Transcriptome Characterization of Gene Profiling During Early Stage of Nitric Oxide-Induced Adventitious Rooting in Mung Bean Seedlings

  • Shi-Weng LiEmail author
  • Yan Leng
  • Rui-Fang Shi


Nitric oxide (NO) functions as a signaling molecule modulating diverse developmental and physiological processes in plants. NO was recently shown to strongly induce the formation of adventitious roots in plants. A transcriptome analysis was performed using RNA-Seq and qRT-PCR technologies to obtain further insights into the gene expression profile underlying NO-induced adventitious rooting. Sodium nitroprusside (SNP), a widely used NO donor, significantly up-regulated the GO terms and pathways oxidoreductase activity, wounding response, water deprivation response, microtubule-based process, cell cycle, cell wall synthesis, photosynthesis, hydrolase activity at the root induction stage, response to stress, cell wall loosening and biogenesis, ethylene signaling at the root initiation stage. In total, 2582 and 2588 differentially expressed genes (DEGs, fold change ≥ 2) were selected in plants receiving the 6- and 24-h SNP treatments, respectively. The analysis of the most highly differentially expressed genes (RPKM ≥ 10 and fold change ≥ 2) shows that NO significantly regulated the expression of genes involved in nitrogen compound response, stress response, oxidative stress response, cell wall modification, signal transduction, protein processing, secondary metabolism, metabolic processes, and transcription factors (TFs), as well as plant hormone signaling. Notably, the expression of a large number of genes encoding peroxidase (POD) isoforms was significantly differentially regulated by SNP. Furthermore, qRT-PCR results indicated that NO significantly up-regulated the expression of several genes with known functions in pathways such as auxin signaling and stress response, as well as TF genes, at the root induction and initiation stages. The evidence obtained implies that NO up-regulated the expression of genes that are involved in the key cellular processes leading to the root formation.


Vigna radiata (L.) R. Wilczek Adventitious roots Nitric oxide (NO) Transcriptome Gene expression 





1-Aminocyclopropane-1-carboxylic acid


1-Aminocyclopropane-1-carboxylic acid oxidase


1-Aminocyclopropane-1-carboxylic acid synthase


Arabidopsis histidine kinase


Alternative oxidase


Apetala2/Ethylene response factor


Ascorbate peroxidase


Auxin response factor






Brassinosteroid insensitive 1


Brassinosteroid insensitive 1-associated receptor kinase 1-like




Basic leucine zipper


Casparian strip membrane protein-like




Cyclic guanosine monophosphate


Chalcone synthase


Differentially expressed genes


DHA reductase


Dof zinc finger protein


EIN3-binding F-box protein 1-like


Ethylene-insensitive protein


Ethylene-overproduction protein


Gibberellin 2/3-beta-dioxygenase


Gibberellins 2/20 oxidase


GATA transcription factor


Glycoside hydrolase


Gretchen hagen 3


Gene ontology


Glutathione peroxidase


Glutathione reductase


Glutathione S-transferase


Homeobox-leucine zipper protein


Heat shock proteins


Heat shock transcription factors


Indole-3-butyric acid


Automatic annotation server


Kyoto encyclopedia of genes and genomes


Clusters of orthologous groups for eukaryotic complete genomes


Lateral organ boundaries-domain


Late embryogenesis abundant


Lateral organ boundaries


Leucine-rich repeat


Mitogen-activated protein kinase


Monodehydroascorbate reductase




No apical meristem


Nitric oxide


NCBI non-redundant protein








Quinone oxidoreductase-like protein


Real-time quantitative polymerase chain reaction


Root apical meristem




Reactive oxygen species


Reads per kb per million reads




Sodium nitroprusside


Superoxide dismutase


Transcription factors


WRKYGQK domain protein


Zinc finger protein



This work was financially supported by the National Natural Science Foundation of China (31760110 and 31560121).

Author Contributions

LSW conceived and designed the experimental plan, analyzed, and interpreted the sequence data, and drafted the manuscript. LY and SRF performed the experiments and analyzed the sequence data. All authors read and approved the final manuscript.

