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A response of the imbibed dormant red rice caryopsis to biotic challenges involves extracellular pH increase to elicit superoxide production

Published online by Cambridge University Press:  24 July 2018

Sepideh Ghotbzadeh  and
Alberto Gianinetti
Sepideh Ghotbzadeh
Affiliation:
Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan University of Technology, Isfahan, PO Box 84156–83111, Iran
Alberto Gianinetti*
Affiliation:
Council for Agricultural Research and Economics – Research Centre for Genomics and Bioinformatics, via S. Protaso 302, 29017 Fiorenzuola D'Arda (PC), Italy
*
Author for correspondence: Alberto Gianinetti, Email: [email protected]
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Abstract

Seeds often survive in the soil in a dormant state, but their persistence is endangered by micro-organisms that could feed on them. Seed–microbe interactions in the soil are, however, poorly understood. We used dormant caryopses of red rice to study the defence response induced by pronase, a mixture of proteases secreted by Streptomyces griseus, a non-pathogenic bacterium. Pronase was shown to activate the plant immune reaction, indicating that its activity was recognized as a potential microbial attack. The defence reaction included extracellular alkalinization and superoxide production, and the former was necessary to activate the latter, since buffering at pH 6 inhibited the oxidative burst. Alkalinization was sufficient to trigger the oxidative burst, as superoxide production increased when caryopses were incubated in buffered solutions of increasing pH without pronase. Release of proanthocyanidins was observed, with or without pronase. These diverse mechanisms are hypothesized to cooperate in reinforcing seed protection. Finally, time profiles of superoxide production by dormant and non-dormant red rice caryopses during imbibition did not support a relationship between extracellular superoxide and dormancy breaking or germination. Thus, the role of this reactive oxygen species in red rice imbibed caryopses appears to be essentially aimed at defence against attacks by challenging micro-organisms.

Keywords

dormant seedextracellular alkalinizationOryza sativa f. spontaneaproanthocyanidinspronaseseed persistenceweedy rice
Type
Research Paper
Information
Seed Science Research , Volume 28 , Issue 4 , December 2018 , pp. 261 - 271
Copyright
Copyright © Cambridge University Press 2018 

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References

Able, AJ, Guest, DI and Sutherland, MW (1998) Use of a new tetrazolium-based assay to study the production of superoxide radicals by tobacco cell cultures challenged with avirulent zoospores of Phytophthora parasitica var nicotianae. Plant Physiology 117, 491–499. doi: 10.1104/pp.117.2.491Google Scholar
Alhasan, R and Njus, D (2008) The epinephrine assay for superoxide: why dopamine does not work. Analytical Biochemistry 381, 142–147. doi: 10.1016/j.ab.2008.06.030Google Scholar
Alkan, N, Davydov, O, Sagi, M, Fluhr, R and Prusky, D (2009) Ammonium secretion by Colletotrichum coccodes activates host NADPH oxidase activity enhancing host cell death and fungal virulence in tomato fruits. Molecular Plant-Microbe Interactions 22, 1484–1491. doi: 10.1094/MPMI-22-12-1484Google Scholar
Altunkaya, A, Gökmen, V and Skibsted, LH (2016) pH dependent antioxidant activity of lettuce (L. sativa) and synergism with added phenolic antioxidants. Food Chemistry 190, 25–32. doi: 10.1016/j.foodchem.2015.05.069Google Scholar
Antony-Babu, S and Goodfellow, M (2008) Biosystematics of alkaliphilic streptomycetes isolated from seven locations across a beach and dune sand system. Antonie van Leeuwenhoek 94, 581–591. doi: 10.1007/s10482-008-9277-4Google Scholar
