受青枯菌诱导的花生根酵母双杂交文库构建和AhRRS5互作蛋白的筛选

doi:10.3724/SP.J.1006.2021.04254

Abstract

Abstract:

The overexpression of peanut AhRRS5 gene can significantly improve tobacco resistance to bacterial wilt in previous studies. To further explore signaling pathway of the NBS-LRR resistance protein AhRRS5 responding to Ralstonia solanacearum infection in peanut, the interaction proteins of AhRRS5 were screened by yeast two hybrid technology based on the construction of peanut root normalized three-frame libraries induced by Ralstonia solanacearum. Total RNA was extracted from peanut roots at different time points after Ralstonia solanacearum infection. The mRNA was isolated and purified, then double stranded cDNA was synthesized and normalized. The primary and secondary libraries were constructed by homologous recombination method. The titer of the secondary library was 1.44 × 10 ⁷ cfu mL^-1, the recombination rate was 100%, and the average length encoded by the inserted cDNA was more than 1000 bp. The bait vector pGBKT7-AhRRS5 was constructed by enzyme digestion and ligation method. Result showed that there was no toxicity and auto-activation in the yeast cells. The AD library plasmid and bait vector pGBKT7-AhRRS5 were co-transformed into yeast Y2H gold strain. After several screening and rotation verification, 12 candidate proteins were obtained, which were involved in plant growth and development, energy metabolism, hormone signal transduction, stress response and so on. The interaction of AhRRS5 with AhSBT1.6 was further confirmed by bimolecular fluorescence complementation assays (BiFC) in vivo. The relative expression levels of AhSBT1.6 genes revealed that there were significant differences in different tissues based on transcriptome profiling, indicating the potential involvement of AhSBT1.6 in regulating bacterial with resistance in peanut. This study lays a foundation for further study on the mechanism of NBS-LRR resistance protein AhRRS5 and its interaction protein in bacterial wilt resistance defense of peanut.

Key words: peanut, bacterial wilt, yeast-two-hybrid, interaction protein, AhSBT1.6, BiFC

CHEN Yu-Ting, LIU Lu, CHU Pan-Pan, WEI Jia-Xian, QIAN Hui-Na, CHEN Hua, CAI Tie-Cheng, ZHUANG Wei-Jian, ZHANG Chong. Construction of yeast two-hybrid cDNA library induced by Ralstonia solanacearum and interaction protein screening for AhRRS5 in peanut[J].Acta Agronomica Sinica, 2021, 47(11): 2134-2146.

Figures/Tables 8

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Table 1

Sequence analysis of candidate interacrting protein by yeast two-hybrid system"

