Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Molecular cloning and functional characterisation of the tomato E3 ubiquitin ligase SlBAH1 gene

Shu-Mei Zhou A , Sai-Han Wang A , Chao Lin A , Yun-Zhi Song A , Xin-Xin Zheng A , Feng-Ming Song B C and Chang-Xiang Zhu A C
+ Author Affiliations
- Author Affiliations

A State Key Laboratory of Crop Biology, Shandong Key Laboratory of Crop Biology, College of Life Science, Shandong Agricultural University, Taian, Shandong 271018, PR China.

B Institute of Biotechnology, Zhejiang University, Hangzhou, Zhejiang 310029, PR China.

C Corresponding authors. Emails: zhchx@sdau.edu.cn; fmsong@zju.edu.cn

Functional Plant Biology 43(11) 1091-1101 https://doi.org/10.1071/FP16003
Submitted: 6 January 2016  Accepted: 1 July 2016   Published: 29 July 2016

Abstract

Emerging evidence suggests that E3 ligases play critical roles in diverse biological processes, including pathogen resistance in plants. In the present study, an ubiquitin ligase gene (SlBAH1) was cloned from a tomato plant, and the functions of the gene were studied. The SlBAH1 gene contained 1002 nucleotides and encodes a protein with 333 amino acids. The SlBAH1 protein contains a SPX domain and a RING domain. SlBAH1 displayed E3 ubiquitin ligase activity in vitro. SlBAH1 was shown to localise in the nucleus, cytoplasm and plasma membrane by a subcellular localisation assay. The expression of SlBAH1 was induced by various hormones and Botrytis cinerea Pers. treatment. SlBAH1-silencing in plants obtained by virus-induced gene silencing (VIGS) technology enhanced resistance to B. cinerea, and the expression of pathogenesis-related (PR) genes, including PR1, PR2, PR4, PR5, and PR7, was significantly increased. These results indicate that the SlBAH1-dependent activation of defence-related genes played a key role in the enhanced fungal resistance observed in the SlBAH1-silenced plants and may be related to the SA-dependent and JA-dependent signalling pathways.

Additional keywords: Botrytis cinerea, disease resistance.


References

Bernoux M, Ellis JG, Dodds PN (2011) New insights in plant immunity signaling activation. Current Opinion in Plant Biology 14, 512–518.
New insights in plant immunity signaling activation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht12jtL7K&md5=8ae2b72ebc7a3ac3f42dced39a802763CAS | 21723182PubMed |

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 5, e14426
ATL9, a RING zinc finger protein with E3 ubiquitin ligase activity implicated in chitin-and NADPH oxidase-mediated defense responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtlSlsQ%3D%3D&md5=5614862d79ed66abdc1fc997f0cfbe61CAS | 21203445PubMed |

Bu Q, Li H, Zhao Q, Jiang H, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Wang D, Li C (2009) The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development. Plant Physiology 150, 463–481.
The Arabidopsis RING finger E3 ligase RHA2a is a novel positive regulator of abscisic acid signaling during seed germination and early seedling development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlvFahsb4%3D&md5=ac195dc9db0f1ab10aee865afa68d4b1CAS | 19286935PubMed |

Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. The Plant Cell 20, 2586–2602.
Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFWms7nE&md5=a919a3be322d2c4bdc72651b12954cccCAS | 18849490PubMed |

Cheung MY, Zeng NY, Tong SW, Li FW, Zhao KJ, Zhang Q, Sun SS, Lam HM (2007) Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana. Journal of Experimental Botany 58, 4147–4159.
Expression of a RING-HC protein from rice improves resistance to Pseudomonas syringae pv. tomato DC3000 in transgenic Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlymtbk%3D&md5=c82f050c9ae60113481f5ed902268ccdCAS | 18182423PubMed |

Chisholm ST, Coaker G, Day B, Staskawicz BJ (2006) Host-microbe interactions: shaping the evolution of the plant immune response. Cell 124, 803–814.
Host-microbe interactions: shaping the evolution of the plant immune response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit1Kltbw%3D&md5=421d64eaf16c0eca1627ef48a91185f1CAS | 16497589PubMed |

