CrxV Regulates the Virulence of <i>Xanthomonas oryzae</i> pv. <i>oryzae</i>

LIN Yunuan; HOU Yunyu; MI Duo; LI Chunxia; TAO Jun

doi:10.15886/j.cnki.rdswxb.2021.04.006

Volume 12 Issue 4

Dec. 2021

Turn off MathJax

Article Contents

Article Navigation > Journal of Tropical Biology > 2021 > 12(4): 0000-4

LIN Yunuan, HOU Yunyu, MI Duo, LI Chunxia, TAO Jun. CrxV Regulates the Virulence of Xanthomonas oryzae pv. oryzae[J]. Journal of Tropical Biology, 2021, 12(4): 0000-4. doi: 10.15886/j.cnki.rdswxb.2021.04.006

Citation:

LIN Yunuan, HOU Yunyu, MI Duo, LI Chunxia, TAO Jun. CrxV Regulates the Virulence of Xanthomonas oryzae pv. oryzae[J]. Journal of Tropical Biology, 2021, 12(4): 0000-4. doi: 10.15886/j.cnki.rdswxb.2021.04.006

CrxV Regulates the Virulence of Xanthomonas oryzae pv. oryzae

doi: 10.15886/j.cnki.rdswxb.2021.04.006

LIN Yunuan^{1, 2
,},
HOU Yunyu¹,
MI Duo²,
LI Chunxia^{2
,
,},
TAO Jun²

1.
School of Life and Pharmaceutical Sciences, Hainan University
2.
College of Tropical Crops, Hainan University, Haikou, Hainan 570228, China

Received Date: 2021-04-24
Rev Recd Date: 2021-11-15

Available Online: 2021-12-20

Publish Date: 2021-12-25

Abstract

Proteins containing GGDEF and EAL domains are involved in the synthesis and degradation of the cell´s second messenger c-di-GMP. They are important regulators for bacteria to respond to the external environment, and may be involved in the interaction between pathogen and host. We analyzed the effect of CrxV containing a GGDEF and an EAL domain on the virulence and some related virulent factors of Xanthomonas oryzae pv. oryzae (Xoo), a causal agent of bacterial leaf blight of rice. We used the homology recombination method to construct crxV mutant (ΔcrxV), and then the leaf clipping method to analyze the infection ability of the wild-type strain, ΔcrxV, and its complementary strain (C-ΔcrxV) on rice leaves. We also compared the motility, the contents of biofilm, extracellular polysaccharides and extracellular enzymes of these strains. The results showed that the ΔcrxV mutant had lower virulence than the wild-type and complementary strains. Compared with the wild-type and complementary strains, the ΔcrxV mutant was significantly higher in biofilm content, but no significant difference was observed in its motility, extracellular polysaccharides and extracellular enzymes. These results demonstrate that the CrxV may positively regulate the virulence of Xoo through negative regulation of biofilm formation.
- CrxV,
- C-di-GMP,
- biofilm,
- virulence,
- Xanthomonas oryzae pv. oryzae