克隆编号 Clone ID	蛋白名称 Protein name			基因编号 Gene ID		ORF是否完整 Complete ORF or not		功能 Function
Y2H-1	类枯草杆菌蛋白酶SBT1.6 Subtilisin-like protease SBT1.6			AH13G08570.1		是 Yes		调控植物发育和衰老, 应对环境胁迫和病原侵染发挥关键作用。 Regulate plant development and senescence, challenge to environmental stress and pathogen infection.
Y2H-2	半胱氨酸蛋白酶类RD21a Cysteine proteinase RD21a			AH16G42150.1		否 No		植物发育, 参与植物逆境胁迫和细胞程序性死亡, 响应病原菌侵染等。 Regulate plant development, involve in plant stress and programmed cell death, and response to pathogen infection, etc.
Y2H-3	类BEL1同源结构域蛋白1 BEL1-like homeodomain protein 1			AH12G34520.1		是 Yes		调控植物分生组织发育等。 Regulate the development of plant meristem.
Y2H-4	类糊精硫醇蛋白酶 Thiol protease aleurain-like			AH13G27250.1		是 Yes		植物代谢, 参与植物逆境胁迫和细胞程序性死亡, 响应病原菌侵染等。 Plant metabolism, involve in plant stress and programmed cell death, response to pathogen infection, etc.
Y2H-5	组蛋白赖氨酸N-甲基转移酶SUVR3 Histone-lysine N-methyltransferase SUVR3			AH10G29030.1		否 No		氨基酸降解。 Amino acid degradation.
Y2H-6	40S核糖体蛋白Sa-1 40S ribosomal protein Sa-1			AH19G26400.1		否 No		参与DNA修复、细胞凋亡以及基因表达调控等。 Involve in DNA repair, apoptosis and gene expression regulation.
克隆编号 Clone ID		蛋白名称 Protein name	基因编号 Gene ID		ORF是否完整 Complete ORF or not		功能 Function
Y2H-7		类枯草杆菌蛋白酶SBT1.6 Subtilisin-like protease SBT1.6	AH13G08570.1		是 No		调控植物发育和衰老, 应对环境胁迫和病原侵染发挥关键作用。 Regulate plant development and senescence, challenge to environmental stress and pathogen infection.
Y2H-8		未知蛋白 Unknown protein	AH20G21850.1		是 Yes		未知。 Unknown.
Y2H-9		V型质子ATP酶亚基C V-type proton ATPase subunit C	AH20G03980.1		否 No		氧化磷酸化。 Oxidative phosphorylation.
Y2H-10		脱水诱导蛋白Di19-3 Dehydration-induced 19 homolog 3	AH16G09740.1		否 No		响应非生物胁迫。 Response to abiotic stress.
Y2H-11		焦磷酸合酶 Pyrophosphate synthase	AH02G15900.1		是 Yes		脂质代谢和离子吸收相关。 Lipid metabolism and ion absorption.
Y2H-12		乙酰鸟氨酸脱乙酰酶 Acetylornithine deacetylase	AH05G03880.1		否 No		氨基酸生物合成相关。 Amino acid biosynthesis.

