Skip to main content

Oxygen Deficiency-Induced Root-to-Shoot Communication

  • Chapter
  • First Online:
Long-Distance Systemic Signaling and Communication in Plants

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 19))

Abstract

During anoxic condition, moving from the root which represents the primary oxygen-sensing organ, the plant effects a redefinition of the metabolism across the whole body. During such a phenotypical and physiological reshaping of the plant, the changes in a single organ may affect and determine metabolic adjustments elsewhere in order to assure plant survival. Here, we review the main mechanisms adopted in roots subject to anoxia, considering different tolerance degrees and different strategies, and how these adaptations reflect on the behaviour of the entire organism.

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 169.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 219.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 219.99
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

  • Ahmed S, Nawata E, Sakuratani T (2006) Changes of endogenous ABA and ACC, and their correlations to photosynthesis and water relations in mungbean (Vigna radiata (L.) Wilczak cv. KPS1) during waterlogging. Environ Exp Bot 57:278–284

    Article  CAS  Google Scholar 

  • Aiken RM, Smucker AJM (1996) Root system regulation of whole plant growth. Annu Rev Phytopathol 34:325–346

    Article  PubMed  CAS  Google Scholar 

  • Andersen PC, Lombard PB, Westwood MN (1984) Effect of root anaerobiosis on the water relations of several Pyrus species. Physiol Plant 62:245–252

    Article  Google Scholar 

  • Andreev VY, Vartapetian BB (1992) Induction of alcoholic and lactic fermentation in the early stages of anaerobic incubation of higher plants. Phytochemistry 31:1859–1861

    Article  CAS  Google Scholar 

  • Arbona V, Gomez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27:241–250

    Article  CAS  Google Scholar 

  • Armstrong W (1979) Aeration in higher plants. Adv Bot Res 7:225–332

    Article  CAS  Google Scholar 

  • Armstrong J, Armstrong W (2005) Rice: sulphide-induced barriers to root radial oxygen loss, Fe2+ and water uptake, and lateral root emergence. Ann Bot 96:625–638

    Article  PubMed  CAS  Google Scholar 

  • Arru L, Fornaciari S (2010) Root oxygen deprivation and leaf biochemistry in trees. In: Mancuso S, Shabala S (eds) Waterlogging signaling and tolerance in plants. Springer, Heidelberg, pp 181–195

    Chapter  Google Scholar 

  • Atkinson CJ, Harrison-Murray RS, Taylor JM (2008) Rapid flood-induced stomatal closure accompanies xylem sap transportation of root-derived acetaldehyde and ethanol in Forsythia. Environ Exp Bot 64:196–205

    Article  CAS  Google Scholar 

  • Babourina O, Rengel Z (2010) Ion transport in aquatic plants. In: Mancuso S, Shabala S (eds) Waterlogging signaling and tolerance in plants. Springer, Heidelberg, pp 221–238

    Chapter  Google Scholar 

  • Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signaling. Nature 448:938–942

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Chang R (2005) Sensing and signaling in response to oxygen deprivation in plants and other organisms. Ann Bot 96:507–518

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339

    Article  PubMed  CAS  Google Scholar 

  • Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, Voesenek LACJ, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17:129–138

    Article  PubMed  CAS  Google Scholar 

  • Baluška F, Kubica Š, Hauskrecht M (1990) Postmitotic ‘isodiametric’ cell growth in the maize root apex. Planta 181:269–274

    Article  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (1996) Specialized zones of development in roots: view from the cellular level. Plant Physiol 112:3–4

    PubMed  Google Scholar 

  • Baluška F, Volkmann D, Barlow PW (2001) A polarity crossroad in the transition growth zone of maize root apices: cytoskeletal and developmental implications. J Plant Growth Regul 20:170–181

    Article  Google Scholar 

  • Baluška F, Mancuso S, Volkmann D, Barlow PW (2010) Root apex transition zone: a signaling–response nexus in the root. Trends Plant Sci 15:402–408

    Article  PubMed  CAS  Google Scholar 

  • Banti V, Mafessoni F, Loreti E, Alpi A, Perata P (2010) The heat-inducible transcription factor HsfA2 enhances anoxia tolerance in Arabidopsis. Plant Physiol 152:1471–1483

    Article  PubMed  CAS  Google Scholar 

  • Barlow PW (2003) The root cap: cell dynamics, cell differentiation and cap function. J Plant Growth Regul 21:261–286

    Article  CAS  Google Scholar 

  • Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J (2002) RopGAP4- dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296:2026–2028

    Article  PubMed  CAS  Google Scholar 

  • Beerling D (2007) The emerald planet. How plants changed Earth’s history. Oxford University Press, New York