Compliance with Ethical Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

344_2019_9993_MOESM1_ESM.pdf (107 kb)
Supplementary material 1 (PDF 107 kb)
344_2019_9993_MOESM2_ESM.xlsx (50 kb)
Supplementary material 2 (XLSX 49 kb). Table S2: Top list of the differentially regulated GOs
344_2019_9993_MOESM3_ESM.xlsx (16 kb)
Supplementary material 3 (XLSX 15 kb). Table S3: Top list of the differentially regulated KOs
344_2019_9993_MOESM4_ESM.xlsx (56 kb)
Supplementary material 4 (XLSX 56 kb). Table S4: List of DEGs in the sample pair NO6 vs. Wat6
344_2019_9993_MOESM5_ESM.xlsx (54 kb)
Supplementary material 5 (XLSX 54 kb). Table S5: List of DEGs in the sample pair NO24 vs. Wat24
344_2019_9993_MOESM6_ESM.xlsx (24 kb)
Supplementary material 6 (XLSX 24 kb). Table S6: List of differentially expressed genes of transcription factors
344_2019_9993_MOESM7_ESM.xlsx (13 kb)
Supplementary material 7 (XLSX 12 kb). Table S7: List of differentially expressed genes associated with plant hormone signaling
344_2019_9993_MOESM8_ESM.pdf (131 kb)
Supplementary material 8 (PDF 130 kb). Table S8: Comparation of DEGs that respond to SNP and IBA