Table 1

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References 63

[1]	Wicker E, Grassart L, Coranson-Beaudu R, Mian D, Guilbaud C, Fegan M, Prior P. Ralstonia solanacearum strains from Martinique (French West Indies) exhibiting a new pathogenic potential. Appl Environ Microbiol, 2007, 73: 6790-6801. doi: 10.1128/AEM.00841-07
[2]	Zhang C, Chen H, Cai T C, Deng Y, Zhuang R R, Zhang N, Zeng Y H, Zheng Y X, Tang R H, Pan R L, Zhuang W J. Overexpression of a novel peanut NBS-LRR gene AhRRS5 enhances disease resistance to Ralstonia solanacearum in tobacco. Plant Biotechnol J, 2017, 15: 39-55. doi: 10.1111/pbi.2017.15.issue-1
[3]	何礼远, 康耀卫. 植物青枯菌(Pseudomonas solanacearum)致病机理. 自然科学进展, 1995, (1):9-18.
	He L Y, Kang Y W. Pathogenic mechanism of Pseudomonas solanacearum in plant. Nat Sci Prog, 1995, (1):9-18 (in Chinese with English abstract).
[4]	张明红. 花生青枯病的发生与综合防治. 农业科技通讯. 2019, (6):290-292.
	Zhang M H. Occurrence and integrated control of peanut bacterial wilt. Agricul Sci Tech Commun, 2019, (6):290-292 (in Chinese).
[5]	Kalia S, Rathour R. Current status on mapping of genes for resistance to leaf- and neck-blast disease in rice. 3 Biotech, 2019, 9: 209-223. doi: 10.1007/s13205-019-1738-0 pmid: 31093479
[6]	Deslandes L, Pileur F, Liaubet L, Camut S, Can C, Williams K, Holub E, Beynon J, Arlat M, Marco Y. Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. Mol Plant Microbe Interact, 1998, 11: 659-667. doi: 10.1094/MPMI.1998.11.7.659
[7]	Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng D X, Bittner-Eddy P, Beynon J, Marco Y. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci USA, 2002, 99: 2404-2409. doi: 10.1073/pnas.032485099
[8]	Deslandes L, Olivier J, Peeters N, Feng D X, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proc Natl Acad Sci USA, 2003, 100: 8024-8029. doi: 10.1073/pnas.1230660100
[9]	Bernoux M, Timmers T, Jauneau A, Brière C, de Wit J G M P, Marco Y, Deslandes L. RD19, an Arabidopsis cysteine protease required for RRS1-R-mediated resistance, is relocalized to the nucleus by the Ralstonia solanacearum PopP2 effector. Plant Cell, 2008, 20: 2252. doi: 10.1105/tpc.108.058685 pmid: 18708476
[10]	Tasset C, Bernoux M, Jauneau A, Pouzet C, Brière C, Jacquinod K S, Rivas S, Marco Y, Deslandes L. Autoacetylation of the Ralstonia solanacearum effector PopP2 targets a lysine residue essential for RRS1-R-mediated immunity in Arabidopsis. PLoS Pathog, 2010, 6: e1001202. doi: 10.1371/journal.ppat.1001202
[11]	Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y. RRS1 and RPS4 provide a dual resistance-gene system against fungal and bacterial pathogens. Plant J, 2010, 60: 218-226. doi: 10.1111/tpj.2009.60.issue-2
[12]	Ma Y, Guo H L, Hu L X, Martinez P P, Moschou N P, Cevik V, Ding P T, Duxbury Z, Sarris F P, Jones D G J. Arabidopsis distinct modes of depression of an immune receptor complex by two different bacterial effectors. Proc Natl Acad Sci USA, 2018, 115: 10218-10227. doi: 10.1073/pnas.1811858115
[13]	Sarris F P, Duxbury Z, Huh U S, Ma Y, Segonzac C, Sklenar J, Derbyshire P, Cevik V, Rallapalli G, Saucet B S, Wirthmueller L, Menke L H F, Sohn K H, Jones D G J. A Plant immune receptor detects pathogen effectors that target WRKY transcription factors. Cell, 2015, 161: 1089-1100. doi: 10.1016/j.cell.2015.04.024