References

[1]	HEENGGE R. Principles of c-di-GMP signalling in bacteria [J]. Nature Reviews Microbiology, 2009, 7(4): 263 − 273. doi: 10.1038/nrmicro2109
[2]	ROSS P, WEINHOUSE H, ALONI Y, et al. Regulation of cellulose synthesis in Acetobacter xylinumby cyclic diguanylic acid [J]. Nature, 1987, 325(6101): 279 − 281. doi: 10.1038/325279a0
[3]	HENGGE R. Novel tricks played by the second messenger c-di-GMP in bacterial biofilm formation [J]. The EMBO Journal, 2013, 32(3): 322 − 323. doi: 10.1038/emboj.2012.351
[4]	JENAL U, REINDERS A, LORI C. Cyclic di-GMP: second messenger extraordinaire [J]. Nature Reviews Microbiology, 2017, 15(5): 271 − 284. doi: 10.1038/nrmicro.2016.190
[5]	OCHSNER U A, WILDERMAN P J, VASIL A I, et al. GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes [J]. Molecular Microbiology, 2002, 45(5): 1277 − 1287. doi: 10.1046/j.1365-2958.2002.03084.x
[6]	KARAOLIS D. K, RASHID M H, CHYTHANYA R., et al. c-di-GMP (3'-5'-cyclic diguanylic acid) inhibits Staphylococcus aureus cell-cell interactions and biofilm formation [J]. Antimicrob Agents Chemother, 2005, 49(3): 1029 − 1038. doi: 10.1128/AAC.49.3.1029-1038.2005
[7]	ALDRIDGE P, JENAL U. Cell cycle-dependent degradation of a flagellar motor component requires a novel-type response regulator [J]. Molecular Microbiology, 1999, 32(2): 379 − 391. doi: 10.1046/j.1365-2958.1999.01358.x
[8]	HECHT G B, NEWTON A. Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus [J]. Journal of Bacteriology, 1995, 177(21): 6223 − 6229. doi: 10.1128/jb.177.21.6223-6229.1995
[9]	SOMMER J M, NEWTON A. Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus [J]. Journal of Bacteriology, 1989, 171(1): 392 − 401. doi: 10.1128/jb.171.1.392-401.1989
[10]	DE SOUZA A A, IONESCU M, BACCARI C, et al. Phenotype overlap in Xylellafastidiosa Is controlled by the cyclic di-GMP Phosphodiesterase Eal in response to antibiotic exposure and diffusible signal factor-mediated cell-cell signaling [J]. Applied and Environmental Microbiology, 2013, 79(11): 3444 − 3454. doi: 10.1128/AEM.03834-12
[11]	NINO-LIU D O, RONALD P C, BOGDANOVE A J. Xanthomonas oryzaepathovars: model pathogens of a model crop [J]. Molecular Plant Pathology, 2006, 7(5): 303 − 324. doi: 10.1111/j.1364-3703.2006.00344.x
[12]	YANG F, QIAN S, TIAN F, et al. The GGDEF-domain protein GdpX1 attenuates motility, exopolysaccharide production and virulence in Xanthomonas oryzaepv. oryzae [J]. Journal of Applied Microbiology, 2016, 120(6): 1646 − 1657. doi: 10.1111/jam.13115
[13]	XUE D, TIAN F, YANG F, et al. Phosphodiesterase EdpX1 Promotes Xanthomonas oryzaepv. oryzaevirulence, exopolysaccharide production, and biofilm formation [J]. Applied and Environmental Microbiology, 2018, 84(22): e01717 − 18.
[14]	YANG F, TIAN F, SUN L, et al. A novel two-component system PdeK/PdeR regulates c-di-GMP turnover and virulence of Xanthomonas oryzaepv. oryzae [J]. Molecular Plant-Microbe Interactions, 2012, 25(10): 1361 − 1369. doi: 10.1094/MPMI-01-12-0014-R
[15]	LL Y R, ZOU H S, CHE Y Z, et al. A novel regulatory role of hrpD6 in regulating hrp-hrc-hpagenes in Xanthomonas oryzaepv. oryzicola [J]. Molecular Plant-Microbe Interactions, 2011, 24(9): 1086 − 1101. doi: 10.1094/MPMI-09-10-0205
[16]	SCHAFER A, TAUCH A, JAGER W, et al. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum [J]. Gene, 1994, 145(1): 69 − 73. doi: 10.1016/0378-1119(94)90324-7
[17]	ZHU PL. , ZHAO S, TANG J L, et al. ThersmA-like gene rsmA_Xooof Xanthomonasoryzaepv. oryzaeregulates bacterial virulence and production of diffusible signal factor [J]. Molecular Plant Pathology, 2011, 12(3): 227 − 237. doi: 10.1111/j.1364-3703.2010.00661.x
[18]	DILUZIO W R, TURNER L, MAYER M, et al. Escherichia coli swim on the right-hand side [J]. Nature, 2005, 435(7046): 1271 − 1274. doi: 10.1038/nature03660
[19]	YU C, CHEN H, TIAN F, et al. A ten gene-containing genomic island determines flagellin glycosylation: implication for its regulatory role in motility and virulence of Xanthomonas oryzae pv. oryzae [J]. Molecular Plant Pathology, 2018, 19(3): 579 − 592. doi: 10.1111/mpp.12543
[20]	TANG J L, LIU Y N, BARBER C E, et al. Genetic and molecular analysis of a cluster of rpfgenes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris [J]. MGG Molecular & General Genetics, 1991, 226(3): 409 − 417.
[21]	TIAN F, YU C, LI H, et al. Alternative sigma factor RpoN2 is required for flagellar motility and full virulence of Xanthomonas oryzaepv. oryzae [J]. Microbiological Research, 2015, 170: 177 − 183. doi: 10.1016/j.micres.2014.07.002
[22]	BÜTNER D, BONAS U. Regulation and secretion of Xanthomonas virulence factors [J]. FEMS Microbiology Reviews, 2010, 34(2): 107 − 133. doi: 10.1111/j.1574-6976.2009.00192.x
[23]	JHA G , RAJESHWARI R , SONTI R V. Bacterial type two secretion system secreted proteins: Double-edged swords for plant pathogens[J]. Molecular Plant-Microbe Interactions, 2005, 18 (9): 891-898.
[24]	LI H, XUE D, TIAN F, et al. Xanthomonas oryzaepv. oryzae response regulator triP regulates virulence and exopolysaccharide production via interacting with c-di-GMP phosphodiesterase pdeR [J]. Molecular Plant-Microbe Interactions, 2019, 32(6): 729 − 739. doi: 10.1094/MPMI-09-18-0260-R