Barna, B, Fodor, J, Harrach, BD, Pogány, M and Király, Z (2012) The Janus face of reactive oxygen species in resistance and susceptibility of plants to necrotrophic and biotrophic pathogens. Plant Physiology and Biochemistry 59, 37–43. doi: 10.1016/j.plaphy.2012.01.014Google Scholar
Baz, M, Tran, D, Kettani-Halabi, M, Samri, SE, Jamjari, A, Biligui, B, Meimoun, P, El-Maarouf-Bouteau, H, Garmier, M, Saindrenan, P, Ennaji, MM, Barakate, M and Bouteau, F (2012) Calcium- and ROS-mediated defence responses in BY2 tobacco cells by nonpathogenic Streptomyces sp. Journal of Applied Microbiology 112, 782–792. doi: 10.1111/j.1365-2672.2012.05248.xGoogle Scholar
Beyer, WF and Fridovich, I (1989) Characterization of a superoxide dismutase mimic prepared from desferrioxamine and MnO2. Archives of Biochemistry and Biophysics 271, 149–156. doi: 10.1016/0003-9861(89)90265-8Google Scholar
Bignell, DRD, Huguet-Tapia, JC, Joshi, MV, Pettis, GS and Loria, R (2010) What does it take to be a plant pathogen: genomic insights from Streptomyces species. Antonie van Leeuwenhoek 98, 179–194. doi: 10.1007/s10482-010-9429-1Google Scholar
Bolwell, GP, Butt, VS, Davies, DR and Zimmerlin, A (1995) The origin of the oxidative burst in plants. Free Radical Research 23, 517–532. doi: 10.3109/10715769509065273Google Scholar
Bolwell, GP and Wojtaszek, P (1997) Mechanisms for the generation of reactive oxygen species in plant defence – a broad perspective. Physiological and Molecular Plant Pathology 51, 347–366. doi: 10.1006/pmpp.1997.0129Google Scholar
Camejo, D, Martí, MC, Jiménez, A, Cabrera, JC, Olmos, E and Sevilla, F (2011) Effect of oligogalacturonides on root length, extracellular alkalinization and O2−-accumulation in alfalfa. Journal of Plant Physiology 168, 566–575. doi: 10.1016/j.jplph.2010.09.012Google Scholar
Camejo, D, Guzmán-Cedeño, Á and Moreno, A (2016) Reactive oxygen species, essential molecules, during plant–pathogen interactions. Plant Physiology and Biochemistry 103, 10–23. doi: 10.1016/j.plaphy.2016.02.035Google Scholar
Chater, KF, Biró, S, Lee, KJ, Palmer, T and Schrempf, H (2010) The complex extracellular biology of Streptomyces. FEMS Microbiology Reviews 34, 171–198. doi: 10.1111/j.1574-6976.2009.00206.xGoogle Scholar
Chen, C and Thakker, DR (2002) The fallacy of using adrenochrome reaction for measurement of reactive oxygen species formed during cytochrome P450-mediated metabolism of xenobiotics. Journal of Pharmacology and Experimental Therapeutics 300, 417–420. doi: 10.1124/jpet.300.2.417Google Scholar
Cheng, Z (2016) A Pseudomonas aeruginosa -secreted protease modulates host intrinsic immune responses, but how? BioEssays 38, 1084–1092. doi: 10.1002/bies.201600101Google Scholar
Cheng, Z, Li, J-F, Niu, Y, Zhang, X-C, Woody, OZ, Xiong, Y, Djonović, S, Millet, Y, Bush, J, McConkey, BJ, Sheen, J and Ausubel, FM (2015) Pathogen-secreted proteases activate a novel plant immune pathway. Nature 521, 213–216. doi: 10.1038/nature14243Google Scholar
Dalling, JW, Davis, AS, Schutte, BJ and Arnold, AE (2011) Seed survival in soil: interacting effects of predation, dormancy and the soil microbial community. Journal of Ecology 99, 89–95. doi: 10.1111/j.1365-2745.2010.01739.xGoogle Scholar
Doke, N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiological Plant Pathology 23, 345–357. doi: 10.1016/0048-4059(83)90019-XGoogle Scholar
Doke, N (1985) NADPH-dependent O2− generation in membrane fractions isolated from wounded potato tubers inoculated with Phytophthora infestans. Physiological Plant Pathology 27, 311–322. doi: 10.1016/0048-4059(85)90044-XGoogle Scholar
