Skip to main content

The Auxin-Nitric Oxide Highway: A Right Direction in Determining the Plant Root System

  • Chapter
Gasotransmitters in Plants

Abstract

Nitric oxide (NO) appeared as a novel signal molecule in plants at the end of the twentieth century. Since then, new discoveries on the participation of NO in the regulation of plant biology have not stopped. One of the most yet intriguing aspects that are under strong investigation is the extension and scope of the NO involvement in the control of cell redox balance and hormone-regulated processes. In this chapter, we addressed both issues connecting root growth with the NO-mediated posttranslational modification S-nitrosylation on the auxin receptor transport inhibitor response 1 (TIR1) and on the antioxidant enzyme ascorbate peroxidase 1 (APX1). Auxin is probably the best studied plant hormone influencing root growth and development. Even if the components of the signaling cascade leading to the induction of auxin-responsive genes have been elucidated, here we describe the last findings explaining the molecular mechanisms underlying the requirement of NO to get a full response to auxin stimulus.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abel S, Theologis A (1996) Early genes and auxin action. Plant Physiol 111:9–17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Airaki M, Sànchez-Moreno L, Leterrier M, Barroso JB, Palma JM, Corpas FJ (2011) Detection and quantification of S-nitrosoglutathione (GSNO) in pepper (Capsicum annuum L.) plant organs by LC-ES/MS. Plant Cell Physiol 52:2006–2015

    Article  CAS  PubMed  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Arc E, Galland M, Godin B, Cueff G, Rajjou L (2013) Nitric oxide implication in the control of seed dormancy and germination. Front Plant Sci 4:1–13

    Google Scholar 

  • Bai X, Yang L, Tian M, Chen J, Shi J, Yang Y, Hu X (2011) Nitric oxide enhances desiccation tolerance of recalcitrant Antiaris toxicaria seeds via protein S-nitrosylation and carbonylation. PLoS One 6:e20714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bashandy T, Guilleminot J, Vernoux T, Caparros-Ruiz D, Ljung K, Meyer Y, Reichheld J-P (2010) Interplay between the NADP-linked thioredoxin and glutathione systems in Arabidopsis auxin signaling. Plant Cell 22:376–391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538

    Article  CAS  PubMed  Google Scholar 

  • Begara-Morales JC, Sánchez-Calvo B, Chaki M, Mata-Pérez C, Valderrama R, Padilla MN, López-Jaramillo J, Luque F, Corpas FJ, Barroso JB (2015) Differential molecular response of monodehydroascorbate reductase and glutathione reductase by nitration and S-nitrosylation. J Exp Bot 66:5983–5996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besson-Bard A, Gravot A, Richaud P, Auroy P, Duc C, Gaymard F, Taconnat L, Renou JP, Pugin A, Wendehenne D (2009) Nitric oxide contributes to cadmium toxicity in Arabidopsis by promoting cadmium accumulation in roots and by up-regulating genes related to iron uptake. Plant Physiol 149:1302–1315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Broniowska KA, Diers AR, Hogg N (2013) S-nitrosoglutathione. Biochim Biophys Acta 1830:3173–3181

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Calderón Villalobos LIA, Lee S, De Oliveira C, Ivetac A, Brandt W, Armitage L et al (2012) A combinatorial TIR1/AFB–Aux/IAA co-receptor system for differential sensing of auxin. Nat Chem Biol 8:477–485

    Article  PubMed  Google Scholar 

  • Chapman EJ, Estelle M (2009) Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet 43:265–285

    Article  CAS  PubMed  Google Scholar 

  • Chen YH, Kao CH (2012) Calcium is involved in nitric oxide-and auxin-induced lateral root formation in rice. Protoplasma 249:187–195

    Article  CAS  PubMed  Google Scholar 

  • Córdoba-Pedregosa DC, Córdoba F, Villalba JM, González-Reyes JA (2003) Zonal changes in ascorbate and hydrogen peroxide contents, peroxidase, and ascorbate-related enzyme activities in onion roots. Plant Physiol 131:697–706

