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Licensed Unlicensed Requires Authentication Published by De Gruyter February 12, 2018

Transcriptome profiling reveals an IAA-regulated response to adventitious root formation in lotus seedling

  • Cheng Libao EMAIL logo , Jiang Runzhi , Yang Jianjun , Xu Xiaoyong , Zeng Haitao and Li Shuyan EMAIL logo
An erratum for this article can be found here: https://doi.org/10.1515/znc-2018-0133

Abstract

Adventitious roots (ARs) of lotus (Nelumbonucifera Gaertn.) play a critical role in water and nutrient uptake. We found that exogenously applied 10-μM indole-3-acetic acid (IAA) promoted the formation of ARs, while 150-μM IAA significantly inhibited the emergence of ARs. However, little is known about these different responses to various concentrations of IAA at the molecular level. This study, therefore, examined the gene expression profiling in four libraries treated with 10- and 150-μM IAA based on the high-throughout tag sequencing technique. Approximately 2.4×107 clean tags were obtained after the removal of low-quality tags from each library respectively, among which about 10% clean tags were unambiguous tag-mapped genes to the reference genes. We found that some genes involved in auxin metabolism showed a similar tendency for expression in the A/CK and C/CK libraries, while three genes were enhanced their expression only in the A/CK libraries. Two transcription factors including B3 domain-containing protein At2g36080-like and trihelix transcription factor were up-regulated for transcriptional level in the A/C libraries. The expressions of six important genes related to AR formation were significantly different in the A/CK and C/CK libraries. In summary, this study provides a comprehensive understanding of gene expression regulated by IAA involved in AR formation in lotus.

Acknowledgments

The authors thank some members of BIG for their cooperation in obtaining the data during the AR formation of the lotus by the RNA-seq technique. The authors also thank Edanz Group Ltd. for their editorial assistance. This work was supported by the modern agriculture of Yangzhou (YZ2017044), the Innovation Project of Jiangsu Province and Yangzhou University (SJCX17_0629) and the Natural Science Foundation of Jiangsu Province, China, Funder ID: 10.13039/501100004608 (BK20151307).

  1. Conflict of interest statement: The authors declare no conflict of interest.

References

1. Shen-Miller J. Sacred lotus, the long-living fruits of China Antique. Seed Sci Res 2002;14:131–43.10.1079/SSR2002112Search in Google Scholar

2. Ming R, VanBuren R, Liu YL, Yang M, Han YP, Li LT. Genome of the long-living sacred lotus (Nelumbo nucifera Gaertn.). Genome Biol 2013;14:R41.10.1186/gb-2013-14-5-r41Search in Google Scholar PubMed PubMed Central

3. Liu RX, Chen SM, Jiang JF, Zhu L, Zheng C, Han S, et al. Proteomic changes in the base of chrysanthemum cuttings during adventitious root formation. BMC Genomics 2013;14:919.10.1186/1471-2164-14-919Search in Google Scholar PubMed PubMed Central

4. Borgi W, Ghedira K, Chouchane N. Antiinflammatory and analgesic activities of zizyphus lotus root barks. Fitoterapia 2007;78:16–9.10.1016/j.fitote.2006.09.010Search in Google Scholar PubMed

5. Renato BR, Hechenleitner AA, Cavalcanti OA. Extraction, structural modification and characterization of lotus roots polysaccharides (Nelumbo nucifera Gaertn.). Lat Am J Pharm 2007;26:706–10.Search in Google Scholar

6. Delarue M, Prinsen E, Onckelen VH, Caboche M, Bellini C. Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. Plant J 1998;14:603–11.10.1046/j.1365-313X.1998.00163.xSearch in Google Scholar PubMed

7. Falasca G, Zaghi D, Possenti M, Altamura MM. Adventitious root formation in Arabidopsis thaliana thin cell layers. Plant Cell Rep 2004;23:17–25.10.1007/s00299-004-0801-3Search in Google Scholar PubMed

8. Li SW, Leng Y, Feng L, Zeng XY. Involvement of abscisic acid in regulation Antioxidative defense systems and IAA-oxidase activity and improving adventitious rooting in mung bean [Vignaradiata (L.)Wilczek] seedlings under cadmium stress. Environ Sci Pollut Res 2014;21:525–37.10.1007/s11356-013-1942-0Search in Google Scholar PubMed