  1. Ahlfors R, Brosché M, Kollist H, Kangasj J (2009) Nitric oxide modulates ozone-induced cell death, hormone biosynthesis and gene expression in Arabidopsis thaliana. Plant J 58:1–12CrossRefPubMedGoogle Scholar
  2. Alonso JM, Hirayama T, Roman G, Nourizadeh S, Ecker JR (1999) EIN2, a bifunctional transducer of ethylene and stress responses in Arabidopsis. Science 284:2148–2152CrossRefPubMedGoogle Scholar
  3. Arce D, Spetale F, Krsticevic F, Cacchiarelli P, Las Rivas J, Ponce S, Pratta G, Tapia E (2018) Regulatory motifs found in the small heat shock protein (sHSP) gene family in tomato. BMC Genomics 19(Suppl 8):860CrossRefPubMedPubMedCentralGoogle Scholar
  4. Audic S, Claverie JM (1997) The significance of digital gene expression profiles. Genome Res 7:986–995CrossRefPubMedGoogle Scholar
  5. Bai X, Todd CD, Desikan R, Yang Y, Hu X (2012) N-3-oxo-decanoyl-l-homoserine-lactone activates auxin-induced adventitious root formation via hydrogen peroxide- and nitric oxide-dependent cyclic GMP signaling in mung bean. Plant Physiol 158:725–736CrossRefPubMedGoogle Scholar
  6. Bannenberg G, Martinez M, Hamberg M, Castresana C (2009) Diversity of the enzymatic activity in the lipoxygenase gene family of Arabidopsis thaliana. Lipids 44:85–95CrossRefPubMedGoogle Scholar
  7. Batish DR, Kaur S, Singh HP, Kohli RK (2008) Interaction between nitric oxide and superoxide anion regulates adventitious root formation in mung bean (Vigna radiata) hypocotyls. Nitric Oxide 19:S43–S72CrossRefGoogle Scholar
  8. Benjamin IJ, McMillan DR (1998) Stress (heat shock) proteins: molecular chaperones in cardiovascular biology and disease. Circ Res 832:117–132CrossRefGoogle Scholar
  9. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc 57:289–300Google Scholar
  10. Besson-Bard A, Astiera J, Rasula S, Wawera I, Dubreuil-Maurizia C, Jeandrozb S, Wendehennea D (2009) Current view of nitric oxide-responsive genes in plants. Plant Sci 177:302–309CrossRefGoogle Scholar
  11. Borges JC, Ramos CH (2005) Protein folding assisted by chaperones. Protein Pept Lett 12:257–261CrossRefPubMedGoogle Scholar
  12. Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, Madden TL (2009) BLAST + : architecture and applications. BMC Bioinform 10:421CrossRefGoogle Scholar
  13. Cao D, Cheng H, Wu W, Soo HM, Peng J (2006) Gibberellin mobilizes distinct DELLA-dependent transcriptomes to regulate seed germination and floral development in Arabidopsis. Plant Physiol 142:509–525CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chamizo-Ampudia A, Sanz-Luque E, Llamas A, Galvan A, Fernandez E (2017) Nitrate reductase regulates plant nitric oxide homeostasis. Trends Plant Sci 22:163–174CrossRefPubMedGoogle Scholar
  15. Chen YH, Chao YY, Hsu Y, Hong CY, Kao C (2012) Heme oxygenase is involved in nitric oxide- and auxin-induced lateral root formation in rice. Plant Cell Rep 31:1085–1091CrossRefPubMedGoogle Scholar
  16. Conesa A, Gotz S, García-Gómez JM, Terol J, Talón M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle Scholar
  17. Correa-Aragunde Noelia Foresi, Lamattina Lorenzo (2015) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J Exp Bot 66:2913–2921CrossRefPubMedGoogle Scholar
  18. Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905CrossRefPubMedGoogle Scholar
  19. Correa-Aragunde N, Graziano M, Chevalier C, Lamattina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588CrossRefPubMedGoogle Scholar
  20. Devaiah BN, Karthikeyan AS, Raghothama KG (2007) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol 143:1789–1801CrossRefPubMedPubMedCentralGoogle Scholar
  21. Dixon DP, Lapthorn A, Edwards R (2002) Plant glutathione transferases. Genome Biol 3:300041–3000410CrossRefGoogle Scholar
  22. Ederli L, Reale L, Madeo L, Ferranti F, Gehring C, Fornaciari M, Romano B, Pasqualini S (2009) NO release by nitric oxide donors in vitro and in planta. Plant Physiol Bioch 47:42–48CrossRefGoogle Scholar
  23. Eudes A, Pollet B, Sibout R, Do CT, Seguin A, Lapierre C, Jouanin L (2006) Evidence for a role of CAD1 in lignification of elongating stems of Arabidopsis thaliana. Planta 225:23–39CrossRefPubMedGoogle Scholar
  24. Fabijan D, Yeung E, Mukherjee I, Reid DM (1981) Adventitious rooting in hypocotyls of sunflower (Helianthus annuus) seedlings I Correlative influences and developmental sequence. Physiol Plant 53:578–588CrossRefGoogle Scholar
