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Transcriptome and proteome analysis reveal new insight into proximal and distal responses of wheat to foliar infection by Xanthomonas translucens

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Garcia-Seco, Daniel [IRD, Cirad, Univ. Montpellier] Chiapello, Marco [Dipartimento di Biotecnologie e Scienze della Vita, Università degli Studi dell’Insubria, Varese, Italy] Bracale, Marcella [Dipartimento di Biotecnologie e Scienze della Vita, Università degli Studi dell’Insubria, Varese, Italy] Pesce, Céline [UCL] Bagnaresi, Paolo [Council for agricultural research and economics (CREA) - Genomics Research Centre, Piacenza, Italy] Koebnik, Ralf [IRD, Cirad, Univ. Montpellier]

The molecular details of local plant response against Xanthomonas translucens infection is largely unknown. Moreover, there is no knowledge about effects of the pathogen on the root’s transcriptome and proteome. Therefore, we investigated the global gene and protein expression changes both in leaves and roots of wheat (Triticum aestivum) 24 h post leaf infection of X. translucens. This simultaneous analysis allowed us to obtain insight into possible metabolic rearrangements in above- and belowground tissues and to identify common responses as well as specific alterations. At the site of infection, we observed the implication of various components of the recognition, signaling, and amplification mechanisms in plant response to the pathogen. Moreover, data indicate a massive down-regulation of photosynthesis and confirm the chloroplast as crucial signaling hub during pathogen attack. Notably, roots responded as well to foliar attack and their response significantly differed from that locally triggered in infected leaves. Data indicate that roots as a site of energy production and synthesis of various secondary metabolites may actively influence the composition and colonisation level of root-associated microbes. Finally, our results emphasize the accumulation of jasmonic acid, pipecolic acid and/or the downstream mediator of hydrogen peroxide as long distal signals from infected leaves to roots.

Document type Article de périodique (Journal article) – Article de recherche
Access type Accès restreint
Publication date 2017
Language Anglais
Journal information "Scientific Reports" - Vol. 7, no.1, p. 1-13 (2017)
Peer reviewed yes
Publisher Nature Publishing Group (London)
issn 2045-2322
e-issn 2045-2322
Publication status Publié
Affiliation UCL - SST/ELI/ELIM - Applied Microbiology
Keywords Bacterial host response ; Gene regulation ; Plant immunity ; 3130
Links
  1. Jones Jonathan D. G., Dangl Jeffery L., The plant immune system, 10.1038/nature05286
  2. Pfeilmeier Sebastian, Caly Delphine L., Malone Jacob G., Bacterial pathogenesis of plants: future challenges from a microbial perspective : Challenges in Bacterial Molecular Plant Pathology, 10.1111/mpp.12427
  3. Soler Roxina, Erb Matthias, Kaplan Ian, Long distance root–shoot signalling in plant–insect community interactions, 10.1016/j.tplants.2012.08.010
  4. Erb Matthias, Lenk Claudia, Degenhardt Jörg, Turlings Ted C.J., The underestimated role of roots in defense against leaf attackers, 10.1016/j.tplants.2009.08.006
