Bioinformatics and Expression Pattern Analysis of E3 Ubiquitin Ligase Gene PRT1 in Sugarcane

doi:10.7668/hbnxb.20193378

Abstract

Abstract:

In order to explore the interaction between ScPRT1 and Sporisorium scitamineum genes in sugarcane,this study used Saccharum spontaneum and Saccharum as research objects.The ScPRT1(GenBank Accession Number:MT747433)gene was cloned by RT-PCR and was analyzed by bioinformatics,quantitative Real-time PCR and subcellular localization.Bioinformatics analysis showed that the full-length cDNA of the ScPRT1 gene was 1 621 bp,including a complete open reading frame with 1 260 bp in length and encodes 419 amino acids.The ScPRT1 protein with two RING domains and one ZZ domain,was 46.56 ku in molecular weight and was an acidic and unstable hydrophilic protein with nuclear localization signal and no signal peptide.The higher structural elements of protein were mainly random coil.The results of qRT-PCR analysis showed that ScPRT1 was higher expressed in stem pith than in bud,epidermis and leaf.And ScPRT1 was significantly up-regulated under abscisic acid(ABA)stress and in the smut-resistant variety but significantly down-regulated in the smut-susceptible variety under Sporisorium scitamineum stress.The result of subcellular localization showed that ScPRT1 was localized in the nucleus.In the co-expression network between ScPRT1 and Sporisorium scitamineum genes,three genes that encoded effectors with aromatic amino acid residues at the N-terminal were found co-expressing with ScPRT1,and their proteins may interact directly.It is speculated that ScPRT1 plays an important role in sugarcane hormone signal transduction and response to smut infection.

Key words: Sugarcane, ScPRT1, Ubiquitin ligase, Bioinformatics, Expression pattern

LI Shanshan, HUANG Mengting, QING Yuhong, XU Jing, HUANG Junmei, LING Hui, QUE Youxiong, HUANG Ning. Bioinformatics and Expression Pattern Analysis of E3 Ubiquitin Ligase Gene PRT1 in Sugarcane[J]. Acta Agriculturae Boreali-Sinica, 2023, 38(1): 168-177. doi: 10.7668/hbnxb.20193378.

/ / Recommend / Download Citations

URL: http://www.hbnxb.net/EN/10.7668/hbnxb.20193378

http://www.hbnxb.net/EN/Y2023/V38/I1/168

Figures/Tables 7

Tab.1 Primers used in this study

引物Primer	正义链/反义链引物序列(5'—3') Sense primer/Anti-sense primer (5'—3')
ScPRT1	GTGGCCAGACGAATCGAGG/TTTCGTTCACGCAGTTCATCC
YFP-ScPRT1	CGAACGATACTCGAGGTCGACATGACAAGTTTGTACAAAAAAGTTGGGT/GCTCACCATACTAGTGGATCCGAGTGCCTGATCCTCCTCGT
q-ScPRT1	TCATGCCCTCTCTGTACGGA/AATGCACCAGGAGCTACCAC
SARMp1	TGGACTTGGTCAGTTGGAAACA/TGTTCCTGAAGCCTATGTTGCT
ACAD	CGTGGCATGGATCTGATGGT/AGCCTGCTCCAGTTCAATCC
CUL	TGCTGAATGTGTTGAGCAGC/TTGTCGCGCTCCAAGTAGTC
CAC	ACAACGTCAGGCAAAGCAAA/AGATCAACTCCACCTCTGCG

Fig.1 Identification and analysis of PRT1 gene in Saccharum spontaneum and Saccharum hybrid cultivar A.Analysis of conserved domain of PRT1s from S.spontaneum and S. hybrid cultivar;B.Chromosomal location of PRT1s in S.spontaneum;C.Prediction of cis-elements of PRT1s in S.spontaneum;D.Sequence alignment of PRT1s from S.spontaneum and S. hybrid cultivar.

