Skip to main content
SpringerLink
Log in

The Arabidopsis ubiquitin ligases ATL31 and ATL6 control the defense response as well as the carbon/nitrogen response

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

In higher plants, the metabolism of carbon (C) and nitrogen nutrients (N) is mutually regulated and referred to as the C and N balance (C/N). Plants are thus able to optimize their growth depending on their cellular C/N status. Arabidopsis ATL31 and ATL6 encode a RING-type ubiquitin ligases which play a critical role in the C/N status response (Sato et al. in Plant J 60:852–864, 2009). Since many ATL members are involved in the plant defense response, the present study evaluated whether the C/N response regulators ATL31 and ATL6 are involved in defense responses. Our results confirmed that ATL31 and ATL6 expression is up-regulated with the microbe-associated molecular patterns elicitors flg22 and chitin as well as with infections with Pseudomonas syringae pv. tomato DC3000 (Pst. DC3000). Moreover, transgenic plants overexpressing ATL31 and ATL6 displayed increased resistance to Pst. DC3000. In accordance with these data, loss of ATL31 and ATL6 function in an atl31 atl6 double knockout mutant resulted in reduced resistance to Pst. DC3000. In addition, the molecular cross-talk between C/N and the defense response was investigated by mining public databases. The analysis identified the transcription factors MYB51 and WRKY33, which are involved in the defense response, and their transcripts levels correlate closely with ATL31 and ATL6. Further study demonstrated that the expression of ATL31, ATL6 and defense marker genes including MYB51 and WRKY33 were regulated by C/N conditions. Taken together, these results indicate that ATL31 and ATL6 function as key components of both C/N regulation and the defense response in Arabidopsis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Alonso JM et al (2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301:653–657

    Article  PubMed  Google Scholar 

  • Berrocal-Lobo M, Stone S, Yang X, Antico J, Callis J, Ramonell KM, Somerville S (2010) ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin- and NADPH oxidase-mediated defense responses. PLoS ONE 23:e14426

    Article  Google Scholar 

  • Citovsky V, Zaltsman A, Kozlovsky SV, Gafni Y, Krichevsky A (2009) Proteasomal degradation in plant-pathogen interactions. Semin Cell Dev Biol 20:1048–1054

    Article  PubMed  CAS  Google Scholar 

  • Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101

    Article  PubMed  CAS  Google Scholar 

  • Coruzzi G, Bush DR (2001) Nitrogen and carbon nutrient and metabolite signaling in plants. Plant Physiol 125:61–64

    Article  PubMed  CAS  Google Scholar 

  • Curtis MD, Grossniklaus U (2003) A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol 133:462–469

    Article  PubMed  CAS  Google Scholar 

  • Degrave A, Fagard M, Perino C, Brisset MN, Gaubert S, Laroche S, Patrit O, Barny MA (2008) Erwinia amylovora type three-secreted proteins trigger cell death and defense responses in Arabidopsis thaliana. Mol Plant Microbe Interact 21:1076–1086

    Article  PubMed  CAS  Google Scholar 

  • Durrant WE, Rowland O, Piedras P, Hammond-Kosack KE, Jones JD (2000) cDNA-AFLP reveals a striking overlap in race-specific resistance and wound response gene expression profiles. Plant Cell 12:963–977

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant Microbe Interact 19:711–724

    Article  PubMed  CAS  Google Scholar 

  • Gigolashvili T, Berger B, Mock HP, Müller C, Weisshaar B, Flügge UI (2007) The transcription factor HIG1/MYB51 regulates indolic glucosinolate biosynthesis in Arabidopsis thaliana. Plant J 50:886–901

    Article  PubMed  CAS  Google Scholar 

  • Glawischnig E (2007) Camalexin. Phytochemistry 68:401–406

    Article  PubMed  CAS  Google Scholar 

  • Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959

    Article  PubMed  CAS  Google Scholar 

  • Gómez-Ariza J, Campo S, Rufat M, Estopà M, Messeguer J, San Segundo B, Coca M (2007) Sucrose-mediated priming of plant defense responses and broad-spectrum disease resistance by overexpression of the maize pathogenesis-related PRms protein in rice plants. Mol Plant Microbe Interact 20:832–842