Proportional views

通讯作者: 陈斌, bchen63@163.com

1.
沈阳化工大学材料科学与工程学院沈阳 110142

Figures(6) / Tables(1)

Get Citation

PDF

XML

Article views(886) PDF downloads(112) Cited by()

Proportional views

HTML

环二鸟苷酸（c-di-GMP）是细菌中普遍存在的第二信使分子，首次在葡糖酸醋酸杆菌中被发现，是纤维素合酶的异构激活因子^[1-2]。其后的研究结果表明，c-di-GMP参与调节各种生物过程如致病性、运动性、生物被膜、胞外多糖及胞外酶等^[3-4]。胞内c-di-GMP水平受含有GGDEF、EAL或HD-GYP结构域蛋白的调控：GGDEF蛋白负责c-di-GMP合成，而EAL或HD-GYP蛋白参与c-di-GMP的分解^[5]。GGDEF结构域含有约180个氨基酸残基，具有保守的Gly-Gly-Asp-Glu- Phe氨基酸残基序列^[6]。在新月形杆菌（Caulobacter crescentus）中，GGDEF结构域蛋白PleD具有双鸟苷酸环化酶活性，调控细菌的运动功能，促进细胞从运动转向静止^[7-9]。EAL结构域长约250个氨基酸，Glu–Ala–Leu序列高度保守，可调控细菌生物被膜的形成和运动性^[10]。有时GGDEF和EAL结构域共存于同一个蛋白中，可能只有其中1个结构域有功能。例如，铜绿假单胞菌BifA含有GGDEF和EAL结构域，但其没有c-di-GMP合成却有分解活性^[5]。稻黄单胞菌水稻致病变种（Xanthomonas oryzae pv. oryzae, Xoo）是引起水稻白叶枯病的病原菌^[11]，可对水稻造成严重的产量损失。C-di-GMP代谢相关蛋白同样参与Xoo致病力的调控，如：① GGDEF结构域蛋白GdpX1具有合成c-di-GMP的活性，调节Xoo的运动能力、胞外多糖的含量以及致病力^[12]；② EAL结构域蛋白PXO_03877具有降解c-di-GMP的活性，增强细菌的致病性、运动性、胞外多糖合成以及生物被膜的形成能力^[13]；③ GGDEF/EAL结构域蛋白PdeR与组氨酸激酶PdeK组成双组份系统，磷酸化的PdeR具有分解c-di-GMP的能力，pdeR突变降低Xoo的致病性、胞外多糖及生物被膜的含量，但对运动性和胞外酶无明显影响^[14]。本研究分析了Xoo中另一个GGDEF/EAL结构域蛋白CrxV对运动性、生物被膜、胞外多糖以及胞外酶等毒力因子的调控作用，为进一步分析c-di-GMP在Xoo与水稻互作中的作用奠定基础。

1. 材料与方法

1.1. 材料

Xoo野生型菌株PXO99A、大肠杆菌DH5a、基因敲除载体pK18mobSacB、过表达载体菌株pHM1等均由笔者所在的实验室保存；一般化学药品购自广州化学试剂公司；PCR试剂购自诺唯赞生物科技有限公司；内切酶和连接酶购自NEB生物科技有限公司；快速质粒小提试剂盒、琼脂凝胶DNA回收试剂盒等购自天根生物科技有限公司；IR24水稻用于检测Xoo的致病力；用SMART软件（http://smart.embl-heidelberg.de/）分析蛋白保守结构域。