Fig.2 Bioinformatics analysis of sugarcane ScPRT1 A.The agarose electrophoretic result of PCR product of S.hybrid cultivar PRT1 gene:M.Marker 1 kb plus DNA Marker(Transgen,Beijing,China);B.Conserved domain prediction of PRT1 in S.hybrid cultivar;C.Nucleotide sequence of the PRT1 gene and its encoded amino acid sequence in S. hybrid cultivar;D.Tertiary structure of PRT1 in S. hybrid cultivar.

Fig.3 Expression of ScPRT1 gene in different tissues Different lowercase letters indicate significant difference(P<0.05).The same as Fig.4.

Fig.4 Expression of ScPRT1 gene under different stresses A.Salicylic acid,Methyl jasmonate and abscisic acid stress;B.Sporisorium scitamineum stress.

Fig.5 The subcellular localization of ScPRT1 in the epidermal cells of Nicotiana benthamiana leaf The images were taken with fluorescence,bright field,and merge field.35S∷YFP.The transient expression of empty vector pCAMPIA2300-YFP.35S∷ScPRT1∷YFP.The transient expression of vector PCAMBIA2300-ScPRT1-YFP.

Fig.6 Construction and analysis of co-expression network between ScPRT1 and Sporisorium scitamineum A.Co-expression network of S.hybrid cultivar PRT1 and Sporisorium scitamineum genes;B.Structural analysis of effector protein of Sporisorium scitamineum in co-expression network.