    Article  PubMed  Google Scholar 

  • Herbers K, Takahata Y, Melzer M, Mock HP, Hajirezaei M, Sonnewald U (2000) Regulation of carbohydrate partitioning during the interaction of potato virus Y with tobacco. Mol Plant Pathol 1:51–59

    Article  PubMed  CAS  Google Scholar 

  • Hondo D, Hase S, Kanayama Y, Yoshikawa N, Takenaka S, Takahashi H (2007) The LeATL6-associated ubiquitin/proteasome system may contribute to fungal elicitor-activated defense response via the jasmonic acid-dependent signaling pathway in tomato. Mol Plant Microbe Interact 20:72–81

    Article  PubMed  CAS  Google Scholar 

  • Hruz T, Laule O, Szabo G, Wessendorp F, Bleuler S, Oertle L, Widmayer P, Gruissem W, Zimmermann P (2008) Genevestigator V3: a reference expression database for the meta-analysis of transcriptomes. Adv Bioinform 2008:420747

    Google Scholar 

  • Huber SC, MacKintosh C, Kaiser WM (2002) Metabolic enzymes as targets for 14-3-3 proteins. Plant Mol Biol 50:1053–1063

    Article  PubMed  CAS  Google Scholar 

  • Ichikawa T, Nakazawa M, Kawashima M, Iizumi H, Kuroda H, Kondou Y, Tsuhara Y, Suzuki K, Ishikawa A, Seki M, Fujita M, Motohashi R, Nagata N, Takagi T, Shinozaki K, Matsui M (2006) The FOX hunting system: an alternative gain-of-function gene hunting technique. Plant J 45:974–985

    Article  Google Scholar 

  • Jirage D, Tootle TL, Reuber TL, Frost LN, Feys BJ, Parker JE, Ausubel FM, Glazebrook J (1999) Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proc Natl Acad Sci USA 96:13583–13588

    Article  PubMed  CAS  Google Scholar 

  • Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol Plant Microbe Interact 20:900–911

    Article  PubMed  CAS  Google Scholar 

  • Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC, Chua NH (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J 56:550–561

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Zhang H, Yang Y, Li G, Yang Y, Wang X, Basnayake BM, Li D, Song F (2008) Functional analysis reveals pleiotropic effects of rice RING-H2 finger protein gene OsBIRF1 on regulation of growth and defense responses against abiotic and biotic stresses. Plant Mol Biol 68:17–30

    Article  PubMed  CAS  Google Scholar 

  • Lu D, Lin W, Gao X, Wu S, Cheng C, Avila J, Heese A, Devarenne TP, He P, Shan L (2011) Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science 332:1439–1442

    Article  PubMed  CAS  Google Scholar 

  • Manosalva PM, Bruce M, Leach JE (2011) Rice 14-3-3 protein (GF14e) negatively affects cell death and disease resistance. Plant J 68:777–787

    Article  PubMed  CAS  Google Scholar 

  • Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653

    Article  PubMed  CAS  Google Scholar 

  • Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon:nitrogen availability. Plant Physiol 128:472–481

    Article  PubMed  CAS  Google Scholar 

  • Mittelstrass K, Treutter D, Plessl M, Heller W, Elstner EF, Heiser I (2006) Modification of primary and secondary metabolism of potato plants by nitrogen application differentially affects resistance to Phytophthora infestans and Alternaria solani. Plant Biol 8:653–661

    Article  PubMed  CAS  Google Scholar 

  • Morita-Yamamuro C, Tsutsui T, Sato M, Yoshioka H, Tamaoki M, Ogawa D, Matsuura H, Yoshihara T, Ikeda A, Uyeda I, Yamaguchi J (2005) The Arabidopsis gene CAD1 controls programmed cell death in the plant immune system and encodes a protein containing a MACPF domain. Plant Cell Physiol 46:902–912

    Article  PubMed  CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    Article  CAS  Google Scholar 