1.2. 突变体与互补菌株的构建及其致病力分析

将crxV基因上下游各约500 bp的序列通过PCR扩增、酶切（HindIII/XbaI与XbaI/EcoRI）回收后连接到自杀性载体pK18mobSacB（HindIII/EcoRI酶切），获得敲除载体pK-crxV，电击转化PXO99^A菌株，采用同源重组2次交换的方法构建突变体ΔcrxV^[15-16]。利用PCR方法扩增crxV基因片段，酶切（HindIII/EcoRI）回收后连接互补载体pHM1（HindIII/EcoRI酶切），然后转化ΔcrxV获得互补菌株C-ΔcrxV（引物序列见表1）。为便于比较，野生型菌株和ΔcrxV也转入空载体pHM1。采用剪叶法检测致病力，将突变体菌株ΔcrxV-pHM1、野生型菌株PXO99^A-pHM1和互补菌株C-ΔcrxV接种至生长期为60 d的水稻叶片上，14 d后统计水稻的发病情况。

引物 Primer	序列 Sequences	用途 Usages
CrxVFF	GCACAAGCTTTCGCAGTTCGTGCTGGCAGT	crxV deletion
CrxVFR	GCACTCTAGAATGCAGGCGCATCGACCTCA
CrxVRF	GCACTCTAGATGCATGCGCCAACTCGGCAT
CrxVRR	GCACAATTCCAAGGCCTTCAAGAGCTACG
CrxVhmF	TATGACCATGATTACGCCAAGCTTGATGCGCCTGCATACCCGCATC	ΔcrxV complement
CrxVhmR	TGTAAAACGACGGCCAGTGAATTCATCAACTGTGCCAGGAACTG	ΔcrxV complement
注：“—”表示酶切位点　　Note: restriction enzyme sites are underlined

Table 1. Primers used in this study

1.3. 胞外酶活性检测

参照文献[17]的方法检测胞外酶的活性，将突变体菌株ΔcrxV-pHM1、野生型菌株PXO99A-pHM1和互补菌株C-ΔcrxV置28 ℃条件下液体培养48 h后，取1 mL培养物用ddH₂O洗涤2遍，用1 mL ddH₂O重悬菌体。取3 µL重悬液分别接种至纤维素检测培养基、淀粉酶检测培养基和蛋白酶检测培养基上，在28 ℃条件下静置培养5 d。PGA培养基：1 g·mL⁻¹ Tryptone、1 g·mL⁻¹葡萄糖、0.1 g·mL⁻¹ L-谷氨酸钠、1.5% agar；纤维素检测培养基为PGA培养基+0.5%羧甲基纤维素；淀粉酶检测培养基为PGA培养基+0.1%可溶性淀粉；蛋白酶检测培养基为PGA培养基+2%脱脂奶粉。纤维素酶活性测定方法： 0.1%刚果红染色30 min，用1mol·L⁻¹的NaCl溶液洗2次，观察酶水解直径(cm)；淀粉酶活性测定方法：1：100 I₂/KI (0.08% mol·L⁻¹ I₂，3.2 mol·L⁻¹ KI)溶液染色10 min，观察酶水解直径（cm）；蛋白酶活性测定方法：直接在蛋白培养基上观察水解光圈（cm）。每个试验重复3次。

1.4. 游动性检测

参照文献[18]的方法检测游动性。用牙签蘸取1.3节中的菌重悬液，垂直接种于含0.25%琼脂的游动性培养基（0.03%Tryptone, 0.03%Yeast-extract, 0.25%agar）底部，在28 ℃条件下静置培养4 d，测量菌株在培养基表面游动的直径（cm）并统计。重复3次。

1.5. 生物被膜及胞外多糖试验

参照文献[19-20]的方法检测生物被膜的形成及胞外多糖的产生。取单克隆细菌在PSA中培养48 h后，取2 mL菌在5 500 r·min⁻¹条件下离心3 min，收集菌体，用M210培养基（5 g·L⁻¹蔗糖； 8 g·L⁻¹酶水解酪素； 4 g·L⁻¹ Yeast-extract； 3 g·L⁻¹ K₂HPO₄；0.3 g·L⁻¹ MgSO₄ · 7H₂O，pH7.0）洗涤2次，再加入M210重悬，把重悬液的OD₆₀₀调至0.5。生物被膜实验：取2 mL重悬液（OD₆₀₀=0.5）接种至玻璃试管，在28 ℃下静置培养4 d，缓慢倒出玻璃试管底的培养基，用H₂O洗涤3遍，0.1%结晶紫染色液染色30 min，再用H₂O洗涤3遍，加入3 mL90%乙醇溶解，在OD₅₉₀下测吸光值。胞外多糖实验：取2 µL重悬液（OD₆₀₀=0.5）接种至PGA培养基表面，在28 ℃下静置培养4 d，观察菌落表面形态。试验重复3次。