    Article  Google Scholar 

  • Corpas FJ, Barroso JB (2015) Functions of nitric oxide (NO) in roots during development and under adverse stress conditions. Plants 4:240–252

    Article  PubMed  PubMed Central  Google Scholar 

  • Corpas FC, Barroso JB, Carreras A, Quirós M, León AM, Romero-Puertas MC, Esteban FJ, Valderrama R, Palma JM, Sandalio LM, Gomez M, del Río LA (2004) Cellular and subcellular localization of endogenous nitric oxide in young and senescent pea plants. Plant Physiol 136:2722–2733

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Graziano M, Chevalier C, Lamatina L (2006) Nitric oxide modulates the expression of cell cycle regulatory genes during lateral root formation in tomato. J Exp Bot 57:581–588

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Foresi N, Lamattina L (2013a) Structure diversity of nitric oxide synthases (NOS): the emergence of new forms in photosynthetic organisms. Front Plant Sci 4:1–3

    Article  Google Scholar 

  • Correa-Aragunde N, Foresi N, Delledonne M, Lamattina L (2013b) Auxin induces redox regulation of ascorbate peroxidase 1 activity by S-nitrosylation/denitrosylation balance resulting in changes of root growth pattern in Arabidopsis. J Exp Bot 64:3339–3349

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Cejudo FJ, Lamattina L (2015a) Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in Arabidopsis. Ann Bot 116:695–702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Correa-Aragunde N, Foresi N, Lamattina L (2015b) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J Exp Bot 66:2913–2921

    Article  CAS  PubMed  Google Scholar 

  • Correa-Aragunde N, Foresi N, Lamattina L (2016) Auxin and nitric oxide: a counterbalanced partnership ensures the redox cue control required for determining root growth pattern. In: Wendehenne D (ed) Adv Bot Res (Special Issue Nitric oxide and Signaling in Plants) 77:41–54

    Google Scholar 

  • Dabrowska G (2007) Characteristics of the plant ascorbate peroxidase family. Acta Biol Cracoviensa 49:7–17

    Google Scholar 

  • Davies PJ (1995) Plant hormones: physiology, biochemistry and molecular biology. Kluwer Academic, Dordrecht, pp 39, 65

    Book  Google Scholar 

  • De Gara L, de Pinto MC, Arrigoni O (1997) Ascorbate synthesis and ascorbate peroxidase activity during the early stage of wheat germination. Physiol Plant 100:894–900

    Article  Google Scholar 

  • De Pinto MC, Tommasi F, De Gara L (2002) Changes in the antioxidant systems as part of the signaling pathway responsible for the programmed cell death activated by nitric oxide and reactive oxygen species in Tobacco Bright-Yellow 2 cells. Plant Physiol 130:698–708

    Article  PubMed  PubMed Central  Google Scholar 

  • De Pinto MC, Locato V, Sgobba A, Romero-Puertas MDC, Gadaleta C, Delledonne M, De Gara L (2013) S-nitrosylation of ascorbate peroxidase is part of programmed cell death signaling in tobacco Bright Yellow-2 cells. Plant Physiol 163:1766–1775

    Article  PubMed  PubMed Central  Google Scholar 

  • del Giudice J, Cam Y, Damiani I, Fung-Chat F, Meilhoc E, Bruand C, Brouquisse R, Puppo A, Boscari A (2011) Nitric oxide is required for an optimal establishment of the Medicago truncatula-Sinorhizobium meliloti symbiosis. New Phytol 191:405–417

    Article  PubMed  PubMed Central  Google Scholar 

  • Desikan R, Griffiths R, Hancock J, Neill S (2002) A new role for an old enzyme: nitrate reductase-mediated nitric oxide generation is required for abscisic acid-induced stomatal closure in Arabidopsis thaliana. Proc Natl Acad Sci USA 99:16314–16318

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Estelle M (2005a) The F-box protein TIR1 is an auxin receptor. Nature 435:441–445

    Article  CAS  PubMed  Google Scholar 

  • Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L et al (2005b) Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 9:109–119