    Google Scholar 

  • Bell EL, Klimova TA, Eisenbart J, Moraes CT, Murphy MP, Budinger GRS, Chandel NS (2007) The Qo site of the mitochondrial complex III is required for the transduction of hypoxic signaling via reactive oxygen species production. J Cell Biol 177:1029–1036

    Article  PubMed  CAS  Google Scholar 

  • Benschop JJ, Jackson MB, Gühl K, Vreeburg RAM, Croker SJ, Peeters AJM, Voesenek LACJ (2005) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768

    Article  PubMed  CAS  Google Scholar 

  • Besson-Bard A, Pugin A, Wendehenne D (2008) New insights into nitric oxide signaling in plants. Annu Rev Plant Biol 59:21–39

    Article  PubMed  CAS  Google Scholar 

  • Birner PT, Steudel E (1993) Effects of anaerobic conditions on water and solute relations and on active transport in roots of maize (Zea mays L.). Planta 190:474–483

    Article  CAS  Google Scholar 

  • Blanke MM, Cooke DT (2004) Effects of flooding and drought on stomatal activity, transpiration, photosynthesis, water potential and water channel activity in strawberry stolons and leaves. Plant Growth Regul 42:153–160

    Article  CAS  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  PubMed  CAS  Google Scholar 

  • Borisjuk L, Rolletschek H (2008) Nitric oxide is a versatile sensor of low oxygen stress in plants. Plant Signal Behav 3:391–393

    Article  PubMed  Google Scholar 

  • Bradford KJ, Hsiao TC (1982) Stomatal behaviour and water relations of waterlogged tomato plants. Plant Physiol 70:1508–1513

    Article  PubMed  CAS  Google Scholar 

  • Braendle R, Crawford RMM (1999) Plants as amphibians. Perspect Plant Ecol Evol Syst 2:56–78

    Article  Google Scholar 

  • Bramley H, Tyerman S (2010) Root water transport under waterlogged conditions and the roles of aquaporins. In: Mancuso S, Shabala S (eds) Waterlogging signaling and tolerance in plants. Springer, Heidelberg, pp 151–180

    Chapter  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J (2005) Genomewide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660

    Article  PubMed  CAS  Google Scholar 

  • Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755

    Article  PubMed  CAS  Google Scholar 

  • Building MH (2001) Long-term anoxia tolerance in leaves of Acorus calamus L. and Iris pseudacorus L. J Exp Bot 52:2213–2225

    Google Scholar 

  • Burrows WJ, Carr DJ (1969) Effects of flooding root system of sunflower plants on cytokinin content in xylem sap. Physiol Plant 22:1105–1112

    Article  PubMed  CAS  Google Scholar 

  • Chang R, Jang CJH, Branco-Price C, Nghiem P, Bailey-Serres J (2012) Transient MPK6 activation in response to oxygen deprivation and reoxygenation is mediated by mitochondria and aids seedling survival in Arabidopsis. Plant Mol Biol 78:109–122

    Article  PubMed  CAS  Google Scholar 

  • Chen X, Pierik R, Peeters AJM, Poorter H, Visser EJ, Huber H, de Kroon H, Voesenek LACJ (2010) Endogenous ABA as a key switch for natural variation in flooding-induced shoot elongation. Plant Physiol 154:969–977

    Article  PubMed  CAS  Google Scholar 

  • Chirkova TV, Leffler S, Novitskaya LO (1995) Some peculiarities of chloroplast and mitochondria state in leaves of wheat and rice seedlings under conditions of anoxia and long-term darkness. Fiziol Rast (Moscow) 42:368–376 (Russ J Plant Physiol Eng Transl)

    Google Scholar 

  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Global gene expression responses to waterlogging in roots and leaves of Cotton (Gossypium hirsutum L.). Plant Cell Physiol 51:21–37

    Article  PubMed  CAS  Google Scholar 

  • Clark DG, Gubrium EK, Barrett JE, Nell TA, Klee HJ (1999) Root formation in ethylene-insensitive plants. Plant Physiol 121:53–60

    Article  PubMed  CAS  Google Scholar 

  • Colmer TD (2003) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 91:301–309

    Article  PubMed  CAS  Google Scholar 

  • Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681

    Article  Google Scholar 

  • Copolovici L, Niinemets U (2010) Flooding induced emissions of volatile signaling compounds in three tree species with differing waterlogging tolerance. Plant Cell Environ 33:1582–1594

    PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signaling during plant flooding. Plant Physiol Biochem 42:273–282

    Article  PubMed  CAS  Google Scholar 

  • De Pinto MC, Locato V, De Gara L (2012) Redox regulation in plant programmed cell death. Plant Cell Environ 35:234–244

    Article  PubMed  CAS  Google Scholar 

  • Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide, and nitric oxide signaling in stomatal guard cells. J Exp Bot 55:205–212

