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Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection

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Abstract

Poplars are challenged by a wide range of pathogens during their lifespan, and have an innate immunity system that activates defence responses to restrict pathogen growth. Large-scale expression studies of poplar–rust interactions have shown concerted transcriptional changes during defence responses, as in other plant pathosystems. Detailed analysis of expression profiles of metabolic pathways in these studies indicates that photosynthesis and respiration are also important components of the poplar response to rust infection. This is consistent with our current understanding of plant pathogen interactions as defence responses impose substantive demands for resources and energy that are met by reorganization of primary metabolism. This review applies the results of poplar transcriptome analyses to current research describing how plants divert energy from plant primary metabolism for resistance mechanisms.

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References

  • Arnold TM, Schultz JC (2002) Induced sink strength as a prerequisite for induced tannin biosynthesis in developing leaves of Populus. Oecologia 130:585–593

    Article  Google Scholar 

  • Azaiez A, Boyle B, Levée V, Séguin A (2009) Transcriptome profiling in hybrid poplar following interactions with Melamp-sora rust fungi. Mol Plant Microbe Interact 22:190–200

    Article  CAS  PubMed  Google Scholar 

  • Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482

    Article  PubMed  Google Scholar 

  • Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: Plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026

    Article  CAS  PubMed  Google Scholar 

  • Bocock PN, Morse AM, Dervinis C, Davis JM (2008) Evolution and diversity of invertase genes in Populus trichocarpa. Planta 227:565–576

    Article  CAS  PubMed  Google Scholar 

  • Bolton MD (2009) Primary metabolism and plant defense—fuel for the fire. Mol Plant Microbe Interact 22:487–497

    Article  CAS  PubMed  Google Scholar 

  • Bolton MD, Kolmer JA, Xu WW, Garvin DF (2008) Lr34-mediated leaf rust resistance in wheat: transcript profiling reveals a high energetic demand supported by transient recruitment of multiple metabolic pathways. Mol Plant Microbe Interact 21:1515–1527

    Article  CAS  PubMed  Google Scholar 

  • Bonfig KB, Schreiber U, Gabler A, Roitsch T, Berger S (2006) Infection with virulent and avirulent P. syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves. Planta 225:1–12

    Article  CAS  PubMed  Google Scholar 

  • Chen C, Meyermans H, Burggraeve B, De Rycke RM, Inoue K, De Vleesschauwer V, Steenackers M, Van Montagu MC, Engler GJ, Boerjan WA (2000) Cell-specific and conditional expression of caffeoyl-coenzyme A-3-O-methyltransferase in poplar. Plant Physiol 123:853–867

    Article  CAS  PubMed  Google Scholar 

  • Cheng Q, Cao YZ, Pan HX, Wang MX, Huang MR (2008) Isolation and characterization of two genes encoding polygalacturonase-inhibiting protein from Populus deltoides. J Genet Genomics 35:631–638

    Article  CAS  PubMed  Google Scholar 

  • Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124:803–814

    Article  CAS  PubMed  Google Scholar 

  • Clifton R, Millar AH, Whelan J (2006) Alternative oxidases in Arabidopsis: a comparative analysis of differential expression in the gene family provides new insights into function of non-phosphorylating bypasses. Biochim Biophys Acta 1757:730–741

    Article  CAS  PubMed  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang L (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390

    Article  CAS  Google Scholar 

  • Duplessis S, Major I, Martin F, Séguin A (2009) Poplar and pathogen interactions: insights from Populus genome-wide analyses of resistance and defense gene families and gene expression profiling. Crit Rev Plant Sci 28:309–334

    Article  CAS  Google Scholar 

  • Essmann J, Schmitz-Thom I, Schön H, Sonnewald S, Weis E, Scharte J (2008) RNA interference-mediated repression of cell wall invertase impairs defense in source leaves of tobacco. Plant Physiol 147:1288–1299