References 51

[1]	Arruda P. Genetically modified sugarcane for bioenergy generation[J]. Current Opinion in Biotechnology, 2012, 23(3):315-322.doi:10.1016/j.copbio.2011.10.012. doi: 10.1016/j.copbio.2011.10.012 pmid: 22093808
[2]	班权伦. 甘蔗种植现状和发展对策浅议[J]. 南方农业, 2016, 10(5):29-30.doi:10.19415/j.cnki.1673-890x.2016.15.015. doi: 10.19415/j.cnki.1673-890x.2016.15.015
	Ban Q L. Ban Q L. Discussion on the present situation and development countermeasures of sugarcane planting[J]. South China Agriculture, 2016, 10(5):29-30.
[3]	Que Y X, Su Y C, Guo J L, Wu Q B, Xu L P. A global view of transcriptome dynamics during Sporisorium scitamineum challenge in sugarcane by RNA-Seq[J]. PLoS One, 2014, 9(8):e106476.doi:10.1371/journal.pone.0106476. doi: 10.1371/journal.pone.0106476 URL
[4]	Ling H, Fu X Q, Huang N, Zhong Z F, Su W H, Lin W X, Cui H T, Que Y X. A sugarcane smut fungus effector simulates the host endogenous elicitor peptide to suppress plant immunity[J]. The New Phytologist, 2022, 233(2):919-933.doi:10.1111/nph.17835. doi: 10.1111/nph.17835 URL
[5]	Xu F Q, Xue H W. The ubiquitin-proteasome system in plant responses to environments[J]. Plant,Cell & Environment, 2019, 42(10):2931-2944.doi:10.1111/pce.13633. doi: 10.1111/pce.13633
[6]	Wang J, Qin H, Zhou S R, Wei P C, Zhang H W, Zhou Y, Miao Y C, Huang R F. The ubiquitin-binding protein OsDSK2a mediates seedling growth and salt responses by regulating gibberellin metabolism in rice[J]. The Plant Cell, 2020, 32(2):414-428.doi:10.1105/tpc.19.00593. doi: 10.1105/tpc.19.00593 pmid: 31826965
[7]	Ma X Y, Zhang C, Kim D Y, Huang Y Y, Chatt E, He P, Vierstra R D, Shan L B. Ubiquitylome analysis reveals a central role for the ubiquitin-proteasome system in plant innate immunity[J]. Plant Physiology, 2021, 185(4):1943-1965.doi:10.1093/plphys/kiab011. doi: 10.1093/plphys/kiab011 pmid: 33793954
[8]	Kats I, Khmelinskii A, Kschonsak M, Huber F, Knieβ R A, Bartosik A, Knop M. Mapping degradation signals and pathways in a eukaryotic N-terminome[J]. Molecular Cell, 2018, 70(3):488-501.doi:10.1016/j.molcel.2018.03.033. doi: S1097-2765(18)30236-3 pmid: 29727619
[9]	Timms R T, Zhang Z Q, Rhee D Y, Harper J W, Koren I, Elledge S J. A glycine-specific N-degron pathway mediates the quality control of protein N-myristoylation[J]. Science, 2019, 365(6448):eaaw4912.doi:10.1126/science.aaw4912. doi: 10.1126/science.aaw4912 URL
[10]	Deng F Y, Guo T W, Lefebvre M, Scaglione S, Antico C J, Jing T, Yang X, Shan W X, Ramonell K M. Expression and regulation of ATL9,an E3 ubiquitin ligase involved in plant defense[J]. PLoS One, 2017, 12(11):e0188458.doi:10.1371/journal.pone.0188458. doi: 10.1371/journal.pone.0188458 URL
[11]	Li W, Zhong S H, Li G J, Li Q, Mao B Z, Deng Y W, Zhang H J, Zeng L J, Song F M, He Z H. Rice RING protein OsBBI1 with E3 ligase activity confers broad-spectrum resistance against Magnaporthe oryzae by modifying the cell wall defence[J]. Cell Research, 2011, 21(5):835-848.doi:10.1038/cr.2011.4. doi: 10.1038/cr.2011.4