    Article  PubMed  CAS  Google Scholar 

  • Dordas C, Rivoal J, Hill RD (2003) Plant haemoglobins, nitric oxide and hypoxic stress. Ann Bot 91:173–178

    Article  PubMed  CAS  Google Scholar 

  • Dordas C, Hasinoff BB, Rivoal J, Hill RD (2004) Class I hemoglobins, nitrate and NO levels in hypoxic maize cell suspension cultures. Planta 219:66–72

    Article  PubMed  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard S (1979) Ethylene-promoted adventitious rooting and the development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147:83–88

    Article  CAS  Google Scholar 

  • Drew MC, Jackson MB, Giffard SC, Campbell R (1981) Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency. Planta 153:217–224

    Article  CAS  Google Scholar 

  • Ehlert C, Maurel C, Tardieu F, Simonneau T (2009) Aquaporin-mediated reduction in maize root hydraulic conductivity impacts cell turgor and leaf elongation even without changing transpiration. Plant Physiol 150:1093–1104

    Article  PubMed  CAS  Google Scholar 

  • Else MA, Jackson MB (1998) Transport of 1-aminocyclopropane-1- carboxylic acid (ACC) in the transpiration stream of tomato (Lycopersicon esculentum) in relation to foliar ethylene production and petiole epinasty. Aust J Plant Physiol 25:453–458

    Article  CAS  Google Scholar 

  • Else MA, Tiekstra AE, Croker SJ, Davies WJ, Jackson MB (1996) Stomatal closurein flooded tomato plants involves abscisic acid and a chemically unidentified anti-transpirant in xylem sap. Plant Physiol 112:239–247

    PubMed  CAS  Google Scholar 

  • Else MA, Coupland D, Dutton L, Jackson MB (2001) Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiol Plant 111:46–54

    Article  CAS  Google Scholar 

  • Else MA, Taylor JM, Atkinson CJ (2006) Anti-transpirant activity in xylem sap from flooded tomato (Lycopersicon esculentum Mill.) plants is not due to pH-mediated redistributions of root- or shoot-sourced ABA. J Exp Bot 57:3349–3357

    Article  PubMed  CAS  Google Scholar 

  • Else MA, Janowiak F, Atkinson CJ, Jackson MB (2009) Root signals and stomatal closure in relation to photosynthesis, chlorophyll a fl uorescence and adventitious rooting of flooded tomato plants. Ann Bot 103:313–323

    Article  PubMed  CAS  Google Scholar 

  • Ershova A, Popova N, Berdnikova O (2011) Production of reactive oxygen species and antioxidant enzymes of pea and soybean plants under hypoxia and high CO2 concentration in medium. Russ J Plant Physiol 58:982–990

    Article  CAS  Google Scholar 

  • Evans DE (2004) Aerenchyma formation. New Phytol 161:35–49

    Article  Google Scholar 

  • Everard JD, Drew MC (1989) Water relations of sunflower (Helianthus annuus L.) shoots during exposure of the root system to oxygen deficiency. J Exp Bot 40:1255–1264

    Article  Google Scholar 

  • Felle HH (2010) pH signaling during anoxia. In: Mancuso S, Shabala S (eds) Waterlogging signaling and tolerance in plants. Springer, Heidelberg, pp 79–98

    Chapter  Google Scholar 

  • Felle HH, Herrmann A, Hanstein S, Hückelhoven R, Kogel KH (2004) Apoplastic pH signaling in barley leaves attacked by the powdery mildew fungus Blumeria graminis f. sp. hordei. Mol Plant-Microbe Interact 17:118–123

    Article  PubMed  CAS  Google Scholar 

  • Felle HH, Herrman A, Hueckelhoven R, Kogel K-H (2005) Root-to-shoot signaling: apoplastic alkalinization, a general stress response and defence factor in barley (Hordeum vulgare). Protoplasma 227:17–24

    Article  PubMed  CAS  Google Scholar 

  • Fu XY, Peng SX, Yang S, Chen YH, Zhang JY, Mo WP, Zhu JY, Ye YX, Huang XM (2012) Effects of flooding on grafted annona plants of different scion/rootstock combinations. Agric Sci 3:249–256

    Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factorlike genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Sanchez F, Syvertsen JP, Gimeno V, Botia P, Perez-Perez JG (2007) Responses to flooding and drought stress by two citrus rootstock seedlings with different water-use efficiency. Physiol Plant 130:532–542

    Article  CAS  Google Scholar 

  • Geigenberger P (2003) Response of plant metabolism to too little oxygen. Curr Opin Plant Biol 6:247–256

    Article  PubMed  CAS  Google Scholar 

  • Geisler-Lee J, Caldwell C, Gallie DR (2010) Expression of the ethylene biosynthetic machinery in maize roots is regulated in response to hypoxia. J Exp Bot 61:857–871

