Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (5): 855-867.doi: 10.3864/j.issn.0578-1752.2024.05.003

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Identification of the Bru1 Genomic Region for Brown Rust Resistance and Functional Analysis of Candidate Resistance Genes in Sugarcane

WU QiBin1(), XIE WanJie1(), ZHONG Hui1, FENG ChunYan1, PAN HaoRan1, QI YiYing1, ZHANG JiSen2(), WANG HengBo1()   

  1. 1 College of Agriculture, Fujian Agriculture and Forestry University/National Engineering Research Center for Sugarcane/Key Laboratory of Sugarcane Biology and Genetic Breeding (Fujian), Ministry of Agriculture and Rural Affairs, Fuzhou 350002
    2 State Key Laboratory for Conservation and Utilization of Subtropical Agro-bioresources, Guangxi University, Nanning 530004
  • Received:2023-08-28 Accepted:2023-09-25 Online:2024-03-01 Published:2024-03-06
  • Contact: ZHANG JiSen, WANG HengBo

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Abstract:

【Objective】Sugarcane brown rust, caused by Puccinia melanocephala H. Sydow & P. Sydow, is one of the most destructive fungal diseases in sugarcane industry, leading to a reduction in sucrose content by 10% to 36%. Previous studies revealed that the major gene(s) for brown rust resistance was located in the Bru1 genomic region. The cloning of crucial candidate genes and their functional investigation should provide important candidate gene resources for breeding new sugarcane cultivars resistant to brown rust.【Method】In this study, the contig-level genomic information of sugarcane cultivar ROC22 was obtained by utilizing the PacBio Sequel Ⅱ sequencing platform, and the Bru1 region associated with brown rust candidate resistance gene was identified, annotated, cloned, and analyzed for tissue specificity, expression patterns in resistant and susceptible sugarcane cultivars, subcellular localization, and transient overexpression.【Result】The results demonstrated that, firstly, using tightly associated molecular markers R12H16 and 9O20-F4 within the Bru1 region, a total of 33 genes were annotated from this region, and five candidate resistance genes (Brrg99, Brrg103, Brrg108, Brrg115, and Brrg116) were selected based on the typical/conserved domains of the resistance genes. Secondly, the full-length sequence cDNA sequence of the Brrg116 gene with an open reading frame of 729 bp and encoding 242 amino acid residues, was cloned from sugarcane cultivar ROC22. The gene sequence was aligned with the genomic databases of Saccharum spontaneum, S. officinarum, and the closely related diploid species sorghum. A high degree of sequence similarity was observed between S. spontaneum and S. officinarum, exceeding 98%. In contrast, its similarity with sorghum was 93.77%. Phylogenetic tree analysis suggests that this gene may originate from S. spontaneum species during sugarcane domestication. qRT-PCR analysis showed its constitutive expression in various tissues of sugarcane cultivars, particularly with the highest expression level in the +1 leaf, which was 5.2 times higher than in the bud. Furthermore, significantly differential expression of Brrg116 was observed at 6 h and 72 h post-inoculation with the brown rust pathogen in resistant and susceptible sugarcane cultivars. Subcellular localization analysis indicated that the encoded protein of this gene was located on the cell membrane. Finally, the Brrg116 gene was transiently overexpressed in Nicotiana benthamiana leaves, followed by inoculation with Fusarium solani var. coeruleum. The color of Nicotiana benthamiana leaves showed a gradual deepening phenotype by 3,3'-diaminobenzidine (DAB) staining. The genes related to hypersensitive response, salicylic acid, and ethylene synthesis had a sustained upregulation pattern, evidencing that the expression of these genes can enhance plant disease resistance.【Conclusion】Brrg116 was constitutively expressed in different sugarcane tissues and in response to brown rust pathogen infection, it showed a rapidly induced expression pattern in the resistant sugarcane cultivar. Overexpression of Brrg116 could trigger defense responses through hormone signaling pathways such as salicylic acid and ethylene. It is thus hypothesized that this gene may play a significant regulatory role in enhancing plant disease resistance.