    Article  CAS  PubMed  Google Scholar 

  • Di Dato V, Musacchia F, Petrosino G, Patil S, Montresor M, Sanges R, Ferrante MI (2015) Transcriptome sequencing of three Pseudo-nitzschia species reveals comparable gene sets and the presence of nitric oxide synthase genes in diatoms. Sci Rep 5

    Google Scholar 

  • Dunand C, Crèvecoeur M, Penel C, Penel C (2006) Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. New Phytol 174:332–341

    Article  Google Scholar 

  • Fares A, Rossignol M, Peltier J-B (2011) Proteomics investigation of endogenous S-nitrosylation in Arabidopsis. Biochem Biophys Res Commun 416:331–336

    Article  CAS  PubMed  Google Scholar 

  • 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 147:1936–1946

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foreman J, Demidchik V, Bothwell JHF, Mylona P, Miedema H, Torres MA, Linstead P, Costa S, Brownlee C, Jones JDG, Davies JM, Dolan L (2003) Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature 422:442–446

    Article  CAS  PubMed  Google Scholar 

  • Foresi N, Correa-Aragunde N, Parisi G, Caló G, Salerno G, Lamattina L (2010) Characterization of a nitric oxide synthase from the plant kingdom: NO generation from the green alga Ostreococcus tauri is light irradiance and growth phase dependent. Plant Cell 22:3816–3830

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Foresi N, Mayta ML, Lodeyro AF, Scuffi D, Correa-Aragunde N, Garcia-Mata C, Casalongue C, Carrillo N, Lamattina L (2015) Expression of the tetrahydrofolate-dependent nitric oxide synthase from the green alga Ostreococcus tauri increases tolerance to abiotic stresses and influences stomatal development in Arabidopsis. Plant J 82:806–821

    Article  CAS  PubMed  Google Scholar 

  • Friml J (2003) Auxin transport - shaping the plant. Curr Opin Plant Biol 6:7–12

    Article  CAS  PubMed  Google Scholar 

  • Gapper C, Dolan L (2006) Control of plant development by reactive oxygen species 1. Cell 141:341–345

    CAS  Google Scholar 

  • Geldner N, Friml J, Stierhof Y-D, Jurgens G, Palme K (2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

    Article  CAS  PubMed  Google Scholar 

  • Gibbs DJ, Nurulhikma MI, Movahedi M, Lozano-Juste J, Mendiondo GM, Berckhan S, de la Rosa NM, Conde JV, Sousa-Correia C, Pearce SP, Bassel GW, Hamali B, Talloji P, Tomé DFA, Coego A, Beynon J, Alabadí D, Bachmair A, León J, Gray JE, Theodoulou FL, Holdsworth MJ (2014) Nitric oxide sensing in plants is mediated by proteolytic control of group VII ERF transcription factors. Mol Cell 53:369–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giraldo JP, Landry MP, Faltermeier SM, McNicholas TP, Iverson NM, Boghossian AA, Reuel NF, Hilmer AJ, Sen F, Brew JA, Strano MS (2014) Plant nanobionics approach to augment photosynthesis and biochemical sensing. Nat Mater 13:400–408

    Article  CAS  PubMed  Google Scholar 

  • Gray WM, Kepinski S, Rouse D, Leyser O, Estelle M (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature 414:271–276

    Article  CAS  PubMed  Google Scholar 

  • Gupta KJ, Zabalza A, van Dongen JT (2009) Regulation of respiration when the oxygen availability changes. Physiol Plant 137:383–391

    Article  CAS  PubMed  Google Scholar 

  • Hasanuzzaman M, Hossain MA, Fujita M (2011) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnol Rep 5:353–365

    Article  Google Scholar 

  • He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305:1968–1971

    Article  CAS  PubMed  Google Scholar 

  • Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iglesias MJ, Terrile MC, Bartoli CG, D’Ippolito S, Casalongué CA (2010) Auxin signaling participates in the adaptative response against oxidative stress and salinity by interacting with redox metabolism in Arabidopsis. Plant Mol Biol 74:215–222