[14]	Ngou P M B, Ahn H K, Ding P T, Redkar A, Brown H, Ma Y, Youles M, Tomlinson L, Jones D G J. Estradiol-inducible AvrRps4 expression reveals distinct properties of TIR-NLR-mediated effector-triggered immunity. J Exp Bot, 2020, 71: 2186-2197. doi: 10.1093/jxb/erz571
[15]	Saucet B S, Ma Y, Sarris F P, Furzer J O, Sohn K H, Jones D G J. Two linked pairs of Arabidopsis TNL resistance genes independently confer recognition of bacterial effector AvrRps4. Nat Commun, 2015, 6: 6338. doi: 10.1038/ncomms7338 pmid: 25744164
[16]	Godiard L, Sauviac L, Torii K U, Grenon O, Mangin B, Grimsley N H, Marco Y. ERECTA, an LRR receptor-like kinase protein controlling development pleiotropically affects resistance to bacterial wilt. Plant J, 2003, 36: 353-365. doi: 10.1046/j.1365-313X.2003.01877.x
[17]	Martin G B, Brommonschenkel S H, Chunwongse J, Frary A, Ganal M W, Spivey R, Wu T, Earle E D, Tanksley S D. Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science, 1993, 262: 1432-1436. pmid: 7902614
[18]	Scofield S R, Tobias C M, Rathjen J P, Chang J F, Lavelle D T, Michelmore R W, Staskawicz B J. Molecular basis of gene-for-gene specificity in bacterial speck disease of tomato. Science, 1996, 274: 2063-2065. pmid: 8953034
[19]	Deslandes L, Olivier J, Peeters N, Feng D X, Khounlotham M, Boucher C, Somssich I, Genin S, Marco Y. Physical interaction between RRS1-R, a protein conferring resistance to, bacterial wilt, and PopP2, a type III effector targeted to the plant, nucleus. Proc Natl Acad Sci USA, 2003, 100: 8024-8029. doi: 10.1073/pnas.1230660100
[20]	Mackey D, Belkhadir Y, Alonso J M, Ecker J M, Dangl J L. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell, 2003, 112: 380-389.
[21]	刘阳娜. 利用酵母双杂交系统筛选GmDREB5的互作蛋白及核蛋白筛选系统(NTT)的建立. 西北农林科技大学硕士学位论文, 陕西杨凌, 2007.
	Liu Y N. Screening of Interactor Protein with Soybean Transcription Factor, GmDREB5, Using Yeast Two-Hybrid System and Construction of a Nuclear Transcription Trap (NTT) System. MS Thesis of Northwest A&F University, Yangling, Shaanxi, China, 2007 (in Chinese with English abstract).
[22]	徐萍萍. 利用酵母双杂交技术筛选与马铃薯StERF5转录因子相互作用的蛋白质. 甘肃农业大学硕士学位论文, 甘肃兰州, 2018.
	Xu P P. Screening Proteins Interacting with StERF5 Transcription Factor of Potato by Yeast Two-hybrid Technique. MS Thesis of Gansu Agricultural University, Lanzhou, Gansu, China, 2018 (in Chinese with English abstract).
[23]	刘永惠, 沈一, 沈悦, 陈志德. 利用酵母双杂交系统筛选花生AhMYB44互作蛋白. 植物遗传资源学报, 2020, 21: 201-207.
	Liu Y H, Shen Y, Shen Y, Chen Z D. Yeast two-hybrid screening of the proteins interacting with AhMYB44 from peanut. J Plant Genet Resour, 2020, 21: 201-207 (in Chinese with English abstract).
[24]	朱佳慧, 徐秋芳, 袁平平, 倪海平, 周益军, 蒋选利, 杜何为. 水稻幼苗酵母双杂交cDNA文库的构建及鉴定. 江苏农业科学, 2018, 46(9):47-50.
	Zhu J H, Xu Q F, Yuan P P, Ni H P, Zhou Y J, Jiang X L, Du W H. Construction and identification of yeast two-hybrid cDNA library of rice seedlings. J Jiangsu Agric Sci, 2018, 46(9):47-50 (in Chinese).
[25]	马芳芳, 蒋明义. 外源ABA处理的玉米叶片酵母双杂交cDNA文库的构建及评价. 江苏农业科学, 2016, 44(4):58-61.
	Ma F F, Jiang M Y. Construction and evaluation of yeast two-hybrid cDNA library of corn leaf under exogenous ABA treatment. Jiangsu J Agric Sci, 2016, 44(4):58-61 (in Chinese).
[26]	许向阳, 裴童, 吴泰茹, 王子玉, 赵婷婷, 李景富, 杨欢欢, 姜景彬, 张贺. Cf-19介导的抗番茄叶霉病(Cladosporium fulvum)免疫应答酵母双杂交cDNA文库构建和鉴定. 东北农业大学学报, 2020, 51(5):10-16.
	Xu X Y, Pei T, Wu T R, Wang Z Y, Zhao T T, Li J F, Yang H H, Jiang J B, Zhang H. Construction and identification of yeast two-hybrid cDNA library for Cf-19 mediated resistance to Cladosporium fulvum infection in tomato. J Northeast Agric Univ, 2019, 51(5):10-16 (in Chinese with English abstract).