  5. Orłowska Elżbieta, Fiil Alice, Kirk Hanne-Grethe, Llorente Briardo, Cvitanich Cristina, Differential gene induction in resistant and susceptible potato cultivars at early stages of infection by Phytophthora infestans, 10.1007/s00299-011-1155-2
  6. Conrath Uwe, Molecular aspects of defence priming, 10.1016/j.tplants.2011.06.004
  7. Reymond Philippe, Farmer Edward E., Jasmonate and salicylate as global signals for defense gene expression, 10.1016/s1369-5266(98)80264-1
  8. Denancé Nicolas, Sánchez-Vallet Andrea, Goffner Deborah, Molina Antonio, Disease resistance or growth: the role of plant hormones in balancing immune responses and fitness costs, 10.3389/fpls.2013.00155
  9. De Vleesschauwer David, Gheysen Godelieve, Höfte Monica, Hormone defense networking in rice: tales from a different world, 10.1016/j.tplants.2013.07.002
  10. Vicente Joana G., Holub Eric B., Xanthomonas campestrispv.campestris(cause of black rot of crucifers) in the genomic era is still a worldwide threat to brassica crops : Xanthomonas campestrispv.campestris, 10.1111/j.1364-3703.2012.00833.x
  11. NIÑO-LIU DAVID O., RONALD PAMELA C., BOGDANOVE ADAM J., Xanthomonas oryzae pathovars: model pathogens of a model crop, 10.1111/j.1364-3703.2006.00344.x
  12. Griffin Eric A., Carson Walter P., The Ecology and Natural History of Foliar Bacteria with a Focus on Tropical Forests and Agroecosystems, 10.1007/s12229-015-9151-9
  13. Rademaker J. L. W., Norman D. J., Forster R. L., Louws F. J., Schultz M. H., de Bruijn F. J., Classification and Identification ofXanthomonas translucensIsolates, Including Those Pathogenic to Ornamental Asparagus, 10.1094/phyto-96-0876
  14. Thieme F., Koebnik R., Bekel T., Berger C., Boch J., Buttner D., Caldana C., Gaigalat L., Goesmann A., Kay S., Kirchner O., Lanz C., Linke B., McHardy A. C., Meyer F., Mittenhuber G., Nies D. H., Niesbach-Klosgen U., Patschkowski T., Ruckert C., Rupp O., Schneiker S., Schuster S. C., Vorholter F.-J., Weber E., Puhler A., Bonas U., Bartels D., Kaiser O., Insights into Genome Plasticity and Pathogenicity of the Plant Pathogenic Bacterium Xanthomonas campestris pv. vesicatoria Revealed by the Complete Genome Sequence, 10.1128/jb.187.21.7254-7266.2005
  15. da Silva A. C. R., Ferro J. A., Reinach F. C., Farah C. S., Furlan L. R., Quaggio R. B., Monteiro-Vitorello C. B., Sluys M. A. Van, Almeida N. F., Alves L. M. C., do Amaral A. M., Bertolini M. C., Camargo L. E. A., Camarotte G., Cannavan F., Cardozo J., Chambergo F., Ciapina L. P., Cicarelli R. M. B., Coutinho L. L., Cursino-Santos J. R., El-Dorry H., Faria J. B., Ferreira A. J. S., Ferreira R. C. C., Ferro M. I. T., Formighieri E. F., Franco M. C., Greggio C. C., Gruber A., Katsuyama A. M., Kishi L. T., Leite R. P., Lemos E. G. M., Lemos M. V. F., Locali E. C., Machado M. A., Madeira A. M. B. N., Martinez-Rossi N. M., Martins E. C., Meidanis J., Menck C. F. M., Miyaki C. Y., Moon D. H., Moreira L. M., Novo M. T. M., Okura V. K., Oliveira M. C., Oliveira V. R., Pereira H. A., Rossi A., Sena J. A. D., Silva C., de Souza R. F., Spinola L. A. F., Takita M. A., Tamura R. E., Teixeira E. C., Tezza R. I. D., Trindade dos Santos M., Truffi D., Tsai S. M., White F. F., Setubal J. C., Kitajima J. P., Comparison of the genomes of two Xanthomonas pathogens with differing host specificities, 10.1038/417459a
