Nitric Oxide and Hydrogen Peroxide in Root Organogenesis

  • Javier Raya-González
  • Jesús Salvador López-Bucio
  • José López-BucioEmail author


Nitric oxide (NO) and reactive oxygen species (ROS) are central messengers in the way plants respond to environmental and hormonal stimuli and for the configuration of root architecture. ROS determine the boundaries between the meristem and cell elongation zone of the primary root and act in concert with NO to promote lateral root primordia maturation and epidermal cell differentiation. Overall, the capacity of roots to acquire nutrients such as phosphate, nitrate, and sulfate is determined by NO and ROS via their effects on root hair development and expression of genes for improving nutritional responses or orchestrating the activities of proteins of all major hormonal pathways, including auxin, ethylene, jasmonic acid, brassinosteroids, and abscisic acid. Specifically, ROS target phosphatases and transcription factors of two main families, MYB and BHLH, these later being probably recruited by the mediator complex to the promoters of genes for transcription. Here, we review the information about the functions and mechanisms of NO and ROS modulated-root organogenesis, including growth, patterning, and differentiation.


Nitric oxide Reactive oxygen species Root growth Lateral root formation Root hair development Stem cell niche Phytohormones 


  1. Airaki M, Leterrier M, Valderrama R, Chaki M, Begara-Morales JC, Barroso JB, del Río LA, Palma JM, Corpas FJ (2015) Spatial and temporal regulation of the metabolism of reactive oxygen and nitrogen species during the early development of pepper (Capsicum annuum) seedlings. Ann Bot 116:679–693PubMedPubMedCentralCrossRefGoogle Scholar
  2. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  3. Bai S, Li M, Yao T, Wang H, Zhang Y, Xiao L, Wang J, Zhang Z, Hu Y, Liu W, He Y (2012) Nitric oxide restrain root growth by DNA damage induced cell cycle arrest in Arabidopsis thaliana. Nitric Oxide 26:54–60PubMedCrossRefGoogle Scholar
  4. Bhosale R, Giri J, Pandey BK, Giehl RFH, Hartmann A, Traini R, Truskina J, Leftley N, Hanlon M, Swarup K, Rashed A, Voß U, Alonso J, Stepanova A, Yun J, Ljung K, Brown KM, Lynch JP, Dolan L, Vernoux T, Bishopp A, Wells D, von Wirén N, Bennett MJ, Swarup R (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun 9:1409PubMedPubMedCentralCrossRefGoogle Scholar
  5. Campos-Cuevas JC, Pelagio-Flores R, Raya-González J, Méndez-Bravo A, Ortiz-Castro R, López-Bucio J (2008) Tissue culture of Arabidopsis thaliana explants reveals a stimulatory effect of alkamides on adventitious root formation and nitric accumulation. Plant Sci 174:165–173CrossRefGoogle Scholar
  6. Cederholm H, Lyer-Pascuzzi AS, Benfey P (2012) Patterning the primary root in Arabidopsis. WIREs Dev Biol 1:675–691CrossRefGoogle Scholar
  7. Chen YH, Kao CH (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249:187–195PubMedCrossRefGoogle Scholar
  8. Chen Z, Gu Q, Yu X, Huang L, Xu S, Wang R, Shen W, Shen W (2018) Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann Bot 121:1127–1136PubMedCrossRefGoogle Scholar
  9. Corpas FJ, Barroso JB (2015) Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants (Basel) 22:240–252CrossRefGoogle Scholar