    Article  CAS  PubMed  Google Scholar 

  • Innocenti G, Pucciariello C, Le Gleuher M, Hopkins J, de Stefano M, Delledonne M, Puppo A, Baudouin E, Frendo P (2007) Glutathione synthesis is regulated by nitric oxide in Medicago truncatula roots. Planta 225:1597–1602

    Article  CAS  PubMed  Google Scholar 

  • Jaffrey, S.R. and Snyder, S.H. (2001). The biotin switch method for the detection of S-nitrosylated proteins. Science STKE 86:pl1

    Google Scholar 

  • Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiol 142:1246–1255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jeandroz S, Wipf D, Stuehr D, Lamattina L, Melkonian M, Tian Z, Zhu Y, Carpenter E, Wong Gane K-S, Wendehenne D (2016) Occurrence, structure, and evolution of nitric oxide synthase-like proteins in the plant kingdom. Sci Signal 9:re2. doi:10.1126/scisignal.aad4403

  • Kasprowicz A, Szuba A, Volkmann D, Baluška F, Wojtaszek P (2009) Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J Exp Bot 60:1605–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kato H, Takemoto D, Kawakita K (2013) Proteomic analysis of S‐nitrosylated proteins in potato plant. Physiol Plant 148:371–386

    Article  CAS  PubMed  Google Scholar 

  • Kepinski S, Leyser O (2005) The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature 435:446–451

    Article  CAS  PubMed  Google Scholar 

  • Keyster M, Klein A, Egbich I, Jacobs A, Ludidi N (2011) Nitric oxide increases the enzymatic activity of three ascorbate peroxidase isoforms in soybean root nodules. Plant Signal Behav 6:956–961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim J-H, Heller DA, Jin H, Barone PW, Song C, Zhang J, Trudel LJ, Wogan GN, Tannenbaum SR, Strano MS (2009) The rational design of nitric oxide selectivity in single-walled carbon nanotube near-infrared fluorescence sensors for biological detection. Nat Chem 1:473–481

    Article  CAS  PubMed  Google Scholar 

  • Kolbert Z, Bartha B, Erdei L (2008) Osmotic stress- and indole-3-butyric acid-induced NO generation are partially distinct processes in root growth and development in Pisum sativum. Physiol Plant 133:406–416

    Article  CAS  PubMed  Google Scholar 

  • Kumar A, Castellano I, Patti FP, Palumbo A, Buia MC (2015) Nitric oxide in marine photosynthetic organisms. Nitric Oxide 47:34–39

    Article  CAS  PubMed  Google Scholar 

  • Kwak JM, Nguyen V, Schroeder JI (2006) The role of reactive oxygen species in hormonal responses. Plant Physiol 141:323–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwon E, Feechan A, Yun B-W, Hwang B-H, Pallas J, Kang J-G, Loake G (2012) AtGSNOR1 function is required for multiple developmental programs in Arabidopsis. Planta 236:887–900

    Article  CAS  PubMed  Google Scholar 

  • Lad L, Mewies M, Raven EL (2002) Substrate binding and catalytic mechanism in ascorbate peroxidase: evidence for two ascorbate binding sites. Biochemistry 41:13774–13781

    Article  CAS  PubMed  Google Scholar 

  • Lamattina L, Garcia-Mata C, Graziano M, Pagnussat G (2003) Nitric oxide: the versatility of an extensive signal molecule. Annu Rev Plant Biol 54:109–136

    Article  CAS  PubMed  Google Scholar 

  • 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 57:1341–1351

    Article  CAS  PubMed  Google Scholar 

  • Lanteri ML, Laxalt AM, Lamattina L (2008) Nitric oxide triggers phosphatidic acid accumulation via phospholipase D during auxin-induced adventitious root formation in cucumber. Plant Physiol 147:188–198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laspina NV, Groppa MD, Tomaro ML, Benavides MP (2005) Nitric oxide protects sunflower leaves against Cd-induced oxidative stress. Plant Sci 169:323–330

    Article  CAS  Google Scholar 

  • Lau S, Shao N, Bock R, Jürgens G, De Smet I (2009) Auxin signaling in algal lineages: fact or myth? Trends Plant Sci 14:182–188