  25. Fernández-Marcos M, Sanz L, Lewis, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical meristem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci USA 108(45):18506–108511CrossRefPubMedGoogle Scholar
  26. Flores T, Todd CD, Tovar-Mendez A, Dhanoa PK, Correa-Aragunde N, Hoyos ME, Brownfield DM, Mullen RT, Lamattina L, Polacco JC (2008) Arginase-negative mutants of Arabidopsis exhibit increased nitric oxide signaling in root development. Plant Physiol 147:1936–1946CrossRefPubMedPubMedCentralGoogle Scholar
  27. Floryszak-Wieczorek J, Milczarek G, Arasimowicz M, Ciszewski A (2006) Do nitric oxide donors mimic endogenous NO-related response in plants? Planta 224:1363–1372CrossRefPubMedGoogle Scholar
  28. Fotopoulos V, Antoniou C, Filippou P, Mylona P, Fasoula D, Ioannides I (2014) Application of sodium nitroprusside results in distinct antioxidant gene expression patterns in leaves of mature and senescing Medicago truncatula plants. Protoplasma 251:973–978CrossRefPubMedGoogle Scholar
  29. Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652CrossRefPubMedPubMedCentralGoogle Scholar
  30. Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, Kowalczyk M, Păcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527CrossRefPubMedPubMedCentralGoogle Scholar
  31. Harshavardhan VT, Van Son L, Seiler C, Junker A, Weigelt-Fischer K, Klukas C, Altmann T, Sreenivasulu N, Baumlein H, Kuhlmann M (2014) AtRD22 and AtUSPL1, members of the plant-specific BURP domain family involved in Arabidopsis thaliana drought tolerance. PLoS ONE 9:e110065CrossRefPubMedPubMedCentralGoogle Scholar
  32. Hatzilazarou SP, Syros TD, Yupsanis TA, Bosabalidis AM, Economou AS (2006) Peroxidases, lignin and anatomy during in vitro and ex vitro rooting of gardenia (Gardenia jasminoides Ellis) microshoots. J Plant Physiol 163:827–836CrossRefPubMedGoogle Scholar
  33. Hirota A, Kato T, Fukaki H, Aida M, Tasaka M (2007) The auxin-regulated AP2/EREBP gene PUCHI is required for morphogenesis in the early lateral root primordium of Arabidopsis. Plant Cell 19:2156–2168CrossRefPubMedPubMedCentralGoogle Scholar
  34. Holmes P, Djordjevic MA, Imin N (2010) Global gene expression analysis of in vitro root formation in Medicago truncatula. Fun Plant Biol 37:1117–1131CrossRefGoogle Scholar
  35. Hu X, Yang J, Li C (2015) Transcriptomic response to nitric oxide treatment in Larix olgensis Henry. Int J Mol Sci 16:28582–28597CrossRefPubMedPubMedCentralGoogle Scholar
  36. Huang AX, She XP, Huang C, Song TS (2007) The dynamic distribution of NO and NADPH-diaphorase activity during IBA-induced adventitious root formation. Physiol Plant 130:240–249CrossRefGoogle Scholar
  37. Huang AX, She XP, Cao BH, Ren Y (2011) Distribution of hydrogen peroxide during adventitious roots initiation and development in mung bean hypocotyls cuttings. Plant Growth Regul 4:109–118CrossRefGoogle Scholar
  38. Ishihara A, Kawata N, Matsukawa T, Iwamura H (2000) Induction of N-hydroxycinnamoyltyramine synthesis and tyramine N-hydroxycinnamoyltransferase (THT) activity by wounding in maize leaves. Biosci Biotechnol Biochem 64:1025–1031CrossRefPubMedGoogle Scholar
  39. Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real–time PCR. BMC Mol Biol 9:59CrossRefPubMedPubMedCentralGoogle Scholar
  40. Jiang HW, Liu MJ, Chen IC, Huang CH, Chao LY, Hsieh HL (2010) A glutathione S-transferase regulated by light and hormones participates in the modulation of Arabidopsis seedling development. Plant Physiol 154:1646–1658CrossRefPubMedPubMedCentralGoogle Scholar
  41. Jin C, Du S, Zhang Y, Lin X, Tang C (2009) Differential regulatory role of nitric oxide in mediating nitrate reductase activity in roots of tomato (Solanum lycocarpum). Ann Bot 104:9–17CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kolbert Z, Bartha B, Erdei LJ (2008) Exogenous auxin-induced NO synthesis is nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975CrossRefPubMedGoogle Scholar
  43. Konishi M, Sugiyama M (2003) Genetic analysis of adventitious root formation with a novel series of temperature–sensitive mutants of Arabidopsis thaliana. Development 130:5637–5647CrossRefPubMedGoogle Scholar
  44. Langmead B, Salzberg SL (2012) Fast gapped–read alignment with bowtie 2. Nat Methods 9:357–359CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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. Plant Cell 25:3329–3346CrossRefPubMedPubMedCentralGoogle Scholar