  10. Corpas FJ, Gupta DK, Palma JM (2015) Production sites of reactive oxygen species (ROS) in organelles from plant cells. In: Gupta DK, Palma JM, Corpas FJ (eds) Reactive oxygen species and oxidative damage in plants under stress. Springer, Basel, pp 1–19Google Scholar
  11. Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905PubMedCrossRefPubMedCentralGoogle Scholar
  12. De Tullio MC, Jiang K, Feldman LJ (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiol Biochem 45:328–336CrossRefGoogle Scholar
  13. Dindas J, Scherzer S, Roelfsema MRG, von Meyer K, Müller HM, Al-Rasheid KAS, Palme K, Dietrich P, Becker D, Bennett MJ, Hedrich R (2018) AUX1-mediated root hair auxin influx governs SCF(TIR1/AFB)-type Ca(2+) signaling. Nat Commun 9:1174PubMedPubMedCentralCrossRefGoogle Scholar
  14. Dolzblasz A, Gola EM, Sokołowska K, Smakowska-Luzan E, Twardawska A, Janska H (2018) Impairment of meristem proliferation in plants lacking the mitochondrial protease AtFTSH4. Int J Mol Sci 19:853PubMedCentralCrossRefGoogle Scholar
  15. Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520PubMedCrossRefGoogle Scholar
  16. Du Y, Scheres B (2018) Lateral root formation and the multiple roles of auxin. J Exp Bot 69:155–167PubMedCrossRefPubMedCentralGoogle Scholar
  17. Efroni I, Mello A, Nawy T, Ip PL Rahni R, DelRose N, Powers A, Satija R, Birnbaum KD (2016) Root regeneration triggers an embryo-like sequence guided by hormonal interactions. Cell 165:1721–1733PubMedPubMedCentralCrossRefGoogle Scholar
  18. Fernández-Marcos M, Sanz L, Lewis DR, Muday GK, Lorenzo O (2011) Nitric oxide causes root apical mersitem defects and growth inhibition while reducing PIN-FORMED 1 (PIN1)-dependent acropetal auxin transport. Proc Natl Acad Sci U S A 108:18506–18511PubMedPubMedCentralCrossRefGoogle Scholar
  19. Fernández-Marcos M, Desvoyes B, Manzano C, Liberman LM, Benfey PN, del Pozo JC, Gutierrez C (2017) Control of Arabidopsis lateral root primordium boundaries by MYB36. New Phytol 213:105–112PubMedCrossRefPubMedCentralGoogle Scholar
  20. 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 147:1936–1946PubMedPubMedCentralCrossRefGoogle Scholar
  21. Foreman J, Demidchik V, Bothwell JH, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JD, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446PubMedCrossRefPubMedCentralGoogle Scholar
  22. Foyer CH, Ruban AV, Noctor G (2017) Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochem J 474:877–883PubMedPubMedCentralCrossRefGoogle Scholar
  23. Freschi L (2013) Nitric oxide and phytohormone interactions: current status and perspectives. Front Plant Sci 4:398PubMedPubMedCentralCrossRefGoogle Scholar
  24. Gutiérrez-Alanís D, Ojeda-Rivera JO, Yong-Villalobos L, Cardenas-Torres L, Herrera-Estrella L (2018) Adaptation to phosphate scarcity: tips from Arabidopsis roots. Trend Plant Sci 23:721–730CrossRefGoogle Scholar
  25. Ha JH, Kim JH, Kim SG, Sim HS, Lee G, Halitschke R, Baldwin IT, Kim JI, Park CM (2018) Shoot phytochrome B modulates reactive oxygen species homeostasis in roots via abscisic acid signaling in Arabidopsis. Plant J 94:790–798PubMedCrossRefGoogle Scholar
  26. Hernández-Barrera A, Velarde-Buendía A, Zepeda I, Sánchez F, Quinto C, Sánchez-López R, Cheung AY, Wu HM, Cardenas L (2015) Hyper, a hydrogen peroxide sensor, indicates the sensitivity of the Arabidopsis root elongation zone to aluminum treatment. Sensors 15:855–867PubMedCrossRefGoogle Scholar