9. Sorin CL, John D, Camus BI, Ljung K, Kowalczyk M, Geiss G, et al. Auxin and light control of adventitious rooting in Arabidopsis Require ARGONAUTE1. Plant Cell 2005;17:1343–59.10.1105/tpc.105.031625Search in Google Scholar PubMed PubMed Central

10. Geiss G, Gutierrez L, Bellini C. Adventitious root formation: new insights and perspectives. Annu Plant Rev 2009;37:127–56.10.1002/9781444310023.ch5Search in Google Scholar

11. Ahkami A, Scholz U, Steuernagel B, Strickert M, Haensch KT, Druege U, et al. Comprehensive transcriptome analysis unravels the existence of crucial genes regulating primary metabolism during adventitious root formation in petunia hybrida. PLoS One 2014;9:e100997.10.1371/journal.pone.0100997Search in Google Scholar PubMed PubMed Central

12. Zhi-Guo E, Ge L, Wang L. Molecular mechanism of adventitious root formation in rice. Plant Growth Regul 2012;68:325–31.10.1007/s10725-012-9721-3Search in Google Scholar

13. Da Costa CT, de Almeida MR, Ruedell CM, Schwambach J, Maraschin FS, Fett-Neto AG. When stress and development go hand in hand: main hormonal controls of adventitious rooting in cuttings. Front Plant Sci 2012;4:133.10.3389/fpls.2013.00133Search in Google Scholar PubMed PubMed Central

14. Abeles FB, Morgan PW, Saltveit Jr ME. Ethylene in plant biology. San Diego: Academic Press, 1992.Search in Google Scholar

15. Mergemann H, Sauter M. Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 2000;124:609–14.10.1104/pp.124.2.609Search in Google Scholar PubMed PubMed Central

16. Rovere D, Fattorini L, Angeli SD, Veloccia A, Falasca G, Altamura MM. Auxin and cytokinin control formation of the quiescent centre in the adventitious root apex of Arabidopsis. Ann Bot 2013;112:1395–407.10.1093/aob/mct215Search in Google Scholar PubMed PubMed Central

17. Fukaki H, Tasaka M. Hormone interactions during lateral root formation. Plant Mol Biol 2009;69:437–49.10.1007/s11103-008-9417-2Search in Google Scholar PubMed

18. Mensuali-Sodi A, Panizza M, Tognoni F. Endogenous ethylene requirement for adventitious root induction and growth in tomato cotyledons and lavandin microcuttings in vitro. Plant Growth Regul 1995;17:205–12.10.1007/BF00024727Search in Google Scholar

19. Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ. Root formation in ethylene-insensitive plants. Plant Physiol 1999;121:53–9.10.1104/pp.121.1.53Search in Google Scholar PubMed PubMed Central

20. Pluss R, Jenny T, Meier H. IAA-induced adventitious root formation in greenwood cuttings of Populustremula and formation of 2-indolone-3-acetylaspartic acid, a new metabolite of exogenously applied indole-3-acetic acid. Physiol Plant 1989;75:89–96.10.1111/j.1399-3054.1989.tb02068.xSearch in Google Scholar

21. Ludwig-Muller J, Vertocnik A, Town CD. Analysis of indole-3-butyric acid induce adventitious root formation on Arabidopsis stem segments. J Exp Bot 2005;56:2095–105.10.1093/jxb/eri208Search in Google Scholar PubMed

22. Nag S, Saha K, Choudhuri MA. Role of auxin and polyamines in adventitious root formation in relation to changes in compounds involved in rooting. J Plant Growth Regul 2001;20:182–94.10.1007/s003440010016Search in Google Scholar

23. Rout GR. Effect of auxins on adventitious root development from single node cuttings of Camellia sinensis (L.) Kuntze and associated biochemical changes. Plant Growth Regul 2006;48:111–7.10.1007/s10725-005-5665-1Search in Google Scholar