  16. Lee B.-M., The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice, 10.1093/nar/gki206
  17. , Mayer K. F. X., Rogers J., Dole el J., Pozniak C., Eversole K., Feuillet C., Gill B., Friebe B., Lukaszewski A. J., Sourdille P., Endo T. R., Kubalakova M.,  ihalikova J., Dubska Z., Vrana J.,  perkova R.,  imkova H., Febrer M., Clissold L., McLay K., Singh K., Chhuneja P., Singh N. K., Khurana J., Akhunov E., Choulet F., Alberti A., Barbe V., Wincker P., Kanamori H., Kobayashi F., Itoh T., Matsumoto T., Sakai H., Tanaka T., Wu J., Ogihara Y., Handa H., Maclachlan P. R., Sharpe A., Klassen D., Edwards D., Batley J., Olsen O.-A., Sandve S. R., Lien S., Steuernagel B., Wulff B., Caccamo M., Ayling S., Ramirez-Gonzalez R. H., Clavijo B. J., Wright J., Pfeifer M., Spannagl M., Martis M. M., Mascher M., Chapman J., Poland J. A., Scholz U., Barry K., Waugh R., Rokhsar D. S., Muehlbauer G. J., Stein N., Gundlach H., Zytnicki M., Jamilloux V., Quesneville H., Wicker T., Faccioli P., Colaiacovo M., Stanca A. M., Budak H., Cattivelli L., Glover N., Pingault L., Paux E., Sharma S., Appels R., Bellgard M., Chapman B., Nussbaumer T., Bader K. C., Rimbert H., Wang S., Knox R., Kilian A., Alaux M., Alfama F., Couderc L., Guilhot N., Viseux C., Loaec M., Keller B., Praud S., A chromosome-based draft sequence of the hexaploid bread wheat (Triticum aestivum) genome, 10.1126/science.1251788
  18. Sato Shusei, Tabata Satoshi, Hirakawa Hideki, Asamizu Erika, Shirasawa Kenta, Isobe Sachiko, Kaneko Takakazu, Nakamura Yasukazu, Shibata Daisuke, Aoki Koh, Egholm Michael, Knight James, Bogden Robert, Li Changbao, Shuang Yang, Xu Xun, Pan Shengkai, Cheng Shifeng, Liu Xin, Ren Yuanyuan, Wang Jun, Albiero Alessandro, Dal Pero Francesca, Todesco Sara, Van Eck Joyce, Buels Robert M., Bombarely Aureliano, Gosselin Joseph R., Huang Minyun, Leto Jonathan A., Menda Naama, Strickler Susan, Mao Linyong, Gao Shan, Tecle Isaak Y., York Thomas, Zheng Yi, Vrebalov Julia T., Lee JeMin, Zhong Silin, Mueller Lukas A., Stiekema Willem J., Ribeca Paolo, Alioto Tyler, Yang Wencai, Huang Sanwen, Du Yongchen, Zhang Zhonghua, Gao Jianchang, Guo Yanmei, Wang Xiaoxuan, Li Ying, He Jun, Li Chuanyou, Cheng Zhukuan, Zuo Jianru, Ren Jianfeng, Zhao Jiuhai, Yan Liuhua, Jiang Hongling, Wang Bao, Li Hongshuang, Li Zhenjun, Fu Fuyou, Chen Bingtang, Han Bin, Feng Qi, Fan Danlin, Wang Ying, Ling Hongqing, Xue Yongbiao, Ware Doreen, Richard McCombie W., Lippman Zachary B., Chia Jer-Ming, Jiang Ke, Pasternak Shiran, Gelley Laura, Kramer Melissa, Anderson Lorinda K., Chang Song-Bin, Royer Suzanne M., Shearer Lindsay A., Stack Stephen M., Rose Jocelyn K. C., Xu Yimin, Eannetta Nancy, Matas Antonio J., McQuinn Ryan, Tanksley Steven D., Camara Francisco, Guigó Roderic, Rombauts Stephane, Fawcett Jeffrey, Van de Peer Yves, Zamir Dani, Liang Chunbo, Spannagl Manuel, Gundlach Heidrun, Bruggmann Remy, Mayer Klaus, Jia Zhiqi, Zhang Junhong, Ye Zhibiao, Bishop Gerard J., Butcher Sarah, Lopez-Cobollo Rosa, Buchan Daniel, Filippis Ioannis, Abbott James, Dixit Rekha, Singh Manju, Singh Archana, Kumar Pal Jitendra, Pandit Awadhesh, Kumar Singh Pradeep, Kumar Mahato Ajay, Dogra Vivek, Gaikwad Kishor, Raj Sharma Tilak, Mohapatra Trilochan, Kumar