  46. Li J, Chory J (1997) A putative leucine-rich repeat receptor kinase involved in brassinosteroid signal transduction. Cell 90:929–938CrossRefPubMedGoogle Scholar
  47. Li SW, Xue L (2010) The interaction between H2O2 and NO, Ca2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. Vitro Cell Dev Biol-Plant 46:142–148CrossRefGoogle Scholar
  48. Li SW, Xue L, Xu S, Feng H, An L (2009) Hydrogen peroxide acts as a signal molecule in the adventitious root formation of mung bean seedlings. Environ Exp Bot 65:63–71CrossRefGoogle Scholar
  49. Li KL, Bai X, Li Y, Cai H, Ji W, Tang LL, Wen YD, Zhu YM (2011) GsGASA1 mediated root growth inhibition in response to chronic cold stress is marked by the accumulation of DELLAs. J Plant Physiol 168:2153–2160CrossRefPubMedGoogle Scholar
  50. Li YH, Zou MH, Feng BH, Huang X, Zhang Z, Sun GM (2012) Molecular cloning and characterization of the genes encoding an auxin efflux carrier and the auxin influx carriers associated with the adventitious root formation in mango (Mangifera indica L) cotyledon segments. Plant Physiol Bioch 55:33–42CrossRefGoogle Scholar
  51. Li SW, Shi RF, Leng Y (2015) De novo characterization of the mung bean transcriptome and transcriptomic analysis of adventitious rooting in seedlings using RNA-Seq. PLoS ONE 10:e0132969CrossRefPubMedPubMedCentralGoogle Scholar
  52. Li SW, Shi RF, Leng Y, Zhou Y (2016) Transcriptomic analysis reveals the gene expression profile that specifically responds to IBA during adventitious rooting in mung bean seedlings. BMC Genomics 17:43CrossRefPubMedPubMedCentralGoogle Scholar
  53. Lindermayr C, Saalbach G, Durner J (2005) Proteomic identification of S-nitrosylated proteins in Arabidopsis. Plant Physiol 137:921–930CrossRefPubMedPubMedCentralGoogle Scholar
  54. Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB–domain protein required for adventitious root formation in rice. Plant J 43:47–56CrossRefPubMedGoogle Scholar
  55. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real time quantitative PCR and the 2−△△Ct method. Methods 25:402–408CrossRefGoogle Scholar
  56. Mauriat M, Petterle A, Bellini C, Moritz T (2014) Gibberellins inhibit adventitious rooting in hybrid aspen and Arabidopsis by affecting auxin transport. Plant J 78:372–384CrossRefPubMedGoogle Scholar
  57. Méndez-Bravo A, Raya-González J, Herrera-Estrella L, López-Bucio J (2010) Nitric oxide is involved in alkamide-induced lateral root development in Arabidopsis. Plant Cell Physiol 51:1612–1626CrossRefPubMedGoogle Scholar
  58. Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M (2007) KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 35(suppl 2):W182–W185CrossRefPubMedPubMedCentralGoogle Scholar
  59. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628CrossRefPubMedGoogle Scholar
  60. Negi S, Sukumar P, Liu X, Cohen JD, Muday GK (2010) Genetic dissection of the role of ethylene in regulating auxin-dependent lateral and adventitious root formation in tomato. Plant J 61:3–15CrossRefPubMedGoogle Scholar
  61. Neill S, Bright J, Desikan R, Hancock J, Harrison J, Wilson I (2008) Nitric oxide evolution and perception. J Exp Bot 59:25–35CrossRefPubMedGoogle Scholar
  62. Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell 16:1365–1377CrossRefPubMedPubMedCentralGoogle Scholar
  63. Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pagnussat GC, Lanteri ML, Lombardo MC (2004) Nitric oxide mediates the indole acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286CrossRefPubMedPubMedCentralGoogle Scholar
  65. Palmieri MC, Sell S, Huang X, Scherf M, Werner T, Durner J, Lindermayr C (2008) Nitric oxide–responsive genes and promoters in Arabidopsis thaliana: a bioinformatics approach. J Exp Bot 59:177–186CrossRefPubMedGoogle Scholar
  66. Parani M, Rudrabhatla S, Myers R, Weirich H, Smith B, Leaman DW, Goldman SL (2004) Microarray analysis of nitric oxide responsive transcripts in Arabidopsis. Plant Biotech J 2:359–366CrossRefGoogle Scholar
  67. Qi F, Xiang Z, Kou N, Cui W, Xu D, Wang R, Wang R, Zhu D, Shen W (2017) Nitric oxide is involved in methane-induced adventitious root formation in cucumber. Physiol Plant 159:366–377CrossRefPubMedGoogle Scholar
  68. Ranocha P, Denancé N, Vanholme R, Freydier A, Martinez Y, Hoffmann L, Köhler L, Pouzet C, Renou JP, Sundberg B (2010) Walls are thin1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast–localized protein required for secondary wall formation in fibers. Plant J 633:469–483CrossRefGoogle Scholar