Key words: sugarcane, Bru1 genomic region, brown rust disease, candidate resistance gene, diagnostic markers

Table 1

Primers used in the study"

名称
Name		 引物序列
Primer sequences (5°-3°)		 备注
Note
Brrg116-F CAAGAAATGGGCAAGAGGATG 基因克隆
Gene cloning
Brrg116-R TTGTGAATCAGCCTTGCATTT
Brrg116-QF ACCTCCCTGACTCCTTTCAT 定量PCR引物
qRT-PCR primers
Brrg116-QR CACTTAGTTGCTCCATGTCCTC
GAPDH-F CACGGCCACTGGAAGCA 甘蔗内参基因
Sugarcane reference gene
GAPDH-R TCCTCAGGGTTCCTGATGCC
NtEF-1α-F
NtEF-1α-R		 TGCTGCTGTAACAAGATGGATGC
GAGATGGGGACAAAGGGGATT		 烟草内参基因
Tobacco reference gene
pMDC202-Brrg116-F CTCGACTCTAGAACTAGTCAAGAAATGGGCAAGAGGATG 过表达载体构建
Construction of overexpression vector
pMDC202-Brrg116-R ATTTTTTCTACCGGTACCTTGTGAATCAGCCTTGCATTT
pSuper-1300-Brrg116-F GGGGCCCGGGGTCGACCAAGAAATGGGCAAGAGGATG 亚细胞定位载体构建
Construction of subcellular localization vector
pSuper-1300-Brrg116-R CCCTTGCTCACCATGGTACCTTGTGAATCAGCCTTGCATTT

Fig. 1

Comparison of Bru1 genomic sequences with BAC sequences of markers R12H16 and 9O20-F4 and prediction of candidate genes Genetic map of CG Ⅶ-1: The genome sequence of sugarcane cultivar ROC22; R12H16 and 9O20-F4: Two markers closely linked to the Bru1 locus; CIR12E3 and CIR9O20: The BAC library sequences where the markers are located. The partial content of the figure is from research reports by COSTET, et al[6]"

Fig. 2

Multiple sequence alignment and phylogenetic analysis of multiple alleles of Brrg116 A: Displayed the representative orthologous gene sequences of S. spontaneum, S. officinarum, sugarcane cultivar, and sorghum; B: Showed the phylogenetic tree of Brrg116 multiple alleles. Pink indicated the multiple alleles from S. spontaneum. Light blue indicated the multiple alleles from S. spontaneum. Green indicated the multiple alleles from the closely related Sorghum bicolor"

Fig. 3

Tissue-specific expression of Brrg116 gene in sugarcane"

Fig. 4

The relative expression pattern of Brrg116 genes under brown rust infection ROC22 and YT60 are brown rust resistant and susceptible sugarcane cultivars, respectively"

Fig. 5

Subcellular localization of Brrg116 protein pSuper1300-35S::GFP and pSuper1300-35S::Brrg116::GFP vectors were represented empty and recombinant plasmids, respectively. Bar scale =50 µm"

Fig. 6

The symptom of Nicotiana benthamiana disease and the content of H2O2 and the expression of immune-related genes A and B represented the phenotype and DAB staining results of tobacco leaves inoculated with Fusarium solani var. coeruleum after Brrg116 gene transiently overexpressed in tobacco leaves. Symptom 1 d, 3 d and 7 d indicated the time of inoculation of Fusarium solani var. coeruleum after transient overexpression of the Brrg116 gene, respectively. C: The expression levels of genes related to tobacco hypersensitivity response and SA and ethylene synthesis after overexpression of Brrg116 gene. Different lowercase letters indicate significant differences at the P<0.05 probability level"

[1]
OZ M T, ALTPETER A, KARAN R, MEROTTO A, ALTPETER F. CRISPR/Cas9-mediated multi-allelic gene targeting in sugarcane confers herbicide tolerance. Frontiers in Genome Editing, 2021, 3: 673566.

doi: 10.3389/fgeed.2021.673566
[2]
高小宁, 吴自林, 黄咏虹, 刘睿, 齐永文. 甘蔗叶片响应褐锈病菌(Puccinia melanocephala)侵染的转录组分析. 中国农学通报, 2021, 37(24): 102-109.

doi: 10.11924/j.issn.1000-6850.casb2020-0622
GAO X N, WU Z L, HUANG Y H, LIU R, QI Y W. Response of sugarcane leaves to the infection of Puccinia melanocephala: Transcriptomic analysis. Chinese Agricultural Science Bulletin, 2021, 37(24): 102-109. (in Chinese)
[3]
DAUGROIS J H, GRIVET L, ROQUES D, HOARAU J Y, LOMBARD H, GLASZMANN J C, D'HONT A. A putative major gene for rust resistance linked with a RFLP marker in sugarcane cultivar ‘R570’. Theoretical and Applied Genetics, 1996, 92(8): 1059-1064.