Singh Nagendra, Causse Mathilde, Rothan Christophe, Schiex Thomas, Noirot Céline, Bellec Arnaud, Klopp Christophe, Delalande Corinne, Berges Hélène, Mariette Jérôme, Frasse Pierre, Vautrin Sonia, Zouine Mohamed, Latché Alain, Rousseau Christine, Regad Farid, Pech Jean-Claude, Philippot Murielle, Bouzayen Mondher, Pericard Pierre, Osorio Sonia, Fernandez del Carmen Asunción, Monforte Antonio, Granell Antonio, Fernandez-Muñoz Rafael, Conte Mariana, Lichtenstein Gabriel, Carrari Fernando, De Bellis Gianluca, Fuligni Fabio, Peano Clelia, Grandillo Silvana, Termolino Pasquale, Pietrella Marco, Fantini Elio, Falcone Giulia, Fiore Alessia, Giuliano Giovanni, Lopez Loredana, Facella Paolo, Perrotta Gaetano, Daddiego Loretta, Bryan Glenn, Orozco Modesto, Pastor Xavier, Torrents David, van Schriek Marco G. M., Feron Richard M.C., van Oeveren Jan, de Heer Peter, daPonte Lorena, Jacobs-Oomen Saskia, Cariaso Mike, Prins Marcel, van Eijk Michiel J. T., Janssen Antoine, van Haaren Mark J. J., Jo Sung-Hwan, Kim Jungeun, Kwon Suk-Yoon, Kim Sangmi, Koo Dal-Hoe, Lee Sanghyeob, Hur Cheol-Goo, Clouser Christopher, Rico Alain, Hallab Asis, Gebhardt Christiane, Klee Kathrin, Jöcker Anika, Warfsmann Jens, Göbel Ulrike, Kawamura Shingo, Yano Kentaro, Sherman Jamie D., Fukuoka Hiroyuki, Negoro Satomi, Bhutty Sarita, Chowdhury Parul, Chattopadhyay Debasis, Datema Erwin, Smit Sandra, Schijlen Elio G. W. M., van de Belt Jose, van Haarst Jan C., Peters Sander A., van Staveren Marjo J., Henkens Marleen H. C., Mooyman Paul J. W., Hesselink Thamara, van Ham Roeland C. H. J., Jiang Guoyong, Droege Marcus, Choi Doil, Kang Byung-Cheol, Dong Kim Byung, Park Minkyu, Kim Seungill, Yeom Seon-In, Lee Yong-Hwan, Choi Yang-Do, Li Guangcun, Gao Jianwei, Liu Yongsheng, Huang Shengxiong, Fernandez-Pedrosa Victoria, Collado Carmen, Zuñiga Sheila, Wang Guoping, Cade Rebecca, Dietrich Robert A., Rogers Jane, Knapp Sandra, Fei Zhangjun, White Ruth A., Thannhauser Theodore W., Giovannoni James J., Angel Botella Miguel, Gilbert Louise, Gonzalez Ramon, Luis Goicoechea Jose, Yu Yeisoo, Kudrna David, Collura Kristi, Wissotski Marina, Wing Rod, Schoof Heiko, Meyers Blake C., Bala Gurazada Aishwarya, Green Pamela J., Mathur Saloni, Vyas Shailendra, Solanke Amolkumar U., Kumar Rahul, Gupta Vikrant, Sharma Arun K., Khurana Paramjit, Khurana Jitendra P., Tyagi Akhilesh K., Dalmay Tamas, Mohorianu Irina, Walts Brandon, Chamala Srikar, Brad Barbazuk W., Li Jingping, Guo Hui, Lee Tae-Ho, Wang Yupeng, Zhang Dong, Paterson Andrew H., Wang Xiyin, Tang Haibao, Barone Amalia, Luisa Chiusano Maria, Raffaella Ercolano Maria, D’Agostino Nunzio, Di Filippo Miriam, Traini Alessandra, Sanseverino Walter, Frusciante Luigi, Seymour Graham B., Elharam Mounir, Fu Ying, Hua Axin, Kenton Steven, Lewis Jennifer, Lin Shaoping, Najar Fares, Lai Hongshing, Qin Baifang, Qu Chunmei, Shi Ruihua, White Douglas, White James, Xing Yanbo, Yang Keqin, Yi Jing, Yao Ziyun, Zhou Liping, Roe Bruce A., Vezzi Alessandro, D’Angelo Michela, Zimbello Rosanna, Schiavon Riccardo, Caniato Elisa, Rigobello Chiara, Campagna Davide, Vitulo Nicola, Valle Giorgio, Nelson David R., De Paoli Emanuele, Szinay Dora, de Jong Hans H., Bai Yuling, Visser Richard G. F., Klein Lankhorst René M., Beasley Helen, McLaren