    Article  PubMed  CAS  Google Scholar 

  • Graham LG (1996) Green algae to land plants: an evolutionary transition. J Plant Res 109:7737–7742

    Article  Google Scholar 

  • Gruntman M, Novoplansky A (2004) Physiologically mediated self/non-self discrimination in roots. Proc Natl Acad Sci USA 101:3863–3867

    Article  PubMed  CAS  Google Scholar 

  • Guzy RD, Schumacker PT (2006) Oxygen sensing by mitochondria at complex III: the paradox of increased reactive oxygen species during hypoxia. Exp Physiol 91:807–819

    Article  PubMed  CAS  Google Scholar 

  • Hasanuzzaman M, Gill SS, Fujita M (2012) Physiological role of nitric oxide in plants grown under adverse environmental conditions. In: Tuteja N, Gill SS (eds) Plant acclimation to environmental stress, Chap 11. Springer, New York

    Google Scholar 

  • Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 460:1026–1030

    Article  PubMed  CAS  Google Scholar 

  • He CJ, Morgan PW, Drew MC (1994) Induction of enzymes associated with lysigenous aerenchyma formation in roots of Zea mays during hypoxia or nitrogen starvation. Plant Physiol 105:861–865

    PubMed  CAS  Google Scholar 

  • Hinz M, Wilson IW, Yang J, Buerstenbinder K, Llewellyn D, Dennis ES, Sauter M, Dolferus R (2010) Arabidopsis RAP2.2: an ethylene response transcription factor that is important for hypoxia survival. Plant Physiol 144:218–231

    Google Scholar 

  • Hodges A (2009) Root decisions. Plant Cell Environ 32:628–640

    Article  Google Scholar 

  • Holzinger R, Sandoval-Soto L, Rottenberger S, Crutzen PJ, Kesselmeier J (2000) Emissions of volatile organic compounds from Quercus ilex L. measured by proton transfer reaction mass spectrometry under different environmental conditions. J Geophys Res 105:20573–20579

    Article  CAS  Google Scholar 

  • Igamberdiev AU, Hill RD (2004) Nitrate, NO and haemoglobin in plant adaptation to hypoxia: an alternative to classic fermentation pathways. J Exp Bot 55:2473–2482

    Article  PubMed  CAS  Google Scholar 

  • Igamberdiev AU, Baron K, Manaćh-Little N, Stoimenova M, Hill RD (2005) The haemoglobin/nitric oxide cycle: involvement in flooding stress and effects on hormone signaling. Ann Bot 96:557–564

    Article  PubMed  CAS  Google Scholar 

  • Illéš P, Schlicht M, Pavlovkin J, Lichtscheidl I, Baluška F, Ovečka M (2006) Aluminium toxicity in plants: internalisation of aluminium into cells of the transition zone in Arabidopsis root apices relates to changes in plasma membrane potential, endosomal behaviour, and nitric oxide production. J Exp Bot 57:4201–4213

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa H, Evans ML (1992) Induction of curvature in maize roots by calcium or by thigmostimulation. Role of postmitotic isodiametric growth zone. Plant Physiol 100:762–768

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB (2002) Long-distance signaling from roots to shoots assessed: the flooding story. J Exp Bot 53:175–181

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB, Hall KC (1987) Early stomatal closure in waterlogged pea plants is mediated by abscisic acid in the absence of foliar water deficits. Plant Cell Environ 10:121–130

    CAS  Google Scholar 

  • Jackson MB, Gales K, Campbell DJ (1978) Effect of waterlogged soil conditions on the production of ethylene and on water relationships in tomato plants. J Exp Bot 29:183–193

    Article  CAS  Google Scholar 

  • Jackson MB, Fenning TM, Drew MC, Saker LR (1985) Stimulation of ethylene production and gas-space (aerenchyma) formation in adventitious roots of Zea mays L. by small partial pressures of oxygen. Planta 165:486–492

    Article  CAS  Google Scholar 

  • Jackson MB, Young S, Hall KC (1988) Are roots a source of abscisic acid for the shoots of flooded pea plants? J Exp Bot 39:1631–1637

    Article  CAS  Google Scholar 

  • Jackson MB, Saker LR, Crisp CM, Else MA, Janowiak F (2003) Ionic and pH signaling from roots to shoots of flooded tomato plants in relation to stomatal closure. Plant Soil 253:103–113

    Article  CAS  Google Scholar 

  • Jackson MB, Ishizawa K, Ito O (2009) Evolution and mechanisms of plant tolerance to flooding stress. Ann Bot 103:137–142

    Article  PubMed  CAS  Google Scholar 

  • Janowiak F, Else MA, Jackson MB (2002) A loss of photosynthetic efficiency does not explain stomatal closure in flooded tomato plants. In: Advances of agricultural sciences problem issues, Issue 481. Ecophysiological aspects of plants responses to stress factors. Polish Academy of Sciences, Warsaw, pp 229–234