    Article  CAS  PubMed  Google Scholar 

  • Leach J, Keyster M, du Plessis M, Ludidi N (2010) Nitric oxide synthase activity ir required for development of functional nodules in soybean. J Plant Physiol 167:1584–1591

    Article  CAS  PubMed  Google Scholar 

  • Lin A, Wang Y, Tang J, Xue P, Li C, Liu L, Hu B, Yang F, Loake GJ, Chu C (2012) Nitric oxide and protein S-nitrosylation are integral to hydrogen peroxide-induced leaf cell death in rice. Plant Physiol 158:451–464

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr C, Durner J (2009) S-Nitrosylation in plants: pattern and function. J Proteomics 73:1–9

    Article  CAS  PubMed  Google Scholar 

  • Lindermayr C, Sell S, Muller B, Leister D, Durner J (2010) Redox regulation of the NPR1-TGA1 system of Arabidopsis thaliana by nitric oxide. Plant Cell 22:2894–2907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lira-Ruan V, Mendivil SN, Dubrovsky JG (2013) Heuristic aspect of the lateral root initiation index: a case study of the role of nitric oxide in root branching. Appl Plant Sci 1:1300029

    Article  Google Scholar 

  • Lombardo MC, Lamattina L (2012) Nitric oxide is essential for vesicle formation and trafficking in Arabidopsis root hair growth. J Exp Bot 63:4875–4885

    Article  CAS  PubMed  Google Scholar 

  • Lombardo C, Graziano C, Polacco J, Lamattina L (2006) Nitric oxide is a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  PubMed Central  Google Scholar 

  • Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312:1520–1523

    Article  CAS  PubMed  Google Scholar 

  • 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 85:49–61

    Article  CAS  PubMed  Google Scholar 

  • Mandelman D, Jamal J, Poulos TL (1998) Identification of two electron-transfer sites in ascorbate peroxidase using chemical modification, enzyme kinetics, and crystallography. Biochemistry 37:17610–17617

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Ruiz A, Cadenas S, Lamas S (2011) Nitric oxide signaling: classical, less classical, and nonclassical mechanisms. Free Radic Biol Med 51:17–29

    Article  PubMed  Google Scholar 

  • Medina-Andrés R, Lira-Ruan V (2012) In silico characterization of a nitrate reductase gene family and analysis of the predicted proteins from the moss Physcomitrella patens. Commun Integr Biol 5:19–25

    Article  PubMed  PubMed Central  Google Scholar 

  • Medina-Andres R, Solano-Peralta A, Saucedo-Vázquez JP, Napsucialy-Mendivil S (2015) The nitric oxide production in the moss Physcomitrella patens is mediated by nitrate reductase. PLoS One 10(3):e0119400

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 51:1612–1626

    Article  PubMed  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Montrichard F, Alkhalfioui F, Yano H, Vensel WH, Hurkman WJ, Buchanan BB (2009) Thioredoxin targets in plants: the first 30 years. J Proteomics 72:452–474

    Article  CAS  PubMed  Google Scholar 

  • Mur LA, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5:pls052

    Google Scholar 

  • Nibau C, Gibbs DJ, Coates JC (2008) Branching out in new directions: the control of root architecture by lateral root formation. New Phytol 179:595–614

    Article  CAS  PubMed  Google Scholar 

  • Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C et al (2005) 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ortega-Galisteo AP, Rodríguez-Serrano M, Pazmiño DM, Gupta DK, Sandalio LM, Romero-Puertas MC (2012) S-nitrosylated proteins in pea (Pisum sativum L.) leaf peroxisomes: changes under abiotic stress. J Exp Bot 63:2089–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osmont KS, Sibout R, Hardtke CS (2007) Hidden branches: developments in root system architecture. Annu Rev Plant Biol 58:93–113

    Article  CAS  PubMed  Google Scholar 

  • Overvoorde PJ, Okushima Y, Alonso JM, Chan A, Chang C, Ecker JR et al (2005) Functional genomic analysis of the AUXIN/INDOLE-3-ACETIC ACID gene family members in Arabidopsis thaliana. Plant Cell 17:3282–3300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paciorek T, Zazimalova E, Ruthardt N, Petrasek J, Stierhof Y-D, Kleine-Vehn J, Morris DA, Emans N, Jurgens G, Geldner N, Friml J (2005) Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–1256

