JE, Benfey PN (1997a). Lateral root formation in Arabidopsis thaliana. Plant Physiol 114:277–277.
65. Malamy JE, Benfey PN (1997b). Organization and cell differentiation in lateral roots of Arabidopsis thaliana. Development 124:33–44.
66. Hall BG (2013). Building Phylogenetic Trees from Molecular Data with MEGA. Molecular biology and evolution 30:1229–1235. doi: 10.1093/molbev/mst012 23486614
Štítky
Genetika Reprodukční medicínaČlánek vyšel v časopise
PLOS Genetics
2019 Číslo 10
- S prof. Jitkou Abrahámovou o genetice v onkologii jakožto klíči k prevenci i cílené léčbě
- Primární hyperoxalurie – aktuální možnosti diagnostiky a léčby
- Souvislost haplotypu M2 genu pro annexin A5 s opakovanými reprodukčními ztrátami
- Doporučení pro diagnostiku a léčbu akutních jaterních porfyrií
- Intrauterinní inseminace a její úspěšnost
Nejčtenější v tomto čísle
- Spatiotemporal cytoskeleton organizations determine morphogenesis of multicellular trichomes in tomato
- Loss of thymidine kinase 1 inhibits lung cancer growth and metastatic attributes by reducing GDF15 expression
- TSEN54 missense variant in Standard Schnauzers with leukodystrophy
- Viral quasispecies