    Google Scholar 

  • Jia WS, Davies WJ (2007) Modification of leaf apoplastic pH in relation to stomatal sensitivity to root-sourced ABA signals. Plant Physiol 143:68–77

    Article  PubMed  CAS  Google Scholar 

  • Jung KH, Seo YS, Walia H, Cao P, Fukao T, Canlas PE, Amonpant F, Bailey-Serres J, Ronald PC (2010) The submergence tolerance regulator Sub1A mediates stress-responsive expression of AP2/ERF transcription factors. Plant Physiol 152:1674–1692

    Article  PubMed  CAS  Google Scholar 

  • Kasprowicz A, Szuba A, Volkmann D, Baluška F, Wojtaszek F (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  PubMed  CAS  Google Scholar 

  • Kawase M (1981) Anatomical and morphological adaptation of plants to waterlogging. Hortic Sci 16:30–34

    CAS  Google Scholar 

  • Kende H, van der Knaap E, Cho H-T (1998) Deepwater rice: a model plant to study stem elongation. Plant Physiol 118:1105–1110

    Article  PubMed  CAS  Google Scholar 

  • Kieffer M, Neve J, Kepinski S (2009) Defining auxin response contexts in plant development. Curr Opin Plant Biol 13:12–20

    Article  PubMed  CAS  Google Scholar 

  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494

    Article  PubMed  CAS  Google Scholar 

  • Konings H (1982) Ethylene-promoted formation of aerenchyma in seedling roots of Zea mays L. under aerated and non-aerated conditions. Physiol Plant 54:119–124

    Article  CAS  Google Scholar 

  • Kozlowski TT (1984) Responses of woody plants to flooding. In: Kozlowski TT (ed) Flooding and plant growth. Academic, New York, pp 129–163

    Google Scholar 

  • Kramer PJ (1940) Causes of decreased absorption of water by plants in poorly aerated media. Am J Bot 27:216–220

    Article  CAS  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  PubMed  CAS  Google Scholar 

  • Kumar B, Pandey DM, Goswami CL, Jain S (2004) Effect of growth regulators on photosynthesis, transpiration and related parameters in water stressed cotton. Biol Plant 44:475–478

    Article  Google Scholar 

  • Kumutha D, Ezhilmathi K, Sairam RK, Srivastava GC, Deshmukh PS, Meena RC (2009) Waterlogging induced oxidative stress and antioxidant activity in pigeonpea genotypes. Biol Plant 53:75–84

    Article  CAS  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  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Lasanthi-Kudahettige R, Magneschi L, Loreti E, Gonzali S, Licausi F, Novi G, Beretta O, Vitulli F, Alpi A, Perata P (2007) Transcript profiling of the anoxic rice coleoptile. Plant Physiol 144:218–231

    Article  PubMed  CAS  Google Scholar 

  • Lecourieux D, Ranjeva R, Pugin A (2006) Calcium in plant defence signaling pathways. New Phytol 171:249–269

    Article  PubMed  CAS  Google Scholar 

  • Lee KW, Chen PW, Lu CA, Chen S, Ho THD, Yu SM (2009) Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding. Sci Signal 2:ra61

    Google Scholar 

  • Lee SC, Mustroph A, Sasidharan R, Vashisht D, Pedersen O, Oosumi T, Voesenek LACJ, Bailey-Serres J (2011) Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia. New Phytol 190:457–471

    Article  PubMed  CAS  Google Scholar 

  • Leterrier M, Valderrama R, Chaki M, Airaki M, Palma JM, Barroso JB, Corpas FJ (2012) Function of nitric oxide under environmental stress conditions. In: Khan NA, Nazar R, Iqbal N, Anjum NA (eds) Phytohormones and abiotic stress tolerance in plants. Springer, Berlin, pp 99–113

    Chapter  Google Scholar 

  • Licausi F (2011) Regulation of the molecular response to oxygen limitations in plants. New Phytol 190:550–555

    Article  PubMed  CAS  Google Scholar 

  • Licausi F, van Dongen JT, Giuntoli B, Novi G, Santaniello A, Geigenberger P, Perata P (2010) HRE1 and HRE2, two hypoxia-inducible ethylene response factors, affect anaerobic responses in Arabidopsis thaliana. Plant J 62:302–315

    Article  PubMed  CAS  Google Scholar 

  • Licausi F, Kosmacz M, Weits DA, Giuntoli B, Giorgi FM, Voesenek LACJ, Perata P, van Dongen JT (2011) Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization. Nature 479:419–422

    Article  PubMed  CAS  Google Scholar 

  • Limami AM, Glévarec G, Ricoult C, Cliquet JB, Planchet E (2008) Concerted modulation of alanine and glutamate metabolism in young Medicago truncatula seedlings under hypoxic stress. J Exp Bot 59:2325–2335

