Abstract
Ca2+ is an ubiquitous intracellular molecule which is used as a second messenger to control many physiological activities in plant cells. In the present work, the relationship between calcium localization and the hypersensitive response (HR)—one of the most crucial and indispensable pathway to resist a pathogen—was studied in the wheat-wheat strip rust system using cytochemical technique. Our results show that calcium is involved in the interaction between wheat and wheat stripe rust. In the incompatible interaction associated with necrosis of host mesophyll cells, an influx of Ca2+ from the intercellular space to the cytoplasm and finally an efflux to the intercellular space again was detected in an incompatible interaction. Calcium precipitates were also observed in mesophyll cells adjacent to necrotic cells. On the contrary, calcium flow was not significantly altered in a compatible interaction. These results suggest that calcium might induce HR as a secondary messenger in the incompatible interaction of wheat and wheat stripe rust.
Similar content being viewed by others
Abbreviations
- dpi:
-
Days post inoculation
- EGTA:
-
Ethylene glycol tetraacetic acid
- GT:
-
Germ tube
- HC:
-
Host cells
- HMC:
-
Haustorial mother cells
- hpi:
-
Hours post inoculation
- HR:
-
Hypersensitive response
- IH:
-
Infection hyphae
- IS:
-
Intercellular space
- IT:
-
Infection type
- NC:
-
Necrotic cells
- PAMP:
-
Pathogen-associated molecular patterns
- PR:
-
Pathogenesis-related
- Pst :
-
Puccinia striiformis Westend f. sp. tritici Erikss.
- PTI:
-
PAMP-triggered immunity
- ROS:
-
Reactive oxygen species
- SV:
-
Substomatal vesicle
- TEM:
-
Transmission electron microscopy
- WGA:
-
Wheat germ agglutinin
References
Ali R, Ma W, Lemtiri-Chlieh F, Tsaltas D, Leng Q, Bodman SV, Berkowitz GA (2007) Death don’t have no mercy and neither does calcium: Arabidopsis cyclic nucleotide gated channel and innate immunity. Plant Cell 19:1081–1095
Allen GJ, Chu SP, Harrington CL, Schumacher K, Hoffmann T, Tang YY, Grill E, Schroeder JI (2001) A defined range of guard cell calcium oscillation parameters encodes stomatal movements. Nature 411:1053–1057
Appleton J, Morris DC (1979) The use of the potassium pyroantimonate-osmium method as a means of identifying and localizing calcium at the ultrastructural level in the cells of calcifying systems. J Histochem Cytochem 27:676–680
Atkinson MM, Keppler LD, Orlandi EW, Baker CJ, Mischke CF (1990) Involvement of plasma membrane calcium influx in bacterial induction of the K+/H+ and hypersensitive responses in tobacco. Plant Physiol 92:215–221
Atkinson MM, Midland SL, Sims JJ, Keen NT (1996) Syringolide 1 triggers Ca2+ influx, K+ efflux, and extracellular alkalization in soybean cells carrying the disease-resistance gene Rpg4. Plant Physiol 112:297–302
Baker CJ, Orlandi EW (1995) Active oxygen in plant pathogenesis. Annu Rev Phytopathol 33:299–321
Bateman DF (1964) An induced mechanism of tissue resistance to polygalacturonase in Rhizoctonia-infected hypocotyls of bean. Phytopathology 54:438–445
Bibikova TN, Zhigilei A, Gilroy S (1997) Root hair growth in Arabidopsis thaliana is directed by calcium and an endogenous polarity. Planta 203:495–505
Blume B, Nürnberger T, Nass N, Scheel D (2000) Receptor-mediated increase in cytoplasmic free calcium required for activation of pathogen defense in parsley. Plant Cell 12:1425–1440
Bonilla I, El-Hamdaoui A, Bolaños L (2004) Boron and calcium increase Pisum sativum seed germination and seedling development under salt stress. Plant Soil 267:97–107
Bush DS (1995) Calcium regulation in plant cells and its role in signaling. Annu Rev Plant Physiol Plant Mol Biol 46:95–122
Bux H, Rasheed A, Siyal MA, Kazi AG, Napar AA, Mujeeb-Kazi A (2012) An overview of stripe rust of wheat (Puccinia striiformis f. sp. tritici) in Pakistan. Arch Phytopathol Plant Protect 45:2278–2289