  69. Rentel MC, Lecourieux D, Ouaked F, Usher SL, Petersen L, Okamoto H et al (2004) OXI1 kinase is necessary for oxidative burst-mediated signalling in Arabidopsis. Nature 427:858–861CrossRefPubMedGoogle Scholar
  70. Rigal A, Yordanov YS, Perrone I, Karlberg A, Tisserant E, Bellini C, Busov VB, Martin F, Kohler A, Bhalerao R, Legué V (2012) The aintegumenta like1 homeotic transcription factor PtAIL1 controls the formation of adventitious root primordia in poplar. Plant Physiol 160:1996–2006CrossRefPubMedPubMedCentralGoogle Scholar
  71. Roppolo D, Boeckmann B, Pfister A, Boutet E, Rubio MC, Dénervaud-Tendon V, Vermeer JE, Gheyselinck J, Xenarios I, Geldner N (2014) Functional and evolutionary analysis of the casparian strip membrane domain protein family. Plant Physiol 165:1709–1722CrossRefPubMedPubMedCentralGoogle Scholar
  72. Saito S, Hirai N, Matsumoto C, Ohigashi H, Ohta D, Sakata K, Mizutani M (2004) Arabidopsis CYP707As encode (+)-abscisic acid 8′-hydroxylase, a key enzyme in the oxidative catabolism of abscisic acid. Plant Physiol 134:1439–1449CrossRefPubMedPubMedCentralGoogle Scholar
  73. Saxena C, Samantaray S, Rout GR, Das P (2000) Effect of auxins on in vitro rooting of Plumbungo zeylanica: peroxidase activity as a marker for root induction. Biol Plant 43:121–124CrossRefGoogle Scholar
  74. She XP, Huang AX (2004) Change of nitric oxide and NADPH-diaphorase during the generation and the development of adventitious roots in mung bean hypocotyls cuttings. Act Bot Sin 46:1049–1055Google Scholar
  75. Shi JH, Yang ZB (2011) Is ABP1 an auxin receptor yet? Mol Plant 4:635–640CrossRefPubMedPubMedCentralGoogle Scholar
  76. Shi HT, Li RJ, Cai W, Liu W, Fu ZW, Lu YT (2012) In vivo role of nitric oxide in plant response to abiotic and biotic stress. Plant Signal Behav 7:438–440CrossRefGoogle Scholar
  77. Shi H, Ye T, Zhu JK, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. J Exp Bot 65:4119–4131CrossRefPubMedPubMedCentralGoogle Scholar
  78. Sorin C, Negroni L, Balliau T, Corti H, Jacquemot MP, Davanture M, Sandberg G, Zivy M, Bellini C (2006) Proteomic analysis of different mutant genotypes of Arabidopsis led to the identification of 11 proteins correlating with adventitious root development. Plant Physiol 140:349–364CrossRefPubMedPubMedCentralGoogle Scholar
  79. Spartz AK, Ren H, Park MY, Grandt KN, Lee SH, Murphy AS et al (2014) SAUR inhibition of PP2C-D phosphatases activates plasma membrane H+-ATPases to promote cell expansion in Arabidopsis. Plant Cell 26:2129–2142CrossRefPubMedPubMedCentralGoogle Scholar
  80. Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC (2005) Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627CrossRefPubMedPubMedCentralGoogle Scholar
  81. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617CrossRefPubMedGoogle Scholar
  82. Sun H, Li J, Song W, Tao J, Huang S, Chen S et al (2015a) Nitric oxide generated by nitrate reductase increases nitrogen uptake capacity by modulating lateral root formation and inorganic nitrogen uptake rate in rice. J Exp Bot 66:2449–2459CrossRefPubMedPubMedCentralGoogle Scholar
  83. Sun C, Liu L, Yu Y, Liu W, Lu L, Jin C (2015b) Nitric oxide alleviates aluminum–induced oxidative damage through regulating the ascorbate-glutathione cycle in roots of wheat. J Integr Plant Biol 57:550–561CrossRefPubMedGoogle Scholar
  84. Terrile MC, París R, Calderón-Villalobos LIA, Iglesias MJ, Lamattina L, Estelle M (2012) Nitric oxide in fluencies auxin signaling through S–nitrosylation of the Arabidopsis TRANSPORT INHIBITORRESPONSE1 auxin receptor. Plant J 70:492–500CrossRefPubMedPubMedCentralGoogle Scholar
  85. Tewari RK, Hahn Eun-Joo, Paek Kee-Yoeup (2008) Function of nitric oxide and superoxide anion in the adventitious root development and antioxidant defence in Panax ginseng. Plant Cell Rep 27:563–573CrossRefPubMedGoogle Scholar
  86. Thamilarasan SK, Park JI, Jung HJ, Nou IS (2014) Genome-wide analysis of the distribution of AP2/ERF transcription factors reveals duplication and CBFs genes elucidate their potential function in Brassica oleracea. BMC Genomics 15:422CrossRefPubMedPubMedCentralGoogle Scholar