  27. Heyman J, Cools T, Canher B, Shavialenka S, Traas J, Vercauteren I, Van den Daele H, Persiau G, De Jaeger G, Sugimoto G, De Veylder L (2016) The heterodimeric transcription factor complex ERF115-PAT1 grants regeneration competence. Nat Plant 2:16165CrossRefGoogle Scholar
  28. Kolbert Z, Bartha B, Erdei L (2008) Exogenous auxin-induced NO synthesis in nitrate reductase-associated in Arabidopsis thaliana root primordia. J Plant Physiol 165:967–975PubMedCrossRefPubMedCentralGoogle Scholar
  29. Kong X, Tian H, Yu Q, Zhang F, Wang R, Gao S, Xu W, Liu J, Shani E, Fu C, Zhou G, Zhang L, Zhang X, Ding Z (2018) PHB3 maintains root stem cell niche identity through ROS-responsive AP2/ERF transcription factors in Arabidopsis. Cell Rep 22:1350–1363PubMedCrossRefPubMedCentralGoogle Scholar
  30. Kwon E, Feechan A, Yun BW, Hwang BH, Pallas JA, Kang JG, Loake GJ (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236:887–900PubMedCrossRefGoogle Scholar
  31. Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. J Exp Bot 57:1341–1351PubMedCrossRefGoogle Scholar
  32. Lee HJ, Ha JH, Kim SG, Choi HK, Kim ZH, Han YJ, Kim JI, Oh Y, Fragoso V, Shin K, Hyeon T, Choi HG, Oh KH, Baldwin IT, Park CM (2016) Stem-piped light activates phytochrome B to trigger light responses in Arabidopsis thaliana roots. Sci Signal 9:ra106PubMedCrossRefGoogle Scholar
  33. Liao WB, Zhang ML, Huang GB, Yu JH (2012) Ca2+ and CaM are involved in NO- and H2O2-induced adventitious root development in marigold. J Plant Growth Regul 31:253–264CrossRefGoogle Scholar
  34. Lin CY, Huang LY, Chi WC, Huang TL, Kakimoto T, Tsai CR, Huang HJ (2015) Pathways involved in vanadate-induced root hair formation in Arabidopsis. Physiol Plant 153:137–148PubMedCrossRefGoogle Scholar
  35. Liu M, Zhang H, Fang X, Zhang Y, Jin C (2018) Auxin acts downstream of ethylene and nitric oxide to regulate magnesium deficiency-induced root hair development in Arabidopsis thaliana. Plant Cell Physiol 59:1452–1465PubMedGoogle Scholar
  36. Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33PubMedPubMedCentralCrossRefGoogle Scholar
  37. López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Curr Opin Plant Biol 6:280–287PubMedCrossRefGoogle Scholar
  38. López-Bucio J, Acevedo-Hernández G, Molina-Torres J, Herrera-Estrella L (2006) Novel signals for plant development. Curr Opin Plant Biol 9:523–529PubMedCrossRefGoogle Scholar
  39. Lv B, Tian H, Zhang F, Liu J, Lu S, Bai M, Li C, Ding Z (2018) Brassinosteroids regulate root growth by controlling reactive oxygen species homeostasis and dual effect on ethylene synthesis in Arabidopsis. PLoS Genet 14:e1007144PubMedPubMedCentralCrossRefGoogle Scholar
  40. Ma F, Wang L, Li J, Samma MK, Xie Y, Wang R, Wang J, Zhang J, Shen W (2014) Interaction between HY1 and H2O2 in auxin-induced lateral root formation in Arabidopsis. Plant Mol Biol 85:49–61PubMedCrossRefGoogle Scholar
  41. Mabuchi K, Maki H, Itaya T, Suzuki T, Nomoto M, Sakaoka S, Morikami A, Higashiyama T, Tada Y, Busch W, Tsukagoshi H (2018) MYB30 links ROS signaling, root cell elongation, and plant immune responses. Proc Natl Acad Sci U S A 115:E4710–E4719PubMedPubMedCentralCrossRefGoogle Scholar