Chen XM (2005) Epidemiology and control of strip rust (Puccinia striiformis f. sp. Tritici) on wheat. Can J Plant Pathol 27:314–337
Cheong YH, Kim KN, Pandey GK, Gupta R, Grant JJ, Luan S (2003) CBL1, a calcium sensor that differentially regulates salt, drought, and cold responses in Arabidopsis. Plant Cell 15:1833–1845
Dangl JL, Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833
Dat JF, Pellinen R, Beeckman T, Cotte BV, Langebartels C, Kangasjärvi J, Inzé D, Breusegem FV (2003) Changes in hydrogen peroxide homeostasis trigger an active cell death process in tobacco. Plant J 33:621–632
David DJ (1959) Determination of calcium in plant material by atomic-absorption spectrophotometry. Analyst 84:536–545
Delledonne M, Zeier J, Marocco A, Lamb C (2001) Signal interactions between nitric oxide and reactive oxygen intermediates in the plant hypersensitive disease resistance response. Proc Natl Acad Sci U S A 98:13454–13459
Digonnet C, Aldon D, Leduc N, Dumas C, Rougier M (1997) First evidence of a calcium transient in flowering plants at fertilization. Development 124:2867–2874
Doorn WG, Beers EP, Dangl JL, Franklin-Tong VE, Gallois P, Hara-Nishimura I, Jones AM, Kawai-Yamada M, Lam E, Mundy J, Mur LA, Petersen M, Smertenko A, Taliansky M, Van Breusegem F, Wolpert T, Woltering E, Zhivotovsky B, Bozhkov PV (2011) Morphological classification of plant cell deaths. Cell Death Differ 18:1241–1246
Eastell R, Vieira NE, Yergey AL (1989) One-day test using stable isotopes to measure true fractional calcium absorption. J Bone Miner Res 4:463–468
Egrie JC, Campbell JA, Flangas L, Siegel FL (1977) Regional, cellular and subcellular distribution of calcium-activated cyclic nucleotide phosphodiesterase and calcium-dependent regulator in porcine brain. J Neurosci 28:1207–1213
Favali MA, Gaggiato G (1986) Subcellular distribution of potassium antimonate precipitates in plant tissue 3. Ginkgo Biloba L. leaves. Cytobios 48:133–141
Ferguson IB (1984) Calcium in plant senescence and fruit ripening. Plant Cell Environ 7:477–489
Gao G, Jin LP, Xie KY, Qu DY (2009) The potato StLTPa7 gene displays a complex Ca-associated pattern of expression during the early stage of potato-Ralstonia solanacearum interaction. Mol Plant Pathol 10:15–27
Gilchrist DG (1998) Programmed cell death in plant disease: the purpose and promise of cellular suicide. Annu Rev Phytopathol 36:393–414
Grant JJ, Yun BW, Loake GJ (2000a) Oxidative burst and cognate redox signalling reported by luciferase imaging: identification of a signal network that functions independently of ethylene, SA and Me-JA but is dependent on MAPKK activity. Plant J 24:569–582
Grant M, Brown I, Adams S, Knight M, Ainslie A, Mansfield J (2000b) The RPM1 plant disease resistance gene facilitates a rapid and sustained increase in cytosolic calcium that is necessary for the oxidative burst and hypersensitive cell death. Plant J 23:441–450
Harder DE, Samborski DJ, Rohringer R, Rimmer SR, Kim WK, Chong J (1979) Electron microscopy of susceptible and resistant near-isogenic (sr6/Sr6) lines of wheat infected by Pucciizia grainiitis tritici. III. Ultrastructure of incompatible interactions. Can J Bot 57:2626–2634
Harrison BD, Stefanac Z, Roberts IM (1970) Role of mitochondria in the formation of X-bodies in cells of Nicotiana clevelandii infected by tobacco rattle viruses. J Gen Virol 6:127–140
Hayat MA (1975) Positive staining for electron microscopy. Van Nostrand Reinhold Company, New York, pp 80–93
Heath MC, Nimichuk ZL, Xu H (1997) Plant nuclear migrations as indications of critical interactions between resistant and susceptible cowpea epidermal cells and invasion hyphae of the cowpea rust fungus. New Phytol 135:689–700