[12]	Han P L, Dong Y H, Gu K D, Yu J Q, Hu D G, Hao Y J. The apple U-box E3 ubiquitin ligase MdPUB29 contributes to activate plant immune response to the fungal pathogen Botryosphaeria dothidea[J]. Planta, 2019, 249(4):1177-1188.doi:10.1007/s00425-018-03069-z. doi: 10.1007/s00425-018-03069-z
[13]	李晓辉. 黄瓜泛素E3连接酶基因的克隆及表达分析[D]. 郑州: 河南农业大学, 2014.
	Li X H. Cloning and expression analysis of E3Ubiquitin ligases in Cucumis sativus L.[D]. Zhengzhou: Henan Agricultural University, 2014.
[14]	Gibbs D J, Bailey M, Tedds H M, Holdsworth M J. From start to finish:amino-terminal protein modifications as degradation signals in plants[J]. The New Phytologist, 2016, 211(4):1188-1194.doi:10.1111/nph.14105. doi: 10.1111/nph.14105 URL
[15]	Holdsworth M J, Vicente J, Sharma G, Abbas M, Zubrycka A. The plant N-degron pathways of ubiquitin-mediated proteolysis[J]. Journal of Integrative Plant Biology, 2020, 62(1):70-89.doi:10.1111/jipb.12882. doi: 10.1111/jipb.12882
[16]	Stary S, Yin X J, Potuschak T, Schlögelhofer P, Nizhynska V, Bachmair A. PRT1 of Arabidopsis is a ubiquitin protein ligase of the plant N-end rule pathway with specificity for aromatic amino-terminal residues[J]. Plant Physiology, 2003, 133(3):1360-1366.doi:10.1104/pp.103.029272. doi: 10.1104/pp.103.029272 URL
[17]	Dong H, Dumenil J, Lu F H, Na L, Vanhaeren H, Naumann C, Klecker M, Prior R, Smith C, McKenzie N, Saalbach G, Chen L L, Xia T, Gonzalez N, Seguela M, Inze D, Dissmeyer N, Li Y H, Bevan M W. Ubiquitylation activates a peptidase that promotes cleavage and destabilization of its activating E3 ligases and diverse growth regulatory proteins to limit cell proliferation in Arabidopsis[J]. Genes & Development, 2017, 31(2):197-208.doi:10.1101/gad.292235.116. doi: 10.1101/gad.292235.116 URL
[18]	Chen I H, Chang J E, Wu C Y, Huang Y P, Hsu Y H, Tsai C H. An E3 ubiquitin ligase from Nicotiana benthamiana targets the replicase of Bamboo mosaic virus and restricts its replication[J]. Molecular Plant Pathology, 2019, 20(5):673-684.doi:10.1111/mpp.12784. doi: 10.1111/mpp.12784 pmid: 30924604
[19]	张玉叶, 黄宁, 肖新换, 黄珑, 苏炜华, 许莉萍, 阙友雄. 甘蔗B12D基因全长cDNA克隆与表达分析[J]. 热带生物学报, 2014, 5(2):111-119.doi:10.15886/j.cnki.rdswxb.2014.02.011. doi: 10.15886/j.cnki.rdswxb.2014.02.011
	Zhang Y Y, Huang N, Xiao X H, Huang L, Su W H, Xu L P, Que Y X. Cloning and expression analysis of full cDNA of B12D gene in sugarcane[J]. Journal of Tropical Biology, 2014, 5(2):111-119.
[20]	Ling H, Wu Q B, Guo J L, Xu L P, Que Y X. Comprehensive selection of reference genes for gene expression normalization in sugarcane by real time quantitative rt-PCR[J]. PLoS One, 2014, 9(5):e97469.doi:10.1371/journal.pone.0097469. doi: 10.1371/journal.pone.0097469 URL
[21]	Que Y X, Xu L P, Wu Q B, Liu Y F, Ling H, Liu Y H, Zhang Y Y, Guo J L, Su Y C, Chen J B, Wang S S, Zhang C G. Genome sequencing of Sporisorium scitamineum provides insights into the pathogenic mechanisms of sugarcane smut[J]. BMC Genomics, 2014, 15(1):996.doi:10.1186/1471-2164-15-996. doi: 10.1186/1471-2164-15-996 URL