Choi HW, Kim YJ, Lee SC, Hong JK, Hwang BK (2007) Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens. Plant Physiology 145, 890–904.
Hydrogen peroxide generation by the pepper extracellular peroxidase CaPO2 activates local and systemic cell death and defense response to bacterial pathogens.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlemsrbN&md5=fb10d4299cf471c5b9b70ad0a64bb031CAS | 17905862PubMed |

Ciechanover A, Orian A, Schwartz AL (2000) Ubiquitin-mediated proteolysis: biological regulation via destruction. BioEssays 22, 442–451.
Ubiquitin-mediated proteolysis: biological regulation via destruction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslWlsbk%3D&md5=f48efb7838cec2df894fd07943d33cbfCAS | 10797484PubMed |

Craig A, Ewan R, Mesmar J, Gudipati V, Sadanandom A (2009) E3 ubiquitin ligases and plant innate immunity. Journal of Experimental Botany 60, 1123–1132.
E3 ubiquitin ligases and plant innate immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFShs74%3D&md5=13455eff63e7d2981b8e41c83e274e6eCAS | 19276192PubMed |

Delauré SL, Van Hemelrijck W, De Bolle MFC, Cammue BPA, De Coninck BMA (2008) Building up plant defenses by breaking down proteins. Plant Science 174, 375–385.
Building up plant defenses by breaking down proteins.Crossref | GoogleScholarGoogle Scholar |

Dhawan R, Luo H, Foerster AM, Abuqamar S, Du HN, Briggs SD, Mittelsten Scheid O, Mengiste T (2009) HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis. The Plant Cell 21, 1000–1019.
HISTONE MONOUBIQUITINATION1 interacts with a subunit of the mediator complex and regulates defense against necrotrophic fungal pathogens in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFylu78%3D&md5=57d1e4222e804d978092245c8f9ea9edCAS | 19286969PubMed |

Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant-pathogen interactions. Nature Reviews. Genetics 11, 539–548.
Plant immunity: towards an integrated view of plant-pathogen interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovFOhtrs%3D&md5=7d34e3b31b0854f0b426cc15d60e7f4aCAS | 20585331PubMed |

Dreher K, Callis J (2007) Ubiquitin, hormones and biotic stress in plants. Annals of Botany 99, 787–822.
Ubiquitin, hormones and biotic stress in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnt1alt70%3D&md5=c937a59fefd408ad8fbe50c3f9c79019CAS | 17220175PubMed |

Egashira H, Kuwashima A, Ishiguro H, Fukushima K, Kaya T, Imanishi S (2000) Screening of wild accessions resistant to gray mold (Botrytis cinerea Pers.) in Lycopersicon. Acta Physiologiae Plantarum 22, 324–326.
Screening of wild accessions resistant to gray mold (Botrytis cinerea Pers.) in Lycopersicon.Crossref | GoogleScholarGoogle Scholar |

Fang S, Weissman AM (2004) A field guide to ubiquitylation. Cellular and Molecular Life Sciences 61, 1546–1561.

Fu ZQ, Dong X (2013) Systemic acquired resistance: turning local infection into global defense. Annual Review of Plant Biology 64, 839–863.
Systemic acquired resistance: turning local infection into global defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXosFSku7s%3D&md5=54bde97538b987ec8a58706fc7f5fe28CAS | 23373699PubMed |

Guerra D, Mastrangelo AM, Lopez-Torrejon G, Marzin S, Schweizer P, Stanca AM, del Pozo JC, Cattivelli L, Mazzucotelli E (2012) Identification of a protein network interacting with TdRF1, a wheat RING ubiquitin ligase with a protective role against cellular dehydration. Plant Physiology 158, 777–789.
Identification of a protein network interacting with TdRF1, a wheat RING ubiquitin ligase with a protective role against cellular dehydration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOktLk%3D&md5=11282ce6a16d1598520e79a7ac2f1ac8CAS | 22167118PubMed |

Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell 14, 889–902.
Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWktro%3D&md5=231f4a54020186073cf0d4255a3b1241CAS | 11971143PubMed |

Jones JDG, Dangl JL (2006) The plant immune system. Nature 444, 323–329.
The plant immune system.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1SgtbzO&md5=8c3478940ede75d28698c9946ce7d46eCAS |