Karen, Nicholson Christine, Riddle Claire, Gianese Giulio, Sato Shusei, Tabata Satoshi, Mueller Lukas A., Huang Sanwen, Du Yongchen, Li Chuanyou, Cheng Zhukuan, Zuo Jianru, Han Bin, Wang Ying, Ling Hongqing, Xue Yongbiao, Ware Doreen, Richard McCombie W., Lippman Zachary B., Stack Stephen M., Tanksley Steven D., Van de Peer Yves, Mayer Klaus, Bishop Gerard J., Butcher Sarah, Kumar Singh Nagendra, Schiex Thomas, Bouzayen Mondher, Granell Antonio, Carrari Fernando, De Bellis Gianluca, Giuliano Giovanni, Bryan Glenn, van Eijk Michiel J. T., Fukuoka Hiroyuki, Chattopadhyay Debasis, van Ham Roeland C. H. J., Choi Doil, Rogers Jane, Fei Zhangjun, Giovannoni James J., Wing Rod, Schoof Heiko, Meyers Blake C., Khurana Jitendra P., Tyagi Akhilesh K., Dalmay Tamas, Paterson Andrew H., Wang Xiyin, Frusciante Luigi, Seymour Graham B., Roe Bruce A., Valle Giorgio, de Jong Hans H., Klein Lankhorst René M., The tomato genome sequence provides insights into fleshy fruit evolution, 10.1038/nature11119
  19. Yu J., A Draft Sequence of the Rice Genome (Oryza sativa L. ssp. indica), 10.1126/science.1068037
  20. Wichmann Fabienne, Asp Torben, Widmer Franco, Kölliker Roland, Transcriptional responses of Italian ryegrass during interaction with Xanthomonas translucens pv. graminis reveal novel candidate genes for bacterial wilt resistance, 10.1007/s00122-010-1470-y
  21. Dey S., Wenig M., Langen G., Sharma S., Kugler K. G., Knappe C., Hause B., Bichlmeier M., Babaeizad V., Imani J., Janzik I., Stempfl T., Huckelhoven R., Kogel K.-H., Mayer K. F. X., Vlot A. C., Bacteria-Triggered Systemic Immunity in Barley Is Associated with WRKY and ETHYLENE RESPONSIVE FACTORs But Not with Salicylic Acid, 10.1104/pp.114.249276
  22. Kumar Anirudh, Bimolata Waikhom, Kannan Monica, Kirti P. B., Qureshi Insaf Ahmed, Ghazi Irfan Ahmad, Comparative proteomics reveals differential induction of both biotic and abiotic stress response associated proteins in rice during Xanthomonas oryzae pv. oryzae infection, 10.1007/s10142-014-0431-y
  23. Mahmood Tariq, Jan Asad, Kakishima Makoto, Komatsu Setsuko, Proteomic analysis of bacterial-blight defense-responsive proteins in rice leaf blades, 10.1002/pmic.200600470
  24. Reimers P.J., Leach J.E., Race-specific resistance to Xanthomonas oryzae pv. oryzae conferred by bacterial blight resistance gene Xa-10 in rice (Oryza sativa) involves accumulation of a lignin-like substance in host tissues, 10.1016/s0885-5765(05)80141-9
  25. CHOMZYNSKI P, Single-Step Method of RNA Isolation by Acid Guanidinium Thiocyanate–Phenol–Chloroform Extraction, 10.1006/abio.1987.9999
  26. Li, H. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv Prepr. arXiv1303.3997 (2013).
  27. Love Michael I, Huber Wolfgang, Anders Simon, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, 10.1186/s13059-014-0550-8
  28. Benjamini, Y. & Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society B 57, 289–300, doi: 10.2307/2346101 (1995).
  29. Wiśniewski Jacek R, Zougman Alexandre, Nagaraj Nagarjuna, Mann Matthias, Universal sample preparation method for proteome analysis, 10.1038/nmeth.1322
  30. Bass, J. D., Swcf, A. J., Dabney, A. & Robinson, D. Qvalue: Q-value estimation for false discovery rate control. R Packag. version 2.8.0 (2015).