3. 讨　论

C-di-GMP分别由GGDEF结构域蛋白负责合成和EAL/HD-GYP结构域蛋白负责降解，胞内受体通过感知c-di-GMP水平调控细胞多个代谢途径，影响细菌的生长及环境适应能力。通常低水平的c-di-GMP提高细菌的运动能力，高水平的c-di-GMP则有利于生物被膜的形成，调节细菌的致病能力^[4]。在Xoo中， GGEDF结构域蛋白GdpX1，通过负调控胞外多糖的产生和运动性从而抑制Xoo的致病性^[12]。EAL结构域蛋白PXO_03877具有c-di-GMP水解酶活性，正调控致病性、生物膜的形成和胞外多糖的产生^[13]。PdeR含有保守的GGDEF和EAL结构域，作为响应调节因子与组氨酸激酶PdeK组成双组份系统，正调控Xoo致病性和胞外多糖的产生^[24]。同PdeR类似，CrxV也含有保守的GGDEF和EAL结构域，但其具体工作还不清楚。由于致病性与c-di-GMP的含量可能成负相关^[13,24], crxV突变导致Xoo致病力降低，因此CrxV可能作为c-di-GMP分解酶，其GGDEF结构域可能没有酶活性。虽然研究发现Xoo中影响致病性的c-di-GMP代谢酶都可能调控诸如运动性、胞外多糖和胞外酶等毒力因子的合成或分泌^[13,24]，但crxV突变并不影响这些因子的形成或分泌。有趣的是，crxV突变导致Xoo生物被膜含量显著增加。生物被膜形成和解聚是细菌致病重要的调节过程，缺一不可。因此，CrxV可能负调控生物被膜的解聚，进而正调控病原菌的致病力。以上结果虽然显示CrxV可能通过介导c-di-GMP代谢，影响病原菌生物被膜的含量，调控病原菌的致病力，但CrxV的酶活性及其在生物被膜形成与解聚中的作用还不清楚，尚需做进一步研究。

Reference (24)