doi: 10.1007/BF00224049
[4]
ASNAGHI C, ROQUES D, RUFFEL S, KAYE C, HOARAU J Y, TÉLISMART H, GIRARD J C, RABOIN L M, RISTERUCCI A M, GRIVET L, D'HONT A. Targeted mapping of a sugarcane rust resistance gene (Bru1) using bulked segregant analysis and AFLP markers. Theoretical and Applied Genetics, 2004, 108(4): 759-764.

doi: 10.1007/s00122-003-1487-6 pmid: 14586507
[5]
LE CUNFF L, GARSMEUR O, RABOIN L M, PAUQUET J, TELISMART H, SELVI A, GRIVET L, PHILIPPE R, BEGUM D, DEU M, COSTET L, WING R, GLASZMANN J C, D'HONT A. Diploid/polyploid syntenic shuttle mapping and haplotype-specific chromosome walking toward a rust resistance gene (Bru1) in highly polyploid sugarcane (2n approximately 12x approximately 115). Genetics, 2008, 180(1): 649-660.

doi: 10.1534/genetics.108.091355 pmid: 18757946
[6]
COSTET L, LE CUNFF L, ROYAERT S, RABOIN L M, HERVOUET C, TOUBI L, TELISMART H, GARSMEUR O, ROUSSELLE Y, PAUQUET J, NIBOUCHE S, GLASZMANN J C, HOARAU J Y, D'HONT A. Haplotype structure around Bru1 reveals a narrow genetic basis for brown rust resistance in modern sugarcane cultivars. Theoretical and Applied Genetics, 2012, 125(5): 825-836.

doi: 10.1007/s00122-012-1875-x
[7]
WANG H B, CHEN P H, YANG Y Q, D'HONT A, LU Y H. Molecular insights into the origin of the brown rust resistance gene Bru1 among Saccharum species. Theoretical and Applied Genetics, 2017, 130(11): 2431-2443.

doi: 10.1007/s00122-017-2968-3
[8]
李文凤, 王晓燕, 黄应昆, 张荣跃, 单红丽, 尹炯, 罗志明. 31份甘蔗野生核心种质资源褐锈病抗性鉴定及Bru1基因的分子检测. 作物学报, 2015, 41(5): 806-812.
LI W F, WANG X Y, HUANG Y K, ZHANG R Y, SHAN H L, YIN J, LUO Z M. Identification of resistance to brown rust and molecular detection of Bru1 gene in 31 wild core sugarcane germplasms. Acta Agronomica Sinica, 2015, 41(5): 806-812. (in Chinese)

doi: 10.3724/SP.J.1006.2015.00806
[9]
左为亮. 玉米抗丝黑穗病主效QTL的克隆与抗病机理研究[D]. 北京: 中国农业大学, 2014.
ZUO W L. Cloning and characterization of a major QTL conferring resistance to head smut in maize[D]. Beijing: China Agricultural University, 2014. (in Chinese)
[10]
ZUO W L, CHAO Q, ZHANG N, YE J R, TAN G Q, LI B L, XING Y X, ZHANG B Q, LIU H J, FENGLER K A, ZHAO J, ZHAO X R, CHEN Y S, LAI J S, YAN J B, XU M L. A maize wall-associated kinase confers quantitative resistance to head smut. Nature Genetics, 2015, 47(2): 151-157.

doi: 10.1038/ng.3170 pmid: 25531751
[11]
白团辉, 李莉, 郑先波, 王苗苗, 宋尚伟, 焦健, 宋春晖. 柱状苹果Co基因的筛选与候选基因分析. 中国农业科学, 2019, 52(23): 4350-4363. doi: 10.3864/j.issn.0578-1752.2019.23.015.
BAI T H, LI L, ZHENG X B, WANG M M, SONG S W, JIAO J, SONG C H. Screening and expression analysis of Co candidate genes in columnar apple. Scientia Agricultura Sinica, 2019, 52(23): 4350-4363. doi: 10.3864/j.issn.0578-1752.2019.23.015. (in Chinese)
[12]
刘新龙, 毛钧, 陆鑫, 马丽, Karen Sarah AITKEN, Phillip Andrew JACKSON, 蔡青, 范源洪. 甘蔗SSR和AFLP分子遗传连锁图谱构建. 作物学报, 2010, 36(1): 177-183.
LIU X L, MAO J, LU X, MA L, AITKEN K S, JACKSON P A, CAI Q, FAN Y H. Construction of molecular genetic linkage map of sugarcane based on SSR and AFLP markers. Acta Agronomica Sinica, 2010, 36(1): 177-183. (in Chinese)