Kawasaki T, Nam J, Boyes DC, Holt BF, Hubert DA, Wiig A, Dang JL (2005) A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1 and RPS2 mediated hypersensitive response. The Plant Journal 44, 258–270.
A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1 and RPS2 mediated hypersensitive response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFyhsb7E&md5=e967de3ceac3d5839f8a34a77c0c39a6CAS | 16212605PubMed |

Koiwai H, Tagiri A, Katoh S, Katoh E, Ichikawa H, Minami E, Nishizawa Y (2007) RING-H2 type ubiquitin ligase EL5 is involved in root development through the maintenance of cell viability in rice. The Plant Journal 51, 92–104.
RING-H2 type ubiquitin ligase EL5 is involved in root development through the maintenance of cell viability in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXotVyru7s%3D&md5=9b642d077a80bb2d462ded9bdf58f80eCAS | 17559513PubMed |

Kraft E, Stone SL, Ma L, Su N, Gao Y, Lau OS, Deng XW, Callis J (2005) Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis. Plant Physiology 139, 1597–1611.
Genome analysis and functional characterization of the E2 and RING-type E3 ligase ubiquitination enzymes of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlGmsLbF&md5=d77e645401b1d133d54448e4a781da04CAS | 16339806PubMed |

Lee DG, Ahsan N, Lee SH, Kang KY, Lee JJ, Lee BH (2007) An approach to identify cold-induced low-abundant proteins in rice leaf. Comptes Rendus Biologies 330, 215–225.
An approach to identify cold-induced low-abundant proteins in rice leaf.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktF2gu7c%3D&md5=f59cbf352b9b60f45177c6f4963a2cadCAS | 17434115PubMed |

Lee DH, Choi HW, Hwang BK (2011) The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response. Plant Physiology 156, 2011–2025.
The pepper E3 ubiquitin ligase RING1 gene, CaRING1, is required for cell death and the salicylic acid-dependent defense response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOrur3N&md5=ab5ec4645abb157b0769b5403dcf72dbCAS | 21628629PubMed |

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. The Plant Journal 56, 550–561.
RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsFSnsLnN&md5=d1e6b7c9202b28a6dfba0369836ac625CAS | 18643987PubMed |

Liu Y, Schiff M, Dinesh-Kumar SP (2002) Virus-induced gene silencing in tomato. The Plant Journal 31, 777–786.
Virus-induced gene silencing in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotFyjsbo%3D&md5=74182472a726b655f93202084c2252d5CAS | 12220268PubMed |

Molnár G, Bancoş S, Nagy F, Szekeres M (2002) Characterisation of BRH1, a brassinosteroid-responsive RING-H2 gene from Arabidopsis thaliana. Planta 215, 127–133.
Characterisation of BRH1, a brassinosteroid-responsive RING-H2 gene from Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 12012249PubMed |

Moon J, Parry G, Estelle M (2004) The ubiquitin-proteasome pathway and plant development. The Plant Cell 16, 3181–3195.
The ubiquitin-proteasome pathway and plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKnug%3D%3D&md5=c162d706ab202b8e935ad5dce6492a68CAS | 15579807PubMed |

Oh CS, Martin GB (2011) Effector-triggered immunity mediated by the Pto kinase. Trends in Plant Science 16, 132–140.
Effector-triggered immunity mediated by the Pto kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjtFClsrY%3D&md5=de0e502546e55339f2fd66f9febdca65CAS | 21112235PubMed |

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. The Plant Journal 50, 320–337.
A mutation in NLA, which encodes a RING‐type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvFektbs%3D&md5=71c96b7e96433460b8513d07d6b9d738CAS | 17355433PubMed |

Pieterse CMJ, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nature Chemical Biology 5, 308–316.
Networking by small-molecule hormones in plant immunity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXks12ktL4%3D&md5=505b7f8df952363d1c8adfcc793d71f7CAS |

Schwessinger B, Ronald PC (2012) Plant innate immunity: perception of conserved microbial signatures. Annual Review of Plant Biology 63, 451–482.
Plant innate immunity: perception of conserved microbial signatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1amsbo%3D&md5=070c6ac1db4a0c53bdc1cae474725a0dCAS | 22404464PubMed |