  31. Thimm Oliver, Bläsing Oliver, Gibon Yves, Nagel Axel, Meyer Svenja, Krüger Peter, Selbig Joachim, Müller Lukas A., Rhee Seung Y., Stitt Mark, mapman: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes, 10.1111/j.1365-313x.2004.02016.x
  32. Shacter Emily, Williams Joy A., Lim Michael, Levine Rodney L., Differential susceptibility of plasma proteins to oxidative modification: Examination by western blot immunoassay, 10.1016/0891-5849(94)90169-4
  33. Willmann R., Lajunen H. M., Erbs G., Newman M.-A., Kolb D., Tsuda K., Katagiri F., Fliegmann J., Bono J.-J., Cullimore J. V., Jehle A. K., Gotz F., Kulik A., Molinaro A., Lipka V., Gust A. A., Nurnberger T., Arabidopsis lysin-motif proteins LYM1 LYM3 CERK1 mediate bacterial peptidoglycan sensing and immunity to bacterial infection, 10.1073/pnas.1112862108
  34. Gimenez-Ibanez Selena, Hann Dagmar R., Ntoukakis Vardis, Petutschnig Elena, Lipka Volker, Rathjen John P., AvrPtoB Targets the LysM Receptor Kinase CERK1 to Promote Bacterial Virulence on Plants, 10.1016/j.cub.2009.01.054
  35. Liu B., Li J.-F., Ao Y., Qu J., Li Z., Su J., Zhang Y., Liu J., Feng D., Qi K., He Y., Wang J., Wang H.-B., Lysin Motif-Containing Proteins LYP4 and LYP6 Play Dual Roles in Peptidoglycan and Chitin Perception in Rice Innate Immunity, 10.1105/tpc.112.102475
  36. Yadeta Koste A., Elmore James M., Creer Athena Y., Feng Baomin, Franco Jessica Y., Rufian Jose Sebastian, He Ping, Phinney Brett, Coaker Gitta, A Cysteine-Rich Protein Kinase Associates with a Membrane Immune Complex and the Cysteine Residues Are Required for Cell Death, 10.1104/pp.16.01404
  37. Singh Prashant, Zimmerli Laurent, Lectin receptor kinases in plant innate immunity, 10.3389/fpls.2013.00124
  38. Bourdais Gildas, Burdiak Paweł, Gauthier Adrien, Nitsch Lisette, Salojärvi Jarkko, Rayapuram Channabasavangowda, Idänheimo Niina, Hunter Kerri, Kimura Sachie, Merilo Ebe, Vaattovaara Aleksia, Oracz Krystyna, Kaufholdt David, Pallon Andres, Anggoro Damar Tri, Glów Dawid, Lowe Jennifer, Zhou Ji, Mohammadi Omid, Puukko Tuomas, Albert Andreas, Lang Hans, Ernst Dieter, Kollist Hannes, Brosché Mikael, Durner Jörg, Borst Jan Willem, Collinge David B., Karpiński Stanisław, Lyngkjær Michael F., Robatzek Silke, Wrzaczek Michael, Kangasjärvi Jaakko, , Large-Scale Phenomics Identifies Primary and Fine-Tuning Roles for CRKs in Responses Related to Oxidative Stress, 10.1371/journal.pgen.1005373
  39. Pan, L., Yang, N., Liu, Z., Wu, J. & WAng, G. The multifunction of CLAVATA2 in plant development and immunity. Front. Plant Sci. 7, 1573 (2016).