Heller A, Witt-Geiges T (2013) Oxalic acid has an additional, detoxifying function in Sclerotinia sclerotiorum pathogenesis. PLoS ONE 8. doi:10.1371/journal.pone.0072292
Hepler PK (1994) The role of calcium in cell division. Cell Calcium 16:322–330
Hoth M, Button DC, Lewis RS (2000) Mitochondrial control of calcium-channel gating: a mechanism for sustained signaling and transcriptional activation in T lymphocytes. Proc Natl Acad Sci U S A 97:10607–10612
Issa AA, Abdel-Basset R, Adam MS (1995) Abolition of heavy toxicity on Kirchneriella lunaris (Chlorophyta) by calcium. Ann Bot-London 75:189–192
Jabs T, Tschöpe M, Colling C, Hahlbrock K, Scheel D (1997) Elicitor-stimulated ion fluxes and O2 - from the oxidative burst are essential components in triggering defense gene activation and phytoalexin synthesis in parsley. Proc Natl Acad Sci 94:4800–4805
Jackson SL, Heath IB (1993) Roles of calcium ions in hyphal tip growth. Microbiol Rev 57(2):367–382
Jiang YW, Huang BR (2001) Effects of calcium on antioxidant activities and water relations associated with heat tolerance in two cool-season grasses. J Exp Bot 52:341–349
Kang ZS, Huang LL, Buchenauer H (2002) Ultrastructural changes and localization of lignin and callose in compatible and incompatible interactions between wheat and Puccinia striiformis. J Plant Dis Prot 109:25–37
Kim MC, Chung WS, Yun DJ, Cho MJ (2009) Calcium and calmodulin-mediated regulation of gene expression in plants. Mol Plant 2:13–21
Kurusu T, Yagala T, Miyao A, Hirochika H, Kuchitsu K (2005) Identification of a putative voltage-gated Ca2+ channel as a key regulator of elicitor-induced hypersensitive cell death and mitogen-activated protein kinase activation in rice. Plant J 42:798–809
Lam E, Kato N, Lawton M (2001) Programmed cell death, mitochondria and the plant hypersensitive response. Nature 411:848–853
Lamotte O, Gould K, Lecourieux D, Sequeira-Legrand A, Lebrun-Garcia A, Durner J, Pugin A, Wendehenne D (2004) Analysis of nitric oxide signaling functions in tobacco cells challenged by the elicitor cryptogein. Plant Physiol 135:516–529
Lazarovits G, Higgins V (1976) Ultrastructure of susceptible, resistant, and immune reactions of tomato to races of Cladosporium fulvum. Can J Bot 54:235–249
Lee TF, McNellis TW (2009) Evidence that the BONZAI1/COPINE1 protein is a calcium and pathogen-responsive defense suppressor. Plant Mol Biol 69:155–166
Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593
Levine A, Pennell RI, Alvarez ME, Palmer R, Lamb C (1996) Calcium-mediated apoptosis in a plant hypersensitive disease resistance response. Curr Biol 6:427–437
Li H, Lin Y, Heath RM, Zhu MX, Yang Z (1999) Control of pollen tube tip growth by a rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–1740
Line RF, Qayoum A (1992) Virulence, aggressiveness, evolution, and distribution of races of Puccinia striiformis (the cause of stripe rust of wheat) in North America 1968-1987. US Dep Agric Agric Res Serv Tech Bull 1788
Ma Q, Shang HS (2009) Ultrastructure of stripe rust (Puccinia striiformis f. sp. tritici) interacting with slow-rusting, highly resistant, and susceptible wheat cultivars. J Plant Pathol 91:597–606
Nemchinov LG, Shabala L, Shabala S (2008) Calcium efflux as a component of the hypersensitive response of Nicotiana benthamiana to Pseudomonas syringae. Plant Cell Physiol 49:40–46
Nühse TS, Bottrill AR, Jones AM, Peck SC (2007) Quantitative phosphoproteomic analysis of plasma membrane proteins reveals regulatory mechanisms of plant innate immune responses. Plant J 51:931–940
Nürnberger T, Scheel D (2001) Signal transmission in the plant immune response. Trends Plant Sci 6:372–379
Otulak K, Garbaczewska G (2010) Ultrastructural events during hypersensitive response of potato cv. Rywal infected with necrotic strains of potato virus Y. Acta Physiol Plant 32:635–644