    Article  CAS  PubMed  Google Scholar 

  • Ferreira RB, Monteiro S, Freitas R, Santos CN, Chen Z, Batista LM, Duarte J, Borges A, Teixeira AR (2007) The role of plant defence proteins in fungal pathogenesis. Mol Plant Pathol 8:677–700

    Article  CAS  Google Scholar 

  • Fotopoulos V, Gilbert MJ, Pittman JK, Marvier AC, Buchanan AJ, Sauer N, Hall JL, Williams LE (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atβfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiol 132:821–829

    Article  CAS  PubMed  Google Scholar 

  • Gérard PR, Husson C, Pinon J, Frey P (2006) Comparison of genetic and virulence diversity of Melampsora larici-populina populations on wild and cultivated poplar and influence of the alternate host. Phytopathology 96:1027–1036

    Article  PubMed  Google Scholar 

  • Jansson S, Douglas CJ (2007) Populus: a model system for plant biology. Annu Rev Plant Biol 58:435–458

    Article  CAS  PubMed  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Katagiri F (2004) A global view of defense gene expression regulation—a highly interconnected signaling network. Curr Opin Plant Biol 7:506–511

    Article  CAS  PubMed  Google Scholar 

  • Laurans F, Pilate G (1999) Histological aspects of a hypersensitive response in poplar to Melampsora larici-populina. Phytopathology 89:233–238

    Article  CAS  PubMed  Google Scholar 

  • Laxalt AM, Cassial RO, Sanllorenti PM, Madrid EA, Andreu AB, Daleo GR, Conde RD, Lamattina L (1996) Accumulation of cytosolic glyceraldehyde-3-phosphate dehydrogenase RNA under biological stress conditions and elicitor treatments in potato. Plant Mol Biol 30:961–972

    Article  CAS  PubMed  Google Scholar 

  • Levée V, Major I, Levasseur C, Tremblay L, MacKay J, Séguin A (2009) Expression profiling and functional analysis of Populus WRKY23 reveals a regulatory role in defense. New Phytol 184:48–70

    Article  PubMed  Google Scholar 

  • Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa × P. deltoides) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant Microbe Interact 20:816–831

    Article  CAS  PubMed  Google Scholar 

  • Newcombe G (1996) The specificity of fungal pathogens of Populus. In: Stettler RF, Bradshaw HD Jr, Heilman PE, Hinckley TM (eds) Biology of Populus and its implications for management and conservation. NRC Research Press, Ottawa, pp 223–246

    Google Scholar 

  • Newcombe G, Ostry M, Hubbes M, Périnet P, Mottet M-J (2001) Poplar diseases. In: Dickmann DI, Isebrands JG, Eckenwalder JE, Richardson J (eds) Poplar culture in North America. NRC Research Press, Ottawa, pp 249–276

    Google Scholar 

  • Pinon J, Frey P (2005) Interactions between poplar clones and Melampsora populations and their implications for breeding for durable resistance. In: Pei MH, McCracken AR (eds) Rust diseases of willow and poplar. CABI Publishing, Cambridge, pp 139–154

    Chapter  Google Scholar 

  • Plaxton WC, Podesta FE (2006) The functional organization and control of plant respiration. Crit Rev Plant Sci 25:159–198

    Article  CAS  Google Scholar 

  • Rinaldi C, Kohler A, Frey P, Duchaussoy F, Ningre N, Couloux A, Wincker P, Le Thiec D, Fluch S, Martin F, Duplessis S (2007) Transcript profiling of poplar leaves upon infection with compatible and incompatible strains of the foliar rust Melamp-sora larici-populina. Plant Physiol 144:347–366

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T, González M-C (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9:606–613

    Article  CAS  PubMed  Google Scholar 

  • Roitsch T, Balibrea ME, Hofmann M, Proels R, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. J Exp Bot 54:513–524

    Article  CAS  PubMed  Google Scholar 

  • Rubin EM (2008) Genomics of cellulosic biofuels. Nature 454:841–845

    Article  CAS  PubMed  Google Scholar 

  • Scalbert A (1991) Antimicrobial properties of tannins. Phytochemistry 30:3875–3883