  40. Mosher Stephen, Kemmerling Birgit, PSKR1 and PSY1R-mediated regulation of plant defense responses, 10.4161/psb.24119
  41. Monaghan Jacqueline, Zipfel Cyril, Plant pattern recognition receptor complexes at the plasma membrane, 10.1016/j.pbi.2012.05.006
  42. Couto Daniel, Zipfel Cyril, Regulation of pattern recognition receptor signalling in plants, 10.1038/nri.2016.77
  43. Forde Brian G., Roberts Michael R., Glutamate receptor-like channels in plants: a role as amino acid sensors in plant defence?, 10.12703/p6-37
  44. Royaert Stefan, Jansen Johannes, da Silva Daniela Viana, de Jesus Branco Samuel Martins, Livingstone Donald S., Mustiga Guiliana, Marelli Jean-Philippe, Araújo Ioná Santos, Corrêa Ronan Xavier, Motamayor Juan Carlos, Identification of candidate genes involved in Witches’ broom disease resistance in a segregating mapping population of Theobroma cacao L. in Brazil, 10.1186/s12864-016-2415-x
  45. Abramovitch Robert B, Martin Gregory B, Strategies used by bacterial pathogens to suppress plant defenses, 10.1016/j.pbi.2004.05.002
  46. Coll N S, Smidler A, Puigvert M, Popa C, Valls M, Dangl J L, The plant metacaspase AtMC1 in pathogen-triggered programmed cell death and aging: functional linkage with autophagy, 10.1038/cdd.2014.50
  47. Mitra Sirsha, Baldwin Ian T., RuBPCase activase (RCA) mediates growth-defense trade-offs: silencing RCA redirects jasmonic acid (JA) flux from JA-isoleucine to methyl jasmonate (MeJA) to attenuate induced defense responses inNicotiana attenuata, 10.1111/nph.12591
  48. Shapiguzov Alexey, Vainonen Julia P., Wrzaczek Michael, Kangasjärvi Jaakko, ROS-talk – how the apoplast, the chloroplast, and the nucleus get the message through, 10.3389/fpls.2012.00292
  49. Miyoshi Kazumaru, Ito Yukihiro, Serizawa Akiko, Kurata Nori, OsHAP3genes regulate chloroplast biogenesis in rice, 10.1046/j.1365-313x.2003.01897.x
  50. Göhre Vera, Jones Alexandra M. E., Sklenář Jan, Robatzek Silke, Weber Andreas P. M., Molecular Crosstalk Between PAMP-Triggered Immunity and Photosynthesis, 10.1094/mpmi-11-11-0301
  51. de Torres Zabala Marta, Littlejohn George, Jayaraman Siddharth, Studholme David, Bailey Trevor, Lawson Tracy, Tillich Michael, Licht Dirk, Bölter Bettina, Delfino Laura, Truman William, Mansfield John, Smirnoff Nicholas, Grant Murray, Chloroplasts play a central role in plant defence and are targeted by pathogen effectors, 10.1038/nplants.2015.74
  52. Zurbriggen Matias D., Carrillo Néstor, Tognetti Vanesa B., Melzer Michael, Peisker Martin, Hause Bettina, Hajirezaei Mohammad-Reza, Chloroplast-generated reactive oxygen species play a major role in localized cell death during the non-host interaction between tobacco and Xanthomonas campestris pv. vesicatoria : Chloroplast ROS in a non-host interaction, 10.1111/j.1365-313x.2009.04010.x
  53. Overmyer Kirk, Brosché Mikael, Kangasjärvi Jaakko, Reactive oxygen species and hormonal control of cell death, 10.1016/s1360-1385(03)00135-3
  54. Daudi A., Cheng Z., O'Brien J. A., Mammarella N., Khan S., Ausubel F. M., Bolwell G. P., The Apoplastic Oxidative Burst Peroxidase in Arabidopsis Is a Major Component of Pattern-Triggered Immunity, 10.1105/tpc.111.093039
  55. Wrzaczek Michael, Brosché Mikael, Kangasjärvi Jaakko, ROS signaling loops — production, perception, regulation, 10.1016/j.pbi.2013.07.002
  56. Tarantino Delia, Vannini Candida, Bracale Marcella, Campa Manuela, Soave Carlo, Murgia Irene, Antisense reduction of thylakoidal ascorbate peroxidase in Arabidopsis enhances Paraquat-induced photooxidative stress and Nitric Oxide-induced cell death, 10.1007/s00425-005-1485-9
  57. Maruta Takanori, Noshi Masahiro, Tanouchi Aoi, Tamoi Masahiro, Yabuta Yukinori, Yoshimura Kazuya, Ishikawa Takahiro, Shigeoka Shigeru, H2O2-triggered Retrograde Signaling from Chloroplasts to Nucleus Plays Specific Role in Response to Stress, 10.1074/jbc.m111.292847