Ferrari, B, Gianinetti, A, Finocchiaro, F and Terzi, V (2015) Rc gene sequence and expression evaluation in a red-kernel rice genotype. Journal of Rice Research 03, 145. doi: 10.4172/2375-4338.1000145Google Scholar
Finocchiaro, F, Ferrari, B, Gianinetti, A, Dall'Asta, C, Galaverna, G, Scazzina, F and Pellegrini, N (2007) Characterization of antioxidant compounds of red and white rice and changes in total antioxidant capacity during processing. Molecular Nutrition and Food Research 51, 1006–1019. doi: 10.1002/mnfr.200700011Google Scholar
Fuerst, EP, Okubara, PA, Anderson, JV and Morris, CF (2014) Polyphenol oxidase as a biochemical seed defense mechanism. Frontiers in Plant Science 5. doi: 10.3389/fpls.2014.00689Google Scholar
Fuerst, EP, James, MS, Pollard, AT and Okubara, PA (2018) Defense enzyme responses in dormant wild oat and wheat caryopses challenged with a seed decay pathogen. Frontiers in Plant Science 8. doi: 10.3389/fpls.2017.02259Google Scholar
Gallagher, RS, Burnham, MB and Fuerst, EP (2014) The chemical ecology of seed persistence in soil seed banks, pp. 178–203 in Gallagher, RS (ed), Seeds: The Ecology of Regeneration in Plant Communities. Wallingford, CABI. doi: 10.1079/9781780641836.0178Google Scholar
Gay, C and Gebicki, JM (2000) A critical evaluation of the effect of sorbitol on the ferric–xylenol orange hydroperoxide assay. Analytical Biochemistry 284, 217–220. doi: 10.1006/abio.2000.4696Google Scholar
Gay, CA and Gebicki, JM (2002) Perchloric acid enhances sensitivity and reproducibility of the ferric–xylenol orange peroxide assay. Analytical Biochemistry 304, 42–46. doi: 10.1006/abio.2001.5566Google Scholar
Gianinetti, A (2016) Anomalous germination of dormant dehulled red rice seeds provides a new perspective to study the transition from dormancy to germination and to unravel the role of the caryopsis coat in seed dormancy. Seed Science Research 26, 124–138. doi: 10.1017/S0960258516000076Google Scholar
Gianinetti, A and Cohn, MA (2008) Seed dormancy in red rice. XIII. Interaction of dry-afterripening and hydration temperature. Seed Science Research 18, 151–159. doi: 10.1017/S0960258508037999Google Scholar
Gianinetti, A and Vernieri, P (2007) On the role of abscisic acid in seed dormancy of red rice. Journal of Experimental Botany 58, 3449–3462. doi: 10.1093/jxb/erm198Google Scholar
Gianinetti, A, Laarhoven, LJJ, Persijn, ST, Harren, FJM and Petruzzelli, L (2007) Ethylene production is associated with germination but not seed dormancy in red rice. Annals of Botany 99, 735–745. doi: 10.1093/aob/mcm008Google Scholar
Gianinetti, A, Finocchiaro, F, Bagnaresi, P, Zechini, A, Faccioli, P, Cattivelli, L, Valè, G and Biselli, C (2018) Seed dormancy involves a transcriptional program that supports early plastid functionality during imbibition. Plants 7, 35. doi: 10.3390/plants7020035Google Scholar
Giannopolitis, CN and Ries, SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314. doi: 10.1104/pp.59.2.309Google Scholar
Graham, HD (1992) Stabilization of the Prussian blue color in the determination of polyphenols. Journal of Agricultural and Food Chemistry 40, 801–805. doi: 10.1021/jf00017a018Google Scholar
Gust, AA, Pruitt, R and Nürnberger, T (2017) Sensing danger: key to activating plant immunity. Trends in Plant Science 22, 779–791. doi: 10.1016/j.tplants.2017.07.005Google Scholar
Han, L, Dong, B, Yang, X, Huang, C, Wang, X and Wu, X (2009) Study on flavonoids in the caryopsis of indica rice Rdh. Agricultural Sciences in China 8, 249–256. doi: 10.1016/S1671-2927(09)60034-1Google Scholar
Jia, L-G, Sheng, Z-W, Xu, W-F, Li, Y-X, Liu, Y-G, Xia, Y-J and Zhang, J-H (2012) Modulation of anti-oxidation ability by proanthocyanidins during germination of Arabidopsis thaliana seeds. Molecular Plant 5, 472–481. doi: 10.1093/mp/ssr089Google Scholar