    Article  PubMed  CAS  Google Scholar 

  • Liu F, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    Article  PubMed  CAS  Google Scholar 

  • Lombardo MC, Graziano M, Polacco JC, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Signal Behav 1:28–33

    Article  PubMed  Google Scholar 

  • Loreti E, Poggi A, Novi G, Alpi A, Perata P (2005) A genome-wide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiol 137:1130–1138

    Article  PubMed  CAS  Google Scholar 

  • Magneschi L, Perata P (2009) Rice germination and seedling growth in the absence of oxygen. Ann Bot 103:181–196

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S, Boselli M (2002) Characterisation of the oxygen fluxes in the division, elongation and mature zones of Vitis roots: influence of oxygen availability. Planta 214:767–774

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S, Marras AM (2006) Adaptative response of Vitis root to anoxia. Plant Cell Physiol 47:401–409

    Article  PubMed  CAS  Google Scholar 

  • Mancuso S, Marras AM, Mugnai S, Schlicht M, Žársky V, Li G, Song L, Xue HW, Baluška F (2007) Phospholipase Dz2 drives vesicular secretion of auxin for its polar cell-cell transport in the transition zone of the root apex. Plant Signal Behav 2:240–244

    Article  PubMed  Google Scholar 

  • Manetas Y (2012) Short evolutionary history of plants. In: Manetas Y (ed) Alice in the land of plants: biology of plants and their importance for planet earth. Springer, Berlin, pp 113–160

    Chapter  Google Scholar 

  • Marciano DPRO, Toledo-Ramos F, Neiva-Alvim M, Magalhaes JR, Costa Franca MG (2010) Nitric oxide reduces the stress effects of aluminum on the process of germination and early root growth of rice. J Plant Nutr Soil Sci 173:885–891

    Article  CAS  Google Scholar 

  • Masi E, Ciszak M, Stefano G, Renna L, Azzarello E, Pandolfi C, Mugnai S, Baluška F, Arecchi FT, Mancuso S (2009) Spatio-temporal dynamics of the electrical network activity in the root apex. Proc Natl Acad Sci USA 106:4048–4053

    Article  PubMed  CAS  Google Scholar 

  • Miller G, Mittler R (2006) Could heat shock transcription factors function as hydrogen peroxide sensors in plants? Ann Bot 98:279–288

    Article  PubMed  CAS  Google Scholar 

  • Mugnai S, Marras AM, Mancuso S (2011) Effect of hypoxic acclimation on anoxia tolerance in Vitis roots: response of metabolic activity and K+ fluxes. Plant Cell Physiol 52:1107–1116

    Article  PubMed  CAS  Google Scholar 

  • Mugnai S, Azzarello E, Baluška F, Mancuso S (2012) Local root apex hypoxia induces no-mediated hypoxic acclimation of the entire root. Plant Cell Physiol 53:912–920

    Article  PubMed  CAS  Google Scholar 

  • Muhlenbock P, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by Lesion Simulating Disease1. Plant Cell 19:3819–3830

    Article  PubMed  CAS  Google Scholar 

  • Mustroph A, Lee SC, Oosumi T, Zanetti ME, Yang H, Ma K, Yaghoubi-Masihi A, Fukao T, Bailey-Serres J (2010) Cross-kingdom comparison of transcriptomic adjustments to low-oxygen stress highlights conserved and plant-specific responses. Plant Physiol 152:1484–1500

    Article  PubMed  CAS  Google Scholar 

  • Nakano T, Suzuki K, Fujimura T, Shinshi H (2006) Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol 140:411–432

    Article  PubMed  CAS  Google Scholar 

  • 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 61:3–15

    Article  PubMed  CAS  Google Scholar 

  • Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35

    Article  CAS  Google Scholar 

  • Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. J Exp Bot 59:165–176

    Article  PubMed  CAS  Google Scholar 

  • Neuman DS, Smith BA (1991) The influence of leaf water status and ABA on leaf growth and stomata of Phaseolus seedlings with hypoxic roots. J Exp Bot 42:1499–1506

    Article  CAS  Google Scholar 

  • Ober ES, Sharp RE (2003) Electrophysiological responses of maize roots to low water potentials: relationship to growth and ABA accumulation. J Exp Bot 54:813–824

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Pauly N, Pucciariello C, Mandon K, Innocenti G, Jamet A, Baudouin E, Herouart D, Frendo P, Puppo A (2006) Reactive oxygen and nitrogen species and glutathione: key players in the legume- Rhizobium symbiosis. J Exp Bot 57:1769–1776

    Article  PubMed  CAS  Google Scholar 

  • Peeters AJM, Cox MCH, Benschop JJ, Vreeburg RAM, Bou J, Voesenek LACJ (2002) Submergence research using Rumex palustris as a model; looking back and going forward. J Exp Bot 53:391–398