  42. Mangano S, Denita-Juarez SP, Choi HS, Marzol E, Hwang Y, Ranocha P, Velasquez SM, Borassi C, Barberini ML, Aptekmann AA, Muschietti JP, Nadra AD, Dunand C, Cho HT, Estevez JM (2017) The molecular link between auxin and ROS-controlled root hair growth. Proc Natl Acad Sci U S A 114:5289–5294PubMedPubMedCentralCrossRefGoogle Scholar
  43. Mangano S, SP D-J, Marzol E, Borassi C, Estevez JM (2018) High auxin and high phosphate impact on RSL2 expression and ROS-homeostasis linked to root hair growth in Arabidopsis thaliana. Front Plant Sci 9:1164PubMedPubMedCentralCrossRefGoogle Scholar
  44. Manzano C, Pallero-Baena M, Casimiro I, De Rybel B, Orman-Ligeza B, Van Isterdael G, Beeckman T, Draye X, Casero P, Del Pozo JC (2014) The emerging role of reactive oxygen species signaling during lateral root development. Plant Physiol 165:1105–1119PubMedPubMedCentralCrossRefGoogle Scholar
  45. Marino D, Dunand C, Puppo A, Pauly N (2012) A burst of plant NADPH oxidases. Trend Plant Sci 17:9–15CrossRefGoogle Scholar
  46. Martínez-de la Cruz E, García-Ramírez E, Vázquez-Ramos JM, Reyes de la Cruz H, López-Bucio J (2015) Auxins differentially regulate root system architecture and cell cycle protein levels in maize seedlings. J Plant Physiol 176:147–156PubMedCrossRefGoogle Scholar
  47. 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 51:1612–1626PubMedCrossRefGoogle Scholar
  48. Méndez-Bravo A, Calderón-Vázquez C, Ibarra-Laclette E, Raya-González J, Ramírez-Chavez E, Molina-Torres J, Guevara-García A, López-Bucio J, Herrera-Estrella L (2011) Alkamides actívate jasmonic acid biosynthesis and signaling pathways and confer resistance to Botrytis cinerea in Arabidopsis thaliana. PLoS One 6(11):e27251PubMedPubMedCentralCrossRefGoogle Scholar
  49. Mittler R (2017) ROS are good. Trend Plant Sci 22:11–19CrossRefGoogle Scholar
  50. Mo M, Yokawa K, Wan Y, Baluska F (2015) How and why do root apices sense light under the soil surface? Front Plant Sci 6:775PubMedPubMedCentralGoogle Scholar
  51. Morquecho-Contreras A, Mendez-Bravo A, Pelagio-Flores R, Raya-Gonzalez J, Ortiz-Castro R, López-Bucio J (2010) Characterization of drr1, an alkamide resistant mutant of Arabidopsis reveals an important role for small lipid amides in lateral root development and plant senescence. Plant Physiol 152:1659–1673PubMedPubMedCentralCrossRefGoogle Scholar
  52. Nowicka AM, Kowalczyk A, Sek S, Stojek Z (2013) Oxidation of DNA followed by conformational change after OH radical attack. Anal Chem 85:355–361PubMedCrossRefPubMedCentralGoogle Scholar
  53. Orman-Ligeza B, Parizot B, de Rycke R, Fernandez A, Himschoot E, Van Breusegem F, Bennett MJ, Périlleux C, Beeckman T, Draye X (2016) RBOH-mediated ROS production facilitates lateral root emergence in Arabidopsis. Development 143:3328–3339PubMedPubMedCentralCrossRefGoogle Scholar
  54. Ortiz-Castro R, Pelagio-Flores R, Méndez Bravo A, Ruíz Herrera LF, Campos-García J, López-Bucio J (2014) Pyocyanin, a virulence factor produced by Pseudomonas aeruginosa, alters root development through reactive oxygen species and ethylene signaling in Arabidopsis. Mol Plant Microbe Interact 27:364–378PubMedCrossRefPubMedCentralGoogle Scholar
  55. Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J (2011) Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol 52:490–508PubMedCrossRefPubMedCentralGoogle Scholar
