Accumulation and scavenging of reactive oxygen species and nitric oxide correlate with stigma maturation and pollen–stigma interaction in sunflower

• Autorzy: Sharma B. , Bhatla S. C.
• Języki publikacji: EN

Abstrakty

EN

During the course of stigma development in sunflower (bud, staminate and pistillate stages), correlation is evident among the accumulation of reactive oxygen species (ROS), nitric oxide (NO), and the activities of ROS scavenging enzymes [superoxide dismutase (SOD) and peroxidase (POD)]. Confocal image analysis shows a gradual increase in ROS and NO accumulation in the stigmatic papillae, which may provide immunity to the developing stigma and function as signalling molecules. A novel, NO-specific probe (MNIP-Cu) has been employed for the detection and quantification of intracellular NO. Mn-SOD (mitochondrial) and Cu/Zn-SOD (cytoplasmic) exhibit differential expression during the staminate stage of stigma development. An increase in total SOD activity at the staminate stage is followed by a peak of POD activity during pistillate stage, thereby indicating the sequential action of the two enzymes in scavenging ROS. An increase in the number of POD isoforms is observed with the passage of stigma development (from three at bud stage to seven at pistillate stage), and two POD isoforms are unique to pistillate stage, thereby highlighting their role in ROS scavenging mechanism. ROS and NO accumulation exhibit reverse trends during pollen–stigma interaction.

• Wydawca: -
• Czasopismo: Acta Physiologiae Plantarum
• Rocznik: 2013
• Tom: 35
• Numer: 09
• Opis fizyczny: p.2777-2787,fig.,ref.

Twórcy

autor

Sharma B.

autor

Bhatla S. C.