    Article  CAS  PubMed  Google Scholar 

  • Pagnussat GC, Simontacchi M, Puntarulo S, Lamattina L, Fı D (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pagnussat GC, Lanteri L, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiol 132:1241–1248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:279–286

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey P, Singh J, Achary VMM, Reddy MK (2015) Redox homeostasis via gene families of ascorbate-glutathione pathway. Front Environ Sci 3:1–14

    Article  Google Scholar 

  • Paponov IA, Teale W, Lang D, Paponov M, Reski R, Rensing SA, Palme K (2009) The evolution of nuclear auxin signalling. BMC Evol Biol 9:1

    Article  Google Scholar 

  • París R, Iglesias MJ, Terrile MC, Casalongué CA (2013) Functions of S-nitrosylation in plant hormone networks. Front Plant Sci 4:10–3389

    Google Scholar 

  • Parry G, Calderon-Villalobos LI, Prigge M, Peret B, Dharmasiri S, Itoh H et al (2009) Complex regulation of the TIR1/AFB family of auxin receptors. Proc Natl Acad Sci 106:22540–22545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pérez AC, Goossens A (2013) Jasmonate signalling: a copycat of auxin signalling? Plant Cell Environ 36(12):2071–2084

    Article  PubMed  Google Scholar 

  • Puyaubert J, Fares A, Rézé N, Peltier J-B, Baudouin E (2014) Identification of endogenously S-nitrosylated proteins in Arabidopsis plantlets: effect of cold stress on cysteine nitrosylation level. Plant Sci 215–216:150–156

    Article  PubMed  Google Scholar 

  • Ramos JA, Zenser N, Leyser O, Callis J (2001) Rapid degradation of auxin/indoleacetic acid proteins requires conserved amino acids of domain II and is proteasome dependent. Plant Cell 13:2349–2360

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rao MV, Paliyath G, Ormrod DP (1996) Ultraviolet-B-and ozone-induced biochemical changes in antioxidant enzymes of Arabidopsis thaliana. Plant Physiol 110:125–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Romero-Puertas MC, Campostrini N, Mattè A, Righetti PG, Perazzolli M, Zolla L, Roepstorff P, Delledonne M (2008) Proteomic analysis of S-nitrosylated proteins in Arabidopsis thaliana undergoing hypersensitive response. Proteomics 8:1459–1469

    Article  CAS  PubMed  Google Scholar 

  • Ros Barceló AR (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216

    Article  Google Scholar 

  • Sagi M, Fluhr R (2006) Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol 141:336–340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheard LB, Tan X, Mao H, Withers J, Ben-Nissan G, Hinds TR et al (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468:400–405

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi YF, Wang DL, Wang C, Culler AH, Kreiser MA, Suresh J et al (2015) Loss of GSNOR1 function leads to compromised auxin signaling and polar auxin transport. Mol Plant 8:1350–1365

    Article  CAS  PubMed  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Shimizu-Mitao Y, Kakimoto T (2014) Auxin sensitivities of all Arabidopsis Aux/IAAs for degradation in the presence of every TIR1/AFB. Plant Cell Physiol 55:1450–1459

    Article  CAS  PubMed  Google Scholar 

  • Singh HP, Kaur S, Batish RD, Sharma VP, Sharma N, Kohli RK (2009) Nitric oxide alleviates arsenic toxicity by reducing oxidative damage in the roots of Oryza sativa (rice). Nitric Oxide 20:289–297

    Article  CAS  PubMed  Google Scholar 

  • Spoel SH, Loake GJ (2011) Redox-based protein modifications: the missing link in plant immune signalling. Curr Opin Plant Biol 14:358–364

    Article  CAS  PubMed  Google Scholar 

  • Stamler JS, Singel DJ, Loscalzo J (1992) Biochemistry nitric oxide and redox-activated forms. Science 258:1898