    Article  PubMed  CAS  Google Scholar 

  • Perata P, Alpi A (1993) Plant responses to anaerobiosis. Plant Sci 93:1–17

    Article  CAS  Google Scholar 

  • Pereira JS, Kozlowski TT (1977) Variations among woody angiosperms in response to flooding. Physiol Plant 45:184–192

    Article  Google Scholar 

  • Pospíšilová J (2003) Participation of phytohormones in the stomatal regulation of gas exchange during water stress. Biol Plant 46:491–506

    Article  Google Scholar 

  • Prado AM, Porterfield DM, Feijo JA (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714

    Article  PubMed  CAS  Google Scholar 

  • Prado AM, Colaco R, Moreno N, Silva AC, Feijo JA (2008) Targeting of pollen tubes to ovules is dependent on nitric oxide(NO) signaling. Mol Plant 1:703–714

    Article  PubMed  CAS  Google Scholar 

  • Pucciariello C, Perata P (2012) Flooding tolerance in plants. In: Shabala S (ed) Plant stress physiology. CAB International, Oxford, pp 148–171

    Chapter  Google Scholar 

  • Pucciariello C, Parlanti S, Banti V, Novi G, Perata P (2012) Reactive oxygen species-driven transcription in Arabidopsis under oxygen deprivation. Plant Physiol 159:184–196

    Article  PubMed  CAS  Google Scholar 

  • Rascio N, Mariani P, Dalla Vecchia F, Zanchin A, Pool A, Larcher W (1994) Ultrastructural and photosynthetic features of leaves and stems of Elodea canadensis. J Plant Physiol 144:314–323

    Article  CAS  Google Scholar 

  • Ratcliffe RG (1997) In vivo NMR studies of the metabolic response of plant tissue to anoxia. Ann Bot 79:39–48

    Article  CAS  Google Scholar 

  • Raven JA (1996) Into the voids: the distribution, function, development and maintenance of gas spaces in plants. Ann Bot 78:137–142

    Article  Google Scholar 

  • Reid DM, Crozier A, Harvey BMR (1969) Effects of flooding on export of gibberellins from root to shoot. Planta 89:376–379

    Article  CAS  Google Scholar 

  • Ricard B, Couee I, Raymond P, Saglio PH, Saint-Ges V, Pradet A (1994) Plant metabolism under hypoxia and anoxia. Plant Physiol Biochem 32:1–10

    CAS  Google Scholar 

  • Ricoult C, Echeverria LO, Cliquet JB, Limami AM (2006) Characterization of alanine aminotransferase (AlaAT) multigene family and hypoxic response in young seedlings of the model legume Medicago truncatula. J Exp Bot 57:3079–3089

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez-Gamir J, Ancillo G, González-Mas MC, Primo-Millo E, Iglesias DJ, Forner-Giner MA (2011) Root signaling and modulation of stomatal closure in flooded citrus seedlings. Plant Physiol Biochem 49:636–645

    Article  PubMed  CAS  Google Scholar 

  • Rottenberger S, Kleiss B, Kuhn U, Wolf A, Piedade MTF, Junk W, Kesselmeier J (2008) The effect of flooding on the exchange of the volatile C2-compounds ethanol, acetaldehyde and acetic acid between leaves of Amazonian floodplain tree species and the atmosphere. Biogeosciences 5:1085–1100

    Article  CAS  Google Scholar 

  • Sairam RK, Kumutha D, Ezhilmathi K, Deshmukh PS, Srivastava GC (2008) Physiology and biochemistry of waterlogging tolerance in plants. Biol Plant 52:401–412

    Article  CAS  Google Scholar 

  • Salmi ML, Morris KE, Roux SJ, Porterfield DM (2007) Nitric oxide and cGMP signaling in calcium-dependent development of cell polarity in Ceratopteris richardii. Plant Physiol 144:94–104

    Article  PubMed  CAS  Google Scholar 

  • Santosa IE, Ram PC, Boamfa EI, Laarhoven LJ, Reuss J, Jackson MB, Harren FJM (2006) Patterns of peroxidative ethane emission from submerged rice seedlings indicate that damage from reactive oxygen species takes place during submergence and is not necessarily a postanoxic phenomenon. Planta 226:193–202

    Article  PubMed  CAS  Google Scholar 

  • Sedbrook JC, Kronebush PJ, Borisy GG, Trewavas AJ, Masson P (1996) Transgenic aequorin reveals organ specific cytosolic Ca2+ responses to anoxia in Arabidopsis thaliana seedlings. Plant Physiol 111:243–257

    Article  PubMed  CAS  Google Scholar 

  • Sobol M, Kordyum E (2009) Distribution of calcium ions in cells of the root distal elongation zone under clinorotation. Microgravity Sci Technol 21:179–185