[27]	曹玲珑, 李冬兵, 熊大斌, 牛洪斌, 姜玉梅, 尹钧. 外源ABA处理大麦胚的均一化cDNA文库的构建. 麦类作物学报, 2014, 34: 912-916.
	Cao L L, Li D B, Xiong D B, Niu H B, Jiang Y M, Yin J. Construction of a normalized cDNA library of barley embryo treated with exogenous ABA. J Triticeae Crops, 2014, 34: 912-916 (in Chinese with English abstract).
[28]	王玉姣, 陈姗姗, 孙柏华, 艾聪聪, 王中洋, 张修国. 辣椒疫霉菌诱导辣椒酵母双杂交cDNA文库的构建及鉴定. 山东农业大学学报(自然科学版), 2018, 49: 379-382.
	Wang Y J, Chen S S, Sun B H, Ai C C, Wang Z Y, Zhang X G. Construction and characterization of yeast two-hybrid cDNA library derived from Capsicum annuum inoculated with Phytophthora capsici. Shandong Agric Univ (Nat Sci Edn), 2018, 49: 379-382 (in Chinese with English abstract).
[29]	张恒, 陈怡名, 张旭, 赵佳, 吴承云, 郝永利, 孙丽, 王海燕, 肖进, 王秀娥. 白粉菌诱导簇毛麦叶片酵母双杂交文库构建及CMPG1-V候选互作蛋白筛选. 南京农业大学学报, 2020, 43: 594-604.
	Zhang H, Chen Y M, Zhang X, Zhao J, Wu C Y, Hao Y L, Sun L, Wang H Y, Xiao J, Wang X E. Construction of yeast two-hybrid cDNA library of Haynaldia villosa leaves induced by Blumeria graminis f. sp. tritici and candidate interaction protein screening for CMPG1-V. J Nanjing Agric Univ, 2020, 43: 594-604 (in Chinese with English abstract).
[30]	Chen H, Zhang C, Cai T C, Deng Y, Zhou S B, Zheng Y X, Ma S W, Tang R H, Varshney K R, Zhuang W J. Identification of low Ca²⁺ stress-induced embryo apoptosis response genes in Arachis hypogaea by SSH-associated library lift (SSHaLL). Plant Biotechnol J, 2016, 14: 682-698. doi: 10.1111/pbi.12415 pmid: 26079063
[31]	Zhuang W J, Chen H, Yang M, Wang J P, Pandey K M, Zhang C, Chang W C, Zhang L S, Zhang X T, Tang R H, Garg V, Wang X J, Tang H B, Chow C N, Wang J P, Deng Y, Wang D P, Khan W A, Yang Q, Cai T C, Bajaj P, Wu K C, Guo B Z, Zhang X Y, Li J J, Liang F, Hu J, Liao B S, Liu S Y, Chitilineni A, Yan H S, Zheng Y X, Shan S H, Liu Q Z, Xie D Y, Wang Z Y, Khan A S, Ali N, Zhao C Z, Li X G, Luo Z L, Zhang S B, Zhuang R R, Peng Z, Wang S Y, Mamadou G, Zhuang Y H, Zhao Z F, Yu W C, Xiong F Q, Quan W P, Yuan M, Li Y, Zou H S, Xia H, Zha L, Fan J P, Yu J G, Xie W P, Yuan J Q, Chen K, Zhao S S, Chu W T, Chen Y T, Sun P C, Meng F B, Zhuo T, Zhao Y H, Li C J, He G H, Zhao Y L, Wang C C, Kavikishor B P, Pan R L, Paterson H A, Wang X Y, Ming R, Varshney K R. The genome of cultivated peanut provides insight into legume karyotypes, polyploid evolution and crop domestication. Nat Genet, 2019, 51: 865-876. doi: 10.1038/s41588-019-0402-2
[32]	Schmittgen T D. Livak K J. Analyzing real-time PCR data by the comparative CT method. Nat Protoc, 2008, 3: 1101-1108. pmid: 18546601
[33]	Gao X H, Jia R Y, Wang M S, Zhu D K, Chen S, Lin M, Yin Z Q, Wang Y, Chen X Y, Cheng A C. Construction and identification of a cDNA library for use in the yeast two-hybrid system from duck embryonic fibroblast cells post-infected with duck enteritis virus. Mol Biol Rep, 2014, 41: 467-475. doi: 10.1007/s11033-013-2881-z
[34]	Niño M C, Kang K K, Cho Y G. Genome-wide transcriptional response of papain-like cysteine protease-mediated resistance against Xanthomonas oryzae pv. oryzae in rice. Plant Cell Rep, 2020, 39: 457-472. doi: 10.1007/s00299-019-02502-1
[35]	Shindo T, Hoorn R A L V D. Papain-like cysteine proteases: key players at molecular battlefields employed by both plants and their invaders. Mol Plant Pathol, 2008, 9: 119-125.