  58. Fedorova Maria, Bollineni Ravi Chand, Hoffmann Ralf, Protein carbonylation as a major hallmark of oxidative damage: Update of analytical strategies : PROTEIN CARBONYLATION: AN ANALYTICAL UPDATE, 10.1002/mas.21381
  59. Morkunas Iwona, Ratajczak Lech, The role of sugar signaling in plant defense responses against fungal pathogens, 10.1007/s11738-014-1559-z
  60. Sonnewald Sophia, Priller Johannes P. R., Schuster Julia, Glickmann Eric, Hajirezaei Mohammed-Reza, Siebig Stefan, Mudgett Mary Beth, Sonnewald Uwe, Regulation of Cell Wall-Bound Invertase in Pepper Leaves by Xanthomonas campestris pv. vesicatoria Type Three Effectors, 10.1371/journal.pone.0051763
  61. Yamada Kohji, Saijo Yusuke, Nakagami Hirofumi, Takano Yoshitaka, Regulation of sugar transporter activity for antibacterial defense in Arabidopsis , 10.1126/science.aah5692
  62. Jang J. C., Hexokinase as a Sugar Sensor in Higher Plants, 10.1105/tpc.9.1.5
  63. Herbers K., Systemic Acquired Resistance Mediated by the Ectopic Expression of Invertase: Possible Hexose Sensing in the Secretory Pathway, 10.1105/tpc.8.5.793
  64. ZEIER JÜRGEN, New insights into the regulation of plant immunity by amino acid metabolic pathways : Amino acid metabolism and plant immunity, 10.1111/pce.12122
  65. Hummel Maureen, Rahmani Fatima, Smeekens Sjef, Hanson Johannes, Sucrose-mediated translational control, 10.1093/aob/mcp086
  66. SENTHIL-KUMAR MUTHAPPA, MYSORE KIRANKUMAR S., Ornithine-delta-aminotransferase and proline dehydrogenase genes play a role in non-host disease resistance by regulating pyrroline-5-carboxylate metabolism-induced hypersensitive response : Proline-P5C metabolism regulates non-host resistance, 10.1111/j.1365-3040.2012.02492.x
  67. Song Jong Tae, Lu Hua, McDowell John M., Greenberg Jean T., A key role for ALD1 in activation of local and systemic defenses in Arabidopsis : A key role for ALD1 in defense signaling, 10.1111/j.1365-313x.2004.02200.x
  68. Navarova H., Bernsdorff F., Doring A.-C., Zeier J., Pipecolic Acid, an Endogenous Mediator of Defense Amplification and Priming, Is a Critical Regulator of Inducible Plant Immunity, 10.1105/tpc.112.103564
  69. Bernsdorff Friederike, Doering Anne-Christin, Gruner Katrin, Schuck Stefan, Bräutigam Andrea, Zeier Jürgen, Pipecolic acid orchestrates plant systemic acquired resistance and defense priming via salicylic acid-dependent and independent pathways, 10.1105/tpc.15.00496
  70. Zimaro Tamara, Gottig Natalia, Garavaglia Betiana S., Gehring Chris, Ottado Jorgelina, Unraveling Plant Responses to Bacterial Pathogens through Proteomics, 10.1155/2011/354801
  71. Lee Sanghyeob, Kim Soo-Yong, Chung Eunjoo, Joung Young-Hee, Pai Hyun-Sook, Hur Cheol-Goo, Choi Doil, EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv. glycines), 10.1007/s10142-003-0099-1
  72. Garcia-Seco Daniel, Zhang Yang, Gutierrez-Mañero Francisco J., Martin Cathie, Ramos-Solano Beatriz, Application of Pseudomonas fluorescens to Blackberry under Field Conditions Improves Fruit Quality by Modifying Flavonoid Metabolism, 10.1371/journal.pone.0142639
  73. Sattler Scott E., Funnell-Harris Deanna L., Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens?†, 10.3389/fpls.2013.00070
  74. Hosmani P. S., Kamiya T., Danku J., Naseer S., Geldner N., Guerinot M. L., Salt D. E., Dirigent domain-containing protein is part of the machinery required for formation of the lignin-based Casparian strip in the root, 10.1073/pnas.1308412110
  75. Nalam Vamsi J., Shah Jyoti, Nachappa Punya, Emerging role of roots in plant responses to aboveground insect herbivory : Root responses to aboveground herbivory, 10.1111/1744-7917.12004
Bibliographic reference Garcia-Seco, Daniel ; Chiapello, Marco ; Bracale, Marcella ; Pesce, Céline ; Bagnaresi, Paolo ; et. al. Transcriptome and proteome analysis reveal new insight into proximal and distal responses of wheat to foliar infection by Xanthomonas translucens. In: Scientific Reports, Vol. 7, no.1, p. 1-13 (2017)
Permanent URL http://hdl.handle.net/2078.1/187414