  87. Trupiano D, Yordanov Y, Regan S, Meilan R, Tschaplinski T, Scippa G, Busov V (2013) Identification, characterization of an AP2/ERF transcription factor that promotes adventitious, lateral root formation in Populus. Planta 238:271–282CrossRefPubMedGoogle Scholar
  88. Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136:1005–1016CrossRefPubMedGoogle Scholar
  89. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562CrossRefPubMedGoogle Scholar
  90. Wang KLC, Yoshida H, Lurin C, Ecker JR (2004) Regulation of ethylene gas biosynthesis by the Arabidopsis ETO1 protein. Nature 428:945–950CrossRefPubMedGoogle Scholar
  91. Wang L, Feng Z, Wang X, Wang X, Zhang X (2010) DEGseq: an R package for identifying differentially expressed genes from RNA-Seq data. Bioinformatics 26:136–138CrossRefPubMedGoogle Scholar
  92. Wang R, Liu X, Liang S, Ge Q, Li Y, Shao J, Qi Y, An L, Yu F (2015) Subgroup of MATE transporter genes regulates hypocotyl cell elongation in Arabidopsis. J Exp Bot 66:6327–6343CrossRefPubMedGoogle Scholar
  93. Welander M, Geier T, Smolka A, Ahlman A, Fan J, Zhu LH (2014) Orign, timeing, and gene expression profile of adventitious rooting in Arabicopsis hypocotyls and stems. Am J Bot 101:255–266CrossRefPubMedGoogle Scholar
  94. Wodala B, Ordog A, Horvath F (2010) The cost and risk of using sodium nitroprusside as a NO donor in chlorophyll fluorescence experiments. J Plant Physiol 167:1109–1111CrossRefPubMedGoogle Scholar
  95. Wohlbach DJ, Quirino BF, Sussman MR (2008) Analysis of the Arabidopsis histidine kinase ATHK1 reveals a connection between vegetative osmotic stress sensing and seed maturation. Plant Cell 20:1101–1117CrossRefPubMedPubMedCentralGoogle Scholar
  96. Yamauchi Y, Hasegawa A, Mizutani M, Sugimoto Y (2012) Chloroplastic NADPH-dependent alkenal/one oxidoreductase contributes to the detoxification of reactive carbonyls produced under oxidative stress. FEBS Lett 586:1208–1213CrossRefPubMedGoogle Scholar
  97. Yang W, Zhu C, Ma X, Li G, Gan L, Ng D, Xia K (2013) Hydrogen peroxide is a second messenger in the salicylic acid–triggered adventitious rooting process in mung bean seedlings. PLoS ONE 8(12):e84580CrossRefPubMedPubMedCentralGoogle Scholar
  98. Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:W293–W297CrossRefPubMedPubMedCentralGoogle Scholar
  99. Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y et al (2009) Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol 16:1230–1236CrossRefPubMedGoogle Scholar
  100. Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM (2002) Differential expression and function of Arabidopsis thaliana NHX Na(+)/H(+) antiporters in the salt stress response. Plant J 30:529–539CrossRefPubMedGoogle Scholar
  101. 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 Cell Physiol 42:1025–1033CrossRefPubMedGoogle Scholar
  102. Zago E, Morsa S, Dat JF, Alard P, Ferrarini A, Inze D, Delledonne M, Van Breusegem F (2006) Nitric oxide- and hydrogen peroxide-responsive gene regulation during cell death induction in tobacco. Plant Physiol 141:404–411CrossRefPubMedPubMedCentralGoogle Scholar
  103. Zazimalova E, Krecek P, Skupa P, Hoyerova K, Petrasek J (2007) Polar transport of the plant hormone auxin—the role of PIN-FORMED (PIN) proteins. Cell Mol Life Sci 64:1621–1637CrossRefPubMedGoogle Scholar
  104. Zeng F, Sun F, Li L, Liu K, Zhan Y (2014) Genome-scale transcriptome analysis in response to nitric oxide in birch cells: implications of the triterpene biosynthetic pathway. PLoS ONE 9:e116157CrossRefPubMedPubMedCentralGoogle Scholar
  105. Zhang B, Zheng L, Wang J (2012) Nitric oxide elicitation for secondary metabolite production in cultured plant cells. Appl Microbiol Biot 93:455–466CrossRefGoogle Scholar
  106. Zhang Y, Su J, Cheng D, Wang R, Mei Y, Hu H, Shen W, Zhang Y (2018) Nitric oxide contributes to ethane-induced osmotic stress tolerance in mung bean. BMC Plant Biol 18:207CrossRefPubMedPubMedCentralGoogle Scholar
  107. Zhou Y, Underhill SJ (2016) Breadfruit (Artocarpus altilis) gibberellin 2-oxidase genes in stem elongation and abiotic stress response. Plant Physiol Biochem 98:81–88CrossRefPubMedGoogle Scholar

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© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  1. 1.School of Environmental and Municipal Engineering, Key Laboratory of Extreme Environmental Microbial Resources and Engineering, Gansu ProvinceLanzhou Jiaotong UniversityLanzhouPeople’s Republic of China

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