Bibliografia

• Abu-Soud HM, Hazen SL (2000) Nitric oxide a physiological substrate for mammalian peroxidase. J Biol Chem 248:37524–37532
• Alba CM, de Forchetti SM, Quesada MA, Valpuesta V, Tigier HA (1998) Localization and general properties of developing peach seed coat and endosperm peroxidase isoenzymes. J Plant Growth Regul 17:7–11
• Allen AM, Thorogood CJ, Hegarty MJ, Lexer C, Hiscock SJ (2011) Pollen-pistil interactions and self-incompatibility in Asteraceae: new insights from studies of Senecio squalidus (Oxford ragwort). Ann Bot 108:687–698
• Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399
• Asai S, Mase K, Yoshioka H (2010) Role of nitric oxide and reactive oxygen species in disease resistance to necrotrophic pathogens. Plant Signal Behav 5:872–874
• Barceló AR (1998) Hydrogen peroxide production is a general property of the lignifying xylem from vascular plants. Ann Bot 82:97–103
• Baroncelli S, Lercari B, Cecconi F, Pugliesi C (1990) Light control of elongation of filament in sunflower (Helianthus annuus L.). Photochem Photobiol 52:229–231
• Beauchamp C, Fridovich I (1971) Superoxide dismutase: improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287
• Beltramo C, Marinoni DT, Perrone I, Botta R (2012) Isolation of a gene encoding for a class III peroxidase in female flower of Corylus avellana L. Mol Biol Rep 39:4997–5008
• Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
• Bredemeijer GMM (1984) The role of peroxidases in pistil-pollen interactions. Theor Appl Genet 68:193–206
• Bright J, Hiscock SJ, James PE, Hancock JT (2009) Pollen generates nitric oxide and nitrate: a possible link to pollen-induced allergic responses. Plant Physiol Biochem 47:49–55
• Carter C, Thornburg RW (2004) Is the nectar redox cycle a floral defense against microbial attack? Trends Plant Sci 9:320–324
• Carter C, Healy R, O‘Tool NM, Naqvi SMS, Ren G, Park S, Beattie GA, Horner HT, Thornburg RW (2007) Tobacco nectarines express a novel NADPH oxidase implicated in the defense of floral reproductive tissues against microorganisms. Plant Physiol 143:389–399
• Cosio C, Dunand C (2009) Specific functions of individual class III peroxidase genes. J Exp Bot 60:391–408
• Courtois C, Besson A, Dahan J, Bourque S, Dobrowolska G, Pugin A, Wendehenne D (2008) Nitric oxide signaling in plants: interplays with Ca2+ and protein kinases. J Exp Bot 59:155–163
• Dafni A, Maués MM (1998) A rapid and simple procedure to determine stigma receptivity. Sex Plant Reprod 11:177–180
• De Rafael MA, Valle T, Babiano MJ, Corchete P (2001) Correlation of resistance and H2O2 production in Ulmus pumila and Ulmus campestris cell suspension cultures inoculated with Ophiostoma novo-ulmi. Physiol Plant 111:512–518
• Gadjev I, Stone JM, Gechev TS (2008) Programmed cell death in plants: new insights into redox regulation and the role of hydrogen peroxide. Intl Rev Cell Mol Biol 270:87–144
• Galen C, Plowright RC (1987) Testing the accuracy of using peroxidase activity to indicate stigma receptivity. Can J Bot 65:107–111
• Hiscock SJ, Bright J, McInnis SM, Desikan R, Hancock JT (2007) Signaling on the stigma: Potential new roles for ROS and NO in plant cell signaling. Plant Signal Behav 2:23–24
• Hong L, Shen H, Ye W, Cao H, Wang Z (2008) Secondary pollen presentation and style morphology in the invasive weed Mikania micrantha in South China. Bot Stud 49:253–260
• Howell GJ, Slater AT, Knox RB (1993) Secondary pollen presentation in angiosperms and its biological significance. Aust J Bot 41:417–438
• Jubany-Marı T, Munné-Bosch S, Alegre L (2010) Redox regulation of water stress responses in field-grown plants. Role of hydrogen peroxide and ascorbate. Plant Physiol Biochem 48:351–358
• Karuppanapandian T, Moon J, Kim C, Manoharan, Kim W (2011) Reactive oxygen species in plants: their generation, signal transduction and scavenging mechanism. Aust J Crop Sci 5:709–725
• Koning RE (1983) The roles of plant hormones in style and stigma growth in Gaillardia grandiflora (Asteraceae). Am J Bot 70:978–986
• Manna P, Bhattacharyya S, Das J, Ghosh J, Sill PC (2011) Phytomedical role of Pithecellobium dulse against CCl4 mediated hepatic oxidative impairments and nectrotic cell death. Evid Based Complement Alternat Med 832805 doi: 10.1093/ecam/neq065
• McInnis SM, Costa LM, Gutiérrez-Marcos JF, Henderson CA, Hiscock SJ (2005) Isolation and characterization of a polymorphic stigma-specific class III peroxidase gene from Senecio squalidus L. (Asteraceae). Plant Mol Biol 57:659–677
• McInnis SM, Desikan R, Hancock JT, Hiscock SJ (2006a) Production of reactive oxygen species and reactive nitrogen species by angiosperm stigmas and pollen: potential signaling crosstalk? New Phytol 172:221–228