24. Strader LC, Chen GL, Bartel B. Ethylene directs auxin to control root cell expansion. Plant J 2010;64:874–84.10.1111/j.1365-313X.2010.04373.xSearch in Google Scholar PubMed PubMed Central

25. Kohli A, Sreenivasulu N, Lakshmanan P, Kumar PP. The phytohormone crosstalk paradigm takes center stage in understanding how plants respond to abiotic stresses. Plant Cell Rep 2013;32:945–57.10.1007/s00299-013-1461-ySearch in Google Scholar PubMed

26. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK. Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 2010;61:3–15.10.1111/j.1365-313X.2009.04027.xSearch in Google Scholar PubMed

27. Visser E, Cohen JD, Barendse G, Blom C, Voesenek L. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustrissm. Plant Physiol 1996;112:1687–92.10.1104/pp.112.4.1687Search in Google Scholar PubMed PubMed Central

28. Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 2007;19:2169–85.10.1105/tpc.107.052068Search in Google Scholar PubMed PubMed Central

29. Sieberer T, Leyser O. Plant science. Auxin transport, but in which direction? Science 2006;312:858–60.10.1126/science.1127659Search in Google Scholar PubMed

30. Marchant A, Bhalerao R, Casimiro I, Eklöf J, Casero PJ, Bennett M, et al. AUX1 promotes lateral root formation by facilitating indole-3-acetic acid distribution between sink and source tissues in the Arabidopsis seedling. Plant Cell 2002;14:589–97.10.1105/tpc.010354Search in Google Scholar PubMed PubMed Central

31. Sauer M, Balla J, Luschnig C, Wisniewska J, Reinöhl V, Friml J, et al. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 2006;20:2902–11.10.1101/gad.390806Search in Google Scholar PubMed PubMed Central

32. Xu M, Zhu L, Shou HX, Wu P. A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in Rice. Plant Cell Physiol 2005;46:1674–81.10.1093/pcp/pci183Search in Google Scholar PubMed

33. Liu HJ, Wang SF, Yu XB, Yu J, He XW, Zhang SL, et al. ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 2005;43:47–56.10.1111/j.1365-313X.2005.02434.xSearch in Google Scholar PubMed

34. Hodge A, Berta G, Doussan C, Merchan F, Crespi M. Plant root growth, architecture and function. Plant Soil 2009;321:153–87.10.1007/s11104-009-9929-9Search in Google Scholar

35. Rasmussen A, Hosseini SA, Hajirezaei MR, Druege U, Geelen D. Adventitious rooting declines with the vegetative to reproductive switch and involves a changed auxin homeostasis. J Exp Bot 2015;66:1437–52.10.1093/jxb/eru499Search in Google Scholar PubMed PubMed Central

36. Teale WD, Paponov IA, Palme K. Auxin in action: signaling, transport and the control of plant growth and development. Nat Rev Mol Cell Biol 2006;7:847–59.10.1038/nrm2020Search in Google Scholar PubMed

37. Vanneste S, Friml J. Auxin: a trigger for change in plant development. Cell 2009;136:1005–16.10.1016/j.cell.2009.03.001Search in Google Scholar PubMed

38. Christopher J, Christopher M, Jennings R, Jones S, Fletcher S, Borrell A, et al. QTL for root angle and number in a population developed from bread wheats (Triticumaestivum) with contrasting adaptation to water-limited environments. Theor Appl Genet 2013;126:1563–74.10.1007/s00122-013-2074-0Search in Google Scholar PubMed

39. Rovere FD, Fattorini L, Angeli SD, Veloccia A, Duca SD, Cai G, et al. Arabidopsis SHR and SCR transcription factors and AUX1 auxin influx carrier control the switch between adventitious rooting and xylogenesis in planta and in in vitro cultured thin cell layers. Ann Bot 2015;115:617–28.10.1093/aob/mcu258Search in Google Scholar PubMed PubMed Central

40. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, et al. Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis. Nature 2003;426:147–53.10.1038/nature02085Search in Google Scholar PubMed

41. Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, et al. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 2005;17:1090–104.10.1105/tpc.104.029272Search in Google Scholar PubMed PubMed Central