[22]	Zhang J S, Zhang X T, Tang H B, Zhang Q, Hua X T, Ma X K, Zhu F, Jones T, Zhu X, Bowers J, Wai C M, Zheng C F, Shi Y, Chen S, Xu X M, Yue J J, Nelson D R, Huang L X, Li Z, Xu H M, Zhou D, Wang Y J, Hu W C, Lin J S, Deng Y J, Pandey N, Mancini M, Zerpa D, Nguyen J K, Wang L M, Yu L, Xin Y H, Ge L, Arro J, Han J O, Chakrabarty S, Pushko M, Zhang W P, Ma Y H. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.[J]. Nature Genetics, 2018, 50(11):1565-1573.doi:10.1038/s41588-018-0237-2. doi: 10.1038/s41588-018-0237-2
[23]	Yang Y Y, Gao S W, Su Y C, Lin Z L, Guo J L, Li M J, Wang Z T, Que Y X, Xu L P. Transcripts and low nitrogen tolerance:Regulatory and metabolic pathways in sugarcane under low nitrogen stress[J]. Environmental and Experimental Botany, 2019, 163:97-111.doi:10.1016/j.envexpbot.2019.04.010. doi: 10.1016/j.envexpbot.2019.04.010 URL
[24]	Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. TBtools:An integrative toolkit developed for interactive analyses of big biological data[J]. Molecular Plant, 2020, 13(8):1194-1202.doi:10.1016/j.molp.2020.06.009. doi: 10.1016/j.molp.2020.06.009 URL
[25]	Letunic I, Khedkar S, Bork P. SMART:Recent updates,new developments and status in 2020[J]. Nucleic Acids Research, 2021, 49(D1):D458-D460.doi:10.1093/nar/gkaa937. doi: 10.1093/nar/gkaa937 pmid: 33104802
[26]	Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, van de Peer Y, Rouz P, Rombauts S. PlantCARE,a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences[J]. Nucleic Acids Research, 2002, 30(1):325-327.doi:10.1093/nar/30.1.325. doi: 10.1093/nar/30.1.325 URL
[27]	Wilkins M R, Gasteiger E, Bairoch A, Sanchez J C, Williams K L, Appel R D, Hochstrasser D F. Protein identification and analysis tools in the ExPASy server[J]. Methods in Moleular Biology, 1999, 112:531-552.doi:10.1385/1-59259-584-7:531. doi: 10.1385/1-59259-584-7:531
[28]	Sapay N, Guermeur Y, Deléage G. Prediction of amphipathic in-plane membrane anchors in monotopic proteins using a SVM classifier[J]. BMC Bioinformatics, 2006, 7:255.doi:10.1186/1471-2105-7-255. doi: 10.1186/1471-2105-7-255 pmid: 16704727
[29]	Zhou X G, Li Y, Zhang C X, Zheng W, Zhang G J, Zhang Y. Progressive and accurate assembly of multi-domain protein structures from cryo-EM density maps[J]. Nat Complct Sci, 2022, 2(4):265-275.doi:10.1038/s43588-022-00232-1. doi: 10.1038/s43588-022-00232-1
[30]	Nielsen H, Tsirigos K D, Brunak S, von Heijne G. A brief history of protein sorting prediction[J]. The Protein Journal, 2019, 38(3):200-216.doi:10.1007/s10930-019-09838-3. doi: 10.1007/s10930-019-09838-3
[31]	Nair R, Carter P, Rost B. NLSdb:Database of nuclear localization signals[J]. Nucleic Acids Research, 2003, 31(1):397-399.doi:10.1093/nar/gkg001. doi: 10.1093/nar/gkg001 URL
[32]	黄宁, 惠乾龙, 方振名, 李姗姗, 凌辉, 阙友雄, 袁照年. 甘蔗β-胡萝卜素异构酶基因家族的鉴定、定位和表达分析[J]. 作物学报, 2021, 47(5):882-893.doi:10.3724/SP.J.1006.2021.04128. doi: 10.3724/SP.J.1006.2021.04128
	Huang N, Hui Q L, Fang Z M, Li S S, Ling H, Que Y X, Yuan Z N. Identification,localization and expression analysis of beta-carotene isomerase gene family in sugarcane[J]. Acta Agronomica Sinica, 2021, 47(5):882-893. doi: 10.3724/SP.J.1006.2021.04128 URL
[33]	Huang N, Ling H, Liu F, Su Y C, Su W H, Mao H Y, Zhang X, Wang L, Chen R K, Que Y X. Identification and evaluation of PCR reference genes for host and pathogen in sugarcane-Sporisorium scitamineum interaction system[J]. BMC Genomics, 2018, 19(1):479.doi:10.1186/s12864-018-4854-z. doi: 10.1186/s12864-018-4854-z pmid: 29914370