    Article  CAS  PubMed  Google Scholar 

  • Stolz JF, Basu P (2002) Evolution of nitrate reductase: molecular and structural variations on a common function. Chembiochem 3:198–206

    Article  CAS  PubMed  Google Scholar 

  • Szemenyei H, Hannon M, Long JA (2008) TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 319:1384–1386

    Article  CAS  PubMed  Google Scholar 

  • Tan X, Calderon-Villalobos LIA, Sharon M, Zheng C, Robinson CV, Estelle M, Zheng N (2007) Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature 446:640–645

    Article  CAS  PubMed  Google Scholar 

  • Tanou G, Job C, Raijou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. Plant J 60:795–804

    Article  CAS  PubMed  Google Scholar 

  • Terrile MC, París R, Calderón‐Villalobos LI, Iglesias MJ, Lamattina L, Estelle M, Casalongué CA (2012) Nitric oxide influences auxin signaling through S-nitrosylation of the Arabidopsis TRANSPORT INHIBITOR RESPONSE 1 auxin receptor. Plant J 70(3):492–500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G et al (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448:661–665

    Article  CAS  PubMed  Google Scholar 

  • Tischner R, Planchet E, Kaiser WM (2004) Mitochondrial electron transport as a source for nitric oxide in the unicellular green alga Chlorella sorokiniana. FEBS Lett 576:151–155

    Article  CAS  PubMed  Google Scholar 

  • Tiwari SB, Wang XJ, Hagen G, Guilfoyle TJ (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. Plant Cell 13:2809–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tossi V, Amenta M, Lamattina L, Cassia R (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant Cell Environ 34:909–921

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Du Y, Hou Y-J, Zhao Y, Hsu C-C, Yuan F, Zhu X, Tao WA, Song C-P, Zhu J-K (2015) Nitric oxide negatively regulates abscisic acid signaling in guard cells by S-nitrosylation of OST1. Proc Natl Acad Sci 112:613–618

    Article  CAS  PubMed  Google Scholar 

  • Weijers D, Benkova E, Jäger KE, Schlereth A, Hamann T, Kientz M et al (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. EMBO J 24:1874–1885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Went FW (1928) Wushstoff und wachstum. Rec Trav Bot Neerl 25:1–116

    Google Scholar 

  • Wilkinson JQ, Crawford NM (1993) Identification and characterization of a chlorate-resistant mutant of Arabidopsis thaliana with mutations in both nitrate reductase structural genes NIA1 and NIA2. Mol Gen Genet 239:289–297

    Article  CAS  PubMed  Google Scholar 

  • Yabuta Y, Maruta T, Yoshimura K, Ishikawa T, Shigeoka S (2004) Two distinct redox signaling pathways for cytosolic APX induction under photooxidative stress. Plant Cell Physiol 45:1586–1594

    Article  CAS  PubMed  Google Scholar 

  • Yang H, Mu J, Chen L, Feng J, Hu J, Li L, Zhou J-M, Zuo J (2015) S-nitrosylation positively regulates ascorbate peroxidase activity during plant stress responses. Plant Physiol 167:1604–1615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Moss BL, Jang SS, Prigge M, Klavins E, Nemhauser JL, Estelle M (2013) Mutations in the TIR1 auxin receptor that increase affinity for auxin/indole-3-acetic acid proteins result in auxin hypersensitivity. Plant Physiol 162:295–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu H, Zhang Y, Moss BL, Bargmann BOR, Wang R, Prigge M, Nemhauser JL, Estelle M (2015) Untethering the TIR1 auxin receptor from the SCF complex increases its stability and inhibits auxin response. Nat Plants 1:14030

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lorenzo Lamattina .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Correa-Aragunde, N., París, R., Foresi, N., Terrile, C., Casalongué, C., Lamattina, L. (2016). The Auxin-Nitric Oxide Highway: A Right Direction in Determining the Plant Root System. In: Lamattina, L., García-Mata, C. (eds) Gasotransmitters in Plants. Signaling and Communication in Plants. Springer, Cham. https://doi.org/10.1007/978-3-319-40713-5_6

Download citation

Publish with us

Policies and ethics