  56. Pelagio-Flores R, Muñoz-Parra E, Ortiz-Castro R, López-Bucio J (2012) Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res 53:279–288PubMedCrossRefPubMedCentralGoogle Scholar
  57. Pelagio-Flores R, Ruiz-Herrera LF, López-Bucio J (2016) Serotonin modulates Arabidopsis root growth via changes in reactive oxygen species and jasmonic acid-ethylene signaling. Physiol Plant 158:92–105PubMedCrossRefPubMedCentralGoogle Scholar
  58. Qu Y, Wang Q, Guo J, Wang P, Song P, Jia Q, Zhang X, Kudla J, Zhang W, Zhang Q (2017) Peroxisomal CuAOζ and its product H2O2 regulate the distribution of auxin and IBA-dependent lateral root development in Arabidopsis. J Exp Bot 68:4851–4867PubMedCrossRefPubMedCentralGoogle Scholar
  59. Raya-González J, Ortiz-Castro R, Ruíz-Herrera LF, Kazan K, López-Bucio J (2014) PHYTOCHROME AND FLOWERING TIME1/MEDIATOR25 regulates lateral root formation via auxin signaling in Arabidopsis. Plant Physiol 165:880–894PubMedPubMedCentralCrossRefGoogle Scholar
  60. Raya-González J, López-Bucio JS, Prado-Rodríguez JC, Ruiz-Herrera LF, Guevara-García AA, López-Bucio J (2017) The MEDIATOR genes MED12 and MED13 control Arabidopsis root system configuration influencing sugar and auxin responses. Plant Mol Biol 95:141–156PubMedCrossRefPubMedCentralGoogle Scholar
  61. Rogers ED, Benfey PN (2015) Regulation of plant root system architecture: implications for crop advancement. Curr Opin Biotechnol 32:93–98PubMedCrossRefPubMedCentralGoogle Scholar
  62. Ruiz-Herrera LF, Shane MW, López-Bucio J (2015) Nutritional regulation of root development. WIREs Dev Biol 4:431–443CrossRefGoogle Scholar
  63. Salazar-Henao JE, Vélez-Bermúdez IC, Schmidt W (2016) The regulation and plasticity of root hair patterning and morphogenesis. Development 143:1848–1858PubMedCrossRefPubMedCentralGoogle Scholar
  64. Sanz L, Fernández-Marcos M, Modrego A, Lewis DR, Muday GK, Pollmann S, Dueñas M, Santos-Buelga C, Lorenzo O (2014) Nitric oxide plays a role in stem cell niche homeostasis through its interaction with auxin. Plant Physiol 166:1972–1984PubMedPubMedCentralCrossRefGoogle Scholar
  65. Sanz L, Albertos P, Mateos I, Sánchez-Vicente I, Lechón T, Fernández-Marcos M, Lorenzo O (2015) Nitric oxide (NO) and phytohormones crosstalk during early plant development. J Exp Bot 66:2857–2868PubMedCrossRefPubMedCentralGoogle Scholar
  66. Shen Q, Wang YT, Tian H, Guo FQ (2013) Nitric oxide mediates cytokinin functions in cell proliferation and meristem maintenance in Arabidopsis. Mol Plant 6:1214–1225PubMedCrossRefPubMedCentralGoogle Scholar
  67. Shin R, Berg RH, Schachtman DP (2005) Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol 46:1350–1357PubMedCrossRefPubMedCentralGoogle Scholar
  68. Stadtman ER, Levine RL (2003) Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acid 25:207–218CrossRefGoogle Scholar
  69. Stoeckle D, Thellmann M, Vermeer JE (2018) Breakout-lateral root emergence in Arabidopsis thaliana. Curr Opin Plant Biol 41:67–72PubMedCrossRefGoogle Scholar
  70. Sun H, Feng F, Liu J, Zhao Q (2018) Nitric oxide affects Rice root growth by regulating auxin transport under nitrate supply. Front Plant Sci 9:659PubMedPubMedCentralCrossRefGoogle Scholar
  71. Sundaravelpandian K, Chandrika NNP, Schmidt W (2013) PFT1, a transcriptional Mediator complex subunit, controls root hair differentiation through reactive oxygen species (ROS) distribution in Arabidopsis. New Phytol 197:151–161PubMedCrossRefGoogle Scholar