[34]	Livak K J, Schmittgen T D. Analysis of relative gene expression data using Real-time quantitative PCR and the 2^-ΔΔCT method[J]. Methods, 2001, 25(4):402-408.doi:10.1006/meth.2001.1262. doi: 10.1006/meth.2001.1262 pmid: 11846609
[35]	郑清雷, 余陈静, 姚坤存, 黄宁, 阙友雄, 凌辉, 许莉萍. 甘蔗Rieske Fe/S蛋白前体基因ScPetC的克隆及表达分析[J]. 作物学报, 2020, 46(6):844-857.doi:10.3724/SP.J.1006.2020.94171. doi: 10.3724/SP.J.1006.2020.94171
	Zheng Q L, Yu C J, Yao K C, Huang N, Que Y X, Ling H, Xu L P. Cloning and expression analysis of sugarcane Fe/S precursor protein gene ScPetC[J]. Acta Agronomica Sinica, 2020, 46(6):844-857. doi: 10.3724/SP.J.1006.2020.94171 URL
[36]	Rocafort M, Fudal I, Mesarich C H. Apoplastic effector proteins of plant-associated fungi and oomycetes[J]. Current Opinion in Plant Biology, 2020, 56:9-19.doi:10.1016/j.pbi.2020.02.004. doi: S1369-5266(20)30022-4 pmid: 32247857
[37]	Marchler-Bauer A, Lu S N, Anderson J B, Chitsaz F, Derbyshire M K, Deweese-Scott C, Fong J H, Geer L Y, Geer R C, Gonzales N R, Gwadz M, Hurwitz D I, Jackson J D, Ke Z X, Lanczycki C J, Lu F, Marchler G H, Mullokandov M, Omelchenko M V, Robertson C L, Song J S, Thanki N, Yamashita R A, Zhang D C, Zhang N G, Zheng C J, Bryant S H. CDD:A Conserved Domain Database for the functional annotation of proteins[J]. Nucleic Acids Research, 2010, 39(S1):D225-D229.doi:10.1093/nar/gkq1189. doi: 10.1093/nar/gkq1189 URL
[38]	Berezuk A M, Glavota S, Roach E J, Goodyear M C, Krieger J R, Khursigara C M. Outer membrane lipoprotein RlpA is a novel periplasmic interaction partner of the cell division protein FtsK in Escherichia coli[J]. Scientific Reports, 2018, 8(1):12933.doi:10.1038/s41598-018-30979-5. doi: 10.1038/s41598-018-30979-5 pmid: 30154462
[39]	Jorgenson M A, Chen Y, Yahashiri A, Popham D L, Weiss D S. The bacterial septal ring protein RlpA is a lytic transglycosylase that contributes to rod shape and daughter cell separation in Pseudomonas aeruginosa[J]. Molecular Microbiology, 2014, 93(1):113-128.doi:10.1111/mmi.12643. doi: 10.1111/mmi.12643 pmid: 24806796
[40]	Turek I, Wheeler J, Bartels S, Szczurek J, Wang Y H, Taylor P, Gehring C, Irving H. A natriuretic peptide from Arabidopsis thaliana (AtPNP-A)can modulate catalase 2 activity[J]. Scientific Reports, 2020, 10(1):19632.doi:10.1038/s41598-020-76676-0. doi: 10.1038/s41598-020-76676-0
[41]	Han X W, Altegoer F, Steinchen W, Binnebesel L, Schuhmacher J, Glatter T, Giammarinaro P I, Djamei A, Rensing S A, Reissmann S, Kahmann R, Bange G. A kiwellin disarms the metabolic activity of a secreted fungal virulence factor[J]. Nature, 2019, 565(7741):650-653.doi:10.1038/s41586-018-0857-9. doi: 10.1038/s41586-018-0857-9
[42]	Zylka M J, Sowa N A, Taylor-Blake B, Twomey M A, Herrala A, Voikar V, Vihko P. Prostatic acid phosphatase is an ectonucleotidase and suppresses pain by generating adenosine[J]. Neuron, 2008, 60(1):111-122.doi:10.1016/j.neuron.2008.08.024. doi: 10.1016/j.neuron.2008.08.024 pmid: 18940592