    Article  CAS  Google Scholar 

  • Smedegaard-Petersen V, Stølen O (1981) Effect of energy-requiring defense reactions on yield and grain quality in a powdery mildew-resistant barley cultivar. Phytopathology 71:396–399

    Article  Google Scholar 

  • Smedegaard-Petersen V, Tolstrup K (1985) The limiting effect of disease resistance on yield. Annu Rev Phytopathol 23:475–490

    Article  Google Scholar 

  • Smith CM, Rodriguez-Buey M, Karlsson J, Campbell MM (2004) The response of the poplar transcriptome to wounding and subsequent infection by a viral pathogen. New Phytol 164:123–136

    Article  CAS  Google Scholar 

  • Sutton PN, Gilbert MJ, Williams LE, Hall JL (2007) Powdery mildew infection of wheat leaves changes host solute transport and invertase activity. Physiol Plant 129:787–795

    Article  CAS  Google Scholar 

  • Swarbrick PJ, Schulze-Lefert P, Scholes JD (2006) Metabolic consequences of susceptibility and resistance (race-specific and broad-spectrum) in barley leaves challenged with powdery mildew. Plant Cell Environ 29:1061–1076

    Article  CAS  PubMed  Google Scholar 

  • Tao Y, Xie Z, Chen W, Glazebrook J, Chang H-S, Han B, Zhu T, Zou G, Katagiri F (2003) Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell 15:317–330

    Article  CAS  PubMed  Google Scholar 

  • Van Aken O, Giraud E, Clifton R, Whelan J (2009) Alternative oxidase: a target and regulator of stress responses. Physiol Plant 137:354–361

    Google Scholar 

  • van Loon LC, Rep M, Pieterse CMJ (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44:135–162

    Article  PubMed  Google Scholar 

  • Vanlerberghe GC, Cvetkovska M, Wang J (2009) Is the maintenance of homeostatic mitochondrial signaling during stress a physiological role for alternative oxidase? Physiol Plant 137:392–406

    Google Scholar 

  • Voegele RT, Struck C, Hahn M, Mendgen K (2001) The role of haustoria in sugar supply during infection of broad bean by the rust fungus Uromyces fabae. Proc Natl Acad Sci USA 98:8133–8138

    Article  CAS  PubMed  Google Scholar 

  • Voegele RT, Hahn M, Mendgen K (2009) The Uredinales: cytology, biochemistry, and molecular biology. In: Deising HB (ed) and Esser K (Ser ed) Plant relationships, 2nd edn. The Mycota, vol 5. Springer, Berlin, pp 69–98

  • Walters D, Heil M (2007) Costs and trade-offs associated with induced resistance. Physiol Mol Plant Pathol 71:3–17

    Article  CAS  Google Scholar 

  • Yuan K, Zhang B, Zhang YM, Cheng Q, Wang MX, Huang MR (2008) Identification of differentially expressed proteins in poplar leaves induced by Marssonina brunnea f. sp. multigermtubi. J Genet Genomics 35:49–60

    Article  CAS  PubMed  Google Scholar 

  • Zhang Y, Zhang X, Chen Y, Wang Q, Wang M, Huang M (2007) Function and chromosomal localization of differentially expressed genes induced by Marssonina brunnea f. sp. multigermtubi in Populus deltoides. J Genet Genomics 34:641–648

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Pamela Cheers for editing work and an anonymous reviewer for valuable comments. IM is the recipient of a postdoctoral Visiting Fellowship in Canadian Government Laboratories from the Natural Sciences and Engineering Research Council of Canada (NSERC). This work was supported by grants from NSERC and the Canadian Genomics R&D Initiative to AS and by INRA and Région Lorraine grants to Sébastien Duplessis.

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Correspondence to Ian T. Major.

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Major, I.T., Nicole, MC., Duplessis, S. et al. Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection. Photosynth Res 104, 41–48 (2010). https://doi.org/10.1007/s11120-009-9507-2

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