doi: 10.3724/SP.J.1006.2010.00177
[13]
ZHANG J S, NAGAI C, YU Q Y, PAN Y-B, AYALA-SILVA T, SCHNELL R J, COMSTOCK J C, ARUMUGANATHAN A K, MING R. Genome size variation in three Saccharum species. Euphytica, 2012, 185(3): 511-519.

doi: 10.1007/s10681-012-0664-6
[14]
陈兴龙, 谢锦芳, 巫彬, 冯晓敏, 黄咏虹, 高小宁, 刘睿, 吴嘉云, 陈骏佳, 齐永文. 甘蔗CP84-1198×ROC22杂交群体抗褐锈病Bru1基因分子检测. 甘蔗糖业, 2020, 49(4): 8-13.
CHEN X L, XIE J F, WU B, FENG X M, HUANG Y H, GAO X N, LIU R, WU J Y, CHEN J J, QI Y W. Molecular detection of sugarcane brown rust resistance gene Bru1 in CP84-1198×ROC22 population. Sugarcane and Canesugar, 2020, 49(4): 8-13. (in Chinese)
[15]
ZHANG J S, ZHANG X T, TANG H B, ZHANG Q, HUA X T, MA X K, ZHU F, JONES T, ZHU X G, 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 F, ARRO J, HAN J O, CHAKRABARTY S, PUSHKO M, ZHANG W P, MA Y H, MA P P, LÜ M J, CHEN F M, ZHENG G Y, XU J S, YANG Z H, DENG F, CHEN X Q, LIAO Z Y, ZHANG XX X, LIN Z C, LIN H, YAN H S, KUANG Z, ZHONG W M, LIANG P P, WANG G F, YUAN Y, SHI J X, HOU J X, LIN J X, JIN J J, CAO P J, SHEN Q C, JIANG Q, ZHOU P, MA Y Y, ZHANG X D, XU R R, LIU J, ZHOU Y M, JIA H F, MA Q, QI R, ZHANG Z L, FANG J P, FANG H K, SONG J J, WANG M J, DONG G R, WANG G, CHEN Z, MA T, LIU H, DHUNGANA S R, HUSS S E, YANG X P, SHARMA A, TRUJILLO J H, MARTINEZ M C, HUDSON M, RIASCOS J J, SCHULER M, CHEN L Q, BRAUN D M, LI L, YU Q Y, WANG J P, WANG K, SCHATZ M C, HECKERMAN D, VAN SLUYS M A, SOUZA G M, MOORE P H, SANKOFF D, VANBUREN R, PATERSON A H, NAGAI C, MING R. Allele-defined genome of the autopolyploid sugarcane Saccharum spontaneum L.. Nature Genetics, 2018, 50(11): 1565-1573.

doi: 10.1038/s41588-018-0237-2
[16]
ZHANG Q, QI Y Y, PAN H R, TANG H B, WANG G, HUA X T, WANG Y J, LIN L Y, LI Z, LI Y H, YU F, YU Z H, HUANG Y J, WANG T Y, MA P P, DOU M J, SUN Z Y, WANG Y B, WANG H B, ZHANG X T, YAO W, WANG Y T, LIU X L, WANG M J, WANG J P, DENG Z H, XU J S, YANG Q H, LIU Z J, CHEN B S, ZHANG M Q, MING R, ZHANG J S. Genomic insights into the recent chromosome reduction of autopolyploid sugarcane Saccharum spontaneum. Nature Genetics, 2022, 54(6): 885-896.