42. Stefancic M, Stampar F, Ostereg G. Influence of IAA and IBA on root development and quality of Prunus ‘GiSeIA5’ leafy cuttings. Hort Sci 2005;40:2052–5.Search in Google Scholar

43. Corrêa DR, Fett-Neto AG. Effects of temperature on adventitious root development in microcuttings of Eucalyptus saligna Smith and Eucalyptus globulus Labill. J Therm Biol 2004;29:315–24.10.1016/j.jtherbio.2004.05.006Search in Google Scholar

44. Zhang XL, Qi MF, Xu T, Lu XJ, Li TL. Proteomics profiling of ethylene-induced tomato flower pedicel abscission. J Proteomics 2015;121:67–87.10.1016/j.jprot.2015.03.023Search in Google Scholar PubMed

45. Hamann A. Adventitious root formation in cuttings of loblolly pine (Pinustaeda L.): developmental sequence and effects of maturation. Trees-StructFunct 1998;12:175–80.10.1007/PL00009707Search in Google Scholar

46. Leyser O. Auxin signalling: the beginning, the middle and the end. Curr Opin Plant Biol 2001;4:382–6.10.1016/S1369-5266(00)00189-8Search in Google Scholar PubMed

47. Druege U, Franken P, Lischewski SA, Ahkami AH, Zerche S, Hause B, et al. Transcriptomic analysis reveals ethylene as stimulator and auxin as regulator of adventitious root formation in petunia cuttings. Front Plant Sci 2014;5:494.10.3389/fpls.2014.00494Search in Google Scholar PubMed PubMed Central

48. Lanteri ML, Laxalt AM, Lamattina L. Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 2008;147:188–98.10.1104/pp.107.111815Search in Google Scholar PubMed PubMed Central

49. Li SW, Xue L, Xu S, Feng H, An L. Mediators, genes and signaling in adventitious rooting. Bot Rev 2009;75:230–47.10.1007/s12229-009-9029-9Search in Google Scholar

50. Savitsky PA, Gazaryan IG, Tishkov VI, Lagrimini LM, Ruzgas TR, Gorton L. Oxidation of indole-3-acetic acid by dioxygencatalysed by plant peroxidases: specificity for the enzyme structure. Biochem J 1999;340:579–83.10.1042/bj3400579Search in Google Scholar PubMed

51. Chou CH, Huang YC, Liu ZH. Peroxidase genes differentially respond to auxin during the formation of adventitious roots in soybean hypocotyl. Plant Growth Regul 2010;60:151–61.10.1007/s10725-009-9431-7Search in Google Scholar

52. Cheng LB, Jiang RZ, Yang ML, Li LJ, Li SY. A comparative proteomic analysis for adventitious root formation in lotus root (Nelumbo nucifera Gaertn.). Z Naturforsch C 2016;72:181–96.Search in Google Scholar

53. Kim KJ, Kim KS. Changes of endogenous growth substances during bulb maturation after flowering in Lilium oriental hybrid ‘Casa Blanca’. Acta Hort 2005;673:661–7.10.17660/ActaHortic.2005.673.91Search in Google Scholar

54. Cheng LB, Li SY, Yin JJ, Li LJ, Chen XH. Genome-wide analysis of differentially expressed genes relevant to rhizome formation in lotus root (Nelumbo nucifera. Gaertn). PLoS One 2013;8:e67116.10.1371/journal.pone.0067116Search in Google Scholar PubMed PubMed Central

55. Grichko VP, Glick BR. Ethylene and flooding stress in plants. Plant Physiol Biochem 2001;39:1–9.10.1016/S0981-9428(00)01213-4Search in Google Scholar

56. Cheng LB, Li SY, Xu XY, Hussain J, Yin JJ, Zhang Y, et al. Identification of differentially expressed genes relevant to corm formation in Sagittaria trifolia. PLoS One 2013;8:e54573.10.1371/journal.pone.0054573Search in Google Scholar PubMed PubMed Central

57. Negi S, Ivanchenko MG, Muday GK. Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. Plant J 2008;55:175–87.10.1111/j.1365-313X.2008.03495.xSearch in Google Scholar PubMed PubMed Central