  • Navarro L, Zipfel C, Rowland O, Keller I, Robatzek S, Boller T, Jones JD (2004) The transcriptional innate immune response to flg22. Interplay and overlap with Avr gene-dependent defense responses and bacterial pathogenesis. Plant Physiol 135:1113–1128

    Article  PubMed  CAS  Google Scholar 

  • Ni X, Tian Z, Liu J, Song B, Xie C (2010) Cloning and molecular characterization of the potato RING finger protein gene StRFP1 and its function in potato broad-spectrum resistance against Phytophthora infestans. J Plant Physiol 167:488–496

    Article  PubMed  CAS  Google Scholar 

  • Obayashi T, Hayashi S, Saeki M, Ohta H, Kinoshita K (2009) ATTED-II provides coexpressed gene networks for Arabidopsis. Nucleic Acids Res 37:987–991

    Article  Google Scholar 

  • Peng M, Hannam C, Gu H, Bi YM, Rothstein SJ (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J 50:320–337

    Article  PubMed  CAS  Google Scholar 

  • Ramonell K, Berrocal-Lobo M, Koh S, Wan J, Edwards H, Stacey G, Somerville S (2005) Loss-of-function mutations in chitin responsive genes show increased susceptibility to the powdery mildew pathogen Erysiphe cichoracearum. Plant Physiol 138:1027–1036

    Article  PubMed  CAS  Google Scholar 

  • Roberts MR (2003) Roberts MR (2003) 14-3-3 proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Ros B, Mohler V, Wenzel G, Thümmler F (2008) Phytophthora infestans-triggered response of growth- and defense-related genes in potato cultivars with different levels of resistance under the influence of nitrogen availability. Physiol Plant 133:386–396

    Article  PubMed  CAS  Google Scholar 

  • Rosso MG, Li Y, Strizhov N, Reiss B, Dekker K, Weisshaar B (2003) An Arabidopsis thaliana T-DNA mutagenized population (GABI-Kat) for flanking sequence tag-based reverse genetics. Plant Mol Biol 53:247–259

    Article  PubMed  CAS  Google Scholar 

  • Salinas-Mondragón RE, Garcidueñas-Piña C, Guzmán P (1999) Early elicitor induction in members of a novel multigene family coding for highly related RING-H2 proteins in Arabidopsis thaliana. Plant Mol Biol 40:579–590

    Article  PubMed  Google Scholar 

  • Sato T, Maekawa S, Yasuda S, Sonoda Y, Katoh E, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Goto DB, Ikeda A, Yamaguchi J (2009) CNI1/ATL31, a RING-type ubiquitin ligase that functions in the carbon/nitrogen response for growth phase transition in Arabidopsis seedlings. Plant J 60:852–864

    Article  PubMed  CAS  Google Scholar 

  • Sato T, Maekawa S, Yasuda S, Domeki Y, Sueyoshi K, Fujiwara M, Fukao Y, Goto DB, Yamaguchi J (2011) Identification of 14-3-3 proteins as a target of ATL31 ubiquitin ligase, a regulator of the C/N response in Arabidopsis. Plant J 68:137–146

    Article  PubMed  CAS  Google Scholar 

  • Serrano M, Parra S, Alcaraz LD, Guzmán P (2006) The ATL gene family from Arabidopsis thaliana and Oryza sativa comprises a large number of putative ubiquitin ligases of the RING-H2 type. J Mol Evol 62:434–445

    Article  PubMed  CAS  Google Scholar 

  • Stone SL, Williams LA, Farmer LM, Vierstra RD, Callis J (2006) Keep on going, a ring E3 ligase essential for Arabidopsis growth and development, is involved in abscisic acid signaling. Plant Cell 18:3415–3428

    Article  PubMed  CAS  Google Scholar 

  • Stout MJ, Brovont RA, Duffey SS (1998) Effect of nitrogen availability on expression of constitutive and inducible chemical defenses in tomato, Lycopersicon esculentum. J Chem Ecol 24:945–963

    Article  CAS  Google Scholar 

  • Takai R, Hasegawa K, Kaku H, Shibuya N, Minami E (2001) Isolation and analysis of expression mechanisms of a rice gene, EL5, which shows structural similarity to ATL family from Arabidopsis, in response to N-acetylchitooligosaccharide elicitor. Plant Sci 160:557–583