    Article  CAS  Google Scholar 

  • Sorrell BK, Brix H, Orr PT (1997) Eleocharis sphacelata: internal gas transport pathways and modelling of aeration by pressurized flow and diffusion. New Phytol 136:433–442

    Article  Google Scholar 

  • Subbaiah CC, Bush DS, Sachs MM (2000) Elevation of cytosolic calcium precedes anoxic gene expression in maize suspension-cultured cells. Plant Cell 6:1747–1762

    Google Scholar 

  • Sun BT, Jing Y, Chen KM, Song LL, Chen FJ, Zhang LX (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543

    Article  PubMed  CAS  Google Scholar 

  • Tournaire-Roux C, Sutka M, Javot H, Gout E, Gerbeau P, Luu DT, Bligny R, Maurel C (2003) Cytosolic pH regulates root water transport during anoxic stress through gating of aquaporins. Nature 425:393–397

    Article  PubMed  CAS  Google Scholar 

  • Trewavas A (2009) What is plant behavior? Plant Cell Environ 32:606–616

    Article  PubMed  Google Scholar 

  • van Dongen JT, Frohlich A, Ramirez-Aguilar SJ, Schauer N, Fernie AR, Erban A, Kopka J, Clark J, Langer A, Geigenberger P (2008) Transcript and metabolite profiling of the adaptive response to mild decreases in oxygen concentration in the roots of Arabidopsis plants. Ann Bot 103:269–280

    Article  PubMed  CAS  Google Scholar 

  • Vandenbroucke K, Robbens S, Vandepoele K, Inzé D, Van de Peer Y, Van Breusegem F (2008) Hydrogen peroxide-induced gene expression across kingdoms: a comparative analysis. Mol Biol Evol 25:507–516

    Article  PubMed  CAS  Google Scholar 

  • Verbelen J, Cnodder T, Le J, Vissenberg K, Baluška F (2006) Root apex of Arabidopsis thaliana consists of four distinct zones of growth activities: meristematic zone, transition zone, fast elongation zone, and growth terminating zone. Plant Signal Behav 1:296–304

    Article  PubMed  Google Scholar 

  • Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562

    Article  PubMed  CAS  Google Scholar 

  • Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245

    Article  Google Scholar 

  • Voesenek LACJ, Pierik R (2008) Plant stress profiles. Science 320:880–881

    Article  PubMed  CAS  Google Scholar 

  • Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassiatora L. Plant Cell Physiol 46:1915–1923

    Article  PubMed  CAS  Google Scholar 

  • Wang Y, Chen T, Zhang C, Hao H, Liu P, Zheng M, Baluška F, Šamaj J, Lin J (2009) Nitric oxide modulates the influx of extracellular Ca2+ and actin filament organization during cell wall construction in Pinus bungeana pollen tubes. New Phytol 182:851–862

    Article  PubMed  CAS  Google Scholar 

  • Wilkinson S (1999) pH as a stress signal. Plant Growth Regul 29:87–99

    Article  CAS  Google Scholar 

  • Winch S, Pritchard J (1999) Acid-induced cell wall loosening is confined to the accelerating region of the root growing zone. J Exp Bot 50:1481–1487

    CAS  Google Scholar 

  • Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708

    Article  PubMed  CAS  Google Scholar 

  • Xu ZS, Xia LQ, Chen M, Cheng XG, Zhang RY, Li LC, Zhao YX, Lu Y, Ni ZY, Liu L, Qiu ZG, Ma YZ (2007) Isolation and molecular characterization of the Triticum aestivum L. ethylene-responsive factor 1 (TaERF1) that increases multiple stress tolerance. Plant Mol Biol 65:719–732

    Article  PubMed  CAS  Google Scholar 

  • Yang Z, Fu Y (2007) ROP/RAC GTPase signaling. Curr Opin Plant Biol 10:490–494

    Article  PubMed  CAS  Google Scholar 

  • Yang CY, Hsu FC, Li JP, Wang NN, Shih MC (2011) The AP2/ERF transcription factor AtERF73/HRE1 modulates ethylene responses during hypoxia in Arabidopsis. Plant Physiol 156:202–212

    Article  PubMed  CAS  Google Scholar 

  • Zhang J, Zhang X (1994) Can early wilting of old leaves account for much of the ABA accumulation in flooded leaves? J Exp Bot 45:1335–1342

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Stefano Mancuso .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2013 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Arru, L., Fornaciari, S., Mancuso, S. (2013). Oxygen Deficiency-Induced Root-to-Shoot Communication. In: Baluška, F. (eds) Long-Distance Systemic Signaling and Communication in Plants. Signaling and Communication in Plants, vol 19. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-36470-9_6

Download citation

Publish with us

Policies and ethics