Kärkönen, A and Kuchitsu, K (2015) Reactive oxygen species in cell wall metabolism and development in plants. Phytochemistry 112, 22–32. doi: 10.1016/j.phytochem.2014.09.016Google Scholar
Keppler, LD, Baker, CJ and Atkinson, MM (1989) Active oxygen production during a bacteria-induced hypersensitive reaction in tobacco suspension cells. Phytopathology 79, 974–978. doi: 10.1094/Phyto-79-974Google Scholar
Koeck, M, Hardham, AR and Dodds, PN (2011) The role of effectors of biotrophic and hemibiotrophic fungi in infection. Cellular Microbiology 13, 1849–1857. doi: 10.1111/j.1462-5822.2011.01665.xGoogle Scholar
Kranner, I, Roach, T, Beckett, RP, Whitaker, C and Minibayeva, FV (2010) Extracellular production of reactive oxygen species during seed germination and early seedling growth in Pisum sativum. Journal of Plant Physiology 167, 805–811. doi: 10.1016/j.jplph.2010.01.019Google Scholar
Krishnan, S and Dayanandan, P (2003) Structural and histochemical studies on grain-filling in the caryopsis of rice (Oryza sativa L.). Journal of Biosciences 28, 455–469. doi: 10.1007/BF02705120Google Scholar
Lamb, C and Dixon, RA (1997) The oxidative burst in plant disease resistance. Annual Review of Plant Physiology and Plant Molecular Biology 48, 251–275. doi: 10.1146/annurev.arplant.48.1.251Google Scholar
Levine, A, Tenhaken, R, Dixon, R and Lamb, C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583–593. doi: 10.1016/0092-8674(94)90544-4Google Scholar
Leymarie, J, Vitkauskaité, G, Hoang, HH, Gendreau, E, Chazoule, V, Meimoun, P, Corbineau, F, El-Maarouf-Bouteau, H and Bailly, C (2012) Role of reactive oxygen species in the regulation of Arabidopsis seed dormancy. Plant and Cell Physiology 53, 96–106. doi: 10.1093/pcp/pcr129Google Scholar
Lightfoot, DJ, Mcgrann, GRD and Able, AJ (2017) The role of a cytosolic superoxide dismutase in barley-pathogen interactions. Molecular Plant Pathology 18, 323–335. doi: 10.1111/mpp.12399Google Scholar
Long, RL, Gorecki, MJ, Renton, M, Scott, JK, Colville, L, Goggin, DE, Commander, LE, Westcott, DA, Cherry, H and Finch-Savage, WE (2015) The ecophysiology of seed persistence: a mechanistic view of the journey to germination or demise. Biological Reviews 90, 31–59. doi: 10.1111/brv.12095Google Scholar
Misra, HP and Fridovich, I (1972) The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. Journal of Biological Chemistry 247, 3170–3175.Google Scholar
Moore, D, Robson, GD and Trinci, APJ (2011) 21st Century Guidebook to Fungi. Cambridge, Cambridge University Press.Google Scholar
Oracz, K, Bouteau, HE-M, Farrant, JM, Cooper, K, Belghazi, M, Job, C, Job, D, Corbineau, F and Bailly, C (2007) ROS production and protein oxidation as a novel mechanism for seed dormancy alleviation. The Plant Journal 50, 452–465. doi: 10.1111/j.1365-313X.2007.03063.xGoogle Scholar
Oracz, K, El-Maarouf-Bouteau, H, Kranner, I, Bogatek, R, Corbineau, F and Bailly, C (2009) The mechanisms involved in seed dormancy alleviation by hydrogen cyanide unravel the role of reactive oxygen species as key factors of cellular signaling during germination. Plant Physiology 150, 494–505. doi: 10.1104/pp.109.138107Google Scholar
Pinton, R, Cakmak, I and Marschner, H (1994) Zinc deficiency enhanced NAD(P)H-dependent superoxide radical production in plasma membrane vesicles isolated from roots of bean plants. Journal of Experimental Botany 45, 45–50. doi: 10.1093/jxb/45.1.45Google Scholar
Pourcel, L, Routaboul, J, Cheynier, V, Lepiniec, L and Debeaujon, I (2007) Flavonoid oxidation in plants: from biochemical properties to physiological functions. Trends in Plant Science 12, 29–36. doi: 10.1016/j.tplants.2006.11.006Google Scholar