    Article  Google Scholar 

  • Takai R, Matsuda N, Nakano A, Hasegawa K, Akimoto C, Shibuya N, Minami E (2002) EL5, a rice N-acetylchitooligosaccharide elicitor-responsive RING-H2 finger protein, is a ubiquitin ligase which functions in vitro in co-operation with an elicitor-responsive ubiquitin-conjugating enzyme, OsUBC5b. Plant J 30:447–455

    Article  PubMed  CAS  Google Scholar 

  • Thibaud MC, Gineste S, Nussaume L, Robaglia C (2004) Sucrose increases pathogenesis-related PR-2 gene expression in Arabidopsis thaliana through an SA-dependent but NPR1-independent signaling pathway. Plant Physiol Biochem 42:81–488

    Article  PubMed  CAS  Google Scholar 

  • Tsunoda Y, Sakai N, Kikuchi K, Katoh S, Akagi K, Miura-Ohnuma J, Tashiro Y, Murata K, Shibuya N, Katoh E (2005) Improving expression and solubility of rice proteins produced as fusion proteins in Escherichia coli. Protein Expr Purif 42:268–277

    Article  PubMed  CAS  Google Scholar 

  • Vierstra RD (2009) The ubiquitin-26S protostome system at the nexus of plant biology. Nat Rev Mol Cell Biol 10:385–397

    Article  PubMed  CAS  Google Scholar 

  • Wawrzynska A, Christiansen KM, Lan Y, Rodibaugh NL, Innes RW (2008) Powdery mildew resistance conferred by loss of the ENHANCED DISEASE RESISTANCE1 protein kinase is suppressed by a missense mutation in KEEP ON GOING, a regulator of abscisic acid signaling. Plant Physiol 148:1510–1522

    Article  PubMed  CAS  Google Scholar 

  • Yaeno T, Iba K (2008) BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000. Plant Physiol 148:1032–1041

    Article  PubMed  CAS  Google Scholar 

  • Yang X, Wang W, Coleman M, Orgil U, Feng J, Ma X, Ferl R, Turner JG, Xiao S (2009) Arabidopsis 14-3-3 lambda is a positive regulator of RPW8-mediated disease resistance. Plant J 60:539–550

    Article  PubMed  CAS  Google Scholar 

  • Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419–2428

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants-in-Aid for Scientific Research (no. 2102500100, 2211450100) (JY). This work was also supported by Grant in-Aid to SM for Scientific Research for Plant Graduate Student from Nara Institute of Science and Technology by The Ministry of Education, Culture, Sports, Science and Technology, JAPAN (2009–2010). SM is also supported by Research Fellowships from the Japan Society for the Promotion of Science for Young Scientists (2010–2012). The authors also thank Derek Goto (Hokkaido University) for editing of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Science and Graduate School of Life Science, Hokkaido University, Kita-ku N10-W8, Sapporo, 060-0810, Japan

    Shugo Maekawa, Takeo Sato, Yutaka Asada, Shigetaka Yasuda, Yukako Chiba & Junji Yamaguchi

  2. NARO Hokkaido Agricultural Research Center, Hitsujigaoka, Sapporo, 062-8555, Japan

    Midori Yoshida

  3. Creative Research Institution, Hokkaido University, Sapporo, 001-0021, Japan

    Yukako Chiba

Authors
  1. Shugo Maekawa
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Takeo Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yutaka Asada
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shigetaka Yasuda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Midori Yoshida
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yukako Chiba
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Junji Yamaguchi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Junji Yamaguchi.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 12 kb)

Supplementary material 2 (PPT 2902 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maekawa, S., Sato, T., Asada, Y. et al. The Arabidopsis ubiquitin ligases ATL31 and ATL6 control the defense response as well as the carbon/nitrogen response. Plant Mol Biol 79, 217–227 (2012). https://doi.org/10.1007/s11103-012-9907-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-012-9907-0

Keywords

Search

Navigation