doi: 10.1038/s41588-022-01084-1
[17]
李文凤, 王晓燕, 黄应昆, 张荣跃, 单红丽, 罗志明, 尹炯. 101份中国甘蔗主要育种亲本褐锈病抗性鉴定及Bru1基因的分子检测. 作物学报, 2016, 42(9): 1411-1416
LI W F, WANG X Y, HUANG Y K, ZHANG R Y, SHAN H L, LUO Z M. Identification of resistance to brown rust and molecular detection of Bru1 gene in 101 main sugarcane breeding parents in China. Acta Agronomica Sinica, 2016, 42(9): 1411-1416. (in Chinese)

doi: 10.3724/SP.J.1006.2016.01411
[18]
杜翠翠, 吴明星, 张雅婷, 谢婉婕, 张积森, 王恒波. 甘蔗割手密种糖转运蛋白基因SsSWEET11的克隆与功能分析. 作物学报, 2023, 49(9): 2385-2397.

doi: 10.3724/SP.J.1006.2023.24232
DU C C, WU M X, ZHANG Y T, XIE W J, ZHANG J S, WANG H B. Cloning and functional analysis of sucrose transporter protein SsSWEET11 gene in sugarcane (Saccharum spontaneum L.). Acta Agronomica Sinica, 2023, 49(9): 2385-2397. (in Chinese)
[19]
LIVAK K J, SCHMITTGEN T D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods, 2001, 25(4): 402-408.

doi: 10.1006/meth.2001.1262 pmid: 11846609
[20]
王恒波, 张畅, 吴明星, 李湘, 蒋钟莉, 林容潇, 郭晋隆, 阙友雄. 甘蔗割手密种NAC转录因子ATAF亚家族鉴定及栽培品种ScNAC2基因的功能分析. 作物学报, 2023, 49(1): 46-61.

doi: 10.3724/SP.J.1006.2023.24005
WANG H B, ZHANG C, WU M X, LI X, JIANG Z L, LIN R X, GUO J L, QUE Y X. Genome-wide identification of NAC transcription factors ATAF subfamily in Sacchrum spontaneum and functional analysis of its homologous gene ScNAC2 in sugarcane cultivar. Acta Agronomica Sinica, 2023, 49(1): 46-61. (in Chinese)
[21]
LIU F, SUN T T, WANG L, SU W H, GAO S W, SU Y C, XU L P, QUE Y X. Plant jasmonate ZIM domain genes: Shedding light on structure and expression patterns of JAZ gene family in sugarcane. BMC Genomics, 2017, 18(1): 771.

doi: 10.1186/s12864-017-4142-3
[22]
MAO H Y, WANG W J, SU W H, SU Y C, LIU F, LI C N, WANG L, ZHANG X, XU L P, QUE Y X. Genome-wide identification, phylogeny, and expression analysis of Sec14-like PITP gene family in sugarcane. Plant Cell Reports, 2019, 38(5): 637-655.

doi: 10.1007/s00299-019-02394-1
[23]
SOHN S I, KIM Y H, KIM B R, LEE S Y, LIM C K, HUR J H, LEE J Y. Transgenic tobacco expressing the hrpN(EP) gene from Erwinia pyrifoliae triggers defense responses against Botrytis cinerea. Molecules and Cells, 2007, 24(2): 232-239.
[24]
BROGUE K, CHET I, HOLLIDAY M, CRESSMAN R, BIDDLE P, KNOWLTON S, MAUVAIS C J, BROGLIE R. Transgenic plants with enhanced resistance to the fungal pathogen Rhizoctonia solani. Science, 1991, 254(5035): 1194-1197.

doi: 10.1126/science.254.5035.1194
[25]
CHEN N, GOODWIN P H, HSIANG T. The role of ethylene during the infection of Nicotiana tabacum by Colletotrichum destructivum. Journal of Experimental Botany, 2003, 54(392): 2449-2456.

doi: 10.1093/jxb/erg289
[26]
YANG X P, ISLAM M S, SOOD S, MAYA S, HANSON E A, COMSTOCK J, WANG J P. Identifying quantitative trait loci (QTLs) and developing diagnostic markers linked to orange rust resistance in sugarcane (Saccharum spp.). Frontiers in Plant Science, 2018, 9: 350.

doi: 10.3389/fpls.2018.00350
[27]
李阳阳, 荆蓉蓉, 吕蓉蓉, 石鹏程, 李欣, 王芹, 吴丹, 周清元, 李加纳, 唐章林. 甘蓝型油菜湿害胁迫响应性状的全基因组关联分析及候选基因预测. 作物学报, 2019, 45(12): 1806-1821.