Song XJ, Huang W, Shi M, Zhu MZ, Lin HX (2007) A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase. Nature Genetics 39, 623–630.
A QTL for rice grain width and weight encodes a previously unknown RING-type E3 ubiquitin ligase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXksFersLk%3D&md5=368a4f610f97931824732cc0fbac854eCAS | 17417637PubMed |

Spain BH, Koo D, Ramakrishnan M, Dzudzor B, Colicelli J (1995) Truncated forms of a novel yeast protein suppress the lethality of a G protein α subunit deficiency by interacting with the β subunit. The Journal of Biological Chemistry 270, 25435–25444.
Truncated forms of a novel yeast protein suppress the lethality of a G protein α subunit deficiency by interacting with the β subunit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXovFyltLY%3D&md5=e0970d8788653746301cdbb036ff1234CAS | 7592711PubMed |

Stone SL, Hauksdóttir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiology 137, 13–30.
Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFOmtb4%3D&md5=5e90f8e2ebddac5f4ee7a99264ae689eCAS | 15644464PubMed |

Van Eck L, Schultz T, Leach JE, Scofield SR, Peairs FB, Botha AM, Lapitan NL (2010) Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance. Plant Biotechnology Journal 8, 1023–1032.
Virus-induced gene silencing of WRKY53 and an inducible phenylalanine ammonia-lyase in wheat reduces aphid resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhs1aktL3P&md5=56acf80eadd8593f6e176504d75bb6e1CAS | 20561246PubMed |

Velásquez AC, Chakravarthy S, Martin GB (2009) Virus-induced gene silencing (VIGS) in Nicotiana benthamiana and tomato. Journal of Visualized Experiments 28, 1292–1295.

Viaud M, Fillinger S, Liu W, Polepalli JS, Le Pêcheur P, Kunduru AR, Leroux P, Legendre L (2006) A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea. Molecular Plant–Microbe Interactions 19, 1042–1050.
A class III histidine kinase acts as a novel virulence factor in Botrytis cinerea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xos1Kjsr8%3D&md5=c58d4f6f77422655b70536612ae5eb13CAS | 16941908PubMed |

Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nature Reviews. Molecular Cell Biology 10, 385–397.
The ubiquitin-26S proteasome system at the nexus of plant biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsF2lsLs%3D&md5=4735383e151eb871301cd639013c5fd8CAS | 19424292PubMed |

Wang Y, Ribot C, Rezzonico E, Poirier Y (2004) Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis. Plant Physiology 135, 400–411.
Structure and expression profile of the Arabidopsis PHO1 gene family indicates a broad role in inorganic phosphate homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12nu7Y%3D&md5=b31cbdf0e9a7f84ff1bc3b43a0085f43CAS | 15122012PubMed |

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 Physiology 148, 1032–1041.
BAH1/NLA, a RING-type ubiquitin E3 ligase, regulates the accumulation of salicylic acid and immune responses to Pseudomonas syringae DC3000.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1GmtLjI&md5=d9803616d2d0693dd5bd5e6c66be4395CAS | 18753285PubMed |

Zeng LR, Vega-Sánchez ME, Zhu T, Wang GL (2006) Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions. Cell Research 16, 413–426.
Ubiquitination-mediated protein degradation and modification: an emerging theme in plant-microbe interactions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFSgu7o%3D&md5=a33b75a49e4fa4b59fbe7eb8bf6a8fd5CAS | 16699537PubMed |

Zhang Y, Yang C, Li Y, Zheng N, Chen H, Zhao Q, Gao T, Guo H, Xie Q (2007) SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis. The Plant Cell 19, 1912–1929.
SDIR1 is a RING finger E3 ligase that positively regulates stress-responsive abscisic acid signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXptFKnsrc%3D&md5=f9295112ecf15dff0c4c9e62e0e7d604CAS | 17573536PubMed |

Zhou S, Sun X, Yin S, Kong X, Zhou S, Xu Y, Luo Y, Wang W (2014) The role of the F-box gene TaFBA1 from wheat (Triticum aestivum L.) in drought tolerance. Plant Physiology and Biochemistry 84, 213–223.
The role of the F-box gene TaFBA1 from wheat (Triticum aestivum L.) in drought tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhs1KltbvK&md5=fe864012b7f6b524cf56e278d79e5118CAS | 25299612PubMed |