[36]	Shindo T, Misas-Villamil J C, Hörger A C, Song J, Hoorn R A L V. A role in immunity for Arabidopsis cysteine protease RD21, the ortholog of the tomato immune protease C14. PLoS One, 2012, 7: e29317. doi: 10.1371/journal.pone.0029317
[37]	Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, Gu C, Ilyas M, Win J, Kamoun S, Hoorn R A L V. An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol, 2010, 154: 1794-1804. doi: 10.1104/pp.110.158030
[38]	Bozkurt T O, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, Cano L M, Jones A M, Huitema E, Hoorn R A L V, Kamoun S. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc Natl Acad Sci USA, 2011, 108: 20832-20837. doi: 10.1073/pnas.1112708109
[39]	Pogorelko G V, Parijat S J, William B R, Hütten M, Maier T R, Hewezi T, Paulus J, Hoorn R A L V, Grundler F M, Siddique S, Lionetti V, Zabotina O A, Baum T J. Re-targeting of a plant defense protease by a cyst nematode effector. Plant J, 2019, 98: 1000-1014. doi: 10.1111/tpj.14295
[40]	Linde K V D, Hemetsberger C, Kastner C, Kaschani F, van der Hoorn R A L V D, Kumlehn J, Doehlemann G. A maize cystatin suppresses host immunity by inhibiting apoplastic cysteine proteases. Plant Cell, 2012, 24: 1285-1300. doi: 10.1105/tpc.111.093732
[41]	Linde K V D, Mueller A N, Hemetsberger C, Kashani F, Hoorn R A L V D, Doehlemann G. The maize cystatin CC9 interacts with apoplastic cysteine proteases. Plant Signal Behav, 2012, 7: 1397-1401. doi: 10.4161/psb.21902
[42]	Ziemann S, Linde K V D, Lahrmann U, Acar B, Kaschani F, Colby T, Kaiser M, Ding Y, Schmelz E, Huffaker A, Holton N, Zipfel C, Doehlemann G. An apoplastic peptide activates salicylic acid signalling in maize. Nat Plants, 2018, 4: 172-180. doi: 10.1038/s41477-018-0116-y
[43]	Mueller A N, Ziemann S, Treitschke S, Assmann D, Doehlemann G. Compatibility in the stillage maydis-maize interaction requires inhibition of host cysteine proteases by the fungal effector Pit2. PLoS Pathog, 2013, 9: e1003177. doi: 10.1371/journal.ppat.1003177
[44]	Xu L, Zhu L F, Tu L L, Guo X P, Long L, Sun L Q, Gao W, Zhang X L. Differential gene expression in cotton defense response to Verticillium dahliae by SSH. J Phytopath, 2011, 159: 606-615. doi: 10.1111/j.1439-0434.2011.01813.x
[45]	Zhang S Q, Xu Z P, Sun H, Sun L Q, Shaban M, Yang X Y, Zhu L F. Genome-wide identification of papain-like cysteine proteases in Gossypium hirsutum and functional characterization in response to Verticillium dahliae. Front Plant Sci, 2019, 10: 134. doi: 10.3389/fpls.2019.00134
[46]	Liu Y, Wang K R, Cheng Q, Kong D Y, Zhang X Z, Wang Z B, Wang Q, Xie Q, Yan J J, Chu J F, Ling H Q, Li Q, Miao J M, Zhao B Y. Cysteine protease RD21A regulated by E3 ligase SINAT4 is required for drought-induced resistance to Pseudomonas syringae in Arabidopsis. J Exp Bot, 2020, 71: 5562-5576. doi: 10.1093/jxb/eraa255 pmid: 32453812
[47]	Neuteboom L W, Ng J M, Kuyper M, Clijdesdale O R, Hooykaas P J, van der Zaal B J. Isolation and characterization of cDNA clones corresponding with mRNAs that accumulate during auxin-induced lateral root formation. Plant Mol Biol, 1999, 39: 273-287. pmid: 10080694
[48]	Neuteboom L W, Veth-Tello L M, Clijdesdale O R, Hooykaas P J, Zaal B J. A novel subtilisin-like protease gene from Arabidopsis thaliana is expressed at sites of lateral root emergence. DNA Res, 1999, 6: 13-19. pmid: 10231025