Palukaitis P, Roessinek MJ, Dietzgen RG (1992) Cucumber mosaic virus. Adv Virus Res 41:281–348
Pitt D, Ugalde UO (1984) Calcium in fungi. Plant Cell Environ 7:467–475
Ranf S, Eschen-Lippold L, Pecher P, Lee J, Scheel D (2011) Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J 68:100–113
Rathore VS, Bajaj YP, Wittwer SH (1972) Subcellular localization of zinc and calcium in bean (Phaseolus vulgaris L.) tissues. Plant Physiol 49:207–211
Rengel Z (1992) The role of calcium in salt toxicity. Plant Cell Environ 15:625–633
Slocum RD, Roux SJ (1982) An improved method for the subcellular localization of calcium using a modification of the antimonate precipitation technique. J Histochem Cytochem 30:617–629
VendenBosch KA, Sherrier DJ, Dreyer DA (1995) Light microscopic applications in immunocytochemistry. In: Gelvin SB, Schilperoort RA (eds) Plant Mol Biol Manual, 2nd edn. Kluwer Academic, Dordrecht, pp 1–18
Wang CF (2008) Studies on histology and cytochemistry of oxidative burst during wheat-Puccinia striiformis f. sp. tritici interaction (in Chinese). Dissertation, Northwest A&F University
Wang CF, Huang LL, Buchenauer H, Han QM, Zhang HC, Kang ZS (2007) Histochemical studies on the accumulation of reactive oxygen species (O2 − and H2O2) in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol 71:230–239
Wang CF, Huang LL, Zhang HC, Han QM, Buchenauer H, Kang ZS (2010) Cytochemical localization of reactive oxygen species (O2 − and H2O2) and peroxidase in the incompatible and compatible interaction of wheat-Puccinia striiformis f. sp. tritici. Physiol Mol Plant Pathol 74:221–229
Whitaker M (2010) Calcium in living cells. Elsevier Academic Press, Burlington
Xu H, Heath MC (1998) Role of calcium in signal transduction during the hypersensitive response caused by basidiospore-derived infection of the cowpea rust fungus. Plant Cell 10:585–598
Yang Y, Shah J, Klessig DF (1997) Signal perception and transduction in plant defense responses. Genes Dev 11:1621–1639
Zhang HC (2012) Histological and cytological analyses of adult plant resistance to wheat stripe rust and characterization of non-host resistance of wheat to Uromyces fabae (in Chinese). Dissertation, Northwest A&F University
Zhang HC, Wang CF, Cheng YL, Chen XM, Han QM, Huang LL, Wei GR, Kang ZS (2012) Histological and cytological characterization of adult plant resistance to wheat stripe rust. Plant Cell Rep 31:2121–2137
Acknowledgments
This study has been financially supported by the National Key Basic Research Program of China (2013CB127700), Nature Science Foundation of China (No. 30571205; No. 30900931), 111 Project from the Ministry of Education of China (B07049), and talent-funded project of Northwest A&F University (No. 01140510).
Conflict of interest
All authors declare that they have no conflict of interest. We declare that we have no financial and personal relationships with other people or organizations that can inappropriately influence our work, and there is no professional or other personal interest of any nature or kind in any product, service and/or company that could be construed as influencing the position presented in, or the review of, the manuscript entitled, “Subcellular localization of calcium in the incompatible and compatible interactions of wheat and Puccinia striiformis f. sp. tritici.”
Author information
Authors and Affiliations
Corresponding authors
Additional information
Handling Editor: Adrienne R. Hardham
Rights and permissions
About this article
Cite this article
Yin, S., Wang, C., Jiao, M. et al. Subcellular localization of calcium in the incompatible and compatible interactions of wheat and Puccinia striiformis f. sp. tritici . Protoplasma 252, 103–116 (2015). https://doi.org/10.1007/s00709-014-0659-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00709-014-0659-3