58. Jiang L, Yang SL, Xie LF, Puah CS, Zhang XQ, Yang WC, et al. VANGUARD1 encodes a pectin methyl-esterase that enhances pollen tube growth in the Arabidopsis style and transmitting tract. Plant Cell 2005;17:584–96.10.1105/tpc.104.027631Search in Google Scholar PubMed PubMed Central

59. Siedlecka A, Wiklund S, Péronne MA, Micheli F, Lesniewska J, Sethson I, et al. Pectin methylesterase inhibits intrusive and symplastic cell growth in developing wood cells of Populus. Plant Physiol 2008;146:554–63.10.1104/pp.107.111963Search in Google Scholar PubMed PubMed Central

60. Lacoux J, Gutierrez L, Dantin F, Beaudoin B, Roger D, Laine E. Antisense transgenesis of tobacco with a flax pectin methylesterase affects pollen ornamentation. Protoplasma 2003;22:205–9.10.1007/s00709-003-0019-1Search in Google Scholar PubMed

61. Wu HC, Hsu SF, Luo DL, Chen SJ, Huang WD, Lur HS, et al. Recovery of heat shock-triggered released apoplastic Ca2+ accompanied by pectin methylesterase activity is required for thermotolerance in soybean seedlings. J Exp Bot 2010;61:2843–52.10.1093/jxb/erq121Search in Google Scholar PubMed PubMed Central

62. Wen F, Zhu Y, Hawes MC. Effect of pectin methylesterase gene expression on pea root development. Plant Cell 1999;11:1129–40.10.1105/tpc.11.6.1129Search in Google Scholar PubMed PubMed Central

63. Guenin S, Mareck A, Rayon C, Lamour R, Ndong YA, Domon JM, et al. Identification of pectin methylesterase 3 as a basicpectin methylesterase isoform involved in adventitious rooting in Arabidopsis thaliana. New Phytol 2011;192:114–26.10.1111/j.1469-8137.2011.03797.xSearch in Google Scholar PubMed

64. Thyndman SE, Hasegawa PM, Bressan R. The role of sucrose and nitrogen in adventitious root formation on cultured rose shoots. Plant Cell Tiss Org 1982;1:229–38.10.1007/BF02318919Search in Google Scholar

65. Calamar A, De Klerk GJ. Effect of sucrose on adventitious root regeneration in apple. Plant Cell Tiss Org 2002;70:207–12.10.1023/A:1016356123367Search in Google Scholar

66. Tang Z, Du W, Du XL, Ban YY, Cheng JL. iTRAQ protein profiling of adventitious root formation in mulberry hardwood cuttings. J Plant Growth Regul 2016;35:618–31.10.1007/s00344-015-9567-9Search in Google Scholar

67. Wang YJ, Deng DX, Zhang R, Wang SX, Bian YL, Yin ZT. Systematic analysis of plant-specific B3 domain-containing proteins based on the genome resources of 11 sequenced species. Mol Biol Rep 2012;39:6267–82.10.1007/s11033-012-1448-8Search in Google Scholar PubMed

68. Wang YJ, Deng DX, Shi YT, Miao N, Bian YL, Yin ZT. Diversification, phylogeny and evolution of auxin response factor (ARF) family: insights gained from analyzing maize ARF genes. Mol Biol Rep 2012;39:2401–15.10.1007/s11033-011-0991-zSearch in Google Scholar PubMed

69. Wilmoth JC, Wang SC, Tiwari SB, Joshi AD, Hagen G, Guilfoyle TJ, et al. NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. Plant J 2005;43:118–30.10.1111/j.1365-313X.2005.02432.xSearch in Google Scholar PubMed

70. Chiappetta A, Gagliardi C, Bruno L, Bitonti MB. In vitro culture conditions and OeARF and OeH3 expressions modulate adventitious root formation from oleaster (Oleaeuropaea L. subsp. europaea var. sylvestris) cuttings. SciWorldJ 2014;24:1–9.Search in Google Scholar


Supplemental Material:

The online version of this article offers supplementary material (https://doi.org/10.1515/znc-2017-0188).


Received: 2017-10-11
Revised: 2017-12-05
Accepted: 2018-01-20
Published Online: 2018-02-12
Published in Print: 2018-04-25

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