  72. Tian Y, Fan M, Qin Z, Lv H, Wang M, Zhang Z, Zhou W, Zhao N, Li X, Han C, Ding Z, Wang W, Wang ZY, Bai MB (2018) Hydrogen peroxide positively regulates brassinosteroid signaling through oxidation of the BRASSINAZOLE-RESISTANT1 transcription factor. Nat Commun 9:1063PubMedPubMedCentralCrossRefGoogle Scholar
  73. Tossi V, Lamattina J, Cassia R (2013) Pharmacological and genetical evidence supporting nitric oxide requirement for 2,4-epibrassinolide regulation of root architecture in Arabidopsis thaliana. Plant Signal Behav 8:e24712PubMedPubMedCentralCrossRefGoogle Scholar
  74. Tsukagoshi H (2016) Control of root growth and development by reactive oxygen species. Curr Opin Plant Biol 29:57–63PubMedCrossRefGoogle Scholar
  75. Tsukagoshi H, Busch W, Benfey PN (2010) Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root. Cell 143:606–616PubMedCrossRefGoogle Scholar
  76. Wei Z, Li J (2016) Brassinosteroids regulate root growth, development, and symbiosis. Mol Plant 9:86–100PubMedCrossRefGoogle Scholar
  77. Xia XJ, Zhou YH, Shi K, Zhou J, Foyer CH, Yu JQ (2015) Interplay between reactive oxygen species and hormones in the control of plant development and stress tolerance. J Exp Bot 66:2839–2856PubMedCrossRefPubMedCentralGoogle Scholar
  78. Xiong J, Tao L, Zhu C (2009) Does nitric oxide play a pivotal role downstream of auxin in promoting crown root primordia initiation in monocots? Plant Sig Behav 4:999–1001CrossRefGoogle Scholar
  79. Xu XT, Jin X, Liao WB, Dawuda MM, Li XP, Wang M, Niu LJ, Ren PJ, Zhu YC (2017) Nitric oxide is involved in ethylene-induced adventitious root development in cucumber (Cucumis sativus L.) explants. Sci Hort 215:65–71CrossRefGoogle Scholar
  80. Yamasaki H, Watanabe NS, Sakihama Y, Cohen MF (2016) An overview of methods in plant nitric oxide (NO) research: why do we always need to use multiple methods? Method Mol Biol 1424:1–14CrossRefGoogle Scholar
  81. Yang L, Zhang J, He J, Qin Y, Hua D, Duan Y, Chen Z, Gong Z (2014) ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet 10:e1004791PubMedPubMedCentralCrossRefGoogle Scholar
  82. Yu Q, Tian H, Yue K, Liu J, Zhang B, Li X, Ding Z (2016) A P-loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root. PLoS Genet 12:e1006175PubMedPubMedCentralCrossRefGoogle Scholar
  83. Zhao P, Sokolov LN, Ye J, Tang CY, Shi J, Zhen Y, Lan W, Hong Z, Qi J, Lu GH, Pandey GK, Yang YH (2016) The LIKE SEX FOUR2 regulates root development by modulating reactive oxygen species homeostasis in Arabidopsis. Sci Rep 6:28683PubMedPubMedCentralCrossRefGoogle Scholar
  84. Zhu Y, Wang B, Tang K, Hsu CC, Xie S, Du H, Yang Y, Tao WA, Zhu JK (2017) An Arabidopsis nucleoporin NUP85 modulates plant responses to ABA and salt stress. PLoS Genet 13:e1007124PubMedPubMedCentralCrossRefGoogle Scholar

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© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Javier Raya-González
    • 1
  • Jesús Salvador López-Bucio
    • 2
  • José López-Bucio
    • 1
    Email author
  1. 1.Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico
  2. 2.CONACYT, Instituto de Investigaciones Químico-BiológicasUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico

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