doi: 10.3724/SP.J.1006.2019.94027
LI Y Y, JING R R, LÜ R R, SHI P C, LI X, WANG Q, WU D, ZHOU Q Y, LI J N, TANG Z L. Genome-wide association analysis and candidate genes prediction of waterlogging-responding traits in Brassica napus L. Acta Agronomica Sinica, 2019, 45(12): 1806-1821. (in Chinese)
[28]
阚帅帅. 玉米主效抗丝黑穗病候选基因预测及dCAPS标记开发[D]. 哈尔滨: 东北农业大学, 2012.
QUE S S. Major resistance candidate gene prediction and dCAPS marker development of head smut in maize[D]. Haerbin:Northeaset Agricultural University, 2012. (in Chinese)
[29]
武冰冰, 林凤, 张春雨, 崔娜, 许玉凤, 李楠, 孙权. 玉米大斑病抗性基因Ht2定位区域内候选序列的生物信息学分析. 玉米科学, 2009, 17(4): 11-16.
WU B B, LIN F, ZHANG C Y, CUI N, XU Y F, LI N, SUN Q. Bioinformatics analysis of candidate sequence of resistance gene Ht2 to Exserohilum turcicum in corn. Journal of Maize Sciences, 2009, 17(4): 11-16. (in Chinese)
[30]
刘德新. 陆地棉遗传图谱加密与T1区域纤维品质QTL精细定位及候选基因鉴定[D]. 重庆: 西南大学, 2015.
LIU D X. Maker density increase of genetic map and fine mapping and candidate gene identification of a major QTL controlling fiber quality traits at T1 region in upland cotton[D]. Chongqing: Southwest University, 2015. (in Chinese)
[31]
D'HONT A, GRIVET L, FELDMANN P, GLASZMANN J C, RAO S, BERDING N. Characterisation of the double genome structure of modern sugarcane cultivars (Saccharum spp.) by molecular cytogenetics. Molecular and General Genetics, 1996, 250(4): 405-413.
[32]
GARSMEUR O, DROC G, ANTONISE R, GRIMWOOD J, POTIER B, AITKEN K, JENKINS J, MARTIN G, CHARRON C, HERVOUET C, COSTET L, YAHIAOUI N, HEALEY A, SIMS D, CHERUKURI Y, SREEDASYAM A, KILIAN A, CHAN A, VAN SLUYS M A, SWAMINATHAN K, TOWN C, BERGÈS H, SIMMONS B, GLASZMANN J C, VAN DER VOSSEN E, HENRY R, SCHMUTZ J, D’HONT A. A mosaic monoploid reference sequence for the highly complex genome of sugarcane. Nature Communications, 2018, 9: 2638.

doi: 10.1038/s41467-018-05051-5 pmid: 29980662
[33]
GIANNAKOPOULOU A, BIALAS A, KAMOUN S, VLEESHOUWERS V G A A. Plant immunity switched from bacteria to virus. Nature Biotechnology, 2016, 34(4): 391-392.

doi: 10.1038/nbt.3538 pmid: 27054993
[34]
DANG F F, WANG Y N, YU L, EULGEM T, LAI Y, LIU Z Q, WANG X, QIU A L, ZHANG T X, LIN J, CHEN Y S, GUAN D Y, CAI H Y, MOU S L, HE S L. CaWRKY40, a WRKY protein of pepper, plays an important role in the regulation of tolerance to heat stress and resistance to Ralstonia solanacearum infection. Plant, Cell & Environment, 2013, 36(4): 757-774.
[35]
CHEN C H, JOST M, CLARK B, MARTIN M, MATNY O, STEFFENSON B J, FRANCKOWIAK J D, MASCHER M, SINGH D, PEROVIC D, RICHARDSON T, PERIYANNAN S, LAGUDAH E S, PARK R F, DRACATOS P M. BED domain-containing NLR from wild barley confers resistance to leaf rust. Plant Biotechnology Journal, 2021, 19(6): 1206-1215.

doi: 10.1111/pbi.13542 pmid: 33415836
[36]
MARCHAL C, ZHANG J P, ZHANG P, FENWICK P, STEUERNAGEL B, ADAMSKI N M, BOYD L, MCINTOSH R, WULFF B B H, BERRY S, LAGUDAH E, UAUY C. BED-domain-containing immune receptors confer diverse resistance spectra to yellow rust. Nature Plants, 2018, 4(9): 662-668.

doi: 10.1038/s41477-018-0236-4 pmid: 30150615
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