[49]	Zhao C, Johnson B J, Kositsup B, Beers E P. Exploiting secondary growth in Arabidopsis. Construction of xylem and bark cDNA libraries and cloning of three xylem endopeptidases. Plant Physiol, 2000, 123: 1185-1196. pmid: 10889267
[50]	Berger D, Altmann T. A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev, 2000, 14: 1119-1131.
[51]	Tanaka H, Onouchi H, Kondo M, Haranishimura I H, Nishimura M, Machida C, Machida Y. A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development, 2001, 128: 4681-4689. pmid: 11731449
[52]	Othman R, Nuraziyan A. Fruit-specific expression of papaya subtilase gene. J Plant Physiol, 2010, 167: 131-137. doi: 10.1016/j.jplph.2009.07.015
[53]	D’Erfurth I, Signor C L, Aubert G, Sanchez M, Vernoud V, Darchy B, Lherminier J, Bourion V, Bouteiller N, Bendahmane A, Buitink J, Prosperi J M, Thompson R, Burstin J, Gallardo K. A role for an endosperm-localized subtilase in the control of seed size in legumes. New Phytol, 2012, 196: 738-751. doi: 10.1111/nph.2012.196.issue-3
[54]	Roberts L N, Caputo C, Kade M, Criado M V, Barneix A J. Subtilisin-like serine proteases involved in N remobil-ization during grain filling in wheat. Acta Physiol Plant, 2011, 33: 1997-2001. doi: 10.1007/s11738-011-0712-1
[55]	Ramírez V, López A, Mauch-Mani B, Gil M J, Vera P. An extracellular subtilase switch for immune priming in Arabidopsis. PLoS Pathog, 2013, 9: e1003445. doi: 10.1371/journal.ppat.1003445
[56]	Serrano I, Buscaill P, Audran C, Pouzet C, Jauneau A, Rivas S. A non canonical subtilase attenuates the transcriptional activation of defence responses in Arabidopsis thaliana. eLife, 2016, 5: e19755. doi: 10.7554/eLife.19755
[57]	Pearce G, Yamaguchi Y, Barona G, Ryan C A. A subtilisin-like protein from soybean contains an embedded, cryptic signal that activates defense-related genes. Proc Natl Acad Sci USA, 2010, 107: 14921-14925. doi: 10.1073/pnas.1007568107
[58]	Yamaguchi Y, Barona G, Ryan C A, Pearce G. GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol, 2011, 156: 932-942. doi: 10.1104/pp.111.173096 pmid: 21478368
[59]	Fernández M B, Daleo G R, Guevara M G. Isolation and characterization of a Solanum tuberosum subtilisin-like protein with caspase-3 activity (StSBTc-3). Plant Physiol Biochem, 2015, 86: 137-146. doi: 10.1016/j.plaphy.2014.12.001
[60]	Fan T, Bykova N V, Rampitsch C, Tim X. Identification and characterization of a serine protease from wheat leaves. Eur J Plant Pathol, 2016, 146: 293-304. doi: 10.1007/s10658-016-0914-x
[61]	Duan X P, Zhang Z D, Wang J, Zuo K J. Characterization of a novel cotton subtilase gene GbSBT1 in response to extracellular stimulations and its role in Verticillium resistance. PLoS One, 2016, 11: e0153988. doi: 10.1371/journal.pone.0153988
[62]	Ekchaweng K, Khunjan U, Churngchow N. Molecular cloning and characterization of three novel subtilisin-like serine protease genes from Hevea brasiliensis. Physiol Mol Plant Pathol, 2017, 97: 79-95. doi: 10.1016/j.pmpp.2016.12.007
[63]	Saez-Aguayo S, Ralet M C, Berger A, Botran L, Ropartz D, North M P M. PECTIN METHYLESTERASE INHIBITOR6 promotes Arabidopsis mucilage release by limiting methylesterification of homogalacturonan in seed coat epidermal cells. Plant Cell, 2013, 25: 308-323. doi: 10.1105/tpc.112.106575

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Construction of yeast two-hybrid cDNA library induced by Ralstonia solanacearum and interaction protein screening for AhRRS5 in peanut

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