[1]	HEENGGE R. Principles of c-di-GMP signalling in bacteria [J]. Nature Reviews Microbiology, 2009, 7(4): 263 − 273.
[2]	ROSS P, WEINHOUSE H, ALONI Y, et al. Regulation of cellulose synthesis in Acetobacter xylinumby cyclic diguanylic acid [J]. Nature, 1987, 325(6101): 279 − 281.
[3]	HENGGE R. Novel tricks played by the second messenger c-di-GMP in bacterial biofilm formation [J]. The EMBO Journal, 2013, 32(3): 322 − 323.
[4]	JENAL U, REINDERS A, LORI C. Cyclic di-GMP: second messenger extraordinaire [J]. Nature Reviews Microbiology, 2017, 15(5): 271 − 284.
[5]	OCHSNER U A, WILDERMAN P J, VASIL A I, et al. GeneChip® expression analysis of the iron starvation response in Pseudomonas aeruginosa: identification of novel pyoverdine biosynthesis genes [J]. Molecular Microbiology, 2002, 45(5): 1277 − 1287.
[6]	KARAOLIS D. K, RASHID M H, CHYTHANYA R., et al. c-di-GMP (3'-5'-cyclic diguanylic acid) inhibits Staphylococcus aureus cell-cell interactions and biofilm formation [J]. Antimicrob Agents Chemother, 2005, 49(3): 1029 − 1038.
[7]	ALDRIDGE P, JENAL U. Cell cycle-dependent degradation of a flagellar motor component requires a novel-type response regulator [J]. Molecular Microbiology, 1999, 32(2): 379 − 391.
[8]	HECHT G B, NEWTON A. Identification of a novel response regulator required for the swarmer-to-stalked-cell transition in Caulobacter crescentus [J]. Journal of Bacteriology, 1995, 177(21): 6223 − 6229.
[9]	SOMMER J M, NEWTON A. Turning off flagellum rotation requires the pleiotropic gene pleD: pleA, pleC, and pleD define two morphogenic pathways in Caulobacter crescentus [J]. Journal of Bacteriology, 1989, 171(1): 392 − 401.
[10]	DE SOUZA A A, IONESCU M, BACCARI C, et al. Phenotype overlap in Xylellafastidiosa Is controlled by the cyclic di-GMP Phosphodiesterase Eal in response to antibiotic exposure and diffusible signal factor-mediated cell-cell signaling [J]. Applied and Environmental Microbiology, 2013, 79(11): 3444 − 3454.
[11]	NINO-LIU D O, RONALD P C, BOGDANOVE A J. Xanthomonas oryzaepathovars: model pathogens of a model crop [J]. Molecular Plant Pathology, 2006, 7(5): 303 − 324.
[12]	YANG F, QIAN S, TIAN F, et al. The GGDEF-domain protein GdpX1 attenuates motility, exopolysaccharide production and virulence in Xanthomonas oryzaepv. oryzae [J]. Journal of Applied Microbiology, 2016, 120(6): 1646 − 1657.
[13]	XUE D, TIAN F, YANG F, et al. Phosphodiesterase EdpX1 Promotes Xanthomonas oryzaepv. oryzaevirulence, exopolysaccharide production, and biofilm formation [J]. Applied and Environmental Microbiology, 2018, 84(22): e01717 − 18.
[14]	YANG F, TIAN F, SUN L, et al. A novel two-component system PdeK/PdeR regulates c-di-GMP turnover and virulence of Xanthomonas oryzaepv. oryzae [J]. Molecular Plant-Microbe Interactions, 2012, 25(10): 1361 − 1369.
[15]	LL Y R, ZOU H S, CHE Y Z, et al. A novel regulatory role of hrpD6 in regulating hrp-hrc-hpagenes in Xanthomonas oryzaepv. oryzicola [J]. Molecular Plant-Microbe Interactions, 2011, 24(9): 1086 − 1101.
[16]	SCHAFER A, TAUCH A, JAGER W, et al. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum [J]. Gene, 1994, 145(1): 69 − 73.
[17]	ZHU PL. , ZHAO S, TANG J L, et al. ThersmA-like gene rsmA_Xooof Xanthomonasoryzaepv. oryzaeregulates bacterial virulence and production of diffusible signal factor [J]. Molecular Plant Pathology, 2011, 12(3): 227 − 237.
[18]	DILUZIO W R, TURNER L, MAYER M, et al. Escherichia coli swim on the right-hand side [J]. Nature, 2005, 435(7046): 1271 − 1274.
[19]	YU C, CHEN H, TIAN F, et al. A ten gene-containing genomic island determines flagellin glycosylation: implication for its regulatory role in motility and virulence of Xanthomonas oryzae pv. oryzae [J]. Molecular Plant Pathology, 2018, 19(3): 579 − 592.
[20]	TANG J L, LIU Y N, BARBER C E, et al. Genetic and molecular analysis of a cluster of rpfgenes involved in positive regulation of synthesis of extracellular enzymes and polysaccharide in Xanthomonas campestris pathovar campestris [J]. MGG Molecular & General Genetics, 1991, 226(3): 409 − 417.
[21]	TIAN F, YU C, LI H, et al. Alternative sigma factor RpoN2 is required for flagellar motility and full virulence of Xanthomonas oryzaepv. oryzae [J]. Microbiological Research, 2015, 170: 177 − 183.
[22]	BÜTNER D, BONAS U. Regulation and secretion of Xanthomonas virulence factors [J]. FEMS Microbiology Reviews, 2010, 34(2): 107 − 133.
[23]	JHA G , RAJESHWARI R , SONTI R V. Bacterial type two secretion system secreted proteins: Double-edged swords for plant pathogens[J]. Molecular Plant-Microbe Interactions, 2005, 18 (9): 891-898.
[24]	LI H, XUE D, TIAN F, et al. Xanthomonas oryzaepv. oryzae response regulator triP regulates virulence and exopolysaccharide production via interacting with c-di-GMP phosphodiesterase pdeR [J]. Molecular Plant-Microbe Interactions, 2019, 32(6): 729 − 739.

Name
E-mail
Phone
Title
Content
Verification Code

Message Board