• McInnis SM, Emery DC, Porter R, Desikan R, Hancock JT, Hiscock SJ (2006b) The role of stigma peroxidases in flowering plants: insights from further characterization of stigma-specific peroxidase (SSP) from Senecio squalidus (Asteraceae). J Exp Bot 57:1835–1846
• Miller G, Suzuki N, Ciftci-Yilmaz S, Mittler R (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467
• Mittler R, Vanderauwera S, Suzuki N, Miller G, Tognetti VB, Vandepoele K, Gollery M, Shulaev V, Breusegem FV (2011) ROS signaling: the new wave? Trends Plant Sci 16:300–309
• Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signaling in plants. New Phytol 159:11–35
• Orozco-Cárdenas ML, Narváez-Vásquez J, Ryan CA (2001) Hydrogen peroxide acts as a second messenger for the induction of defense genes in tomato plants in response to wounding, systemin, and methyl jasmonate. Plant Cell 13:179–191
• Ouyang J, Hong H, Shen C, Zhao Y, Ouyang C, Dong L, Zhu J, Guo Z, Zeng K, Chen J, Zhang C, Zhang J (2008) A novel fluorescent probe for the detection of nitric oxide in vitro and in vivo. Free Radical Biol Med 45:1426–1436
• Passardi F, Penel C, Dunand C (2004) Performing the paradoxical: how plant peroxidases modify the cell wall. Trends Plant Sci 9:534–540
• Piterková J, Luhová L, Mieslerová A, Petřivalskỳ (2013) Nitric oxide and reactive oxygen species regulate the accumulation of heat shock proteins in tomato leaves in response to heat shock and pathogen infection. Plant Sci 207:57–65
• Planchet E, Kaiser WM (2006) Nitric oxide production in plants: facts and fictions. Plant Signal Behav 1:46–51
• Prado AM, Porterfield DM, Feijó (2004) Nitric oxide is involved in growth regulation and re-orientation of pollen tubes. Development 131:2707–2714
• Prochazkova D, Sairam RD, Srivastava GC, Singh DV (2001) Oxidative stress and antioxidant activity as the basis of senescence in maize leaves. Plant Sci 161:765–771
• Quan L, Zhang B, Shi W, Li H (2008) Hydrogen peroxide in plants: a versatile molecule of reactive oxygen species network. J Integr Plant Biol 50:2–18
• Sammataro D, Garment MB, Erickson Jr. EH (1985) Anatomical features of the sunflower floret. Helia (FAO, Romania): 25–31
• Sanchez AM, Bosch M, Bots M, Nieuwland J, Feron R, Mariani C (2004) Pistil factors controlling pollination. Plant Cell 16:S98–S106
• Schneiter AA, Miller JF (1981) Description of sunflower growth stages. Crop Sci 21:901–903
• Seligman K, Saviani EE, Oliveira HC, Pinto-Maglio CAF, Salgado I (2008) Floral transition and nitric oxide emission during flower development in Arabidopsis thaliana is affected in nitrate reductase-deficient plants. Plant Cell Physiol 49:1112–1121
• Serrano I, Romero-Puertas MC, Rodriguez-Serrano M, Sandalio LM, Olmedilla A (2012a) Role of peroxynitrite in programmed cell death induced in self-incompatible pollen. Plant Signal Behav 7:1–3
• Serrano I, Romero-Puertas MC, Rodriguez-Serrano M, Sandalio LM, Olmedilla A (2012b) Peroxynitrite mediates programmed cell death both in papillar cells and in self-incompatible pollen in the olive (Olea europaea L.). J Exp Bot 63:1479–1493
• Shine MB, Guruprasad KN, Anand A (2012) Effect of stationary magnetic field strengths of 150 and 200mT on reactive oxygen species production in soybean. Bioelectromagnetics 33:428–437
• Smirnova AV, Matveyeva NP, Polesskaya OG, Yermakov IP (2009) Generation of reactive oxygen species during pollen grain germination. Russ J Dev Biol 40:345–353
• Speranza A, Crinelli R, Scoccianti V, Geitmann A (2012) Reactive oxygen species are involved in pollen tube initiation in kiwifruit. Plant Biol 14:64–76
• Tripathi SM, Singh KP (2008) Hybrid seed production in detergentinduced male sterile Helianthus annuus L. Helia 31:103–111
• Wang YY (2006) Occurrence and characterization of superoxide dismutases in female reproductive structures of Petunia. M.Sc. Thesis. University of Canterbury, New Zealand
• Wilson ID, Hiscock SJ, James PE, Hancock JT (2009) Nitric oxide and nitrite are likely mediators of pollen interactions. Plant Signal Behav 4:416–418
• Yadav MK, Bhatla SC (2011) Localization of lipoxygenase activity on the oil bodies in protoplasts using a novel fluorescence imaging method. Plant Physiol Biochem 49:230–234
• Yadav S, David A, Basuška F, Bhatla SC (2013) Rapid auxin-induced nitric oxide accumulation and subsequent tyrosine nitration of proteins during adventitious root formation in sunflower hypocotyls. Plant Signal Behav doi. doi:10.4161/psb23196
• Zafra A, Rodriguez-Garcia MI, Alché JD (2010) Cellular localization of ROS and NO in olive reproductive tissues during flower development. Plant Biol 10:36
• Zhang X, Zhang L, Dong FC, Gao JF, Galbraith DW, Song CP (2001) Hydrogen peroxide is involved in abscisic acid-induced stomatal closure in Vicia faba. Plant Physiol 126:1438–1448

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