Schopfer, P, Plachy, C and Frahry, G (2001) Release of reactive oxygen intermediates (superoxide radicals, hydrogen peroxide, and hydroxyl radicals) and peroxidase in germinating radish seeds controlled by light, gibberellin, and abscisic acid. Plant Physiology 125, 1591–1602. doi: 10.1104/pp.125.4.1591Google Scholar
Sekizawa, Y, Haga, M, Hirabayashi, E, Takeuchi, N and Takino, Y (1987) Dynamic behavior of superoxide generation in rice leaf tissue infected with blast fungus and its regulation by some substances. Agricultural and Biological Chemistry 51, 763–770. doi: 10.1080/00021369.1987.10868129Google Scholar
Selin, C, de Kievit, TR, Belmonte, MF and Fernando, WGD (2016) Elucidating the role of effectors in plant-fungal interactions: progress and challenges. Frontiers in Microbiology 7, 600. doi: 10.3389/fmicb.2016.00600Google Scholar
Senthilraja, G (2016) Induction of systemic resistance in crop plants against plant pathogens by plant growth-promoting actinomycetes, pp. 193–202 in Subramaniam, G, Arumugam, S and Rajendran, V (eds), Plant Growth Promoting Actinobacteria. Singapore, Springer Singapore. doi: 10.1007/978-981-10-0707-1_12Google Scholar
Sutherland, MW and Learmonth, BA (1997) The tetrazolium dyes MTS and XTT provide new quantitative assays for superoxide and superoxide dismutase. Free Radical Research 27, 283–289. doi: 10.3109/10715769709065766Google Scholar
Sweeney, PJ and Walker, JM (1993) Pronase (EC 3.4.24.4). Methods in Molecular Biology 16, 271–276. doi: 10.1385/0-89603-234-5:271Google Scholar
Sweeney, MT, Thomson, MJ, Pfeil, BE and McCouch, S (2006) Caught red-handed: Rc encodes a basic helix-loop-helix protein conditioning red pericarp in rice. The Plant Cell 18, 283–294. doi: 10.1105/tpc.105.038430Google Scholar
Takeshige, K and Minakami, S (1979) NADH- and NADPH-dependent formation of superoxide anions by bovine heart submitochondrial particles and NADH–ubiquinone reductase preparation. Biochemical Journal 180, 129–135. doi: 10.1042/bj1800129Google Scholar
Taubert, D, Breitenbach, T, Lazar, A, Censarek, P, Harlfinger, S, Berkels, R, Klaus, W and Roesen, R (2003) Reaction rate constants of superoxide scavenging by plant antioxidants. Free Radical Biology and Medicine 35, 1599–1607. doi: 10.1016/j.freeradbiomed.2003.09.005Google Scholar
Torres, MA, Jones, JDG and Dangl, JL (2006) Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373–378. doi: 10.1104/pp.106.079467Google Scholar
Vreeburg, RAM and Fry, SC (2005) Reactive oxygen species in cell walls, pp. 215–249 in Smirnoff, N (ed), Antioxidants and Reactive Oxygen Species in Plants. Oxford, UK, Blackwell Publishing Ltd. doi: 10.1002/9780470988565.ch9Google Scholar
Wu, S, Shan, L and He, P (2014) Microbial signature-triggered plant defense responses and early signaling mechanisms. Plant Science 228, 118–126. doi: 10.1016/j.plantsci.2014.03.001Google Scholar
Yu, X, Feng, B, He, P and Shan, L (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annual Review of Phytopathology 55, 109–137. doi: 10.1146/annurev-phyto-080516-035649Google Scholar
Zar, JH (1999) Biostatistical Analysis, 4th edn. Upper Saddle River, NJ, USA: Prentice Hall.Google Scholar
Ziska, LH, Gealy, DR, Burgos, N, Caicedo, AL, Gressel, J, Lawton-Rauh, AL, Avila, LA, Theisen, G, Norsworthy, J, Ferrero, A, Vidotto, F, Johnson, DE, Ferreira, FG, Marchesan, E, Menezes, V, Cohn, MA, Linscombe, S, Carmona, L, Tang, R and Merotto, A (2015) Weedy (red) rice: an emerging constraint to global rice production. Advances in Agronomy 129, 181–228. doi: 10.1016/bs.agron.2014.09.003Google Scholar
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