[43]	Labourel A, Frandsen K E H, Zhang F, Brouilly N, Grisel S, Haon M, Ciano L, Ropartz D, Fanuel M, Martin F, Navarro D, Rosso M N, Tandrup T, Bissaro B, Johansen K S, Zerva A, Walton P H, Henrissat B, Leggio L L, Berrin J G. A fungal family of lytic polysaccharide monooxygenase-like copper proteins[J]. Nature Chemical Biology, 2020, 16(3):345-350.doi:10.1038/s41589-019-0438-8. doi: 10.1038/s41589-019-0438-8 pmid: 31932718
[44]	田丽, 包满珠, 张蔚. 植物逆境相关RING finger蛋白的研究进展[J]. 湖北农业科学, 2018, 57(6):5-11,19.doi:10.14088/j.cnki.issn0439-8114.2018.06.001. doi: 10.14088/j.cnki.issn0439-8114.2018.06.001
	Tian L, Bao M Z, Zhang W. Research progress on stress-related RING finger proteins in plants[J]. Hubei Agricultural Sciences, 2018, 57(6):5-11,19.
[45]	Chen M J, Ni M. Red and far-red insensitive 2,a ring-domain zinc finger protein,mediates phytochrome-controlled seedling deetiolation responses[J]. Plant Physiology, 2006, 140(2):457-465.doi:10.1104/pp.105.073163. doi: 10.1104/pp.105.073163 URL
[46]	Liu K M, Wang L, Xu Y Y, Chen N, Ma Q B, Li F, Chong K. Overexpression of OsCOIN,a putative cold inducible zinc finger protein,increased tolerance to chilling,salt and drought,and enhanced proline level in rice[J]. Planta, 2007, 226(4):1007-1016.doi:10.1007/s00425-007-0548-5. doi: 10.1007/s00425-007-0548-5 URL
[47]	Xia Z L, Liu Q J, Wu J Y, Ding J Q. ZmRFP1,the putative ortholog of SDIR1,encodes a RING-H2 E3 ubiquitin ligase and responds to drought stress in an ABA-dependent manner in maize[J]. Gene, 2012, 495(2):146-153.doi:10.1016/j.gene.2011.12.028. doi: 10.1016/j.gene.2011.12.028 URL
[48]	Park C H, Chen S B, Shirsekar G, Zhou B, Khang C H, Songkumarn P, Afzal A J, Ning Y S, Wang R Y, Bellizzi M, Valent B, Wang G L. The Magnaporthe oryzae effector AvrPiz-t targets the RING E3 ubiquitin ligase APIP₆ to suppress pathogen-associated molecular pattern-triggered immunity in rice[J]. The Plant Cell, 2012, 24(11):4748-4762.doi:10.1105/tpc.112.105429. doi: 10.1105/tpc.112.105429 URL
[49]	Ma A F, Zhang D P, Wang G X, Wang K, Li Z, Gao Y H, Li H C, Bian C, Cheng J K, Han Y N, Yang S H, Gong Z Z, Qi J S. Verticillium dahliae effector VDAL protects MYB6 from degradation by interacting with PUB25 and PUB26 E3 ligases to enhance Verticillium wilt resistance[J]. The Plant Cell, 2021, 33(12):3675-3699.doi:10.1093/plcell/koab221. doi: 10.1093/plcell/koab221 URL
[50]	孙伟娜, 徐菁, 殷丽华, 徐晓丹, 柯希望, 左豫虎. 小豆EG45基因的亚细胞定位及其在抗病中的功能分析[M]// 彭友良,王文明,陈雪伟. 中国植物病理学会2019年学术年会论文集. 北京: 中国农业科技出版社, 2019:465.doi:10.26914/c.cnkihy.2019.020468. doi: 10.26914/c.cnkihy.2019.020468
	Sun W N, Xu Q, Yin L H, Xu X D, Ke X W, Zuo Y H. Subcellular localization and functional analysis of Adzuki bean EG 45 gene in disease resistance[M]// Peng Y L,Wang W M,Chen X W. Proceedings of the annual meeting of chinese society for plant pathology. Beijing: China Science and Technology Press, 2019:465.
[51]	Bange G, Altegoer F. Plants strike back:Kiwellin proteins as a modular toolbox for plant defense mechanisms[J]. Communicative & Integrative Biology, 2019, 12(1):31-33.doi:10.1080/19420889.2019.1586049. doi: 10.1080/19420889.2019.1586049

Please choose a citation manager

Content to export